Pleurocarpous Mosses: Systematics and Evolution

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The Systematics Association Special Volume Series 71

Pleurocarpous Mosses

Half Title Page

Systematics and Evolution

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The Systematics Association Special Volume Series Series Editor Alan Warren Department of Zoology,The Natural History Museum, Cromwell Road, London SW7 5BD, UK. The Systematics Association promotes all aspects of systematic biology by organizing conferences and workshops on key themes in systematics, publishing books and awarding modest grants in support of systematics research. Membership of the Association is open to internationally based professionals and amateurs with an interest in any branch of biology including palaeobiology. Members are entitled to attend conferences at discounted rates, to apply for grants and to receive the newsletters and mailed information; they also receive a generous discount on the purchase of all volumes produced by the Association. The first of the Systematics Association’s publications The New Systematics (1940) was a classic work edited by its then-president Sir Julian Huxley, that set out the problems facing general biologists in deciding which kinds of data would most effectively progress systematics. Since then, more than 70 volumes have been published, often in rapidly expanding areas of science where a modern synthesis is required. The modus operandi of the Association is to encourage leading researchers to organize symposia that result in a multi-authored volume. In 1997 the Association organized the first of its international Biennial Conferences.This and subsequent Biennial Conferences, which are designed to provide for systematists of all kinds, included themed symposia that resulted in further publications. The Association also publishes volumes that are not specifically linked to meetings and encourages new publications in a broad range of systematics topics. Anyone wishing to learn more about the Systematics Association and its publications should refer to our website at www.systass.org. Other Systematics Association publications are listed after the index for this volume.

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The Systematics Association Special Volume Series 71

Pleurocarpous Mosses

Title Page

Systematics and Evolution

Edited by

Angela E. Newton Natural History Museum London, U.K.

Raymond S. Tangney National Museum Wales Cardiff, U.K.

Boca Raton London New York

CRC Press is an imprint of the Taylor & Francis Group, an informa business

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The cover photo was taken by Neil Bell, and is of Rhizogonium distichum (Sw.) Brid. from Tasmania.

CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2007 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Printed in the United States of America on acid-free paper 10 9 8 7 6 5 4 3 2 1 International Standard Book Number-10: 0-8493-3856-5 (Hardcover) International Standard Book Number-13: 978-0-8493-3856-4 (Hardcover) This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. No part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, please access www.copyright.com (http:// www.copyright.com/) or contact the Copyright Clearance Center, Inc. (CCC) 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. CCC is a not-for-profit organization that provides licenses and registration for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Library of Congress Cataloging-in-Publication Data Pleurocarpous mosses : systematics and evolution / edited by Angela E. Newton and Raymond S. Tangney. p. cm. Includes bibliographical references (p. ). ISBN 0-8493-3856-5 (alk. paper) 1. Pleurocarpous mosses--Classification. 2. Pleurocarpous mosses--Evolution. I. Newton, Angela E. II. Tangney, Raymond S. QK538.P54 2006 588’.2--dc22 Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com

2006048350

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Foreword This is the age of phylogenetics in biology. The working out of rigorous methods for phylogenetic inference in the 1970s and 1980s, combined with the massive influx of new data from the molecular level in the 1990s, resulted in increasingly better-supported and more believable phylogenetic trees for most groups of organisms. At the same time, a plethora of new comparative methods has been developed in order to use phylogenetic trees for understanding an incredibly broad spectrum of biological processes. Phylogenetic tree-thinking has led to fundamental advances in systematics, biogeography, coevolution, community assembly, macroevolution, medicine, behavior, evolution of development, physiology, population genetics, comparative genomics, and many other areas. This progress has been very evident in bryophyte biology as well. It wasn’t that long ago (less than one academic generation) that purely speculative stories about the evolution of major bryophyte groups were the norm, tending to give systematics and phylogeny-building a bad reputation among biologists as a whole. The wrong models were being used in bryology (as elsewhere at the time), with evolution viewed as some kind of ladder, a hold-over of the ancient “Great Chain of Being” concept. Articles and books were filled with arguments about which bryophyte groups are the most primitive or most advanced, and how best to linearly arrange the groups in between from lowest to highest (e.g., debates over whether the Polytrichaceae should go at the beginning or end of a moss flora!). Following another misleading mode of thinking that stems all the way back to Aristotle, people thought they needed to weight characters a priori by their importance (e.g., debates over whether sporophytic or gametophytic characters were more important in showing relationships) or to decide ahead of time what the evolutionary trends were. Every possible scenario about relationships and character change was put forward and supported by force of personality, with little to no objective means available for evaluating competing hypotheses. The Hennigian approach to phylogenetics cuts through these ancient and wrong-headed approaches, by applying the right model (a tree), and providing an objective method for evaluating evidence for branches on that tree one character at a time, without preconceptions, using a rigorous concept of homology. Instead of ordering taxa in a linear arrangement, the question became their relative recency of common ancestry — we realize now that extant taxa cannot be linked up in a linear series; they are all equally “advanced.” Character states on the other hand can (and should) be polarized into a transformation series through time along branches in a phylogenetic tree, with shared derived characters (synapomorphies) serving as evidence for the existence of nested monophyletic groups. By examining many independent characters that can each be inferred separately to have changed along a particular branch in the past, strong support can be built up for a monophyletic group descended from that branch. As in other groups of organisms, our phylogenetic trees are getting ever stronger in bryophytes, while the weak places remaining in the trees are becoming ever more clearly highlighted as targets for future research. What causes lack of resolution in parts of phylogenetic trees? Many biological processes can confuse the reconstruction of history, including hybridization or other forms of horizontal gene transfer, misleading extinctions of ancestral polymorphisms (called “lineage sorting”), and natural selection that may cause convergent evolution. One problematic situation that is of particular relevance to the subject of this book is highly unequal branch lengths, i.e., where short, deep branches may lack enough signal to reconstruct them correctly at some distant future time, and unrelated long branches may appear falsely to be related through accumulated non-homologous character-state matches (known as “long-branch attraction”). There were apparently times in the past, as in the early radiation of pleurocarpous mosses, when things happened fast. Many divergence

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events happened relatively quickly, one after another, allowing little time for character transformations along the temporally short lineages that existed until the next splitting event. In such cases there is precious little data that can potentially address the relative recency of branching order, and such data tends to slowly disappear over time as further mutations obscure the evidence. The pleurocarpous mosses, a morphologically and ecologically diverse group that contains a large proportion of the described species of mosses, have been one of these difficult regions of the tree of life to reconstruct, and are well worth a book-length treatment. The authors bring to bear considerable amounts of new data and careful analytical methods designed to help with such problems as long-branch attraction. It is clear from their efforts that, although such cases of deep and rapid radiation are extremely difficult to approach, they are not impossible. Careful choice of enough suitable markers for those short ancient branches, including slowly evolving genes and morphological characters (which can be really useful in such cases because of their episodic mode of change), has a hope of resolving them. This book provides a fascinating case study of what can happen when a large number of researchers tackle a thorny phylogenetic problem in a cooperative manner, and hopefully will serve as a model for other such efforts. This is the first book of its kind for the bryophytes — which are increasingly being recognized as important organisms for lab research, and as major players in the ecosystem. It is a rare type of book for any group of plants, an attempt to review all that is currently known about their phylogeny, and then to relate that to a full range of important topics regarding their biology. The topics range from overarching backbone relationships to detailed examination of specific taxonomic groups, followed by a variety of evolutionary studies. This is a fine effort by the editors and authors, which should serve to bring these interesting plants to the attention of botanists and evolutionary biologists in general, and stimulate continued efforts to refine the remaining uncertainties and to understand the causes and effects of this important radiation in land plants. Brent D. Mishler

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Preface The application of cladistic analysis and molecular data to the study of relationships of organisms has resulted in a revolution in the systematics of many groups of organisms, not least the mosses. We can now propose hypotheses about relationships in an objective manner, and use topologies resulting from analyses to ask questions about the evolutionary processes underlying the observed patterns. At the same time, there has been a paradigm shift, from the traditional, knowledge-based and synthetical methodology, where individuals “knew” the organisms and suggested classifications on that basis, to a data-based, analytical methodology where matrices of characters (molecular or morphological) are assembled and analysed using computers. Although morphological data and the older methods have been responsible for a very large proportion of our current knowledge at all taxonomic levels, some conclusions based on these have been erroneous, and other problems have proved intractable. The circumscription and relationships of the pleurocarpous mosses present a major example where traditional data have accomplished much but also leave much to be desired. The symposium on pleurocarpous mosses held at Cardiff in September 2004 provided an opportunity for many of the researchers active in the systematics of this group to meet and present the results of their studies. This event was held approximately ten years after the publication of the first major attempt (by Lars Hedenäs, in 1994) to study the relationships of pleurocarpous mosses using cladistic methodology, and gives a broad overview of the progress in our understanding of the relationships of the pleurocarpous mosses. In particular, this book draws on both molecular data and morphology (including morphology of molecules), and synthetical and analytical methodology, to highlight the areas of the pleurocarp phylogeny where there is some resolution, and to identify the regions where there are still intriguing questions to be addressed. In the introductory chapter, Bill Buck reviews the history of pleurocarp classification, identifying a cyclical pattern in the philosophical principles underlying efforts to resolve the classification of the pleurocarps, which revolved around the relative importance of the gametophyte and sporophyte generations as sources of characters. He notes that the classification of pleurocarpous mosses has traditionally lagged behind that of acrocarps (which is a reflection of the morphological diversity and distinctness of the acrocarp groups, in contrast to the morphological plasticity and close relationships of the pleurocarps). In one of the earliest classifications of mosses, based on sporophyte characters, Hedwig included 30 genera of acrocarps but only five genera of pleurocarps, despite the very similar number of species now recognized in these divisions. Subsequently classifications have alternated between emphasizing gametophyte and sporophyte characters, but the advent of molecular data has allowed bryologists to present classifications independent of morphology. Although initial work using one-gene trees resulted in faulty classifications, multiple-gene trees have refined the process. However, the Hypnales, the largest group among the mosses and a key pleurocarp group, still lacks phylogenetic resolution. A combination of multiple genes with carefully observed morphology should provide us with a stable classification. The two following chapters explore the relationships of the earliest-diverging lineages of mosses in which pleurocarpous morphology appeared, emphasizing molecular and morphological data, respectively. The majority of taxa in this region of the phylogeny, including the rhizogonian and hypnodendroid mosses, have a primarily Gondwanan distribution centered in Oceania, and represent only about 1% of the species in the pleurocarpous mosses. Terry O’Brien investigates the distribution of the phylogenetic diversity in pleurocarpous mosses through an analysis of a four-gene cpDNA dataset of 58 exemplar taxa. The results indicate that pleurocarpous and non-pleurocarpous members of the Rhizogoniaceae plus the acrocarpous genera Aulacomnium, Calomnion and Orthodontium

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Participants at the symposium on Pleurocarpous Mosses: Systematics and Evolution. Group photo taken on the steps of the National Museum of Wales, Cardiff, September 2004, by Misha Ignatov. From left to right: Niklas Pedersen; Lars Hedenäs; Philip Stanley; Ray Tangney; Gisela Oliván; Anastasia Gardiner; Terry O’Brien; Alan Orange; Bill Buck; Sean Russell; Neil Bell; Brian O’Shea; Dolores Gonzalez; Liz Kungu; Angie Newton; BoonChuan Ho; Efrain De Luna; Hans Kruijer; Rolf Blöcher; Yelitza León-Vargas; Roy Perry; Katherine Vint; Sanna Huttunen; Nancy Slack; Dietmar Quandt.

are the sister group or near sister group to the hypnodendroid pleurocarps and the Hypnidae (Hypnobryales, Hookeriales and Ptychomniales). These results highlight a marked asymmetry in the phylogenetic distribution of diversity of pleurocapous mosses similar to that found in angiosperms. Looking at the diversity of morphology in these taxa, Neil Bell and Angela Newton examine modular branching structure in exemplars from the rhizogoniaceous grade, in order to isolate discrete architectural types associated with the pleurocarpous condition. These are described and used as a basis for optimization of pleurocarpy sensu stricto onto a phylogeny derived from chloroplast and mitochondrial molecular sequence data. Characters closely associated with pleurocarpy in these taxa are also optimized, and the results used to examine scenarios for the evolution of modular form in the basal pleurocarpous clades. The results reveal that there is disproportionate diversity of pleurocarpous architectural types in the rhizogoniaceous grade compared with the hypnodendroid pleurocarps and the Hypnidae, and that these probably represent successive and varied novel adaptive strategies that utilize the potential of the key innovation of pleurocarpy. Another clade with a position among the early-diverging lineages of pleurocarpous mosses, with affinities to the Hookeriales, is the family Hypopterygiaceae, comprising 21 species distributed among seven or eight genera. These are characterized by a distinctive leaf arrangement and a diversity of branching architectures. In Chapter 4, Hans Kruijer and Rolf Blöcher give an overview of systematic studies in the family and present a phylogenetic study of relationships within the family using a combination of morphological and molecular data. Although their results, based on molecular data for 15 species of Hypopterygiaceae and nine species of related families, show support for monophyly of the family, the traditional circumscription of some of the genera needs to be reviewed. The authors consider that the homoplasy of the morphological characters suggested by the molecular data requires a new view of the morphology and that increased sampling will produce a fuller understanding of the evolutionary history of the family, resulting in a new generic classification of the Hypopterygiaceae. In Chapter 5, Boon-Chuan Ho and Hans Kruijer report on

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the plasticity of growth patterns in Calyptrochaeta, a small genus in the Hookeriaceae (Hookeriales) that grows mainly on decaying wood and tree bases in wet tropical mountain forests in Malesia and adjacent areas. These species display two different growth patterns in which there is no clear differentiation into axes of different hierarchical levels. These growth patterns are characterized by orthotropic axes and sympodial (basal) innovations, and by long plagiotropic axes showing indeterminate growth and monopodial branching. However, observations suggest that the plagiotropic growth pattern represents a character state derived from the orthotropic one, and that their striking difference should not be overestimated in taxonomic research on Calyptrochaeta. In the following section, Chapters 6 to 10 present the results of analyses, primarily of molecular data and using a variety of analytical techniques, to explore the relationships of families within the Hypnales. This group represents about 80% of the pleurocarpous moss species (and a third of all extant moss species) but relationships within and between the families are very poorly known. Sanna Huttunen, Anastasia Gardiner and Michael Ignatov review progress in understanding the Brachytheceaceae, one of the most diverse groups of mosses. Although a backbone phylogeny of the Brachytheciaceae has been suggested, problems remain with some groups. They present new data with additional species, utilizing POY alignment and analysis of the secondary structure of trnL intron. Their results highlight extensive parallelisms in the morphology of major lineages associated with ecological specialization. Most lineages within the family have subaquatic members with morphologies convergent across lineages in characters such as leaf shape, leaf orientation and costal structure. Similarly a tendency to epiphytism across lineages has led to homoplasy in peristome morphology. The authors address these repeated patterns of extreme ecological divergence and whether the divergent morphologies of these taxa should be reflected in paraphyletic genera. In the following chapter, Sanna Huttunen and Dietmar Quandt synthesize results from four phylogenetic analyses of the moss family Meteoriaceae and review the current generic relationships within the family. Phylogenies are used to evaluate morphological evolution within the family and to pinpoint the synapomorphies of the major clades. Previous classifications of the Meteoriaceae are seen to be characterized by extensive homoplasy of morphological, particularly cellular, characters. Although more extensive future sampling will be needed to test monophyly of the genera, at the subfamily level major divisions in the family are recognized, including a new subfamily. Important morphological features at this level are orientation of stem leaves and characters of the axillary hairs and peristome. The Trachypodaceae, long associated with the Meteoriaceae, is resolved as a grade basal to the Meteoriaceae. The Amblystegiaceae have been traditionally circumscribed by their mostly single and long leaf costa, cylindrical and curved spore capsule, and their preference for humid to wet environments. Lars Hedenäs and Alain Vanderpoorten examine the suggestions of late twentieth century studies, analysing comprehensive morphological datasets, that radical reclassification among the Amblystegiaceae was necessary. They found that phylogenetic studies based on both molecular and morphological data resolved many relationships at the generic level and provided strong evidence that the family should be split into the Amblystegiaceae s. str., with the taxa related to Amblystegium, Campylium, Drepanocladus, and Palustriella, and the Calliergonaceae, with the taxa around Calliergon, Scorpidium, and Warnstorfia. However, many relationships within the two families and their genera remain uncertain. For example, within Hygroamblystegium morphological and molecular evolution appear to be uncoupled, suggesting that several currently recognized morpho-species should be synonymized. A team headed by Michael Ignatov, again using a diversity of analytical methods and data, focuses in Chapter 9 on taxa traditionally classified in the Leskeaceae to reassess the relationships of mosses in the order Hypnales. They identify a basal grade and two main clades, and analyse the circumscription and changes in these and subclades under the different analytical methods. The split between Amblystegiaceae s. str. and the Calliergonaceae is again found by these authors although the taxon distribution is not identical. The Leskeaceae as traditionally circumscribed are not monophyletic but found in both main clades. Interestingly, the two main clades have some similarities to the traditional classification of pleurocarpous mosses into Leucodontales

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and Hypnales, a classification abandoned when earlier analyses of molecular data showed that the epiphytic leucodontalean taxa had been derived repeatedly from within the Hypnales. Relationships within the family Amblystegiaceae are examined in greater detail in Chapter 10, where Gisela Oliván, Lars Hedenäs and Angela Newton use molecular data to explore the phylogeny of Hygrohypnum and related taxa. Their results reveal the polyphyly of the genus and demonstrate that the morphological characters traditionally used to circumscribe the genus may reflect convergence. Within the genus there is strong support for two major clades, one with Hygrohypnum styriacum and H. luridum (the type of the genus) and the two species included as representatives of Amblystegiaceae s. str., while the other clade includes the remaining species of the genus plus Platydictya jungermannioides, Campylophyllum halleri and the two taxa chosen as representatives of Calliergonaceae, Calliergon cordifolium and Warnstorfia exannulata. These chapters have gone a long way towards suggesting some major relationships within the Hypnales, but large numbers of taxa are involved and many important families are barely represented. In order to adequately assess relationships of the remaining taxa, additional projects at a similar scale will be required. Morphology has been the primary source of information regarding pleurocarpous moss relationships in the past approximately 200 years, but has also undergone something of a revolution with the advent of cladistic methodology and the necessity to examine characters in sufficient detail to include them in data matrices. In Chapters 11 to 15 morphological character systems are explored in some depth. Lars Hedenäs, provides a review of morphological characters and their use in pleurocarpous moss systematics. The strategy of using a few “key characters,” while highly successful in many groups of organisms, has been distinctly misleading in the pleurocarpous mosses with their high levels of plasticity and parallel evolution of features. Only relatively recently have numerous and more obscure characters been studied systematically in numerous species. He outlines how in the last 20 years cladistics and the inclusion of molecular data for phylogenetic reconstruction have revolutionized our understanding of pleurocarpous moss relationships. As molecular information is largely independent of morphology, the reliability of the latter in reconstructing relationships can now be assessed. He notes that relationships that are well supported by molecular data are frequently suggested by morphology, but that morphology yields more ambiguous results than molecular data, most likely due to incorrect interpretations of homology. The latter is especially serious for taxa with orthotropous (earlier called “erect”), specialized spore capsules. However, morphology sometimes reveals relationships that have not yet been resolved by molecular data. Hedenäs concludes that molecular phylogenies can be fully interpreted only in the light of structural similarities or differences between taxa. Morphological characters used to delimit taxa within the African Entodontaceae are reevaluated by Elizabeth Kungu and Royce Longton. Characters available in both the sporophyte and gametophyte are described and assessed in the light of the restrictions incurred due to morphological reduction. Gametophyte structures are examined for characters to reinforce the taxonomic boundaries based on peristome ornamentation patterns which provide key characters for delimiting both genera and species within the Entodontaceae. However, the use of peristome ornamentation patterns is confounded by the high level of variation associated with peristome reduction. Examination of internal peristome structure demonstrates a relationship with function and proves that the major differences in surface ornamentation between papillose and striate reflect a difference in internal deposition. Morphology indicates that the family as currently recognized is probably not monophyletic and the status of Pylaisiobryum is unresolved. The homologies of stem structures in pleurocarpous mosses, especially pseudoparaphyllia and similar structures are revisited in Chapter 13 by Michael Ignatov and Lars Hedenäs, where they give an overview of current definitions of different stem structures in pleurocarps. Paraphyllia are usually considered as organs not concentrated around branch initials, but their observations reveal that positional and structural homologies in “paraphyllia” and “pseudoparaphyllia” suggest that the distinctions between paraphyllia, pseudoparaphyllia and proximal branch leaves remain unclear. A set of characters for the description of the diversity of foliose structures found at the base of branches

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or around branch initials is suggested, replacing the commonly generalized character of pseudoparaphyllia absence versus presence. The two following chapters (14 and 15) examine specific aspects of the branching structure of pleurocarpous mosses. Angela Newton discusses the history and application of the concepts of acrocarpy and pleurocarpy, and the implications of these features for the exploitation of morphological characters in the systematic study of pleurocarpous mosses. The necessity of “deconstructing” branching architecture into modules is emphasized. The components of branching architecture are analysed, described and figured, including case studies of individual species. Ray Tangney emphasizes structural concepts and examines the way in which architectural terms, as used in the analysis of Tracheophytes, have increased our understanding of branching in mosses. He differentiates between monopodial and sympodial growth and discusses repeated growth units. The concept of the architectural unit, not previously applied to mosses, is utilized to help recognize both the type of branching and the hierarchical level at which branching is occurring, aspects of branching analysis that have had insufficient emphasis. In doing so, differences are highlighted between sequential growth (branching that builds architectural units), and reiterative growth (growth that repeats the architectural units). The origins of pleurocarpous mosses are explored in Chapters 16 and 17, using fossil and molecular data. Reviewing Paleozoic and Mesozoic fossil mosses, Michael Ignatov and Dmitry Shcherbakov address the question of whether pleurocarpous mosses originated before the Cretaceous. They found that some Paleozoic, Triassic and Jurassic fossils are similar to extant pleurocarps in some respects, but that other peculiarities of these fossil mosses make their immediate placement in extant groups problematic. They describe a new genus and species from the Upper Jurassic of Transbaikalia, concluding that this species is probably the fossil most similar to extant pleurocarps among pre-Cenozoic fossils. This new fossil corroborates the conclusions of the team headed by Angela Newton and Niklas Wikström, who explore the patterns of diversification of the pleurocarps and estimate possible dates for their origins using molecular data, calibrated on the fossil date of 450 myr for the origin of land plants. Their results suggest that the earliest-diverging extant lineages in which pleurocarpy is found originated in the mid Jurassic (at 194–161 mya), significantly before the period in which the majority of the extant lineages diversified (about 165–131 mya), probably over a (geologically) short period of time. This radiation coincides with the diversification of the angiosperms in the early Cretaceous and is earlier than the period in which angiosperm forests came to dominate the terrestrial environment in the early Cenozoic, suggesting that pleurocarpous mosses were well established before the appearance of the highly structured forests that now exist. In the final two chapters evolutionary questions are explored. Niklas Pedersen and Angela Newton use Bayesian inference and maximum likelihood methods, with chloroplast and mitochondrial DNA sequence data, to evaluate phylogenetic relationships within the Ptychomniales. The genus Glyphothecium was found to be polyphyletic, and a new genus described. They then use the resulting topology to study evolution of 18 morphological characters, and to test whether the evolution of dwarf males is correlated with morphological variation and the epiphytic habit. Reconstructions of morphological characters using maximum parsimony and maximum likelihood are mostly congruent although maximum likelihood reconstructions indicate high uncertainties at most internal nodes. Correlation tests suggest that the evolution of dwarf males is significantly correlated with twelve of the morphological characters studied. In addition, the correlation tests indicate that the presence of dwarf males may promote morphological evolution. Continuing the theme of comparison between pleurocarps and angiosperms, in Chapter 19 Ray Tangney examines the distribution patterns of pleurocarpous mosses in the Australasian region. His analysis reveals patterns, also known for angiosperms, that form a network of general distribution tracks and highlight different areas within the region. The combination of this general pattern of distribution with vicariance, the spatial separation of closely related taxa, emphasizes a relationship between taxa and localities stronger than that expected if long-distance dispersal was a major determining factor in forming distributions. This suggests a major role for allopatric evolution, and a distinction is drawn between the timing of the origin of taxa and the time of the origin of the

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ancestral range. He concludes that differentiation of taxa may occur at different times within ancestral ranges and therefore that taxa of different ages and taxonomic levels may share the same present-day distribution through congruence of ancestral ranges and interaction with regional geological and ecological processes. Many important families of pleurocarpous mosses could not be included in this symposium, either because they have not been studied in sufficient depth, or through logistical constraints. The sheer size of the pleurocarpous moss clade, combined with the apparent rapid diversification of a large number of individual lineages, makes resolution of the relationships in this group a formidable task. The evidence presented here for the homoplastic nature of many of the morphological characters traditionally used to recognize and circumscribe many of the taxa, especially families, would seem to indicate that use of morphology as a source of systematic data is doomed. Yet at the same time it is evident that by careful examination and critical evaluation of characters, a great deal of useful information can be obtained, that is both interesting in its own right, and as a source of data for systematic and evolutionary studies. Further resolution of the relationships of the pleurocarpous mosses, although challenging, seems to be achievable. As in this symposium volume, building from both directions — dense sampling for genus and family level studies, combined with “backbone” analyses of broadly sampled regions of the topology — will allow us to resolve the relationships of the pleurocarpous mosses, and at the same time, explore some very interesting questions. The input of reviewers for the individual chapters is gratefully acknowledged. Amgueddfa Cymru — National Museum Wales provided facilities for the symposium, and the Natural History Museum contributed logistical support. Thanks also to the many others who supported and encouraged us in this project. Angela Newton Ray Tangney

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Editors Angela Newton is the Research Bryologist at the Natural History Museum, London, where her research focuses on the systematics of bryophytes, in particular the origins and relationships of lineages of pleurocarpous mosses, and the evolution of morphological features in mosses. Her current projects include research on dating the diversification of the pleurocarpous mosses using molecular sequence data, and relating these diversification events to the origins of angiosperm forests; studies of the role of dwarf males in promoting morphological and genetic diversity in mosses; floristic work in Central America and south-east Asia; and monographic studies of the pan-tropical Pterobryaceae. Dr. Newton received her M.Sc. in Plant Systematics at Reading University in 1983 and, after several years working as a curator in a local museum and in local and national biological records centres, moved to the United States, where she received her Ph.D. in Bryophyte Systematics from Duke University, North Carolina in 1993. She then worked as a post-doctoral researcher at the National Museum of Natural History in Washington, D.C. until 1997, then at the Instituto de Ecologia, in Xalapa, Mexico until 1998. She has carried out extensive field work in Central and South America, and in Australasia and is the author of over 30 research publications. She has served as a member of Council on the Systematics Association and the British Bryological Society, and is a member of the International Association of Bryologists, International Association of Plant Taxonomists, American Society of Plant Taxonomists, and the American Bryological and Lichenological Society. Ray Tangney is Head of Cryptogamic Botany and Curator of Bryophytes at Amgueddfa Cymru — National Museum Wales in Cardiff. His primary interests are the systematics, evolution and biogeography of the pleurocarpous mosses. His research is mainly specimen-based taxonomic study, augmented by DNA sequence data, addressing problems of classification and evolution. He also undertakes empirical and theoretical studies on the biogeography of mosses and has a strong interest in spatial patterns in the distributions of related taxa, and on branching in mosses, applying techniques of architectural analysis to problems of branching pattern. He has extensive field experience in New Zealand and its sub-antarctic regions, Australia and New Caledonia, and is the author of 20 research papers. He is undertaking continuing work on a monograph of the Lembophyllaceae and he is contributing treatments of the Polytrichaceae and Lembophyllaceae to the Moss Flora of New Zealand project. He is currently co-editing a book on biogeography in a changing world. Dr. Tangney received his Ph.D. at the University of Otago in 1994 and after teaching there for eight years moved to Wales in 2000. He has served on the Council of the Systematics Association and the British Bryological Society and he is a member of the International Association of Bryologists.

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Contributors Neil E. Bell Department of Botany Natural History Museum Helsinki, Finland

Sanna Huttunen Botanical Museum University of Helsinki Helsinki, Finland

Rolf Blöcher Nees-Institute for Biodiversity of Plants University of Bonn Bonn, Germany

Michael S. Ignatov Main Botanical Garden of Russian Academy of Science Moscow, Russia

Vera K. Bobrova Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia

Hans (J.D.) Kruijer Nationaal Herbarium Nederland Universiteit Leiden Branch Leiden, The Netherlands

William R. Buck Institute of Systematic Botany New York Botanical Garden Bronx, New York Laura Lowe Forrest Department of Plant Biology Southern Illinois University Carbondale, Illinois

E. M. Kungu Royal Botanic Garden Edinburgh, Scotland Royce Longton School of Biological Sciences, Plant Sciences Laboratories University of Reading Reading, UK

Anastasia A. Gardiner Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia

Irina A. Milyutina Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia

Lars Hedenäs Swedish Museum of Natural History Department of Cryptogamic Botany Stockholm, Sweden

Angela E. Newton Department of Botany Natural History Museum London, UK

Boon-Chuan Ho Nationaal Herbarium Nederland Universiteit Leiden Branch Leiden, The Netherlands

Terry J. O’Brien Department of Biological Sciences Rowan University Glassboro, New Jersey

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Gisela Oliván Biology Department Duke University Durham, North Carolina Niklas Pedersen Department of Botany Natural History Museum London, UK Dietmar Quandt Botanisches Institut Technische Universität Dresden Dresden, Germany Dmitry E. Shcherbakov Paleontological Institute Russian Academy of Sciences Moscow, Russia

Ray Tangney Department of Biodiversity and Systematic Biology Amgueddfa Cymru — National Museum Wales Cardiff, UK Alexey V. Troitsky Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia Alain Vanderpoorten Department of Life Sciences University of Liège Liège, Belgium Niklas Wikström Department of Systematic Botany, Evolutionary Biology Centre Uppsala University Norbyvägen, Sweden

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Contents Chapter 1

The History of Pleurocarp Classification: Two Steps Forward, One Step Back..............................................................................................................1

William R. Buck Chapter 2

The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences.............................................................................19

Terry J. O’Brien Chapter 3

Pleurocarpy in the Rhizogoniaceous Grade...............................................................41

Neil E. Bell and Angela E. Newton Chapter 4

Reevaluation of the Phylogeny of the Hypopterygiaceae (Bryophyta) Based on Morphological and Molecular Data ...........................................................65

Hans (J.D.) Kruijer and Rolf Blöcher Chapter 5

Growth Patterns in Calyptrochaeta Desv. (Daltoniaceae).......................................111

Boon-Chuan Ho and Hans (J.D.) Kruijer Chapter 6

Advances in Knowledge of the Brachytheciaceae (Bryophyta)..............................117

Sanna Huttunen, Anastasia A. Gardiner and Michael S. Ignatov Chapter 7

Phylogenetic Relationships within the Moss Family Meteoriaceae in the Light of Different Datasets, Alignment and Analysis Methods....................145

Sanna Huttunen and Dietmar Quandt Chapter 8

The Amblystegiaceae and Calliergonaceae..............................................................163

Lars Hedenäs and Alain Vanderpoorten Chapter 9

On the Relationships of Mosses of the Order Hypnales, with Special Reference to Taxa Traditionally Classified in the Leskeaceae...................177

Michael S. Ignatov, Anastasia A. Gardiner, Vera K. Bobrova, Irina A. Milyutina, Sanna Huttunen, and Alexey V. Troitsky Chapter 10 Phylogeny of Hygrohypnum Lindb. Based on Molecular Data...............................215 Gisela Oliván, Lars Hedenäs, and Angela E. Newton

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Chapter 11 Morphological Characters and Their Use in Pleurocarpous Moss Systematics .....................................................................................................227 Lars Hedenäs Chapter 12 Character Reduction and Peristome Morphology in Entodontaceae: Constraints on an Information Source .....................................................................247 E. M. Kungu, Royce Longton, and L. Bonner (deceased) Chapter 13 Homologies of Stem Structures in Pleurocarpous Mosses, Especially of Pseudoparaphyllia and Similar Structures................................................................269 Michael S. Ignatov and Lars Hedenäs Chapter 14 Branching Architecture in Pleurocarpous Mosses...................................................287 Angela E. Newton Chapter 15 Sympodial and Monopodial Growth in Mosses: Examples from the Lembophyllaceae (Bryopsida) ...........................................................................309 Ray Tangney Chapter 16 Did Pleurocarpous Mosses Originate before the Cretaceous?.................................321 Michael S. Ignatov and Dmitry E. Shcherbakov Chapter 17 Dating the Diversification of the Pleurocarpous Mosses ........................................337 Angela E. Newton, Niklas Wikström, Neil Bell, Laura Lowe Forrest, and Michael S. Ignatov Chapter 18 Phylogenetic and Morphological Studies within the Ptychomniales, with Emphasis on the Evolution of Dwarf Males ...................................................367 Niklas Pedersen and Angela E. Newton Chapter 19 Biogeography of Austral Pleurocarpous Mosses: Distribution Patterns in the Australasian Region .......................................................................................393 Ray Tangney Index ..............................................................................................................................................409

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History of Pleurocarp 1 The Classification: Two Steps Forward, One Step Back William R. Buck CONTENTS Abstract ..............................................................................................................................................1 1.1 Introduction...............................................................................................................................1 1.2 History of Morphology-Based Classifications.........................................................................2 1.3 Molecular-Based Classifications ............................................................................................13 1.4 Conclusions.............................................................................................................................14 References ........................................................................................................................................15

ABSTRACT The classification of pleurocarpous mosses has traditionally lagged behind that of acrocarps. Hedwig had only five genera of pleurocarps, which he based on sporophyte characters. The first modern attempt to understand relationships was by Schimper, who sorted pleurocarps into families. Schimper relied primarily on gametophytic characters to sort out the group. Subsequently, based on Philibert’s peristome studies (focusing primarily on acrocarps), Fleischer proposed a new system that was primarily sporophyte-based. This system was picked up by Brotherus for Die natürlichen Pflanzenfamilien. It wasn’t until about the 1990s that once again a gametophyte-based classification gained favour. The advent of the use of molecular data has allowed bryologists to present classifications free of morphology. Initial work using one-gene trees resulted in faulty classifications. Multiple-gene trees have refined the process. A combination of multiple genes with carefully observed morphology should provide us with a stable classification. To date, though, the largest group among the mosses lacking phylogenetic resolution is the Hypnales.

1.1 INTRODUCTION Since my earliest days as a bryology graduate student, my overriding interest has been in how different mosses, and especially pleurocarps, are related to one another. I initially took the approach that insights into moss phylogeny were best gained through the examination of as many specimens as possible. Through the input of a large amount of data, and thinking about it, I developed my own ideas about pleurocarp relationships. Certainly, as I learned more, and examined more specimens and saw more species in the field, my ideas changed. I have relied heavily on my intuition but will admit that such methodology is difficult to transmit to others. Nevertheless, I have repeatedly been amused when younger people who have used more modern methodologies have wondered, often in irritation, how I “guessed” the same answer that their computers told them. I am not

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psychic. The fact that my study of plants has led me to answers that have been corroborated by other methodologies should be inspirational to others because the answers are there, just waiting to be found. Like many traditional systematists, I was at first leery of results from molecular data because of the odd results that were initially forthcoming. However, my goal of understanding how different pleurocarps are related to one another was more important than the means of how that knowledge was obtained. In 1997, at the annual meeting of the American Bryological and Lichenological Society in Montreal, Canada, both Terry Hedderson and Jon Shaw asked me if I would be interested in going to their labs to do molecular work on pleurocarps. It had never even occurred to me that I might do such a thing. In the end, though, I was most interested in the data. Also, since most people who knew me would have said that I was the last person they would have suspected of doing molecular work, this was also a motivation to give it a try. In the end, I chose to work with Jon Shaw because he was in the United States and I knew him better. That way, if I failed it would be less embarrassing and easier to slink back home. So, although I will definitely be discussing the impact of molecular data on pleurocarp classification, remember that we have over 200 years of history dealing solely with morphology, and so that aspect will dominate my essay. For this purpose I will be updating my earlier paper (Buck, 1991) on the subject. Since the earliest days of moss classification, pleurocarps have been the ugly stepchild of the mosses and have garnered an inappropriately small amount of attention. Based on Crosby et al.’s (2000) Checklist of the Mosses, pleurocarps constitute about 42% of all moss species. Although Hedwig (1801), in Species Muscorum Frondosorum, recognized 30 genera of acrocarps, he recognized but five genera of pleurocarps: Pterigynandrum, Fontinalis, Neckera, Leskea and Hypnum. All known tropical pleurocarps were forced into what are now considered primarily temperate genera. The classification of pleurocarpous mosses has undergone tremendous alterations since the time of Hedwig and his contemporaries. Not only have the classifications themselves changed, but the underlying philosophies upon which they were based have changed. This is particularly interesting because there seems to have been a cyclical pattern in the philosophic basis for pleurocarpous classification. Initially I will highlight the historic philosophic oscillations and the ramifications they have had on classification schemes. As mentioned earlier, the treatments accorded acrocarps and pleurocarps have always been somewhat disparate. This is particularly marked in the early literature. Nevertheless, acrocarp classification has undergone the same kinds of fluctuations that I discuss here for the pleurocarps. Finally, I will discuss the influence of molecular data on pleurocarp classification. In some ways it has been extraordinarily enlightening, but has completely failed us in other areas, at least so far.

1.2 HISTORY OF MORPHOLOGY-BASED CLASSIFICATIONS The very earliest work on mosses was hampered by a lack of both adequate optical equipment and an understanding of the life cycle. Early researchers tried to equate morphological structures in mosses with those in flowering plants. In particular, the capsule, or parts of it, was considered homologous to parts of the flower. For example, both Dillenius (1741) and Linnaeus (1753) considered the moss capsule to be homologous to the flower’s anther. It was not until Hedwig (1782, 1783, 1787–1789) (Figure 1.1) that the sexuality of mosses was understood. Despite the clarity of Hedwig’s prose and illustrations, there was still doubt and dissension. For example, Palisot de Beauvois (in de Jussieu, 1789) proposed that the moss capsule was hermaphroditic, with the spores as male pollen and the columella as the female. He later expanded this view (Palisot de Beauvois, 1805). According to Margadant (1968), his misinterpretation was based on observations of Brownian movement of a crushed columella under the microscope. Although Hedwig’s morphological interpretations were generally accepted and well received, the taxonomic implications he based on them were less popular. For example, Menzies (1798, p.

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FIGURE 1.1 Johann Hedwig (1730–1799).

64) complained that “his genera are too artificial, and that their characters are taken from parts so minute and difficult to examine, that they rather tend to perplex and discourage a young beginner in his investigations, than aid his pursuits in acquiring a scientific knowledge of this intricate tribe.” (You can almost hear those same words today!) Menzies therefore rejected characters such as the number of peristome teeth. Most of Hedwig’s earlier works were concerned primarily with the morphology and physiology of mosses. It was his posthumous Species Muscorum Frondosorum (1801) that took his understanding of mosses and translated it into a classification scheme for the mosses he knew. His classification was generally based on capsule and peristome characters and the position of the male in relation to the female inflorescence, i.e., the sexuality. He courageously described new genera rather than relying solely on the handful of ones used at that time. It is this latter point, the proliferation of genera, that drew the most criticism from cryptogamists of the day (e.g., Smith, 1804). However, he also had his defenders (e.g., Schwägrichen, 1810) who continued his precedence. Florschütz (1960) summarized Hedwig’s impact on bryology of the early nineteenth century. As mentioned earlier, Hedwig (1801) recognized only five pleurocarpous genera, but he made no attempt to speculate upon the relationships between them. The important point here, though, is that the genera were primarily differentiated on characters of the sporophyte. Also, Hedwig, following tradition, referred to perichaetia and perigonia as female and male flowers. This tradition has continued to the present in the use of the term inflorescence for the same structures. This association between capsule and flower is critical not only in understanding classifications of the late eighteenth and early nineteenth centuries, but in understanding assumptions that have persisted to the present. Despite criticism by some, the majority, if not all, of the major bryological workers of the first half of the nineteenth century followed the principles established by Hedwig. In other words, gametophytic characters were superseded in importance by sporophytic ones. For example, Hooker and Taylor (1827), disregarding Hedwig’s (1801) segregation, combined Dicranum and

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FIGURE 1.2 Wilhelm Philipp Schimper (1808–1880).

Fissidens into a single genus because of peristomial similarities. The obvious gametophytic divergences were accorded no taxonomic status. This practice flourished, although to a less extreme extent, until the mid-nineteenth century. The publication of the Bryologia Europaea (Bruch et al., 1836–1855) marked a turning point in the classification of pleurocarpous mosses. Prior to that time all moss families had been, at best, vague concepts and, except for morphologically odd groups (e.g., the Polytrichaceae), most mosses were in a single family. There can be little doubt that Schimper (Figure 1.2) was the driving force behind this advancement. The Bryologia Europaea itself did not provide familial descriptions, but rather, by way of a “Conspectus” at the front of each volume, generic inclusions were indicated for each family. Schimper’s Corollarium (1855), though, corrected that deficiency by offering descriptions of each family as well as revising familial concepts. Schimper’s contributions are particularly impressive in light of the fact that he was not just modifying a previous classification system as later workers were able to do. Rather, he took an unclassified agglomeration of genera and provided, for the first time, a unified classification. Vitt (1984) argued that Schimper primarily refined Bridel-Brideri’s classification (1826–1827), but I disagree, at least for the pleurocarps. Bridel-Brideri merely sorted the pleurocarps into groups based on presence or absence of peristome and whether the peristome was single or double. Schimper’s knowledge allowed him to reject boldly the notion of the overriding importance of the sporophyte in the pleurocarps and to construct a classificatory scheme based primarily on gametophytic characters. He realized that a system of classification based solely on the sporophyte led to the grouping together of many disparate elements. Most telling is his discussion under the description of the Hypno-Leskeaceae (Schimper, 1855, p. 111) (and I liberally translate his difficult Latin): Bryologists who place the priority of a system on the peristome alone, thereby separating closely related taxa, bring together almost the whole cohort of pleurocarpous mosses into one family, and whatever the external appearance may be, which is the only feature available to the inexpert beginner, they refer

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FIGURE 1.3 William Mitten (1819–1906). Hypna to the Leskeaceae and Orthothecia and Leskeae to the Hypnaceae, thereby creating an inextricable chaos in the so-called methodical disposition of mosses which obscures the approach to bryology.

Schimper, therefore, not only created the first modern familial classification of pleurocarpous mosses, but reversed the philosophy upon which the classification was based. His pioneering efforts laid the groundwork from which all subsequent classification attempts diverged. Following closely in the wake of Schimper, Mitten (1859) criticized many of his predecessors, especially Carl Müller and his Synopsis (1848–1851), for relying on sporophytic features. Mitten (Figure 1.3) perceived classifications based on capsular characters as artificial. Unlike Schimper, though, Mitten supplied arguments against sporophytic reliance. He documented the reduction processes of peristomes and was the first to relate them to capsular orientation: “it appears to be a general law, that the more the theca is inclined or pendulous, the greater is the development of the peristome” (Mitten, 1859, p. 3). Mitten placed primary emphasis on the mode of growth and especially on the morphology of the leaves. Although Mitten indeed did rely on some basic peristomial characters in his classification, for the pleurocarps they were used above the familial level. Since Mitten was the premier bryologist of the last half of the nineteenth century, his doctrine prevailed. The one real weakness with both Schimper’s and Mitten’s classifications is that they considered only regional floras. Since most pleurocarpous moss families occur over multi-continental ranges, it is often difficult for a parochial work to account for the total range of morphological variation in a family. Most regional floristicians are not familiar with the total possibilities of generic inclusions. This is particularly relevant for pleurocarps in which most of the families have a tropical center of diversity. However, Brotherus (Figure 1.4) remedied this particular criticism in his treatment (Brotherus, 1901–1909) of the mosses in the first edition of Die natürlichen Pflanzenfamilien. Although flawed by the complexities of such a large undertaking, Brotherus’ opus was the first to encompass all the mosses within a modern scheme based upon a well-considered philosophy. Although some earlier works attempted such a plan, e.g., Bridel-Brideri (1826–1827) and Müller (1848–1851),

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FIGURE 1.4 Viktor Ferdinand Brotherus (1849–1929).

many fewer taxa of pleurocarps were known, pleurocarpic generic concepts were broad and strongly heterogeneous, and relationships were ill conceived. Probably influenced by Schimper in particular, Brotherus’ classification of pleurocarpous mosses (1901–1909) is primarily weighted toward gametophytic characters. In other words, Brotherus took Schimper’s viewpoint and applied it globally to the pleurocarps. It is not unexpected that familial concepts in the pleurocarps would be artificial, since this was truly a first sorting. Many characters were misunderstood, and thus convergences (of both the gametophytic and sporophytic generations) were mistakenly aligned. Brotherus’ work, though, is best seen as the most magnificent expression of a philosophy about to be superseded. In 1884 Philibert (Figure 1.5) began a long series of articles, running until 1902, that changed the outlook of bryophyte classification. In this series, “Études sur le péristome,” Philibert, through the intricate study of peristome morphology with the compound microscope, proposed that classification of mosses be based primarily on peristomial similarities. The corollary was that gametophytic similarities without sporophytic congruencies were merely coincidences of nature not to be taken into account when speculating on relationships. Philibert considered peristomial characters to be evolutionarily conservative and thus the appropriate ones upon which to base a classification. His observations and the conclusions he drew from them marked the end of a gametophytedominated era of classification. Although Philibert’s observations were more detailed than those of Hedwig (indeed, the technological level of Hedwig’s microscopy did not allow such study), they nevertheless had the same general impact. That is, Philibert’s observations led toward a sporophytedominated classification. Philibert never proposed any sort of general classification. It should be noted, though, that Philibert primarily based his conclusions on the observations of acrocarpous mosses. He did discuss pleurocarps in the more general articles (especially those on the endostome), but his primary data were from acrocarps. However, he presented principles upon which a classification could be constructed. It was Max Fleischer (Figure 1.6) who took Philibert’s principles and applied them. Nominally treating a moss flora of Java, Fleischer’s “Die Musci der Flora von Buitenzorg” (1904–1923) greatly exceeded its bounds, and while it dealt with only regional species, it nevertheless discussed all

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FIGURE 1.5 Henri Philibert (1822–1901).

FIGURE 1.6 Max Fleischer (1861–1930).

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STAMMESGESCHICHTLICHE UEBERSICHT DER GATTUNGEN DER SEMATOPHYLLACEAE.

Clastobryopsis

Pterobryaceae

Struckia Clastobryella

Hageniella

Clastobryum Clastobyrophilum Aptychopsis Mastopoma Gammiella Heterophyllium

Acanthocladium Brotherella

Trismegistia Rhaphidorrhynchium

Pylaisiadelpha Schraderella

Schröterella

Sematophyllum

Schraderobryum

Warburgiella

Macrohymenium Rhaphidostichum Acroporium Trichosteleum Acanthorrhynchium

Pterogoniopsis Pterogonidium

Meiothecium

Meiotheciopsis

Potamium Chionostomum

Taxithelium Glossadelphus

Syringothecium

FIGURE 1.7 Diagram of evolutionary speculations in the Sematophyllaceae from Fleischer’s “Die Musci der Flora von Buitenzorg” (1904–1923).

moss genera known at that time. The pleurocarps in particular, perhaps because they came toward the end of the volumes when Fleischer had had more time for reflection, were treated in more detail, and it is the pleurocarps in which he suggested the most changes in classification. What made Fleischer’s monumental work so significant, though, was not just that it pursued Philibert’s principles, but that it was the first attempt to understand the evolutionary relationships among the pleurocarps. This is amply demonstrated by Fleischer’s use of diagrams showing postulated directions of evolution (Figure 1.7). Darwin’s (1859) Origin of Species had been published almost a half century earlier, but bryology has never been in the vanguard of plant sciences in adopting new ideas. The paucity of workers alone has primarily made it a field in which, even into the twentyfirst century, we are still scrambling to catalogue the world’s bryoflora. Therefore, it is significant that Fleischer tried to present a classification for the pleurocarpous mosses that reflected phylogeny. The fact that his understanding of evolution was seriously flawed is easily pardoned by the era in which he lived. Although the alternation of generations was well established by Fleischer’s time (Hofmeister, 1851; Strasburger, 1894) and the strict homology of capsules and flowers had long been abandoned, the consequent assumption of the conservative nature of the capsule remained. Fleischer (see vol. 1, pp. XIII–XVII) still referred to capsules as reproductive organs. Nevertheless, he was the first bryologist to recognize apparently natural relationships between genera and families of pleurocarps that are now taken for granted. His insights were surely gained in part by his intimate familiarity with both his native temperate zone flora, as well as his adopted tropical one in which pleurocarpous mosses are so diverse and abundant. Previous workers, from Hedwig and BridelBrideri to Schimper and Mitten, were familiar only with tropical taxa from dried herbarium specimens sent to them by collectors, who themselves, for the most part, were unfamiliar with the mosses. Fleischer, therefore, in a pioneering effort, was able to make truly significant strides in the

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FIGURE 1.8 Marshall Robert Crosby (1943– ).

classification of pleurocarps by an intimate field knowledge of a broad flora and the application of both Darwinian evolutionary and Philibertian peristomial hypotheses. In the same way that Brotherus (1901–1909) culminated the era in which classification of pleurocarpous mosses was dominated by the gametophyte, later on Brotherus (1924, 1925) took Fleischer’s lead in sporophytic emphasis and applied it across the board to the pleurocarps in the second edition of Die natürlichen Pflanzenfamilien. Dixon (1932) summarized this philosophy in Verdoorn’s Manual of Bryology. The Fleischer–Brotherus system dominated moss systematics to the end of the twentieth century. That is not to say that there have not been attempts to refine the classification, but they have been just that, modifications. For example, Crosby (Figure 1.8), probably the most modern ardent follower of Philibert’s principles, reexamined the Hookeriales and divided them into families along strictly peristomial lines (Crosby, 1974). I used primarily peristomial features in my refinement of the familial concept of the Entodontaceae (Buck, 1980). With a broader perspective, Vitt (1984) presented a family classification of all mosses. Each of these examples, and more could be cited, relied on the assumption, sometimes unstated, that characters of peristomial morphology are conservative and therefore are the best indicators of phylogenetic relationships among the pleurocarps. However, dissension was afoot. In the last two decades of the 1900s there was an ever increasing trend to study new morphological characters, especially gametophytic ones, for use in classification. Initially these studies focused just on the range of variation in characters and their potential for use. For example, Ireland (1971) studied the morphology and distribution of pseudoparaphyllia in North American mosses; Saito (1975) and Norris (1978) initiated the study of axillary hairs; and Crundwell (1979), Koponen (1982), and Hedenäs (1987a) supported the use of rhizoidal morphology and placement in taxonomy. Later workers then applied many of these gametophytic characters to suggest changes in the position of taxa (e.g., Hedenäs, 1987b, 1989). In spite of the fact that the generation emphasized in moss classification had oscillated repeatedly from one to the other, in the modern era there initially seems to have been a reluctance to suggest that the characters revealed by these gametophytic structures might be more useful or significant than those from sporophytic features in understanding familial relationships among the pleurocarps. However, it was these exploratory studies of new characters that were probably most influential in transferring reliance back to the gametophytic generation. The increase of additional

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FIGURE 1.9 Dale Hadley Vitt (1944– ).

characters, in most part unlinked with more traditional ones but that nevertheless correlate with them, has lent greater strength to the argument of gametophyte-based classifications. In 1986, along with Dale Vitt (Figure 1.9), I suggested changes in the classification of pleurocarpous mosses (Buck and Vitt, 1986). Although we explained that our methodology was cladistically influenced, we did not discuss the underlying philosophy upon which the scheme was based. However, many of the changes proposed were based not on peristomial congruencies but gametophytic similarities. Although not thought through at the time, there was obviously a reluctance on our part to go against the established ideas of Fleischer regarding the value of sporophytic versus gametophytic characters in the pleurocarps. However, through the study of additional plant material, it became more and more clear to me, as well as other researchers, that in some cases the reliance on sporophytic characters to build phylogenetic alliances among the pleurocarps not only is suspect but actually can lead to erroneous conclusions. Certainly some peristomial characters are valuable in phylogenetic speculation. Indeed, as pointed out initially by Edwards (1979, 1984) and subsequently by Shaw et al. (1987, 1989) and Shaw and Anderson (1988), basic developmental patterns in moss peristomes are reliable indicators of higher systematic relationships (but probably above the rank of family). Although virtually all the developmental data from these workers were derived from acrocarpous mosses, I have assumed that they are equally applicable to pleurocarps. However, these developmental processes do not necessarily manifest themselves through superficial peristomial structure. For example, a moss may be eperistomate but still have the same developmental pattern as a doubly peristomate one, as in the case of Nematocladia and Helicodontium, both in the Myriniaceae (see Buck, 1982). Reductionary depositional sequences of those cell walls destined to become peristome teeth are independent of basic developmental patterns in the moss capsule. Frequently, similar environmental pressures acting through reductionary sequences on different developmental patterns may result in identical morphological structures, i.e., convergent structures. For example, epiphytic members of both the Leskeaceae and Sematophyllaceae may have exostome teeth with papillose ornamentation. Therefore, peristomial structure and ornamentation may not necessarily be reflective of phylogenetic closeness.

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FIGURE 1.10 Howard Alvin Crum (1922–2002).

It was during my earlier work on the Hookeriales (Buck, 1987, 1988) that the potential deceptiveness of peristomial similarities became clear to me. The Hookeriales are a particularly instructive order from which such observations can be drawn because there are several generic pairs that are virtually inseparable on gametophytic criteria but whose peristomes are very different. Crosby’s (1974) earlier treatment had separated the members of such gametophytically defined pairs into different families. Such a scheme seemed counterintuitive because it required the convergent evolution of whole suites of seemingly unlinked gametophytic character states, not once but several times. Thus, I reversed the life cycle generation traditionally used as the basis for establishing familial classification in the Hookeriales. Not surprisingly, with the addition of molecular data, the classification has changed again (Buck et al., 2004). Howard Crum (Figure 1.10) and I (Buck and Crum, 1990) relied totally on gametophytic characters in defining familial boundaries of the Leskeaceae/Thuidiaceae complex even though traditionally the families were separated on sporophytic differences (sometimes even into different orders). We allowed, within a single family, sporophytic evolution in which fully developed hypnoid peristomes can become greatly reduced. We correlated these reduction sequences with differences in habitat. Although Mitten (1859) first pointed out how peristome complexity is often coupled with capsule orientation (i.e., the more curved the capsule the more perfect the peristome), and such observations have been independently confirmed (e.g., Buck, 1980, p. 77), the implications of this fact on the classification of pleurocarpous mosses have been neglected. In other words, although the basis for the assumption that peristome morphology and ornamentation are conservative has been shown to be faulty, the assumption itself has persisted. Some authors (e.g., Allen et al., 1985, p. 150) have argued that because the peristome develops inside of the protective operculum, its morphology is immune from the environment and thus is conservative. However, the time during which the peristome is functional is at spore dispersal, and it is therefore at that time when natural selection acts upon it, not prior to it. The strength behind the argument that sporophytic characters are modified by environmental parameters is the fact that the same modifications have occurred repeatedly in distantly related groups. For example, reduction series can be seen in genera such as Pylaisia and Platygyrium in the Hypnaceae and Brachymenium and Actinodontium in the Bryaceae. Many epiphytic genera, such as Cryphaea and Pterobryon, also exhibit a suite of modifications, but their terrestrial ancestors are not readily evident.

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FIGURE 1.11 William Russel Buck (1950– ).

Because of the persuasiveness of such arguments, I (Figure 1.11) proposed (Buck, 1991) that a strong reliance on peristomial ornamentation and superficial morphology in the construction of a family classification of pleurocarpous mosses is inappropriate. It has been amply demonstrated, for over 100 years, that sporophyte structure is correlated with habitat. Therefore peristomial characters may not necessarily be conservative. This is not to say that there is no use for the peristome in classification. Rather, its structure often proves to be of most use in separating genera within a family rather than families within an order. I have predicted (Buck, 1991) that all the primitive genera in an order that occur in broadly similar habitats, no matter what family they may be in, would have a similar peristomial structure. Certainly this is the case in the Hypnales where there is little differentiation between the peristomes of Hypnum (Hypnaceae), Brachythecium (Brachytheciaceae), and Thuidium (Thuidiaceae), although these genera have large gametophytic divergences. Although the argument is hundreds of years old, once again we are forced to decide if gametophytic characters are more immune from natural selection than sporophytic ones, and thus more conservative. Like all organisms, mosses, with their dominant gametophyte, certainly are responsive to natural selection; otherwise there would be no way to account for current levels of speciation. However, some characters, through observation, seem to be reliable when speculating on relationships at the family level. Although I (Buck, 1991) argued that costa structure is relatively stable and thus useful in phylogenetic speculation, recent molecular data (Buck et al., 2004) has shown that such is not the case, at least in the Hookeriales. One can only assume that once a robust phylogeny is available for the Hypnales, a similar situation will be found. Other kinds of characters in which the character states have presumed to be stable within pleurocarpous familial limits include cell shape, stem anatomy, axillary hair morphology, and calyptra structure. Future phylogenetic research will probably find these as faulty as assumptions about costal morphology. Nevertheless, the advantage of the gametophyte in postulating relationships is that it has so many more independent characters than does the peristome. Therefore, it can be more obvious when whole groups of characters are correlated. Certainly there can be and are gametophytic convergences, but because of the diverse assemblage of characters available, it is improbable that great numbers of different character states would converge together during evolution.

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It should be emphasized that throughout this essay I have been discussing evolutionary trends, not dogmatic principles with unwavering applicability. Because of the great diversity found within mosses, or even within pleurocarpous taxa, exceptions can be found to every generalization. Nevertheless, because the same general structural modifications have occurred over a broad taxonomic spectrum, I think ecumenical postulation is justified. In concluding this part of the chapter, we have now swung back to the position of Schimper and Mitten, in which gametophytic characters are given more weight in developing phylogenies than are sporophytic characters. Correlations of a diverse group of gametophytic characters currently appear more reliable and provide a more stable basis for familial classification. However, as pointed out by the research of Hedenäs (e.g., 2002) and others, sporophytic characters, when examined critically, can also be useful when they correlate with gametophytic features. Certainly peristome structure should not be ignored, and in some cases it can be extremely revealing. Unfortunately, we have been saddled (e.g., Brotherus, 1924, 1925) with the relatively crude use of sporophytic features (e.g., exostome teeth papillose versus striolate) that has led to misunderstandings of relationships. The use of all characters, without a priori weighting, leads to a more balanced approach to phylogenetic speculation and family classificatory construction.

1.3 MOLECULAR-BASED CLASSIFICATIONS In the last decade, the use of molecular data for understanding phylogeny, and thus forming the bases for classification, has gone from peripheral to primary. However, it has not always been a smooth road, and certainly there have been problems. In the early days of the use of DNA sequencing, the methodology was so time consuming that it limited its usefulness. Few taxa were sampled, and even fewer loci were sequenced. As a result, early application of genomic data to phylogeny resulted in obviously flawed trees because of the use of a single, and often inappropriate, locus. The quality of molecular research has greatly improved, but we can all remember published phylogenies based on a single gene. Almost any two genetic loci will result in different trees, and obviously both cannot accurately reflect the phylogeny of the whole organism. Of course, these different trees are different because they are not the phylogeny of the whole organism, but just that of the gene that was sequenced. Such gene phylogenies may or may not mirror the evolution of the whole organism. This is particularly problematic when sequenced loci are spacers or other genetic areas that do not directly impact the ability of the moss to survive. Such single-gene trees resulted in counterintuitive phylogenies and as a consequence turned some traditional systematists against the whole methodology. Probably no single locus can provide an accurate reflection of phylogeny across all the pleurocarps, let alone all mosses, even if reasonable resolution of all nodes was possible. Despite the flaws inherent in single-gene phylogenetic trees, they nevertheless were an important step in the use and understanding of sequence data (e.g., Goffinet and Vitt, 1998). Certainly they provided some insights into evolutionary relationships that previously had not been discerned on the basis of morphological evidence and study. Such examples are the seemingly close relationships between, for example, Leptobryum and the Meesiaceae (Goffinet et al., 2001) and Anacamptodon and the Amblystegiaceae (Buck et al., 2000). Initial knee-jerk reactions against such seemingly bizarre relationships were replaced by a closer look at the morphologies involved and, indeed, structural similarities could be found. This is similar to early work on the monocots where relationships suggested by molecular data were later verified by tedious but significant structural similarities, such as embryology. Because such relationships that initially seemed improbable have subsequently been verified (or perhaps corroborated is more accurate), the potential use of molecular sequence data has been validated. The fact that single-gene trees are inherently flawed has led to the use of multiple genes to reconstruct phylogenies. When one gene suggests a particular phylogeny, it may give us something to think about, but it would be foolish to follow it slavishly. However, when a whole suite of genes

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indicates the same evolutionary scenario, then it is time to look very closely at the suggested phylogeny. It is hard to imagine that non-linked loci, especially from different compartments that all provide the same story, could possibly be deceptive. This is particularly true when three, and preferably more, loci are sequenced. To my eye, some of the most impressive phylogenetic research on mosses being done today looks at as many genes as possible. The research of Shaw (e.g., Shaw et al., 2004) comes immediately to mind, where he has looked at numerous loci in his Sphagnum research. For the immediately foreseeable future, this seems to be a model to strive for. It is difficult to imagine that the sequencing of the entire genome of more than a handful of bryophytes will be possible anytime soon. It certainly will not be practical for understanding the vast majority of phylogenetic questions in pleurocarps. Some will ask why we should bother to look at a dozen genes when a very similar story can be garnered from just a handful. For those of us involved in pleurocarp research, this should be particularly obvious. By far the largest group of pleurocarpous mosses are the Hypnales, encompassing both the traditional Hypnobryales and the Isobryales (or Leucodontales). Indeed, it was genomic evidence from only a few loci that led us to merge the two traditional groups, and accept the fact that the largely epiphytic and tropical Isobryalean mosses must have evolved repeatedly from terrestrial Hypnobryalean mosses (De Luna et al., 2000; Buck et al., 2000). Through recent research on pleurocarps, phylogenetic systematists have been able to resolve the circumscription of some families, but there is still virtually no resolution to the relationships among the families of the Hypnales. As different as some families may appear to the traditional systematist, molecular data have still been unable to resolve even the most basic backbone. Sure, we can glance at the plants and immediately recognize, for example, the Thuidiaceae from the Brachytheciaceae. However, all evidence we have strongly suggests that the Hypnales have rapidly diversified in relatively recent geological times (cf. Kürschner and Parolly, 1999). Studies such as that by Shaw et al. (2003) have shown that despite the taxonomic diversity of the Hypnales, there is relatively little genetic diversity when compared to the much smaller Hookeriales and Ptychomniales. Understanding the backbone phylogeny of the Hypnales remains the frontier in pleurocarp phylogenetic research. The challenge will be to find appropriate loci to sequence that actually reflect the phylogeny of the order. However, not until such research is completed do we have any real hope for a stable classification for the pleurocarps. One advantage, and simultaneously a disadvantage, of molecular phylogenies is that because it is now so easy to sequence DNA, classifications are rapidly changing. For example, Buck and Goffinet (2000) published a classification for the mosses based primarily on molecular data, but supplemented by morphological data, especially when molecular data were unavailable or ambiguous. This classification was adopted by GenBank. However, in just four years, we (Goffinet and Buck, 2004) have published yet another classification, parts of which are significantly different from our previous classification. At least for the immediate future, such instability will remain a fact of life as we gain greater understanding of the relationships among mosses, and pleurocarps in particular. Fortunately, the nomenclatural novelties remain primarily at higher taxonomic levels and have little effect on species names. Even at the generic and species levels, though, we must expect some alterations as a greater percentage of mosses are sequenced and our understanding of relationships is refined (e.g., Ignatov and Huttunen, 2002). To date, almost all phylogenetic implications derived from molecular data have been reinforced by morphological data. A major exception, though, is in the Amblystegiaceae (Vanderpoorten et al., 2002). It is difficult to know if such incongruities between molecular and morphological data are based on inadequate sampling or reality.

1.4 CONCLUSIONS We now take for granted that our classification should reflect the phylogeny of the plants, and that in and of itself has been a significant step, albeit one that was quietly taken. Nevertheless, it is important that nomenclaturally recognized nodes on trees still be identified by morphological as well

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as molecular characters. If evolutionary distance exists between two groups of mosses, then there should be some visible sign of this divergence and careful observation will reveal it. Therefore, it is probably as important as ever that systematists not abandon studying the actual plants themselves. Any taxonomic category, whether it be from a lowly variety to a mighty order, will not gain favour in the systematic community if it cannot be identified morphologically. When DNA sequencing now takes so little time, that cannot be used as an excuse for not studying the plants themselves. I personally went into systematics because it was the plants themselves that attracted me and by studying them I have come to feel how they are related to one another. Trying to unravel that evolutionary puzzle is what has motivated me. Now, I find myself unsympathetic to the excuse I have heard from all too many students, that “morphology is too hard.” The future of pleurocarp phylogeny and classification is not one of the past based solely on morphology, or one of the present based on seemingly isolated molecular data, but a combination of both molecular and morphological data.

REFERENCES Allen, B. H., Crosby, M. R. and Magill, R. E. (1985 [1986]) A review of the genus Stenodictyon (Musci). Lindbergia, 11: 149–156. Bridel-Brideri, S. E. (1826–1827) Bryologia Universa seu Systematica ad Novam Methodum Dispositio, Historia et Descriptio Omnium Muscorum Frondosorum hucusque Cognitorum cum Synonymia ex Auctoribus Probatissimis. 2 volumes. Barth, Lipsiae. Brotherus, V. F. (1901–1909) Musci. In Die natürlichen Pflanzenfamilien, Vol. 1(3) (ed. A. Engler and K. Prantl). Verlag von W. Engelmann, Leipzig, pp. 277–1246. Brotherus, V. F. (1924) Musci. In Die natürlichen Pflanzenfamilien, Vol. 10, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 143–478. Brotherus, V. F. (1925) Musci. In Die natürlichen Pflanzenfamilien, Vol. 11, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–542. Bruch, P., Schimper, W. P. and Gümbel, W. (1936–1855) Bryologia Europaea seu Generum Muscorum Europaeorum Monographice Illustrata. 6 volumes. Schweizerbart, Stuttgartiae. Buck, W. R. (1980) A generic revision of the Entodontaceae. Journal of the Hattori Botanical Laboratory, 48: 71–159. Buck, W. R. (1982) Nematocladia tesserata genus et species novae (Myriniaceae). Brittonia, 34: 414–416. Buck, W. R. (1987) Taxonomic and nomenclatural rearrangement in the Hookeriales with notes on West Indian taxa. Brittonia, 39: 210–224. Buck, W. R. (1988) Another view of familial delimitation in the Hookeriales. Journal of the Hattori Botanical Laboratory, 64: 29–36. Buck, W. R. (1991) The basis for familial classification of pleurocarpous mosses. Advances in Bryology, 4: 169–185. Buck, W. R. and Crum, H. (1990) An evaluation of familial limits among the genera traditionally aligned with the Thuidiaceae and Leskeaceae. Contributions from the University of Michigan Herbarium, 17: 55–69. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL–trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Buck, W. R., Cox, C. J., Shaw, A. J. and Goffinet, B. (2004 [2005]) Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematics and Biodiversity, 2: 121–145. Crosby, M. R. (1974) Toward a revised classification of the Hookeriaceae (Musci). Journal of the Hattori Botanical Laboratory, 38: 129–141. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (2000) A Checklist of the Mosses. Missouri Botanical Garden, St. Louis.

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Crundwell, A. C. (1979) Rhizoids and moss taxonomy. In Bryophyte Systematics Systematics Association Special Volume 14 (ed. G. C. S. Clarke and J. G. Duckett). pp. 347–363, Academic Press, London. Darwin, C. R. (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, Murray, London. de Jussieu, A. L. (1789) Genera Plantarum Secundum Ordines Naturales Disposita, Juxta Methodum in Horto Regio Parisiensi Exaratum. Herissant and Barrois, Parisii. (See especially pp. 12–14 for A. M. F. J. Palisot de Beauvois’ explanation of moss sexuality.) De Luna, E., Buck, W. R., Akiyama, H., Arikawa, T., Tsubota, H., González, D., Newton, A. E. and Shaw, A. J. (2000) Ordinal phylogeny within the hypnobryalean pleurocarpous mosses inferred from cladistic analysis of three chloroplast DNA sequence data sets: trnL-F, rps4, and rbcL. Bryologist, 103: 242–256. Dillenius, J. J. (1741) Historia Muscorum in Qua Circiter Sexcentae Species Veteres et Novae ad Sua Genera Relatae Describuntur et Iconibus Genuinis Illustrantur cum Appendice et Indice Synonymorum. Sheldoniano, Oxford. Dixon, H. N. (1932) Classification of mosses. In Manual of Bryology (ed. F. Verdoorn). Martinus Nijhoff, The Hague, pp. 397–412. Edwards, S. R. (1979) Taxonomic implications of cell patterns in haplolepidous moss peristomes. In Bryophyte Systematics Systematics Association Special Volume 14 (ed. G. C. S. Clarke and J. G. Duckett). pp. 317–346, Academic Press, London. Edwards, S. R. (1984) Homologies and inter-relationships of moss peristomes. In New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 658–695. Fleischer, M. (1904–1923) Die Musci der Flora von Buitenzorg (zugleich Laubmoosflora von Java), 4 volumes. In Flore de Buitenzorg, Vème Partie. Brill, Leiden. Florschütz, P. A. (1960) Introduction to Hedwig’s “Species Muscorum”. In J. Hedwig, Species Muscorum Frondosorum, Reprint edition, Historiae Naturalis Classica 16: v–xxii. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Goffinet, B. and Vitt, D. H. (1998) Revised generic classification of the Orthotrichaceae based on a molecular phylogeny and comparative morphology. In Bryology for the Twenty-First Century (ed. J. W. Bates, N. W. Ashton and J. G. Duckett). Maney Publishing and the British Bryological Society, Leeds, pp. 143–159. Goffinet, B., Cox, C. J., Shaw, A. J. and Hedderson, T. A. J. (2001) The Bryophyta (mosses): Systematic and evolutionary inferences from a rps4 gene (cpDNA) phylogeny. Annals of Botany, 87: 191–208. Hedenäs, L. (1987a) North European mosses with axillary rhizoids, a taxonomic study. Journal of Bryology, 14: 429–439. Hedenäs, L. (1987b) On the taxonomic position of Tomentypnum Loeske. Journal of Bryology, 14: 729–736. Hedenäs, L. (1989) Some neglected character distribution patterns among the pleurocarpous mosses. Bryologist, 92: 157–163. Hedenäs, L. (2002) Important complexes of intercorrelated character states in pleurocarpous mosses. Lindbergia, 27: 104–121. Hedwig, J. (1782) Fundamentum Historiae Naturalis Muscorum Frondosorum Concernens Eorum Flores, Fructus, Seminalem Propagatonem Adjecta Generum Dispositione Methodica, Iconibus, Illustratis. 2 volumes. S. L. Crusium, Lipsiae. Hedwig, J. (1783) Theoria Generationis et Fructificationis Plantarum Cryptogamicarum Linnaei, mere Propriis Observationibus et Experimentis Superstructa. Academiae Impr. Scientiarum, Petropoli. Hedwig, J. (1787–1789) Descriptio et Adumbratio Microscopico-Analytica Muscorum Frondosorum nec non Aliorum Vegetantium e Classe Cryptogamica Linnaei Novorum Dubiisque Vexatorum. 4 volumes. I. G. Mülleriano, Lipsiae. Hedwig, J. (1801) Species Muscorum Frondosorum Descriptae et Tabulis Aeneis lxxvii Coloratis Illustratae. Joannis Ambrosii Barthii, Lipsiae. Hofmeister, W. (1851) Vergleichende Untersuchungen der Keimung, Entfaltung und Fruchtbildung höherer Kryptogamen (Moose, Farn, Equisetaceen, Rhizocarpeen und Lycopodiaceen) und der Samenbildung der Coniferen. F. Hofmeister, Leipzig.

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Hooker, W. J. and Taylor, T. (1827) Muscologia Britannica; Containing the Mosses of Great Britain and Ireland, Systematically Arranged and Described; with Plates Illustrative of the Characters of the Genera and Species. Second edition, corrected and enlarged. Longman et al., London. Ignatov, M. S. and Huttunen, S. (2002) Brachytheciaceae (Bryophyta) — A family of sibling genera. Arctoa, 11: 245–296. Ireland, R. R. (1971) Moss pseudoparaphyllia. Bryologist, 74: 312–330. Koponen, T. (1982) Rhizoid topography and branching patterns in moss taxonomy. In Bryophyte Taxonomy (ed. P. Geissler and S. W. Greene). Beihefte zur Nova Hedwigia, 71: 95–99. Kürschner, H. and Parolly, G. (1999) Pantropical epiphytic rain forest bryophyte communities — coenosyntaxonomy and floristic-historical implications. Phytocoenologia, 29: 1–52. Linnaeus, C. (1753) Species Plantarum, Exhibentes Plantas Rite Cognitas, ad Genera Relatas, cum Differentiis Specificis, Nominibus Trivialibus, Synonymis Selectis, Locis Natalibus, Secundum Systema Sexuale Digestas. Salvii, Holmiae. Margadant, W. D. (1968) Early Bryological Literature. A Descriptive Bibliography of Selected Publications Treating Musci during the First Decades of the Nineteenth Century and Especially of the Years 1825, 1826 and 1827. Hunt Botanical Library, Pittsburgh. Menzies, A. (1798) A new arrangement of the genus Polytrichum, with some emendations. Transactions of the Linnean Society of London, 4: 63–84, pls. 6, 7. Mitten, W. (1859) Musci Indiae Orientalis; an enumeration of the mosses of the East Indies. Journal of the Proceedings of the Linnean Society, Supplement to Botany, 1: 1–171. Müller, C. (1848–1851) Synopsis Muscorum Frondosorum Omnium Hucusque Cognitorum. 2 volumes. Foerstner, Berolini. Norris, D. H. (1978) New characters in moss taxonomy. American Bryological and Lichenological Society, abstracts of contributed papers presented at the annual meeting. Virginia Polytechnic Institute and State University, Blacksburg. Palisot de Beauvois, A. M. F. J. (1805) Prodrome des Cinquième et Sixième Familles de l’Aethéogamie. Les Mousses. Les Lycopodes. Fournier fils, Paris. Philibert, H. (1884–1902) De l’importance du péristome pour les affinities naturelles des mousses. Revue Bryologique 11: 49–52, 65–72 (1884); Études sur le péristome. Revue Bryologique 11: 80–87 (1884); 12: 67–77, 81–85 (1885); 13: 17–26, 81–86 (1886); 14: 9–11, 81–90 (1887); 15: 6–12, 24–28, 37–44, 50–60, 65–69, 90–93 (1888); 16: 1–9, 39–44, 67–77 (1889); 17: 8–12, 25–29, 39–42 (1890); 23: 36–38, 41–56 (1896); 28: 56–59, 127–130 (1901); 29: 10–13 (1902). Saito, K. (1975) A monograph of the Japanese Pottiaceae (Musci). Journal of the Hattori Botanical Laboratory, 39: 373–537. Schimper, W. P. (1855 [1856]) Corollarium Bryologiae Europaeae, Conspectum Diagnosticum Familiarum, Generum et Specierum, Adnotationes Novae Atque Emendations Complectens. Schweizerbart, Stuttgart. Schwägrichen, C. F. (1810) Über das Hedwig’sche System der Moose und Beschreibung einiger neuer Moose. Neues Journal für die Botanik, 4: 1–19, Tabs. I, II. Shaw, J. and Anderson, L. E. (1988) Peristome development in mosses in relation to systematics and evolution. II. Tetraphis pellucida (Tetraphidaceae). American Journal of Botany, 75: 1019–1032. Shaw, J., Anderson, L. E. and Mishler, B. D. (1987) Peristome development in mosses in relation to systematics and evolution. I. Diphyscium foliosum (Buxbaumiaceae). Memoirs of the New York Botanical Garden, 45: 55–70. Shaw, J., Anderson, L. E. and Mishler, B. D. (1989) Peristome development in mosses in relation to systematics and evolution. III. Funaria hygrometrica, Bryum pseudocapillare, and B. bicolor. Systematic Botany, 14: 24–36. Shaw, J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses. Evolution, 57: 2226–2241. Shaw, J., Cox, C. J. and Boles, S. B. (2004) Phylogenetic relationships among Sphagnum sections: Hemitheca, Isocladus, and Subsecunda. Bryologist, 107: 189–196. Smith, J. E. (1804) Remarks on the generic characters of mosses, and particularly of the genus Mnium. Transactions of the Linnean Society of London, 7: 254–263. Strasburger, E. (1894) The periodic reduction of the number of chromosomes in the life-history of living organisms. Annals of Botany, 8: 281–316.

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Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002) Circumscription, classification, and taxonomy of Amblystegiaceae (Bryopsida) inferred from nuclear and chloroplast DNA sequence data and morphology. Taxon, 51: 115–122, 633. Vitt, D. H. (1984) Classification of the Bryopsida. In New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 696–759.

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Phylogenetic Distribution 2 The of Pleurocarpous Mosses: Evidence from cpDNA Sequences Terry J. O’Brien CONTENTS Abstract ............................................................................................................................................19 2.1 Introduction.............................................................................................................................20 2.2 Materials and Methods ...........................................................................................................23 2.2.1 Sampling and Extraction for DNA Data....................................................................23 2.2.2 DNA Amplification and Sequencing..........................................................................23 2.2.3 Sequence Alignment...................................................................................................28 2.2.4 Phylogenetic Analyses................................................................................................28 2.3 Results.....................................................................................................................................29 2.3.1 Properties of Dataset and Trees .................................................................................29 2.3.2 Tree Congruence and Gene Utility ............................................................................29 2.3.3 Phylogenetic Interpretations.......................................................................................31 2.3.3.1 Position of Hypnidae and Hypnodendroid Pleurocarps .............................31 2.3.3.2 Monophyly of Rhizogoniaceae, and Positions of Aulacomnium, Calomnion and Orthodontium ....................................................................32 2.3.3.3 Position of Rhizogonian Mosses within Bryidae .......................................32 2.3.3.4 Position of Mittenia ....................................................................................32 2.4 Discussion...............................................................................................................................32 2.4.1 Clade Resolution, Branch Support and Phylogenetic Inference ...............................32 2.4.2 Phylogenetic Relationships ........................................................................................33 2.4.2.1 Hypnidae and Hypnodendroid Pleurocarps................................................33 2.4.2.2 Circumscription and Phylogenetic Position of Rhizogoniaceae ................34 2.4.2.3 Position of Aulacomnium ............................................................................36 2.4.3 Phylogenetic Asymmetry in the Rhizogonian Mosses and Crown Pleurocarps .......36 2.5 Conclusions.............................................................................................................................37 Acknowledgments ............................................................................................................................37 References ........................................................................................................................................37

ABSTRACT A maximum parsimony analysis of a four-gene cpDNA dataset of 58 exemplar taxa indicates that pleurocarpous and non-pleurocarpous members of the Rhizogoniaceae plus the acrocarpous genera

19

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Pleurocarpous Mosses: Systematics and Evolution

Aulacomnium, Calomnion and Orthodontium are the sister group or near sister group to the hypnodendroid pleurocarps and the Hypnidae (Hypnobryales, Hookeriales and Ptychomniales). Monophyly of the rhizogonian mosses (including the Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium) is not supported, either due to paraphyly of the principal clades, or poor branch support in the consensus most parsimonious tree (MPT). The rhizogonian mosses have a primarily Gondwanan distribution centered in Oceania, and have about 1% of the species richness in the species-rich clade of hypnodendroid pleurocarps and Hypnidae. These results have implications for studies of diversification, adaptation, disparity, development and genome evolution of the crown pleurocarps, which, with about 5400 species, comprise more than half of extant mosses.

2.1 INTRODUCTION Mosses (Musci) include at least 10,000 species (e.g., Buck and Goffinet, 2000; Shaw et al., 2003) to as many as 12,000 extant species (Crosby et al., 2004; Goffinet and Buck, 2004). The bryalean pleurocarpous mosses (pleurocarps), including the Rhizogonianae and Hypnidae (Goffinet and Buck, 2004), are the focus of this chapter. The pleurocarps include as few as 5300 species (e.g., Shaw et al., 2003) to as many as 6600 species (Crosby et al., 2004). Altogether then, the pleurocarps comprise more than half of all moss species, underlining the importance of accurately knowing their phylogenetic origins and the phylogenetic distribution of the traits that contribute to pleurocarpy. In this chapter, I adopt the following nomenclature. The Hypnidae are as defined by Goffinet and Buck (2004; the Hypnanae sensu Buck and Goffinet, 2000), and include the Ptychomniales, Hookeriales and Hypnales. The hypnodendroid pleurocarps are as defined by Bell and Newton (2004), and include the families Hypnodendraceae, Racopilaceae, Cyrtopodaceae, Pterobryellaceae and Spiridentaceae, all as delimited by Buck and Goffinet (2000) and Goffinet and Buck (2004). The crown pleurocarps include the Hypnidae and hypnodendroid mosses. The rhizogonian mosses include the Rhizogoniaceae (Churchill and Buck, 1982; Buck and Goffinet, 2000; Goffinet and Buck, 2004) as well as Aulacomnium Schwägrichen, Calomnion J. D. Hooker & Wilson in J. D. Hooker and Orthodontium Schwägrichen. What is pleurocarpy, and what is known of its distribution within the Bryidae (bryalean mosses)? Pleurocarpy refers to the developmental origin and position of the archegonia-bearing perichaetia on moss stems. In pleurocarpous mosses, the perichaetia are produced on short, lateral innovations, and hence appear sessile on the stem (La Farge-England,1996; Newton and De Luna, 1999). Consequently, pleurocarpy also describes the origin and position of sporophytes. Recent studies of bryalean pleurocarpous mosses, based on evidence from DNA sequences (De Luna et al., 1999; Newton et al., 2000; Goffinet et al., 2001; Shaw et al., 2003; Bell and Newton 2004; Buck et al., 2005), indicate that they include a monophyletic group of nearly 5300 species, designated as the Hypnidae by Goffinet and Buck (2004). This group has been shown to consist of three major clades, the Hookeriales, Hypnales and Ptychomniales (Buck et al., 2000; Shaw et al., 2003; Buck et al., 2005). However, as noted by Newton and De Luna (1999), Bell and Newton (2004) and Goffinet and Buck (2004), pleurocarpy is not limited to the Hypnidae. Two additional groups with pleurocarpous taxa, the hypnodendroid mosses (Bell and Newton, 2004) and Rhizogoniaceae, include about 175 species. It is noteworthy, however, that the Rhizogoniaceae contain pleurocarpous and non-pleurocarpous taxa, the latter including Cryptopodium Bridel, Hymenodontopsis Herzog, Leptotheca Schwägrichen, Pyrrhobryum Mitten, and Rhizogonium Bridel (La Farge-England, 1996). This indicates that pleurocarpy in the bryalean mosses may have originated more than once, or that pleurocarpy has been lost in some lineages (or both). These observations reveal two important points: (1) the question of the monophyly of bryalean pleurocarps is more than the question of the monophyly of the Hypnidae; and (2) an understanding of the phylogenetic distribution of pleurocarpy is critical to unraveling the character state transformations involved in the evolutionary origin(s) or loss(es) of pleurocarpy.

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The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences

21

The Rhizogoniaceae are a small family of mosses with an essentially Gondwanan distribution centered in Oceania. According to Churchill and Buck (1982), Crosby et al. (2004), Buck and Goffinet (2000) and Goffinet and Buck (2004), the Rhizogoniaceae include eight genera: Cryptopodium, Goniobryum Lindberg, Hymenodon J. D. Hooker & Wilson, Hymenodontopsis, Leptotheca, Mesochaete Lindberg, Pyrrhobryum and Rhizogonium. Early classifications considering the Rhizogoniaceae placed the family in a position phylogenetically distant from the Hypnidae (i.e., Fleischer [1904–1923]; Brotherus [1924–1925]; Vitt [1984] and Koponen [1988]). Within the past two decades, the classification of pleurocarps by Buck and Vitt (1986) and more recent phylogenetic analyses by Hedenäs (1994), Withey (1996), De Luna et al. (1999), Newton and De Luna (1999) and Cox et al. (2000) have all suggested that the nearest relatives of the crown pleurocarps may be within the Rhizogoniaceae. In more recent classifications, Buck and Goffinet (2000) and Goffinet and Buck (2004) included the Rhizogoniaceae in the superorder Rhizogonianae along with the hypnodendroid pleurocarps, apart from the Hypnidae. The phylogeny presented by Bell and Newton (2004) supports that the Rhizogoniaceae are instead a grade of lineages, sister to the monophyletic crown pleurocarps. The genus Aulacomnium is a small group of five or six acrocarpous species. Recent classifications treat Aulacomnium as the sole genus of Aulacomniaceae (Churchill and Buck, 1982; Vitt, 1984; Buck and Goffinet, 2000; Crosby et al., 2004; Goffinet and Buck, 2004), in contrast to earlier treatments by Fleischer (1904–1923) and Brotherus (1924–1925), who also included Leptotheca in the family. There are a variety of conclusions reached by previous authors about the nearest relatives of Aulacomnium within bryalean mosses. Brotherus (1924–1925) included his Aulacomniaceae (Aulacomnium and Leptotheca) in the suborder Bartramiineae, a group that also includes Bartramiaceae, Catoscopiaceae and Meesiaceae. Vitt (1984) proposed that Bartramiaceae, Catascopiaceae and Meesiaceae include the nearest relatives of Aulacomnium, and that the genus is rather distantly related within the non-pleurocarpous bryalean mosses to Rhizogoniaceae. Griffin and Buck (1989) suggested that Aulacomnium might “be nearer to the suborder Rhizogoniineae [= Rhizogoniaceae, in part] than previously thought,” a conjecture that has been supported by some subsequent studies. Buck and Goffinet (2000) and Goffinet and Buck (2004) include Aulacomnium within the basal bryalean mosses, and exclude it from their Rhizogoniales. In most more recent works that have relied on cladistic methods, Aulacomnium is positioned more closely to genera of Rhizogoniaceae. Hedenäs’ (1994) morphological dataset produced a consensus tree with Aulacomnium nested within a paraphyletic group of six genera of Rhizogoniaceae. The consensus MPT from a combined 18S rRNA–rbcL–rps4–trnL dataset assembled by Cox et al. (2000) positions Aulacomnium in a polytomy that includes the rhizogonian genus Pyrrhobryum and the pleurocarpous genera Racopilum, Hypnodendron and Bescherellia, but excludes the Hypnidae sampled. While these more recent studies suggest a close relationship of Aulacomnium and Rhizogoniaceae, their taxon sampling did not permit a clear assessment. More conclusive evidence about the position of Aulacomnium was presented by Bell and Newton (2004), who reported that it is within a grade of Rhizogoniaceae, Calomnion and Orthodontium. The genus Calomnion, which includes nine acrocarpous species (Vitt, 1995), has been regarded as having an unclear phylogenetic position (Vitt, 1984). The peristome is absent in all species, adding difficulty to the interpretation of its nearest relatives. Morphological characters suggest that the genus is a monophyletic group (Vitt, 1995). In Vitt’s (1984) classification, he included Calomnion within the Tetraphidales, a group distantly related to the Bryidae (Newton et al., 2000); however, more recently he suggested that the genus may be either within Tetraphidales or “in the general area of Rhizogoniaceae or the advanced Bryales” (Vitt, 1995). Waters et al. (1996) reported that 18S nrDNA sequences support the inclusion of Calomnion in an acrocarpous diplolepidous group of bryalean mosses, though no group is specified. Buck and Goffinet (2000) and Goffinet and Buck (2004) considered the Rhizogoniaceae to include the nearest relatives of Calomnion, and included the genus in their Rhizogoniales.

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22

Pleurocarpous Mosses: Systematics and Evolution

Buck and Goffinet (2000) and Goffinet and Buck (2004) positioned the acrocarpous genus Orthodontium in their superorder Bryanae, apart from their Rhizogonianae (= Rhizogoniaceae, hypnodendroid mosses and Calomnion). By comparison, Cox et al. (2000) reported a phylogeny from rbcL, rps4, trnL and 18S rRNA sequences which placed the acrocarpous genus Orthodontium as the sister group to the Hypnidae, although they used a small sample of Rhizogoniaceae, hypnodendroid pleurocarps and Hypnidae. More recently, Cox et al. (2004) and Bell and Newton (2004) confirmed the position of Orthodontium in a relationship close to or within pleurocarps. The most recent and intensive study of the phylogenetic distribution of basal bryalean pleurocarps is that of Bell and Newton (2004). They presented combined phylogenetic analyses of a dataset including 60 taxa and three genes, the mitochondrial nad5 region and chloroplast rbcL and rps4 regions. Working independently, I assembled a four-gene dataset of 58 taxa (O’Brien, 2001). The principal difference of the dataset compiled by Bell and Newton (2004) and the dataset used in this study is that I utilized sequences from the atpB–rbcL region, trnL–trnF region, rbcL gene and rps4 gene. Taxon sampling in these studies is similar, though the particular specimens used are different. With respect to the question of the distribution of pleurocarpy, their main findings were that: 1. The Hypnidae (Hypnanae in their paper) and hypnodendroid pleurocarps are sister groups and together form a monophyletic group; 2 The Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium are the nearest relatives of the Hypnidae and hypnodendroid mosses; 3. Monophyly of the Rhizogoniaceae is not supported; 4. The Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium can be tentatively assigned to three different clades. Additionally, they found clades within the rhizogonian grade (Aulacomnium, Calomnion and Orthodontium inclusive) that include both pleurocarpous and non-pleurocarpous taxa, raising the interesting possibility that pleurocarpy either originated more than once or that it was lost by reversion to acrocarpy. In summary, it appears from previous studies that Aulacomnium, Calomnion, Orthodontium, Rhizogoniaceae, the hypnodendroid mosses and Hypnidae should be the continued focus of attention for understanding the distribution of pleurocarpy within the bryalean mosses, and understanding a majority of the species richness of mosses. The use of gene sequences for the inference of phylogeny has been widely adopted in recent years. The costs of producing sequence data often impose a constraint on data collection, so that it remains common practice that a phylogeny is inferred from only one or two genes. An assumption of this practice is that the small sample of genes indicates the true phylogeny. It is known that processes such as gene duplication or deletion, introgression and lineage sorting can affect the inference of phylogeny from gene sequences, leading to the question of whether so few genes are adequate. One approach to assessing this question is to compare the number of shared clades of trees from genes (partitions) of the entire dataset (Johnson and Soltis, 1998). Phylogenetic studies that include several genes, such as this chapter, present the opportunity to evaluate the adequacy of using one or few genes. Understanding the phylogenetic patterns and morphological diversity in the pleurocarps is a central theme of the chapters in this book. In this chapter, I use evidence from four chloroplast gene sequences to address the questions of: (1) the position of Rhizogoniaceae within the basal bryalean mosses (Bryales); (2) monophyly of the Rhizogoniaceae; (3) the phylogenetic positions of Aulacomnium, Calomnion, Orthodontium and Mittenia and (4) relationship of these taxa to the hypnodendroid mosses and Hypnidae. My findings are consistent with the principal phylogenetic conclusions of Bell and Newton (2004). Importantly, my findings are based on two additional gene regions, and so offer a degree of independent support for their study. In addition to these questions

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The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences

23

about phylogenetic pattern, I also evaluate the extent to which data partitions (gene sets) predict the best estimate of phylogeny inferred from combined evidence. Finally, given the phylogenetic results, I consider the asymmetry of species richness in the crown pleurocarps compared to the rhizogonian mosses.

2.2 MATERIALS AND METHODS 2.2.1 SAMPLING

AND

EXTRACTION

FOR

DNA DATA

Table 2.1 includes information on voucher specimens and GenBank accession numbers for all sequences used in this study. Within the bryalean mosses (Bryidae), 58 exemplars and 50 genera were sampled, concentrated in the rhizogonian mosses. The rhizogonian exemplars include three species of Aulacomnium, one each of Calomnion and Orthodontium, and all genera of the Rhizogoniaceae, representing 16 of 35 species of Rhizogoniaceae. Within the Hypnidae, 12 genera were selected from the Hookeriales, Hypnales and Ptychomniales. The hypnodendroid pleurocarps are represented by seven genera, including exemplars of the Hypnodendraceae, Racopilaceae, Cyrtopodaceae, Pterobryellaceae and Spiridentaceae. Non-pleurocarpous Bryidae included four exemplars of the Mniaceae and Bartramiaceae, three Orthotrichaceae, two Meesiaceae, and one each of Leptostomataceae and Rhacocarpaceae. Sampling from more distant relatives of pleurocarps included the haplolepidous mosses Dicranum Hedw., Grimmia Hedw., Mittenia Lindb. and Racomitrium Brid. Funaria Hedw. was included to serve as an outgroup. In summary, the taxon sampling is nonrandom, with the greatest concentration occurring within the rhizogonian mosses. Composite sequences from two or more vouchers within a genus were used if a complete gene set was not available for a species (Table 2.1). In using composite sequences, it was assumed that phylogenetic divergence is small between Operational Taxonomic Units (OTUs) used for composite sequences, relative to the divergence between them and all other OTUs. DNA was extracted from air-dried field collections or herbarium specimens with the DNeasy Plant Kit (Qiagen Inc., Valencia, California). One green shoot tip was used for extractions from large plants, or three to five green shoot tips from small plants. The extraction protocol provided by the manufacturer was used with the following modifications (provided by John Wheeler): (1) ground tissues were incubated in lysate buffer (kit Buffer AP1) 1 to 2 h; and (2) two 50-μl elutions (kit Buffer AE) were used in the final step, with each elution allowed to incubate 30 to 60 min.

2.2.2 DNA AMPLIFICATION

AND

SEQUENCING

Sequences were produced in the Molecular Phylogenetics Laboratory (University and Jepson Herbaria and the Museum of Paleontology, University of California at Berkeley), or obtained from GenBank. DNA sequences were obtained from four cpDNA genes: (1) approximately 400 bp of the atpB gene and the adjacent atpB–rbcL nontranscribed spacer (hereafter referred to as atpB); (2) rbcL; (3) rps4; and (4) the trnL–trnF gene region (hereafter trnL). Primers used for polymerase chain reaction (PCR) amplicons were as follows: atpB–rbcL region, matpB601F, M007R (John Wheeler, personal communication); rbcL, M07 (John Wheeler, personal communication), M636, M740R, M1390R (Lewis et al., 1997); rps4–rps5F, trnSR (Souza-Chies et al., 1997); trnL–trnF region, uniC, uniF (Taberlet et al., 1991). For rbcL, amplicons were produced using M07 and M1390R, and all four rbcL primers were used in cycle sequencing reactions. PCR contained the following components: 1 to 6 μl of DNA extract, 5.0 μl of 10× MgCl2 + PCR Buffer II (Perkin-Elmer Applied Biosystems), 1.0 μl of 10 mM dNTPs, 0.5 μl of each primer pair at 25 μM, 0.25 μl of Amplitaq Gold DNA Polymerase (Perkin-Elmer) and dH2O to a total volume of 50 μl. For most extractions, 1 to 4 μl of DNA yielded visible PCR product. The most frequently successful strategy when PCR reactions failed was to use 2 μl of 10- to 50-fold diluted extract. All PCR reactions were done with a GeneAmp 9600 thermocycler (Perkin-Elmer) or DNA Engine thermocycler (MJ Research). Each PCR reaction was preceded by 10 to 12 min at 95C (a

M. L. Sargent s.n. (UC-Culture) Buck 32568 (NY) J. R. Shevock 12973 (UC) D. H. Norris 87262 (UC) J. R. Shevock 16833 (UC) L. E. Anderson 27577 (UC) H. Streimann 50383 (UC) H. Streimann 61090 (UC) A. Withey 732 (DUKE) T. A. J. Hedderson 11763 (RNG) M. L. Sargent October 8, 1977 (UC-Culture) H. Streimann 61871 (UC) H. Streimann 38403 (RNG) D. Norris 79966 (UC) H. Streimann 57841 (UC) J. E. Beever 90-67 (UC) H. Streimann 54178 (NY) W. B. Schofield 61923 (UC) D. H. Vitt 29705 (UC) D. H. Vitt 29618 (DUKE) Mishler, Hopple & Thrall (DUKE). H. Streimann 56137 (NY) D. V. Basile October 6, 1978 (UC-Culture) B. Allen 20153 (MO) B. Allen Exsiccatae 109 (MO) M. L. Sargent June 6, 1980 (UC-Culture)

Collector, Number (Herbarium)

— — AF226818

AY853989 — AF231084 AF231067 — AF231074

AF413558 — — — — — — — —

AY853975 — AY853999 AY853982 AY853987

AF413551 — AF413556 AF413548 AF413549

Australia, Queensland — New Zealand Australia, Queensland New Zealand New Zealand Canada, British Columbia New Zealand New Zealand U.S., North Carolina Australia U.S., New Jersey — U.S., New York U.S., Illinois

AF231077 — AY853985 AY853976 AY853977 AY853978 AY853979 — AF231097 — AF158176

rbcL

— — AF413557 AF413566 AF413529 AF413534 AF413525 AF413552 — — AF413567

atpB

U.S., Indiana — U.S., California U.S., California U.S., California U.S., North Carolina Australia, New South Wales Australia, Queensland New Caledonia — U.S., Illinois

Locality Information

AF143064 — —

— AF023820 AY857774 AY857774 AY857781 AY306884 AY857772 AY857775 — — AY306907 —

— AF143031 AY857769 AY857790 AY857766 AY857767 AY857768 AY857793 — AF023818 —

rps4

— AF191534 —

— AF023745 AY857810 AY857812 AY857811 AY306718 AY857813 AY857802 — — AY306741 —

— AF161124 AY857808 AY857818 AY857795 AY857797 AY857796 AY857817 — AF023772 —

trnL

24

Fontinalis dalecarlica Bruch & Schimp. in B.S.G. Fontinalis dalecarlica Bruch & Schimp. in B.S.G. Funaria hygrometrica Hedw.

Anacamptodon splachnoides (Froel. ex Brid.) Brid. Anacamptodon splachnoides (Froel. ex Brid.) Brid. Anacolia laevisphaera (Taylor) Flowers in Grout Antitrichia californica Sull. in Lesq. Aulacomnium androgyum (Hedw.) Schwaegr. Aulacomnium heterostichum (Hedw.) Bruch & Schimp. Aulacomnium palustre (Hedw.) Schwaegr. Bescherellia elegantissima Duby Bescherellia elegantissima Duby Brachythecium rutabulum (Hedw.) Schimp. in B.S.G. Brachythecium salebrosum (Hoffm. ex Weber & D. Mohr) Schimp. in B.S.G. Braithwaitea sulcata (Hook.) A. Jaeger Braithwaitea sulcata (Hook.) A. Jaeger Breutelia pendula (Sm.) Mitt. Bryobrothera crenulata (Broth. & Paris) Ther. Calomnion complanatum (Hook. f. & Wilson) Lindb. Cladomnion ericoides (W. J. Hooker) Wils. in J. D. Hooker Conostomum tetragonum (Hedw.) Lindb. Cryptopodium bartramioides (Hook.) Brid. Cryptopodium bartramioides (Hook.) Brid. Dicranum scoparium Hedw. Euptychium robustum Hampe Fontinalis dalecarlica Bruch & Schimp. in B.S.G.

OTU/Taxon

TABLE 2.1 Voucher Specimens and GenBank Accessions for Sequences Used in this Study

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Pleurocarpous Mosses: Systematics and Evolution

Leucodon andrewsianus (H. A. Crum & L. E. Anderson) W. D. Reese & L. E. Anderson Leucolepis acanthoneura (Schwaegr.) Lindb. Macromitrium levatum Mitt. Meesia triquetra (H. Richt.) Angstr. Mesochaete undulata Lindb. Mesochaete undulata Lindb.

Leptotheca gaudichaudii Schwaegr. Leptotheca gaudichaudii Schwaegr. Leucodon julaceus (Hedw.) Sull.

Leptobryum pyriforme (Hedw.) Wilson Leptostomum macrocarpum (Hedw.) Bach. Pyl. Leptostomum macrocarpum (Hedw.) Bach. Pyl. Leptotheca boliviana Herzog Leptotheca boliviana Herzog

R. R. Halse 4883 (UC) T. Pocs, et al. 88102/N (RNG) T. J. O’Brien 2604 (UC) H. Streimann 35245 (CBG) H. Streimann 61888 (UC)

D. H. Norris 49382 (UC) J. E. Beever 90-72 (UC) D. H. Norris 67011 (UC) J. E. Beever 90-74 (UC) A. Withey 739 (DUKE) M. L. Sargent May 19, 1982 (UC-Culture) C. Cox 121 (RNG) Fletcher, s.n. (RNG) G. R. & J. E. Beever 90-71 (UC) S. P. Churchill 16400 (H) B. R. Ramirez & M.S. Gonzalez 9.058 (MO) H. Streimann 51199 (UC) H. Streimann (H) M. L. Sargent August 5 1989 (UC-Culture) W. R. Buck 32502 (NY)

Hymenodon angustifolium Sande Lac. Hymenodon pilifer Hook. f. & Wilson Hymenodontopsis stresemannii Herzog Hypnodendron comatum (Müll. Hal.) Touw Hypnodendron menziesii (Hook.) Paris Leptobryum pyriforme (Hedw.) Wilson

Hookeria acutifolia Hook. & Grev. Hookeria lucens (Hedw.) Sm.

C. J. Cox 148 (RNG) D. H. Norris 80013 (UC) H. Streimann 38105 (RNG) S. Schaffer Nov. 9, 1994 (UC) J. Christy 21771 (DUKE) M. L. Sargent August 30, 1981 (UC-Culture) B. Allen 20123 (MO) C. J. Cox 118 (RNG)

Funaria hygrometrica Hedw. Goniobryum subbasilare (Hook.) Lindb. Goniobryum subbasilare (Hook.) Lindb. Grimmia laevigata (Brid.) Brid. Grimmia pulvinata (Hedw.) Sm. Hookeria acutifolia Hook. & Grev.

U.S., Oregon — U.S., Oregon Australia, Queensland Australia, Queensland

—

New Zealand — Canada, Ontario

— — New Zealand — Colombia

Solomon Islands New Zealand Papua New Guinea New Zealand New Caledonia U.S., Indiana

— —

— New Zealand — U.S., California — U.S., Indiana

AF413564 — AF413560 — AF413535

—

AF413541 — —

— — AF413561 — AF413542

— AF413545 AF413544 AF413553 — —

— —

— AF413543 — — — AF413569

AY854005 — AY853986 AF231086 —

—

AY853980 — AF231075

— — AY853998 — AY854006

— AY853995 AY853997 — AF231093 AF231072

— —

— AY853991 — AF231081 — AF158170

AY857789 AF023813 AY857780 — AY857791

AF143005

AY857778 — —

AF023802 AF023790 — AF023816 —

AY857776 — AY857777 AY857779 — —

AF143071 —

AF023776 — AF023824 — AF222900 —

AY857821 AF023725 AY857820 — AY857798 Continued.

—

— AF023750 —

AF023736 AF023744 — AF023749 —

— AF215906 Continued. — AY857804 AY857803 AY857814 — —

AF023716 — AF023753 — — —

3856_book.fm Page 25 Saturday, March 3, 2007 12:29 PM

The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences 25

Pyrrhobryum spiniforme (Hedw.) Mitt. Pyrrhobryum spiniforme (Hedw.) Mitt.

Plagiopus oederianus (Sw.) H. A. Crum & L. E. Anderson Pterobryella praenitens C. Mueller in Bescherelle Ptychomnion aciculare (Bridel) Mitten Pyrrhobryum bifarium (Hook.) Manuel Pyrrhobryum latifolium (Bosch & Sande Lac.) Mitt. Pyrrhobryum mnioides (Hook.) Manuel Pyrrhobryum mnioides (Hook.) Manuel Pyrrhobryum paramattense (Müll. Stuttg.) Manuel

T. Pocs, et al. 88110/BJ (RNG) D. H. Norris 77595 (UC)

H. Streimann s.n. June 16, 1999 (UC) C. J. Cox 115 (RNG) D. H. Vitt 35884 (ALTA) Hedderson s.n. (RNG) T. A. J. Hedderson 5745 (RNG) B. Goffinet 3162 (ALTA) M.L. Sargent May 11, 1980 (UC-Culture) J. Van Rooy 3459 (UC) H. Streimann 56079 (NY) H. Streimann 43623 (NY) D. H. Norris 79409 (UC) H. Streimann 61831 (UC) H. Streimann 58731 (UC) D. H. Norris 79901 (UC) H. Streimann s.n. June 16, 1999 (UC)

Collector, Number (Herbarium)

Mexico

—

Africa, Lesotho — Australia New Zealand Australia, Queensland Australia, Victoria New Zealand Australia

— — — — — U.S., Indiana

Australia

Locality Information

AF413540 —

AF413559 — — AF413536 AF413538 AF413539 — AF413537

— — — — — —

AF413563

atpB

— AY853984

AF023751 —

AY857773 AF307002 AY306983 AY857784 AY857786 — AY857785 AY857787

AF023796 — AF023800 AF023814 — —

— AF005518 AJ275174 — AF005536 MCU87082 AY853990 — — AY854001 AY854003 — AY854002 AY853983

AY857782

rps4 AY853988

rbcL

Continued. — AY857808

AY857809 AF509536 AY306817 AY857805 AY857806 AY857799 — AY857807

AF023767 — AF023768 AF023727 — —

AY857819

trnL

26

Mnium hornum Hedw. Mnium thomsonii Schimp. Orthodontium lineare Schwaegrichen Orthotrichum lyellii Hook. & Taylor Orthotrichum lyellii Hook. & Taylor Plagiomnium cuspidatum (Hedw.) T. J. Kop.

Mittenia plumula (Mitt. in Hook. f.) Lindb.

OTU/Taxon

TABLE 2.1 (Continued) Voucher Specimens and GenBank Accessions for Sequences Used in this Study

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Pleurocarpous Mosses: Systematics and Evolution

Taiwan Mexico Australia, Queensland

J. Shevock 15061 (UC) D. H. Norris 77393 (UC) H. Streimann 61878 July 28, 1998 (UC) H. Streimann 36688 (RNG) G. R. & J. E. Beever 90-73 (UC) D. H. Norris 79442 (UC) Ray Tangney RT 2-A (UC) A. Eddy 6232 (BM) J. McMurray s.n. (UC) A. Newton Nov 18, 1988 (DUKE) T. A. J. Hedderson 11763 (RNG) C. E. Darigo 2639 (UC) B. Goffinet 3161 (ALTA) T.A.J. Hedderson 11772 (RNG) — New Zealand New Zealand New Caledonia — — U.S., North Carolina — U.S., Alaska — —

— Australia, Victoria

Schaeffer Aug. 9, 1994 (UC) H. Streimann 61955 (UC)

— AF413547 — AF413550 — AF413568 — — AF413565 — —

AF413555 AF413562 AF413546

— AF413554

— AY853994 — AY853972 — — AF158177 — AY854004 AF005539 —

AY853973 AY854000 AY853993

AF231082 AY853974

AF023827 — AY857783 — AF023828 — — AF023819 AY857788 — AF023812

AY857794 AY857792 —

— —

AF023752 — AY857801 — AF023748 — — AF023770 AY857822 — AF023726

AY857816 AY857823 AY857800

— AY857815

Note: Taxon names are from Crosby et al. (2004). Sequences newly produced for this study are in boldface. Locality information is missing if it was not reported in the original publication or in GenBank.

Rhizogonium novae-hollandiae (Brid.) Brid. Rhizogonium novae-hollandiae (Brid.) Brid. Rhizogonium pennatum Hook. f. & Wilson Spiridens reinwardtii Nees Spiridens reinwardtii Nees Thuidium delicatulum (Hedw.) Schimp. in B.S.G. Thuidium delicatulum (Hedw.) Schimp. in B.S.G. Thuidium tamarascinum (Hedw.) Schimp. in B.S.G. Trachycystis flagellaris (Sull. & Lesq.) Lindb. Ulota obtusiuscula Müll. Hal. & Kindb. in Macoun Ulota phyllantha Brid.

Racomitrium fasciculare (Hedw.) Brid. Racopilum cuspidigerum (Schwegr. in Gaudich. in Freyc.) Angstr. Racopilum ferriei Ther. Rhacocarpus purpurascens (Brid.) Paris Rhizogonium graeffeanum (Müll. Stuttg.) A. Jaeger

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hot start) and followed by a 7 min final extension at 72C. The number of cycles, and denaturation, annealing and extension conditions used for each gene are as follows: atpB, 40 to 45 cycles of 95C/40 s, 54 to 57C/40 s, 72C/90 s; rbcL, 40 to 45 cycles of 95C/40 s, 56C/40 s, 72C/90 to 100 s; rps4, 40 cycles of 95C/40 s, 60C/40 s, 72C/75 s; trnL, 45 cycles of 95C/40 s, 58C/20 s, 72C/70 s. PCR products were purified using a microcentrifuge and the QIAQuick PCR Purification Kit (Qiagen, Inc.), with a final elution volume in Buffer EB of 20 to 40 μl. Quantification of PCR products for cycle sequencing was found to be unnecessary for this range of elution volumes. Sequencing reactions from cleaned PCR products were prepared with BigDye Terminator Cycle Sequencing Ready Reaction kits (Perkin-Elmer). Each reaction included 2 to 2.7 μl (1/4 or 1/3 reactions) of Terminator Ready Reaction Mix, 1 to 5 μl of purified PCR product (the highest volumes for weak PCR bands or amplicons >1000 bp), 1.0 μl of 10 mM primer, and dH2O. Sequencing reaction products were purified by precipitation for at least 30 min in 30 μl of 75% isopropanol, centrifugation for 15 min, and aspiration of the supernatants, followed by a second brief precipitation in 100 μl of 75% isopropanol, 5 min centrifugation, aspiration and vacuum centifugation for 30 min. The sequencing reaction products were electrophoresed through 4.8% acrylamide gels in an ABI 377 automated sequencer (Perkin-Elmer), and sequences were generated using ABI system software.

2.2.3 SEQUENCE ALIGNMENT Prior to the alignment of all OTU sequences for a gene, complementary sequences from forward and reverse primer pairs were used to assemble a consensus forward sequence (5 to 3) for each OTU. All consensus forward sequences for each gene were aligned with the computer program CLUSTAL V (Higgins, 1994), using equal matching and gap penalties of ten. Manual corrections to the computer alignment were made by comparing each position among all sequences and examining electropherograms. To minimize systematic error (Swofford et al., 1996), regions of ambiguity were excluded from the phylogenetic analyses. The data matrix is available from the author upon request.

2.2.4 PHYLOGENETIC ANALYSES All analyses were done with PAUP* software, version 4.0b10 (Swofford, 2002). A strict consensus of all MPTs was determined for the following gene sets: all genes (combined evidence; atpB, rbcL, rps4 and trnL), each of the four possible combinations of three genes, and each gene alone. Only the combined evidence tree is presented. In all analyses, included characters are equally weighted. For each gene set, several outgroups (Funariidae or Dicranidae) were substituted into separate analyses to confirm the stability of the ingroup branch topology in the consensus tree. Funaria was used as an outgroup in all final analyses except atpB alone (no atpB sequence was obtained for Funaria). For the atpB analysis, Mittenia was used as an outgroup (Bell and Newton [2004] presented evidence that Mittenia is haplolepidous). The procedure for identifying all MPTs for a gene set consisted of two heuristic searches: (1) identification of all tree islands (Maddison, 1991); and (2) identification of all MPTs from the islands represented by all trees saved from the first search. The support for each branch in the consensus trees was assessed with the decay index (DI: Bremer, 1994; Mishler, 1994) and bootstrap values (1000 replicates, using heuristic searches with random addition). The g1 value (Hillis, 1991; Huelsenbeck, 1991) was calculated with PAUP* from 500,000 randomly generated trees for all data partitions. The observations of Hillis (1991) on g1 values indicate that slightly negative values (approximately –0.2 or less) imply phylogenetic signal in a dataset with many characters. An additional measure of the signal in data is the number of resolved clades (Johnson and Soltis, 1998). To evaluate congruence in data partitions, the total number of resolved clades in trees from one-gene data partition trees was compared to that from the combined

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TABLE 2.2 Statistics for Strict Consensus Trees from Combined and Partial Evidence Dataset

N

Chars.

I

I/N

% Inf.

C.I.

R.I.

MPTs

Steps

Clades

g1

All genes, all taxa All genes, Bryidae only All genes, pleurocarps only atpB only rbcL only rps4 only trnL only All 1-gene sets

58 50 38 38 53 50 53 —

3210 3210 3210 832 1312 632 434 —

740 646 533 184 253 164 119 —

12.8 12.4 14.0 4.84 4.77 3.28 2.25 —

23.1 20.1 16.6 22.1 19.3 26.0 27.4 —

0.412 0.378 0.413 0.438 0.326 0.416 0.402 —

0.521 0.570 0.616 0.651 0.589 0.630 0.637 —

288 123 4 148 4 12 687 —

3704 2633 1832 632 1110 1397 515 —

48 42 31 18 28 16 12 42

–0.6823 –0.7424 –0.7162 –0.8691 –0.4205 –0.4093 –0.6561 —

Note: N = number of taxa; Chars. = alignable characters; I = informative alignable characters; % Inf. = percentage of informative alignable characters; C.I. = consistency index value, calculated without autapomorphies; R.I. = retention index value; MPTs = most parsimonious trees from all identified tree islands (see Materials and Methods); Steps = steps in parsimonious trees; Clades = clades resolved of those in the all-genes consensus tree; g1 = g1 value (Hillis, 1991).

evidence tree (Table 2.2). Although congruence of branch support is also important, it is not considered in this chapter.

2.3 RESULTS 2.3.1 PROPERTIES

OF

DATASET

AND

TREES

Table 2.2 summarizes statistics for the combined evidence (all genes) and partial gene sets. The dataset includes 58 OTUs and 195 gene sequences, of which 130 are original. Data are missing for 37 of a possible 232 sequences for the four genes (the effect of this on clade resolution or support is unknown). The combined evidence data includes 740 informative characters, or 23.1% of all characters, and 12.1 informative characters per OTU. The number of informative characters per taxon (I/N), an estimator of phylogenetic signal (Bremer et al., 1999), increases as more gene partitions are utilized. Values of the g1 statistic range from –0.4093 to –0.8691, indicating that the distribution of trees for all gene sets is skewed towards the shortest trees. This suggests phylogenetic signal in all data partitions considered. The strict consensus MPT from combined evidence (Figure 2.1) includes resolution of 48 clades, with CI = 0.424 and RI = 0.531. Combined evidence yields 288 MPTs from two tree islands. The deletion of all OTUs except the rhizogonian mosses and pleurocarps reduces the number of MPTs to four, and results in an increase of I/N. This suggests that the detectable phylogenetic signal is concentrated within 34 rhizogonian and pleurocarp exemplars. The DI values in the combined evidence consensus tree are approximately proportionate to branch lengths (Figure 2.1 and Figure 2.2; based on ACCTRAN optimization), indicating that over all characters included and all taxa sampled, longer branches consistently accumulate a more pronounced phylogenetic signal than shorter branches. This indicates that polytomies associated with short branches in the tree are generally a consequence of fewer synapomorphies rather than homoplasies.

2.3.2 TREE CONGRUENCE

AND

GENE UTILITY

Table 2.2 indicates tree congruence in one-gene data partitions compared to the combined evidence tree (Figure 2.1; trees from gene partitions not shown). Combined analysis of all genes results in six clades that are not produced in consensus MPTs from one-gene partitions. The consensus MPTs

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Pleurocarpous Mosses: Systematics and Evolution

100 100 73 22 31 4 51 2 2 76 62 6 75 2 100 1 > 40 3

66 2

54 2

2 1 51 2 2 59 3

1

2 60 3 53 2

1

62 2

1

70 4

2

1

58 2 2 94 4

1

1 1 82 5 91 57 5 100 5 > 40 93 100 5 > 40 100 35

1

98 2 18

72 1

61 2

52 2

82 3

93 4 94 16

100 100 34

95 5 52 2

1

99 19

Aulacomnium pal. Aulacomnium and. Aulacomnium het. Mesochaete Pyrrhobryum bifar. Hymenodontopsis Pyrrhobryummnioides Bryobrothers Hookeria Cladomniun Euptychium Ptychomniun Anacamptodon Fontinalis Brachythecium Thuidium Echinophyllum Leucodon Antitichia Spiridena Pterobryella Beacherella Hypnodendron Racopilum cuspid. Racopilum ferriel Braithwaitea Leptotheca gaud. Leptotheca boliv. Hymenodon Orthodontium Cryptopodium Calomniun Pyrrhobryum param. Pyrrhobryum latif. Pyrrhobryum spinif. Goniobryum Rhizogenium pen. gr. Rhizogenium nov. hol. Leptrostomum Leucolepis Trachychstis Mnium Plagiumnium Breutelia Conostomum Plagious Anacolia Rhacocarpus Meesia Leptobryum Orthotrichum Ulota Macromitrium Mittenia Grimmia Racomitrium Dicranum Funaria

A (13)

H y p n (5000) i d (6500) a e

H y p n (110) o d e n B (23)

C (28)

FIGURE 2.1 Strict consensus of 288 MPTs from combined analysis of atpB, rbcL, rps4 and trnL–trnF regions (Length = 3704; Informative characters = 740). Numbers above and below branches are bootstrap values and decay index values, respectively. Circles indicate non-pleurocarpous (acrocarpous or cladocarpous) taxa. Hypnoden = Hypnodendroid pleurocarps (Bell and Newton, 2004). Groups A, B and C are discussed in the text. Numbers in parentheses are species richness, with both lower and upper estimates provided for the Hypnidae.

from one-gene partitions include 25% to 58% of the 48 combined evidence clades. In the one-gene partitions, rbcL predicts the most combined evidence clades (28), whereas trnL and rps4 are relatively poor in resolution of combined evidence (12 and 16, respectively). Gene utility can also be assessed from the number of informative characters (I) and the percentage of informative characters (% Inf.). For this dataset, rbcL has the most informative characters (253), followed by atpB (184), rps4 (164) and trnL (119). The two genes (rps4, trnL) with the highest percentage of informative characters resolve the fewest combined evidence clades.

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Autacomnium pal. Autacomnium and. Autacomnium het. Mesochaete Pyrrhobryum bifar. Hynenodontopsis Pyrrhobryummnioides Bryobrothera Hookeria Cladomnion Euptychium Ptychomnium Anacamptodon Fontinalis Bracythecium Thurdium Echinophyllum Leucodon Antitrichia Spiridena Pterobryella Beacherellia Hypnodendron Braithwaitea Racopilum cuspid. Racopilum ferriei Leptotheca gaud. Leptotheca boliv. Hymenodon Orthodontium Cryptopodium Calomnion Pyrrhobryum param. Pyrrhobryum latif. Pyrrhobryum spinif. Goniobryum Rhizogenium pen. gr. Rhizogenium nov. hol. Leptostomum Leucolepis Mnium Plagiomnium Trachycystis Breutelia Conostomum Plagiopus Anacolia Rhacocarpus Meesia Leptobryum

31

A

H y p n i d a e

H y p n o d e n B

C

Orthotrichum Ulota Macromitrium Mittenia Dicranum Grimnia Racomitrium Funaria

50 changes

FIGURE 2.2 Branch lengths of one of 288 MPTs from parsimony analysis of atpB, rbcL, rps4, and trnL–trnF regions. Group labels correspond with those in Figure 2.1.

2.3.3 PHYLOGENETIC INTERPRETATIONS 2.3.3.1 Position of Hypnidae and Hypnodendroid Pleurocarps The strict consensus tree supports the following interpretations: 1. The Hypnidae and hypnodendroid pleurocarps together constitute a monophyletic group, though with at best a moderate branch support value (DI = 3, bootstrap = 59%);

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2. Within the crown pleurocarps, there is weak support for the monophyly of the Hypnidae (DI = 2; bootstrap = 51%) and moderate support for monophyly of its sister group, the hypnodendroid pleurocarps (DI = 3; bootstrap = 60%); 3. There is weak support (DI = 2; bootstrap = 54%) for the conclusion that the sister group to the Hypnidae and hypnodendroid pleurocarps includes Aulacomnium, Hymenodontopsis, Mesochaete and Pyrrhobryum Section Pyrrhobryum. The taxon sampling precludes further inferences about relationships within the Hypnidae and hypnodendroid pleurocarps. 2.3.3.2 Monophyly of Rhizogoniaceae, and Positions of Aulacomnium, Calomnion and Orthodontium The combined evidence tree does not support the monophyly of Rhizogoniaceae, and offers weak support for the conclusion that it is a paraphyletic group. The Rhizogoniaceae are dispersed in three clades, A to C, which are weakly resolved from each other (DI = 1; bootstrap <50%, and DI = 2; bootstrap = 54%). These branch support values offer either weak or inconclusive support for paraphyly of the Rhizogoniaceae. However, Aulacomnium, Calomnion and Orthodontium are dispersed in clades A to C, indicating that the Rhizogoniaceae alone are non-monophyletic. Clade A, comprised of Aulacomnium, Hymenodontopsis, Mesochaete and Pyrrhobryum Section Bifariella, is moderately supported (DI = 2; bootstrap = 66%). Within clade A, Mesochaete (DI = 4; bootstrap = 73%) is positioned as the sister group to Aulacomnium. The branch support for sister group relationship of Mesochaete with Aulacomnium is also supported by the consensus MPTs from individual analyses of atpB, rbcL and rps4 (not shown). Clade B (DI = 1; bootstrap <50%), comprised of Leptotheca, Hymenodon and Orthodontium, has inconclusive support. Clade C includes Calomnion, Cryptopodium, Goniobryum, Pyrrhobryum Section Pyrrhobryum and Rhizogonium. Internal clades within clade C have higher branch support than the clade as a whole. One well-supported internal clade includes Goniobryum and Rhizogonium (DI = 5; bootstrap = 93%), and a second includes Calomnion, Cryptopodium and Pyrrhobryum Section Pyrrhobryum (DI = 5; bootstrap = 91%). 2.3.3.3 Position of Rhizogonian Mosses within Bryidae For the taxa sampled here, a clade including Leptostomum and all exemplars from Mniaceae s. lat. are the sister group of the rhizogonian mosses, the hypnodendroid pleurocarps and the Hypnidae. However, the support for this interpretation is inconclusive (DI = 1; bootstrap <50%). The sister group of Leptostomum + Mniaceae is a clade that includes Bartramiaceae and Rhacocarpus. 2.3.3.4 Position of Mittenia The phylogenetic position of Mittenia complanata is consistent with inclusion in the haplolepidous mosses rather than diplolepidous-alternate mosses, from a combined evidence analysis using Funaria as an outgroup. Therefore, the use of Mittenia as an outgroup is justified in the atpB analysis. Taxon sampling prevents a more exact inference of its nearest relatives.

2.4 DISCUSSION 2.4.1 CLADE RESOLUTION, BRANCH SUPPORT

AND

PHYLOGENETIC INFERENCE

The issue of whether to rely on combined evidence trees or congruence of trees from separate datasets in phylogenetic inference has received considerable attention (e.g., Bull et al., 1993; de

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Queiroz et al., 1995; Huelsenbeck et al., 1996; Kluge, 1998). For the inference of phylogeny, it has been asserted that it is better to use combined evidence rather than congruence of trees from data partitions (de Queiroz et al., 1995; Kluge, 1998). However, there are two reasons that comparisons of trees from data partitions are useful. First, in some cases, trees from data partitions differ substantially and can reveal important processes such as gene duplication/deletion, introgression, and lineage sorting that effect the inference of phylogeny (de Queiroz et al., 1995; Baldwin et al., 1998; Doyle, 1997; Maddison, 1997; Wendell and Doyle, 1998; Shaw, 2000). A second reason for comparing trees from partitions of the entire dataset is that they provide insights into how well partial evidence predicts the phylogeny from all evidence. This is an important consideration when choosing the extent of gene sampling for any phylogenetic study. In this study, congruences in consensus MPTs from data partitions and the consensus MPT from combined evidence were compared using the number of resolved clades. None of the one-gene partitions predicted more than 58% of the number of combined evidence clades, and all but rbcL data predicted less than 40%. Furthermore, the combined evidence tree includes six emergent clades compared to any trees from the one-gene partitions. It is also noteworthy that rbcL data provided substantially better clade resolution than rps4 data, given that both genes have been commonly used in phylogenetic studies of bryophytes. An implication of these observations is that it should not be expected that a phylogenetic tree from one gene will include satisfactory clade resolution. Poor clade resolution or branch support can be a consequence of the study design. Choices in study design that can lead to poor resolution include restricted taxon sampling, selecting the “wrong” genes (Soltis et al., 1998) and inappropriate character weighting (Albert et al., 1993). The four genes selected in this study clearly differ in phylogenetic signal (as indicated by clade resolution); however, each offers some resolution of relationships. Within rhizogonian mosses, there are several rather weakly supported key nodes along the backbone of the tree that will directly impact inferences about the evolution of pleurocarpy. The choice of additional taxa or genes with the appropriate character variation are two strategies that may prove effective. Poor clade resolution or branch support can also be a result of underlying patterns of evolution. Processes that limit these properties of trees include radiations and extinctions (Baldwin et al., 1998), as well as reticulation and lineage sorting (Wendell and Doyle, 1998). Shaw et al. (2003) presented evidence for a rapid diversification (radiation) in the early history of the Hypnidae, but did not include hypnodendroid pleurocarps or rhizogonian mosses in their study. The results presented by Bell and Newton (2004) and in this study include relatively poor branch support values and short branch lengths supporting three main rhizogonian clades. Given the extent of taxon and character sampling in both of these studies, these observations appear to be caused by real evolutionary pattern. A rapid divergence of the main rhizogonian clades soon after their origin is a possible cause, worthy of further investigation.

2.4.2 PHYLOGENETIC RELATIONSHIPS 2.4.2.1 Hypnidae and Hypnodendroid Pleurocarps The segregation of the crown pleurocarps into two fundamental divisions is supported by the combined evidence presented here, which recognizes one clade comprised of hypnodendroid pleurocarps, and a second of the Hookeriales, Hypnales and Ptychomniales. This outcome coincides with relationships inferred by De Luna et al. (1999) and Newton and De Luna (1999) from a combined rbcL and morphology dataset, and which were confirmed by Bell and Newton (2004) with more extensive taxon sampling and a three-gene dataset. It is noteworthy that this study and the results of Bell and Newton (2004) support the findings of De Luna et al. (1999) from combined morphology and rbcL data. It appears that while morphology alone and single-gene molecular datasets alone may not yield the best inference of phylogeny, their combination can result in a best estimate that will match that from a larger molecular dataset. Thus, when given limited resources

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for obtaining molecular data, obtaining data from carefully studied morphology and one wellchosen gene can be an effective strategy for producing an accurate best estimate tree. The recognition of the hypnodendroid pleurocarps as the sister group to the Hypnidae is an important aspect of understanding the character transformations involved in generating pleurocarpy. Moreover, these results affirm that hypnodendroid pleurocarps are appropriate outgroups in phylogenetic reconstructions of the basal phylogenetic patterns or studies of character variation in the Hypnidae (e.g., Hedenäs, 1999). Buck and Goffinet (2000) and Goffinet and Buck (2004) inserted the hypnodendroid pleurocarps in the superorder Rhizogonianae, apart from the Hypnidae. The phylogeny presented here is in conflict with these classifications. The phylogeny presented here confirms in part the cladistic analyses by Hedenäs (1994) and Withey (1996), and exactly the combined-data cladistic analyses by De Luna et al. (1999), Newton and De Luna (1999) and Bell and Newton (2004) indicating that the hypnodendroid pleurocarps will be a critical study group in understanding pleurocarpy in the Hypnidae. 2.4.2.2 Circumscription and Phylogenetic Position of Rhizogoniaceae The phylogeny presented here places the genera traditionally assigned to Rhizogoniaceae (sensu Churchill and Buck, 1982) in a paraphyletic grade as the nearest relatives of the hypnodendroid pleurocarps and Hypnidae. The nearest relatives of the rhizogonian grade and crown pleurocarps mosses are a clade of Leptostomum R. Brown and Mniaceae s. lat. In the MPT, the sister group to all of these is a clade including either Rhacocarpaceae or Bartramiaceae; however, branch support for this interpretation is minimal, hence a better conclusion is that the sister group to the pleurocarps (rhizogonian mosses included) may include Leptostomataceae, Mniaceae, Rhacocarpaceae and/or Bartramiaceae. The general relationships in the transition from the non-pleurocarpous bryalean mosses to pleurocarpous mosses are consistent with those of Newton and Bell (2004). They are slightly different than those inferred by Cox et al. (2000) from a parsimony analysis of the relationships within the Bryidae; however, it should be noted that I did not sample from Bryaceae or Mielichhoferiaceae. Their reconstruction places Leptostomum in a position sister to the Bryaceae, and Pohlia Hedw. and Mielichhoferia Nees & Hornsch. as the sister group to Mniaceae. A more recent study by Cox et al. (2004) included similar taxon sampling within the Bryidae, with analyses from maximum likelihood and Bayesian inference as well as parsimony. Their best estimate trees indicate that the sister group to the pleurocarps includes Bryaceae, Mielichhoferiaceae and Mniaceae. The position of a clade including Mniaceae sister to Rhizogoniaceae is partially compatible with the interpretations of Koponen (1988 and his earlier works cited therein), who assembled a phylogeny treating Rhizogoniaceae and Mniaceae as an assumed monophyletic group. However, aside from the recognition of near relationships between the families, his interpretations of generic relationships are generally not supported by the present study. Cryptopodium, Hymenodontopsis, Leptotheca and Pyrrhobryum are not included in Mniaceae (which Koponen 1988 defined to include Leucolepis Lindb., Mnium Hedw. and Trachycystis Lindb., as well as these rhizogonian genera). These genera of rhizogonian mosses appear in different major clades within the rhizogonian grade. Koponen’s Rhizogoniaceae, consisting of Goniobryum, Hymenodon, Mesochaete and Rhizogonium, are also not a monophyletic group. The phylogeny presented here provides weak support that the nearest relatives of the pleurocarps is a clade that includes Aulacomnium, Mesochaete, Hymenodontopsis and Pyrrhobryum Section Bifariella (clade A). Trees from both parsimony and maximum likelihood analyses of Bell and Newton (2004) indicate that same sister clade of the hypnodendroid pleurocarps and Hypnidae (although their sampling did not include Hymenodontopsis). Unfortunately, branch support values do not permit a clear understanding of the overall relationships of the three primary clades (A to C) of rhizogonian mosses. Bell and Newton (2004) therefore summarized the basal relationships of the rhizogonian mosses as a polytomy. Regardless of the exact relationships within rhizogonian

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mosses, the fact that the same general phylogenetic position of rhizogonian was found in both studies is an indication of their critical nature in future studies of the crown pleurocarps. Pyrrhobryum was split into two sections by Manuel (1980), who recognized P. Section Bifariella and P. Section Pyrrhobryum. This view is partially supported by my results. I sampled two taxa, P. bifariella and P. mnioides, from Section Bifariella, and three taxa, P. latifolium, P. paramattense and P. spiniforme, from Section Pyrrhobryum. The taxa of Section Bifariella are in a clade (A) that includes Aulacomnium, Hymenodontopsis and Mesochaete, while the taxa of Section Pyrrhobryum sampled are in a clade (C) that includes Calomnion and Cryptopodium. The evidence from this study does not support the inclusion of these sections in a single genus, but supports the circumscription of the sections. Bell and Newton (2004) also found that the sections of Pyrrhobryum are non-monophyletic, and in their trees, the positions of the sections correspond to clades A and C. An additional seven species of Pyrrhobryum are known (Crosby et al., 2004) that were not sampled in this study, and these should be evaluated before taxonomic decisions are made. Both Hymenodontopsis and Hymenodon feature a reduced peristome compared to the fundamental bryalean type. However, Shaw and Anderson (1986) concluded that the modifications differ, indicating that the reductions are not a taxic homology. Species of both genera are epiphytic, usually found on tree ferns and, according to Koponen et al. (1986), resemble each other because of similar habitat rather than a near relationship within rhizogonian mosses. Koponen et al. (1986) note that “the leaf shape, the partially bistratose leaf border with geminate teeth, the dorsally toothed costa and the smooth leaf cells connect Hymenodontopsis more closely with Pyrrhobryum than Hymenodon.” The position of Hymenodontopsis within Pyrrhobryum Section Bifariella is not strongly supported in the combined evidence tree, but is consistent with their suggestions. The combined evidence tree provides weak support for the interpretation that Hymenodon, Leptotheca and Orthodontium are a monophyletic group, a finding also made by Bell and Newton (2004). In my study, this outcome should be viewed with particular caution, as the sequences of Hymenodon are a congeneric composite (Table 2.1), and the composite OTU exhibits inconsistent positions in one-gene trees (results not shown). Assuming these taxa do form a clade, there is an interesting occurrence within it of both acrocarpy (Leptotheca and Orthodontium) and pleurocarpy (Hymenodon). High branch support values are concentrated within clade C, supporting the position of Goniobryum as the sister lineage of Rhizogonium, and that Cryptopodium and Calomnion are a sister group of a clade including Pyrrhobryum Section Pyrrhobryum. There is less convincing support for the monophyly of clade C (DI = 2; bootstrap = 62%). Bell and Newton (2004) reported higher branch support (DI = 5; bootstrap = 81%) for clade C, as well as high branch support values for internal clades of Goniobryum/Rhizogonium and Calomnion/Cryptopodium/Pyrrhobryum Section Pyrrhobryum. On the strength of their findings, Bell and Newton proposed the informal name “core rhizogonioids” for these taxa. The occurrence of both acrocarpy and pleurocarpy in clade C (core rhizogonioids) is worthy of additional study. The combined evidence tree presented here places Calomnion in a well-supported clade that includes Cryptopodium and Pyrrhobryum Section Pyrrhobryum. Within this group, Cryptopodium represents a well-supported sister lineage to Calomnion. Bell and Newton (2004) included two species of Calomnion, C. complanatum and C. brownysei Vitt and H. A. Miller in Vitt in their taxon sampling. They also found that Cryptopodium is the sister group to Calomnion, and that Pyrrhobryum Section Pyrrhobryum is the sister group of the Cryptopodium–Calomnion clade. This clade is noteworthy from the standpoint of understanding the origins of pleurocarpy. Pyrrhobryum Section Pyrrhobryum is pleurocarpous, whereas both Calomnion and Cryptopodium are acrocarpous (see Bell and Newton, 2004, for additional discussion). Several authors (Brotherus, 1924–1925; Vitt, 1984; Buck and Goffinet, 2000; and others, summarized in Shaw, 1985 and Stone, 1986) have proposed classifications in which Mittenia is included within diplolepidous-alternate mosses. Vitt (1984) considered Rhizogoniaceae to be the sister group to Mittenia and Schistostega D. Mohr, whereas Buck and Goffinet (2000) include

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Mittenia within their concept of Rhizogoniales. These views are refuted by Bell and Newton (2004), based on an rps4 sequence of Mittenia, and by results reported here, based on four gene sequences. The tree reported here indicates that Mittenia is more closely related to Dicranum and the Grimmiaceae than Orthotrichaceae or basal bryalean mosses. In view of this, the anomalous peristome of Mittenia should not be interpreted as diplolepidous. The results of Bell and Newton (2004) and this study partly supports the interpretations of Stone (1961, 1986) and Shaw (1985), who studied peristomial structure in Mittenia and concluded that the peristome is not diplolepidous, and perhaps more closely related to haplolepidous mosses. The question remains whether Mittenia is closely related to Schistostega, a hypothesis advanced by Stone (1961, 1986). 2.4.2.3 Position of Aulacomnium The finding that Mesochaete represents the sister group to Aulacomnium is remarkable, and was also reported by Bell and Newton (2004). Mesochaete is endemic to eastern Australia, primarily in subtropical climates (Scott and Stone, 1976; Stone, 1983; Streimann and Curnow, 1989), whereas Aulacomnium is widely distributed in the Northern Hemisphere. With the exception of Bell and Newton (2004) and recent studies showing a near relationship of Aulacomnium and other rhizogonian genera (e.g., Cox et al., 2000, 2004), other literature considering the Rhizogoniaceae or Aulacomnium does not directly suggest that these genera are sister groups or even in the same family (e.g., Brotherus, 1924–1925; Scott and Stone, 1976; Churchill and Buck, 1982; Stone, 1983; Vitt, 1984; Koponen, 1988; Withey, 1996; Buck and Goffinet, 2000). However, Mesochaete has sulcate capsules like Aulacomnium, and has several traits similar to A. heterostichum, the sister group to the remaining species of Aulacomnium (O’Brien, 2001). Both Mesochaete and A. heterostichum occur on shaded mineral mesic soils, bear deciduous apical leaves (Crum and Anderson, 1981; Scott and Stone, 1976) and have undulate, oblong-ovate and asymmetrical leaves with smooth cells and coarsely toothed margins. All of these similarities may be taxic homologies. Mesochaete differs considerably in most of these traits from the remaining species of Aulacomnium, which, other than A. heterostichum, have accumulated apomorphies, resulting in most of its species bearing little morphological resemblance to Mesochaete.

2.4.3 PHYLOGENETIC ASYMMETRY CROWN PLEUROCARPS

IN THE

RHIZOGONIAN MOSSES

AND

It is noteworthy that the Hypnidae and hypnodendroid pleurocarps, consisting of approximately 5400 species, have a sister group (or grade) with few extant species — about 1% of the crown group. Clades A, B and C include 13, 23 and 28 species, respectively. This asymmetry is comparable to that of the angiosperm phylogeny (Qiu et al., 1999), in which the speciose crown group, including nearly 249,000 species, arose from a paraphyletic group of basal lineages including about 1000 species. Is such asymmetry unexpected? Guyer and Slowinski (1991), Farris and Kallersjo (1998) and Salisbury (1999) all demonstrated that structured datasets yield a high frequency of strongly asymmetrical trees, an observation that indicates that asymmetry in a phylogenetic tree does not require exceptional explanation from a biological cause. Alternatively, the asymmetry may be due to factors that have either limited the accumulation of species richness in rhizogonian mosses, or enhanced species richness in the crown pleurocarps (for a discussion of the latter, see Shaw et al., 2003). The latter question should be considered in light of morphological transitions compared with phylogeny. In the absence of this, I consider one factor that may have limited the diversity of the rhizogonian mosses. Specialization for substrate preference may be one cause of low diversity in rhizogonian mosses. Within the group, 19 of 34 species and 5 of 11 genera (excluding Orthodontium) have a substrate preference of tree fern trunks (compare ecological descriptions in Scott and Stone, 1976; Churchill and Buck, 1982; Beever, 1984; Koponen et al., 1986; Karttunen and Bäck, 1988; Beever et al.,

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1992; Vitt, 1995; Yano, 1996; and O’Brien, 2000). Tree fern preference is not confined to one of the three rhizogonian clades (A to C) indicated by this study; rather it is distributed over all of them, principally the genera Calomnion, Cryptopodium, Hymenodon, Hymenodontopsis and Leptotheca. Although branch support in the MPT is not sufficient to confidently interpret the phylogenetic pattern of substrate preference, there are two general explanations: (1) tree fern preference is a derived condition within the group and has arisen independently (by parallelism) at least three times; or (2) tree fern preference is the ancestral condition in all rhizogonian mosses, and has been lost one or more times. Regardless of which explanation is correct, substrate preference may offer a clue to the timing of origins of rhizogonian lineages, suggestive of origins of rhizogonian mosses that predate the diversification of the angiosperms.

2.5 CONCLUSIONS The best estimate of phylogeny presented in this chapter provides additional support for clades identified in the phylogenetic analysis of basal pleurocarps by Bell and Newton (2004). The pleurocarps include the hypnodendroid pleurocarps and their diverse sister group, the Hypnidae. The sister group of the hypnodendroid pleurocarps and Hypnidae is a grade of rhizogonian mosses, which include Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium. Monophyly of the rhizogonian mosses is not supported, although low branch support values within the basal clades indicate a need for additional taxon or character sampling to determine their precise relationships. The rhizogonian mosses include both pleurocarpous genera and the non-pleurocarpous genera Aulacomnium, Calomnion and Cryptopodium, Hymenodontopsis, Leptotheca, Orthodontium, Pyrrhobryum and Rhizogonium. These results have implications for studies of diversification, adaptation, disparity, development and genome evolution of the pleurocarpous mosses.

ACKNOWLEDGMENTS This chapter is derived from a Ph.D. thesis completed at the University of California at Berkeley under the supervision of Brent D. Mishler. Manuscripts were improved from comments by Brent, Tom Bruns, William R. Buck, and two anonymous reviewers. I am especially grateful to John Wheeler for his guidance on technical aspects of obtaining DNA sequences, and to Jessica Beever, Dan Norris and Heinar Streimann for providing specimens. Additional specimens or sequences were provided by Bruce Allen, Lewis Anderson, Paul Davison, Terry Hedderson, David Long, Norton Miller, Stuart McDaniel, Brent Mishler, Barbara Murray, Jim Shevock, Dale Vitt and MO. Financial support was provided by a Regents Fellowship from UC-Berkeley and a Graduate Research Fellowship from the Department of Integrative Biology, UC-Berkeley, and Rowan University.

REFERENCES Albert, V. A., Chase, M. W. and Mishler, B. D. (1993) Character-state weighting for cladistic analysis of protein-coding DNA sequences. Annals of the Missouri Botanical Garden, 80: 752–766. Baldwin, B. G., Crawford, D. J., Francisco-Ortega, J., Kim, S.-C., Sang, T. and Stuessy, T. F. (1998) Molecular phylogenetic insights on the origin and evolution of oceanic island plants. In Molecular Systematics of Plants, II: DNA Sequencing (ed. D. E. Soltis, P. S. Soltis and J. J. Doyle). Kluwer Academic Publishers, Dordrecht, pp. 410–441. Beever, J. B. (1984) Moss epiphytes of tree-ferns in a warm-temperate forest. Journal of the Hattori Botanical Laboratory, 56: 89–95. Beever, J., Allison, K. W. and Child, J. (1992) The Mosses of New Zealand. University of Otago Press, Dunedin. Bell, N. E. and Newton, A. E. (2004) Systematic studies of non-hypnanaean pleurocarps: Establishing a phylogenetic framework for investigating origins of pleurocarpy. Monographs in Systematic Botany from the Missouri Botanical Garden, 98: 290–319.

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Bremer, K. (1994) Branch support and tree stability. Cladistics, 10: 295–304. Bremer, B., Jansen, R. K., Oxelman, B., Backlund, M, Lantz, H. and Kim, K. (1999) More characters or more taxa for a robust phylogeny — case study from the coffee family (Rubiaceae). Systematic Biology, 48: 413–435. Brotherus, V. F. (1924–1925) Musci. In Die natürlichen Pflanzenfamilien, Vols. 10, 11, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–478. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Biology of Bryophytes (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL–trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Buck, W. R., Cox, C. J., Shaw, A. J. and Goffinet, B. (2005) Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematic Biodiversity, 2: 121–145. Bull, J. J., Huelsenbeck, J. P., Cunningham, C. W., Swofford, D. L. and Waddell, P. J. (1993) Partitioning and combining data in phylogenetic analysis. Systematic Biology, 42: 384–397. Churchill, S. P. and Buck, W. R. (1982) A taxonomic investigation of Leptotheca (Rhizogoniaceae). Brittonia, 34: 1–11. Cox, C., Goffinet, B., Newton, A. E., Shaw, A. J. and Hedderson, T. A. J. (2000) Phylogenetic relationships among the diplolepidous-alternate mosses (Bryidae) inferred from nuclear and chloroplast DNA sequences. Bryologist, 103: 224–231. Cox, C. J., Goffinet, B., Shaw, A. J. and Boles, S. B. (2004) Phylogenetic relationships among the mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomic compartments. Systematic Botany, 29: 234–250. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (2004) A Checklist of Mosses. Missouri Botanical Garden, St. Louis. Crum, H. and Anderson, L. E. (1981) Mosses of Eastern North America. Columbia University Press, New York. De Luna, E., Newton, A. E., Withey, A., González, D. and Mishler, B. D. (1999) The transition to pleurocarpy: A phylogenetic analysis of the main diplolepidous lineages based on rbcL sequences and morphology. Bryologist, 102: 634–650. De Luna, E., Buck, W. R., Akiyama, H., Arikawa, T., Tsubota, H., Gonzalez, D., Newton, A. E. and Shaw, A. J. (2000) Ordinal phylogeny within the hypnobryalean pleurocarpous mosses inferred from cladistic analyses of three chloroplast DNA sequence data sets: trnL-F, rps4 and rbcL. Bryologist, 103: 242–256. De Queiroz, A., Donoghue, M. J. and Kim, J. (1995) Separate versus combined analysis of phylogenetic evidence. Annual Review of Ecology and Systematics, 26: 657–681. Doyle, J. J. (1997) Trees within trees: Genes and species, molecules and morphology. Systematic Biology, 46: 537–553. Farris, J. S. and Kallersjo, M. (1998) Asymmetry and explanations. Cladistics, 14: 159–166. Fleischer, M. (1904–1923) Die Musci der Flora von Buitenzorg. 4 volumes. E. J. Brill, Leiden. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Goffinet, B., Shaw, J., Anderson, L. E. and Mishler, B. D. (1999) Peristome development in mosses in relation to systematics and evolution. V. Diplolepideae: Orthotrichaceae. Bryologist, 102: 581–594. Goffinet, B., Cox, C. J., Shaw, A. J. and Hedderson, T. A. J. (2001) The Bryophyta (mosses): systematics and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Annals of Botany, 87: 191–208. Griffin, D. I. and Buck, W. R. (1989) Taxonomic and phylogenetic studies on the Bartramiaceae. Bryologist, 92: 368–380. Guyer, C. and Slowinski, J. (1991) Comparisons of observed phylogenetic topologies with null expectations among three monophyletic lineages. Evolution, 39: 609–622. Hedenäs, L. (1994) The basal pleurocarpous diplolepidous mosses: A cladistic approach. Bryologist, 97: 225–243.

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Hedenäs, L. (1999) How important is phylogenetic history in explaining character states in pleurocarpous mosses? Canadian Journal of Botany, 77: 1723–1743. Higgins, D. G. (1994) CLUSTAL V: Multiple alignment of DNA and protein sequences. In Methods in Molecular Biology; Computer Analysis of Sequence Data, Part II (ed. A. M. Griffin and H. G. Griffin). Humana Press, Totowa, pp. 307–318. Hillis, D. M. (1991) Discriminating between phylogenetic signal and random noise in DNA sequences. In Phylogenetic Analysis of DNA Sequences (ed. M. M. Miyamoto and J. Cracraft). Oxford University Press, New York, pp. 278–294. Huelsenbeck, J. P. (1991) Tree-length distribution skewness: An indicator of phylogenetic information. Systematic Zoology, 40: 257–270. Huelsenbeck, J. P., Bull, J. J. and Cunningham, C. W. (1996) Combining data in phylogenetic analysis. Trends in Ecology and Evolution, 11: 152–158. Ignatov, M. S. (1990) Upper Permian mosses from the Russian Platform [USSR]. Palaeontographica Abteilung B Palaeophytologie, 217: 147–190. Johnson, L. A. and Soltis, D. E. (1998) Assessing congruence: Empirical examples from molecular data. In Molecular Systematics of Plants, II: DNA Sequencing (ed. D. E. Soltis, P. S. Soltis and J. J. Doyle). Kluwer Academic Publishers, Dordrecht, pp. 297–348. Karttunen, K. and Bäck, S. (1988) Taxonomy of Hymenodon (Musci, Rhizogoniaceae). Annales Botanici Fennici, 25: 89–96. Kluge, A. G. (1998) Combined evidence or taxonomic congruence: Cladistics or consensus classification. Cladistics, 14: 151–158. Koponen, T. (1988) The phylogeny and classification of Mniaceae and Rhizogoniaceae (Musci). Journal of the Hattori Botanical Laboratory, 64: 37–46. Koponen, T. and Norris, D. H. (1986) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XVII. Grimmiaceae, Racopilaceae and Hedwigiaceae (Musci). Acta Botanica Fennica, 133: 81–106. Koponen, T., Touw, A. and Norris, D. H. (1986b) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XIV. Rhizogoniaceae (Musci). Acta Botanica Fennica, 133: 1–24. La Farge-England, C. (1996) Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99: 170–186. Lewis, L. A., Mishler, B. D. and Vilgalys, R. (1997) Phylogenetic relationships of the liverworts (Hepaticae), a basal embryophyte lineage, inferred from nucleotide sequence data of the chloroplast gene rbcL. Molecular Phylogenetics and Evolution, 7: 377–393. Maddison, D. R. (1991) The discovery and importance of multiple islands of most-parsimonious trees. Systematic Zoology, 40: 315–328. Maddison, W. P. (1997) Gene trees in species trees. Systematic Biology, 46: 523–536. Manuel, M. G. (1980) Miscellanea Bryologica. II. Classification of Rhizogonium Brid., Penzigiella hookeri Gangulee, and some nomina nuda. Cryptogamie Bryologique et Lichénologie, 1: 67–72. Miller, N. G. (1984) Tertiary and Quaternary fossils. In New Manual of Bryology (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 1194–1232. Mishler, B. D. (1994) Cladistic analysis of molecular and morphological data. American Journal of Physical Anthropology, 94: 143–156. Newton, A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Newton, A. E., Cox, C. J., Wheeler, J. A., Goffinet, B., Hedderson, T. A. J. and Mishler, B. D. (2000) Evolution of the major moss lineages: Phylogenetic analyses based on multiple gene sequences and morphology. Bryologist, 103: 187–211. O’Brien, T. J. (2000) A new synonym in Leptotheca Schwägr. (Musci; Rhizogoniaceae). Tropical Bryology, 18: 13–14. O’Brien, T. J. (2001) Systematic and reproductive studies of Aulacomnium Schwägrichen (Musci). Ph.D. thesis, University of California, Berkeley. Qiu, Y.-L., Lee, J., Bernasconi-Quadroni, F., Soltis, D. E., Soltis, P. S., Zanis, M., Zimmer, E. A., Chen, Z., Savolainen, V. and Chase, M. W. (1999) The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes. Nature (London), 402: 404–407. Salisbury, B. A. (1999) Misinformative characters and phylogeny shape. Systematic Biology, 48: 153–169. Scott, G. A. M. and Stone, I. G. (1976) The Mosses of Southern Australia. Academic Press, New York.

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Shaw, A. J. (1985) Peristome structure in the Mitteniales (ord. nov.: Musci), a neglected novelty. Systematic Botany, 10: 224–233. Shaw, A. J. (2000) Phylogeny of the Sphagnopsida based on chloroplast and nuclear DNA sequences. Bryologist, 103: 277–306. Shaw, A. J. and L. E. Anderson. (1986) Morphology and homology of the peristome teeth in Hymenodon and Hymenodontopsis (Rhizogoniaceae: Musci). Systematic Botany, 11: 446–454. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution, 57: 2226–2241. Soltis, D. E., Soltis, P. S., Mort, M. E., Chase, M. W., Savolainin V., Hoot, S. B. and Morton, C. M. (1998) Inferring complex phylogenies using parsimony: An empirical approach using three large DNA data sets for angiosperms. Systematic Biology, 47: 32–42. Souza-Chies, T. T., Bittar, G., Nadot, S., Carter, L., Besin, E. and Lejeune, B. (1997) Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Systematics and Evolution, 204: 109–123. Stone, I. G. (1961) The gametophore and sporophyte of Mittenia plumula (Mitt.) Lindb. Australian Journal of Botany, 9: 124–151. Stone, I. G. (1983) A re-evaluation of the species of Mesochaete Lindb. (Rhizogoniaceae). Journal of Bryology, 12: 351–357. Stone, I. G. (1986) The relationship between Mittenia plumula (Mitt.) Lindb. and Schistostega pennata (Hedw.) Web and Mohr. Journal of Bryology, 14: 301–314. Streimann, H. and Curnow, J. (1989) Catalogue of Mosses of Australia and its External Territories. Australian Government Publishing Service, Canberra. Swofford, D. L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer Associates, Sunderland. Swofford, D. L., Olsen, G. J., Waddell, P. J. and Hillis, D. M. (1996) Phylogenetic inference. In Molecular Systematics, Ed. 2 (ed. D. M. Hillis, C. Moritz and B. K. Mable). Sinauer Associates, Sunderland, pp. 407–514. Taberlet, P., Gielly, L., Pautou, G. and Bouvet, J. (1991) Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Molecular Biology, 17: 1105–1110. Vitt, D. H. (1984) Classification of the Bryopsida. In New Manual of Bryology (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 696–759. Vitt, D. H. (1995) The genus Calomnion (Bryopsida): Taxonomy, phylogeny, and biogeography. Bryologist, 98: 338–358. Waters, D., Goffinet, B., Vitt, D. and Chapman, R. (1996) The systematic affinities of the Calomniaceae (Bryopsida) based on 18S nrDNA nucleotide sequences. American Journal of Botany, 83 (Supplement): 27. Wendell, J. F. and Doyle, J. J. (1998) Phylogenetic incongruence: Window into genome history and molecular evolution. In Molecular Systematics of Plants, II: DNA Sequencing (ed. D. E. S. Soltis, P. S. Soltis and J. J. Doyle). Kluwer Academic Publishers, Dordrecht, pp. 265–296. Withey, A. (1996) Systematic studies of the Spiridentaceae (Musci). Ph.D. dissertation, Duke University, Durham. Yano, O. (1996) Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP. Briófitas, 1: Mniaceae, Rhizogoniaceae, Racopilaceae, Phyllogoniaceae e Leucobryaceae (Bryales). Hoehnea, 23: 81–98.

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in the 3 Pleurocarpy Rhizogoniaceous Grade Neil E. Bell and Angela E. Newton CONTENTS Abstract ............................................................................................................................................41 3.1 Introduction.............................................................................................................................42 3.1.1 Review: Modularity and Branching Hierarchy..........................................................42 3.1.2 Review: Pleurocarpy, Acrocarpy and Cladocarpy .....................................................44 3.2 Materials and Methods ...........................................................................................................45 3.2.1 Observations of Plant Architecture ............................................................................45 3.2.2 Character Optimizations.............................................................................................45 3.3 Results.....................................................................................................................................47 3.3.1 Observations of Plant Architecture ............................................................................47 3.3.1.1 Rhizogonium distichum, Pyrrhobryum paramattense, and Pyrrhobryum spiniforme .............................................................................47 3.3.1.2 Pyrrhobryum dozyanum, Pyrrhobryum mnioides, Mesochaete taxiforme, Spiridens camusii, and Bescherellia elegantissima ...................48 3.3.1.3 Pyrrhobryum bifarium, Pyrrhobryum vallis-gratiae, and Hypnodendron menziesii .............................................................................49 3.3.1.4 Hymenodon sericeus and Hymenodon pilifer .............................................49 3.3.1.5 Hymenodontopsis stresemannii ...................................................................50 3.3.1.6 Goniobryum subbasilare .............................................................................50 3.3.1.7 Typical Hypnalean Pleurocarp....................................................................50 3.3.1.8 Cryptopodium bartramioides, Leptotheca gaudichaudii, Orthodontium lineare, Calomnion complanatum, and Aulacomnium heterostichum .......................................................................50 3.3.2 Character Optimizations.............................................................................................51 3.4 Discussion...............................................................................................................................52 3.4.1 Coding Strategies and Primary Homology ................................................................61 3.4.2 Scenarios.....................................................................................................................61 Acknowledgments ............................................................................................................................63 References ........................................................................................................................................63

ABSTRACT Modular branching structure in exemplars from the rhizogoniaceous grade, identified in recent analyses as representing the earliest diverging pleurocarpous lineages, is examined in order to isolate discrete architectural types associated with the pleurocarpous condition. These are described and used as a basis for optimization of pleurocarpy sensu stricto onto an existing phylogeny derived from chloroplast and mitochondrial molecular sequence data. Characters closely associated

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with pleurocarpy in these taxa are also optimized, and the results used to examine scenarios for the evolution of modular form in the basal pleurocarpous clades. Brief reviews of modular hierarchical concepts and of pleurocarpy are provided in the introduction. The results reveal that there is disproportionate diversity of pleurocarpous architectural types in the rhizogoniaceous grade compared with the hypnodendroid pleurocarps and the Hypnidae, and that these probably represent successive and varied novel adaptive strategies that utilize the potential of the key innovation of pleurocarpy.

3.1 INTRODUCTION Recent molecular phylogenetic analyses place members of the Southern Hemisphere family Rhizogoniaceae, in addition to Aulacomnium, Calomnion, and Orthodontium, as the earliest diverging lineages (henceforth referred to as grade R; see Figure 3.1) in a clade that includes the higher pleurocarps (Bell and Newton, 2004, 2005; O’Brien, Chapter 2 in this volume). The latter occur as two well-supported clades, the subclass Hypnidae and the “hypnodendroid pleurocarps” sensu Bell and Newton (2005). Some members of grade R are acrocarpous. This grade thus spans the transition from acrocarpy to pleurocarpy, to the extent that intermediate states may be retained in extant taxa. Consistent with this, it is also uniquely variable with respect to combinations of states of characters that define or are closely associated with pleurocarpy. The status of individual members of the Rhizogoniaceae as acrocarps, pleurocarps or cladocarps has long been controversial, reflecting both different usage of these terms and different interpretations of morphology (e.g., Buck and Vitt, 1986; Koponen, 1988; Hedenäs, 1994; La Farge-England, 1996; Newton and De Luna, 1999; Buck et al., 2000; Shaw et al., 2003). The situation is further complicated by variation within the Rhizogoniaceae itself, especially as this does not always correspond to generic-level taxonomy. Although Bell and Newton (2004, 2005) saw most of the Rhizogoniaceae as pleurocarpous, other authors (e.g., Shaw et al., 2003) have equated the pleurocarps with the Hypnidae, implying that both the hypnodendroid pleurocarps and the Rhizogoniaceae are non-pleurocarpous. Although this usage to some extent reflects a systematic rather than a morphological view of pleurocarpy, even under La Farge-England’s (1996) restrictive definition, at least the hypnodendroid taxa are morphologically pleurocarpous. While ultimately it is the distribution of character states that is significant, in the case of pleurocarpy character definition is problematic. Due to the highly complex nature of the condition sensu lato, primary homologies (Patterson, 1982) are difficult to assess and many alternative coding strategies are possible. In this study we present detailed observations of branching architecture and perichaetial position for selected taxa within grade R in the context of modern, modular views of gametophyte structure (Mishler and De Luna, 1991; Newton, cited in Mishler and De Luna, 1991, p.150; La FargeEngland, 1996; Newton and De Luna, 1999). The pleurocarpous condition, and associated characters that are highly variable in the earliest diverging pleurocarp lineages, are optimized onto the phylogeny obtained by Bell and Newton (2004). This in turn allows evaluation of potential scenarios for the evolution of pleurocarpy. Due to lack of support for some critical nodes in the topology obtained under the parsimony criterion in Bell and Newton (2004) and conflict between optimal solutions under parsimony and likelihood, the effect of topology on character optimization is explored. Prior to describing these studies, we briefly review current notions of pleurocarpy as well as closely related concepts of modular branching in mosses.

3.1.1 REVIEW: MODULARITY

AND

BRANCHING HIERARCHY

White (1984) used the term “module” to describe the product of any single apical meristem. In moss gametophytes the apical meristem consists of a single apical cell with three or occasionally two “cutting faces.” Each cell produced directly by fission from the apical cell develops into a metamer, a unit eventually consisting of one leaf, tissue forming epidermis and cortex, and often

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FIGURE 3.1 Strict consensus of 24 MPTs based on three-gene molecular dataset as published in Bell and Newton (2004), with significant groups highlighted. Numbers above branches are bootstrap percentages, numbers below are decay indices. Pleurocarpans taxa (sensu Newton and De Luna, 1999) are in small capitals.

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a lateral bud, which has the potential to produce a new apical cell and hence a new module (Mishler and De Luna, 1991). A module is hence a series of metamers, each derived from a discrete cell lineage beginning with a single cell produced by division of the apical cell. Similarly, the leafy part of a gametophyte is a hierarchy of modules, each produced from a lateral bud on an older module (or, in the case of the first module, an apical cell differentiated from protonemal tissue). Any given module is further characterized by a heteroblastic series (Mishler and De Luna, 1991), as metamer morphology varies progressively from the base (produced when the module is immature) to the apex (produced when the module is mature). Historically, some authors (e.g., Argent, 1973) have referred to the branching of mosses in hierarchical terms. The synthesis of this perspective with a modular view of branching architecture led Newton (cited, for example, in Mishler and De Luna, 1991, p. 150) to define hierarchical levels of modularity in terms of differences in heteroblastic series. Hence, if a branch produced from one module has the same metamer morphology and heteroblastic series as its parent, it is of the same level of modularity, while if it has a distinctly different form it is of another level. Modules are thus referred to as “primary,” “secondary,” etc., depending on the position of the forms they exhibit in this hierarchy. Note the distinction between the hierarchy of individual modules that comprise a plant and the hierarchy of levels of modularity. A primary module may give rise to other primary modules, effectively identical in metamer morphology and heteroblastic series. It may also give rise to more than one type of secondary module, each having a discretely different form but each produced from a branch primordium on a primary module. However, there can be only one type of primary module, the form of which is that of the first module. The essence of these ideas appears to have its origin with Newton in the late 1980s in a series of seminars at Duke University and elsewhere and is cited in Mishler and De Luna (1991, p. 150) as personal communication. Although an explicit description has never been published, modular hierarchical concepts are assumed by La Farge-England (1996) and Newton and De Luna (1999).

3.1.2 REVIEW: PLEUROCARPY, ACROCARPY

AND

CLADOCARPY

The terms Acrocarpi and Pleurocarpi were first used by Nees von Esenbeck et al. (1823) to describe mosses that produce perichaetia “terminally” and “laterally,” respectively. All diplolepidous-alternate mosses produce perichaetia terminally on modules. The perception of a group with “lateral” perichaetia mirrors the existence of a large number of species in which perichaetia are produced terminally on specialized, highly reduced secondary modules. This condition is usually associated with a number of indirectly related features, such as a prostrate growth form, elongated thin-walled areolation and indeterminate primary module growth. The term cladocarpy, first used by Bridel (1826–1927), has been used subsequently to refer either to a third condition of perichaetial position or else has been treated as a form of either pleurocarpy (e.g., Mishler and De Luna, 1991) or of acrocarpy (e.g., the character coding of Hedenäs, 1994). Generally it refers to the production of perichaetia terminally on elongated secondary axes. A precise concept of pleurocarpy remained elusive until relatively recently. Buck and Vitt (1986) defined pleurocarpous mosses as those in which “perichaetial development (and hence the sporophyte) is lateral, with growth continuing apically.” Hedenäs (1994) used a more exacting definition: “archegonia on short specialised branches (always with more or less strongly modified perichaetial leaves).” The problem remained, however, that the distinction between pleurocarpy and “cladocarpy” was a matter of degree. La Farge-England (1996) attempted to define pleurocarpy, acrocarpy and cladocarpy in modular terms and to dispel misconceptions based on imprecise or inconsistent terminology. Pleurocarpy was defined as the production of perichaetia “along the primary module or secondary modules at the terminus of lateral innovations that lack subperichaetial branch primordia or developed branches.” In addition, La Farge-England claimed that juvenile leaf development on perichaetial branches was morphologically different from that of vegetative branches and that perichaetial leaf development was “+/- immediate.” In cladocarpy, perichaetia

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were “produced at the terminus of lateral branches (secondary or tertiary modules) that have subperichaetial branch primordia or developed branches,” and juvenile leaf development at the base of fertile branches was “morphologically similar to that of the vegetative branches.” Although La Farge-England’s terminology and diagrams express the modular hierarchical concepts outlined above, she does not explicitly refer to fertile axes in pleurocarps as a type of secondary module but rather calls them “innovations,” restricting the terms “branch” and “module” to the fertile axes of plants she considers to be acrocarpous or cladocarpous. Newton and De Luna (1999) stated explicitly that the fertile axis in pleurocarps is a secondary module, and that all plants in which the fertile axis is a primary module are acrocarps. As with La Farge-England’s model (1996), the complexities lie in distinguishing short branch cladocarpy from pleurocarpy, a distinction that is fairly discrete in nature but problematic in theory. Newton (personal communication) does not consider La Farge-England’s distinction between types of juvenile leaf development to be reliable, and Newton and De Luna (1999) did not accept that the presence of subperichaetial innovations precludes a plant from being pleurocarpous. Branch primordia may occur on the perichaetial modules of Anomodon longifolius and Warnstorfia exannulata (Hedenäs, 1998), and on those of Amblystegium serpens (Newton, personal communication), all unambiguously derived from within the large clade of “true pleurocarps” and having fertile modules that appear pleurocarpous in all other respects. Newton and De Luna (1999) thus distinguished pleurocarpy on the basis of the extent of development of the fertile module and its leaves at the time when the archegonia are produced. All plants in which distinct vegetative leaves are lacking on fertile modules and developing archegonia are “surrounded only by modified juvenile leaves, with the majority of perichaetial leaves developing after fertilisation” are viewed as pleurocarps. In this study, this definition is broadly accepted, and thus taxa in Pyrrhobryum section Pyrrhobryum and Rhizogonium that produce subperichaetial innovations on fertile modules are nonetheless regarded as pleurocarpous.

3.2 MATERIALS AND METHODS 3.2.1 OBSERVATIONS

OF

PLANT ARCHITECTURE

Specimens of selected taxa from grade R in addition to Hypnodendron menziesii were examined in order to determine underlying modular branching structure and to observe other characters directly related to pleurocarpy, such as presence or absence of subperichaetial innovations. For dioicous species observations were primarily of female plants, although male plants were also examined for some taxa. Thoroughly wetted herbarium specimens were carefully dissected under the dissecting microscope. Many species of Rhizogoniaceae produce multiple basal branches that are loosely attached in the mature plant and matted together with dense rhizoidal growth, making observation of branching structures difficult. Extreme care must be exercised in determining branching order in particular. Both reiterative primary modules and secondary fertile modules are often produced in very basal positions, and determining which shoot gives rise to which may be problematic. Several specimens were examined for each taxon, all of which are in the collections at BM. Voucher specimens are provided in Table 3.1.

3.2.2 CHARACTER OPTIMIZATIONS Pleurocarpy/non-pleurocarpy sensu Newton and De Luna (1999) was optimized onto one of the 24 most parsimonious trees (henceforth referred to as tree A) obtained from the molecular analysis in Bell and Newton (2004). In addition, the effects on optimization of using a slightly different topology (tree B), in which Leptotheca gaudichaudii is sister to Orthodontium lineare (as in the maximum likelihood tree in Bell and Newton, 2004), were explored. No other conflicts between topologies obtained under parsimony and likelihood criteria in Bell and Newton (2004) significantly

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TABLE 3.1 Voucher Specimens for Taxa Examined in the Morphological Studies, and for Scoring of Optimized Characters for Taxa in Grade R and the Hypnodendroid Pleurocarp Clade Taxon

Voucher

Aulacomnium androgynum Aulacomnium heterostichum Bescherellia elegantissima Braithwaitea sulcata Calomnion brownseyi Calomnion complanatum Cryptopodium bartramioides Cyrtopus setosus Goniobryum subbasilare Hymenodon pilifer Hymenodon sericeus Hymenodon sphaerothecius Hymenodontopsis stresemannii Hypnodendron comosum Hypnodendron dendroides Hypnodendron diversifolium Hypnodendron menziesii Hypnodendron spininervium Hypnodendron subspininervium Leptotheca gaudichaudii Mesochaete taxiforme Mesochaete undulata Orthodontium lineare Pterobryella praenitens Pyrrhobryum bifarium Pyrrhobryum dozyanum Pyrrhobryum medium Pyrrhobryum mnioides Pyrrhobryum novae-caledoniae Pyrrhobryum paramattense Pyrrhobryum spiniforme Pyrrhobryum vallis-gratiae Racopilum spectabile Rhizogonium distichum Rhizogonium graeffeanum Rhizogonium novae-hollandiae Rhizogonium pennatum Spiridens camusii

Bell, 1299 Schofield, 10196 Bell, 364 Rodway, s.n. Beveridge, s.n. Child, 2301 Child, 2344 Petrie, s.n. Hyvönen, 2786, (H) Weymouth, 2858 Eddy, 4096 Bell, 363 De Sloover, 46.860 Bell, 648 Gardner, 1 Eddy, 1709 Bell, 385 Bell, 601 Eddy, 6671 Child, 5444 Bell, 464 Bell, 500 Child, 1018 Streimann, 55850 (CBG) Child, 5476 Ikegami, s.n. 10/11/1957 Bell, 349 Bell, 698 Bell, 409 Streimann, 4781 Newton, 4341 Hedderson, 13377 Newton, 5351 Child, 3789 Bell, 429 Bell, 633 Bell, 720 Bell, 416

Note: All BM unless otherwise stated.

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alter optimization of the characters examined. Based partially on character concepts developed during the morphological investigations, presence/absence of subperichaetial innovations and position of perichaetial modules were optimized onto a pruned tree B (tree C). Tree C includes only grade R and the higher pleurocarps, thus minimizing optimization problems associated with inapplicable characters in non-pleurocarpous taxa. Tree A was selected on the basis that it is one of the most parsimonious trees (MPTs) in which Pyrrhobryum dozyanum is resolved as sister to P. section Pyrrhobryum, as in the preferred phylogenetic hypothesis of Bell and Newton (2004, Figure 7). Optimizations are unaltered if the alternative position of Pyrrhobryum dozyanum as sister to the larger clade that includes Cryptopodium and Calomnion is assumed. All other MPTs in Bell and Newton (2004) were otherwise identical to tree A within grade R, other than for resolution within Rhizogonium, all exemplars of which share the same states for all optimized characters. As two nodes in the “backbone” of grade R have no bootstrap support (Figure 3.1), the effects of collapsing these branches was tested for all optimizations. In all cases this either had no effect or else it eliminated the potential for existing equivocal optimization to be resolved by the use of ACCTRAN or DELTRAN alone (accelerated and delayed transformation, Swofford and Maddison, 1987). Character optimization was performed using MacClade 4.03 (Maddison and Maddison, 2001). Where it is not indicated that ACCTRAN or DELTRAN resolving options have been used, diagrams summarize any alternative optimizations and show conflict as equivocal. Vouchers for scoring of characters for taxa in grade R and in the hypnodendroid pleurocarp clade are provided in Table 3.1. Taxa in the Hypnidae were assumed to be pleurocarpous with distally produced perichaetial modules and to lack subperichaetial innovations, and taxa outside of the clade that includes grade R and the higher pleurocarps were assumed not to be pleurocarpous. Perichaetial module position and presence/absence of subperichaetial innovations were considered applicable to pleurocarpous taxa only (see discussion).

3.3 RESULTS 3.3.1 OBSERVATIONS

OF

PLANT ARCHITECTURE

Descriptions of modular branching structure and perichaetial position are provided below for taxa examined in detail. Species having an identical or nearly identical modular structure are treated together. Figure 3.2 provides diagrammatic representations of each distinct structural type identified for pleurocarpous taxa (sensu Newton and De Luna, 1999). 3.3.1.1 Rhizogonium distichum, Pyrrhobryum paramattense, and Pyrrhobryum spiniforme See Figure 3.2A. The production of reduced perichaetial modules basally characterizes the genus Rhizogonium and Pyrrhobryum sect. Pyrrhobryum (Manuel, 1980). On careful dissection it is apparent that the primary modules are erect, determinate, vegetative shoots that branch from the base (or extremely close to the base) to produce further primaries. The secondary perichaetial modules are also derived basally from primary modules and are very short with clearly differentiated perichaetial leaves and no normal vegetative leaves. In contrast with most pleurocarps, perichaetial modules may produce innovations giving rise to further perichaetial modules. Hence, these species are pleurocarps sensu Newton and De Luna (1999), but cladocarps under La Farge-England’s (1996) definitions. The possibility that reduced perichaetial modules could be at the primary level of the branching hierarchy was considered, but in none of the plants examined was there convincing evidence of this. Similarly, all innovations produced on perichaetial modules appeared to develop into other perichaetial modules rather than vegetative primary modules (i.e., the sequence of module types is hierarchical and unidirectional). Individual primary modules often produce both perichaetial mod-

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A

D

B

E

Vegetative primary module (determinate)

C

F

G

Pleurocarpous perichaetial module

Pleurocarpous perichaetial module with subperichaetial innovations Vegetative primary module (continuously growing) Vegetative secondary module (determinate)

FIGURE 3.2 Diagrammatic representations of modular architecture types found in pleurocarpous members of the Rhizogoniaceae, Hypnodendron and typical Hypnalean pleurocarps. (A) Rhizogonium type; (B) Pyrrhobryum sect. Bifariella type; (C) Hypnodendron type; (D) Hymenodon type; (E) Hymenodontopsis type; (F) Goniobryum type; (G) typical Hypnalean pleurocarp (e.g., Eurhynchium).

ules and further primary modules from immediately adjacent positions at the extreme base of the stem, and the continued production of upright determinate shoots basally seems to be the principal method of vegetative propagation. All Rhizogoniaceae are dioicous with the exception of Pyrrhobryum spiniforme, which is synoicous. On studying male plants of R. distichum it became apparent that at least some perigonial modules are produced directly from rhizoids, which themselves emerge from the adaxial edge of leaf axils, a condition that is termed “rhizautoicy” in autoicous moss species. Perigonial modules produced in this manner often produced innovations giving rise to other perigonial modules. 3.3.1.2 Pyrrhobryum dozyanum, Pyrrhobryum mnioides, Mesochaete taxiforme, Spiridens camusii, and Bescherellia elegantissima Although some of these plants are very different in habit, size, orientation and general morphology, they are similar or identical in modular terms (Figure 3.2B). According to Manuel (1980), Pyrrhobryum sect. Bifariella is characterized by perichaetia produced “laterally on gametophores” and rhizoids that often form a tomentum extending some distance up the stem. On examination of Pyrrhobryum dozyanum it is apparent that the upright primary modules are determinate and may innovate from positions within a broad central zone on the shoot, giving rise either to further primaries or to perichaetial modules. Primary modules alone may also reiterate basally. Perichaetial

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modules are very short and were not observed to produce subperichaetial innovations. Pyrrhobryum mnioides differs slightly (at least in the Australasian specimens examined) in that branching of primaries from a distinctly basal position was not observed, although as the lower parts of stems are often decomposed this is difficult to confirm. Mesochaete taxiforme, although having a very different morphology and a semiprostrate growth form, is structurally identical to Pyrrhobryum dozyanum, with determinate vegetative primary modules reiterating from both basal and distal positions and highly reduced perichaetial modules produced distally. Spiridens camusii and Bescherellia elegantissima, robust epiphytes with a horizontal to pendulous growth form, also have the same underlying structure. As in Rhizogonium distichum, male plants of P. mnioides were observed to produce innovations on perigonial modules giving rise to further perigonial modules, although modules arising from rhizoids were not observed. 3.3.1.3 Pyrrhobryum bifarium, Pyrrhobryum vallis-gratiae, and Hypnodendron menziesii See Figure 3.2C. Pyrrhobryum bifarium has a similar branching structure to other members of P. section Bifariella with the addition of a distinct second level of vegetative modularity that confers a dendroid or subdendroid morphology. Fully developed primary modules (effectively stipes) are four-angled at the base, with longly decurrent, spirally arranged leaves that become larger further up the stem. Further primary modules may be produced from the base and, occasionally, from a central position. The secondary vegetative modules are very distinct from the primaries in having distichously arranged, asymmetric leaves that are considerably shorter and more ovate than those of the primary module. As in Hypnodendron, the leaf form and orientation of the primary module switches to resemble that of the secondary modules after these are produced. Again, perichaetial modules are short and sessile, originate from an approximately central position and do not appear to produce innovations. P. bifarium is in fact structurally identical to Hypnodendron menziesii (and other Hypnodendron species), although fewer secondary vegetative modules are produced, plants are much smaller and the overall form is more loosely dendroid. In H. menziesii, as in Pyrrhobryum bifarium, primaries may sometimes reiterate distally as well as basally, although this is not the case for all Hypnodendron taxa (Touw, 1971; Bell and Newton, 2005). Pyrrhobryum vallis-gratiae has a similar structure, although the presence of vegetative secondary modules is less clear-cut. Gametophores usually have a fairly dendroid appearance, with a pronounced heteroblastic series on the older shoots (basal leaves on the “stipe” are highly differentiated from those further up the module). The higher vegetative branches are considerably shorter with a much more compact heteroblastic series, although (unlike in P. bifarium) the mature leaf morphology is very close or identical to that of the primary modules. 3.3.1.4 Hymenodon sericeus and Hymenodon pilifer Species of Hymenodon (Figure 3.2D) are often described as innovating basally (e.g., Koponen et al., 1986), implying that their structure is similar or identical to that of Rhizogonium and Pyrrhobryum sect. Pyrrhobryum. If the dense tangle of rhizoids at the base of the stem is dissected, however, it is apparent that primary modules are usually produced from other primaries some distance up the shoot, although they are generally restricted to the lower quarter. By contrast, perichaetial modules appear always to innovate from primaries in a distinctly basal position. Interpretation can be difficult, as often a primary will arise from another primary some distance from the base and immediately give rise to a basal perichaetial module, giving the false impression that a distally produced perichaetial module is innovating to produce a primary module. In none of the specimens examined was there conclusive evidence of any innovations on perichaetial modules, the latter being very short and typically pleurocarpous.

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3.3.1.5 Hymenodontopsis stresemannii The structure of this plant (Figure 3.2E) initially seems similar to that of Hymenodon, although primary modules tend to innovate from other primaries still further from the base. Unlike in Hymenodon, however, perichaetial modules, although generally restricted to the basal portion of the primary, are not distinctly basal. Typically, a primary module will produce a succession of two or three perichaetial modules from the basal region of the shoot before switching over to the production of further primaries higher up. Structurally the plant is like a “stretched out” Hymenodon, with successive branching of primary modules from central positions creating a complicated network of shoots. Most of this structure is usually obscured by the dense felt of rhizoids that clothes the lower parts of the mature plant. This tomentum appears to be produced from the lower parts of primaries, so as new primaries are produced by innovations higher up the gametophore, new rhizoid growth initiated at the bases of the young shoots extends the tomentum further up the plant. 3.3.1.6 Goniobryum subbasilare This species produces upright, determinate primaries that innovate vegetatively from the base, although perichaetial modules are produced slightly further up the shoot (Figure 3.2F). As such, the structure of the plant is in some respects the opposite of that of Hymenodon, in which perichaetial modules are basal and vegetative branching is more distal. Uniquely in the taxa examined that produce fertile modules distally, subperichaetial innovations giving rise to further perichaetial modules were observed in some specimens. 3.3.1.7 Typical Hypnalean Pleurocarp Although the derived forms of pleurocarpy found in the Hypnidae were not formally examined for this study, Figure 3.2G is provided as an illustration of a typical architectural type found in the group (common in the Hypnaceae or Brachytheciaceae, for example). The higher pleurocarps include a great diversity of forms (see Newton, Chapter 14 and Tangney, Chapter 15 in this volume), but many have a structure similar or identical to that shown in Figure 3.2G, in which the primary module is continuously growing and determinate secondary vegetative modules are produced. Often the primary module will also reiterate from an approximately central position, as illustrated here. The continuous growth of the primary is usually associated with a more or less prostrate habit, and if determinate secondaries are regularly initiated, a pinnate morphology results. Many Hypnales (especially those previously classified in the Leucondontales) do not produce determinate secondaries, and branching may be exclusively by the reiteration of primaries. Such plants have traditionally been described as “sympodial,” although this terminology is misleading and lends itself to misapplication. Many so called “monopodial” plants with abundant and obvious determinate secondary branching are actually sympodial, as branching by primary module reiteration also occurs. Some of the earlier diverging Hypnidae (e.g., in the Ptychomniales and Hypopterygiaceae) have determinate primaries and forms similar to some of those found in grade R and the hypnodendroid pleurocarps, although true basal production of perichaetial modules does not occur and subperichaetial innovations are a rare atavism in isolated lineages. 3.3.1.8 Cryptopodium bartramioides, Leptotheca gaudichaudii, Orthodontium lineare, Calomnion complanatum, and Aulacomnium heterostichum All of these plants are acrocarpous and will be considered together, although they represent at least three slightly different modular architectures. All are members of grade R, although only Cryptopodium and Leptotheca are currently classified in the Rhizogoniaceae.

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Cryptopodium is acrocarpous, despite sharing a large number of gametophytic characters with Pyrrhobryum. Some previous authors (e.g., Sainsbury, 1955) have described it as producing perichaetia both “laterally” and terminally. In fact, there is only a single type of module, which in female plants is terminated by a perichaetium. Modules are often moderately short and produce innovations immediately below the perichaetium, such that a succession of modules superficially gives the impression of a single long stem with lateral perichaetia. The “interrupted” look of such “false” stems, caused by large leaves at the top of one module being succeeded by small ones at the base of the next, reveals their true nature. When two innovations are produced from a single module the false stem appears to “branch.” Not all female specimens of Cryptopodium have this “interrupted false stem” habit, some having individual modules that are more elongated. Male plants have a more conventional acrocarpous habit and consist of modules that are considerably elongated. In Leptotheca, fertile female primary modules branch to give rise to further primaries from immediately underneath the perichaetium. There are usually several new branches initiated from the apex of each mature primary module, these being fairly elongated. Branching is also common from a central position on the primary module, with a clear distinction between the two alternative points of origin. The initiation of apically derived branches is clearly associated with the termination of parent module growth. Calomnion complanatum appears to have the simplest modular structure possible, consisting only of unbranched primary modules producing terminal perichaetia when mature. Often, many individual stems grow closely together and may be matted with rhizoids and/or protonemata at their extreme bases. This, in combination with the very small size of the plants, makes it difficult to exclude the possibility that modules may reiterate from the extreme base, although in none of the stems examined did this appear to be the case. The separate male plants have a similar structure, producing perigonia terminally on unbranched stems. The heteroblastic series is clearly different, however, with leaves very distantly inserted and not obviously distichous and heteromorphous as in female plants. Aulacomnium heterostichum appears to consist of a single type of module, often moderately short, that branches fairly extensively. While modules are often fertile, many others within an individual plant may be sterile. As fertile and nonfertile modules seem otherwise identical and appear fairly random in their relationships to each other, it is assumed that they represent the same type of module. Orthodontium is an unusual plant with unique features. Apparently an acrocarp, many modules are moderately to very short and appear to reiterate. In addition, vegetative, reduced perichaetial and perigonial modules may be derived from stem epidermal cells. These give rise to highly shortened rhizoids that produce a small cluster of cells, one of which will differentiate into an apical cell and produce a short branch. This branch remains loosely attached to the parent module via the short rhizoid and may produce innovations. This form of module production cannot be fitted easily into concepts of module hierarchy, as it involves the production of axes by a method other than branch primordia. The mechanism may be homologous with that of “rhizautoicy,” although it may give rise to perichaetial and vegetative modules in addition to perigonial ones. More study is required to establish homologies between modules produced in this manner by Orthodontium and those derived from normal branching mechanisms in mosses.

3.3.2 CHARACTER OPTIMIZATIONS Figure 3.3A shows the result of optimizing presence or absence of pleurocarpy sensu Newton and De Luna (1999) onto tree A. Pleurocarpy is shown to be independently derived in Hymenodon and in the ancestral lineage of the clade that includes the remainder of grade R and the higher pleurocarps. Aulacomnium (as represented by A. androgynum) and the Calomnion–Cryptopodium clade represent reversals to acrocarpy. Optimizing the same character onto tree B, however, in which Leptotheca gaudichaudii and Orthodontium lineare are assumed to be sisters, produces an ambiguous result for the origin of pleurocarpy with different solutions under ACCTRAN and

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DELTRAN. Under DELTRAN, favouring parallelisms at the expense of reversals, the result is identical to that shown in Figure 3.3A. Under ACCTRAN, there is a single origin of pleurocarpy at the base of grade R and the Leptotheca–Orthodontium clade represents an additional reversal to acrocarpy (Figure 3.3B). The result of optimizing the presence or absence of pleurocarpous subperichaetial innovations onto tree C is shown in Figure 3.4. The character is shown as derived from within grade R, either once, at the base of the clade that includes Rhizogonium, Pyrrhobryum sect. Pyrrhobryum, Goniobryum subbasilare, Pyrrhobryum dozyanum, Cryptopodium and Calomnion (ACCTRAN, Figure 3.4A), or else independently in Pyrrhobryum sect. Pyrrhobryum and the Rhizogonium–Goniobryum clade (DELTRAN, Figure 3.4B). The result is the same if Leptotheca is assumed to be sister to Hymenodon, as in tree A. Thus, if pleurocarpy is assumed to have a single origin (Figure 3.3B), then subperichaetial innovations are derived, either once or twice, from ancestors that were pleurocarpous but lacked them. If pleurocarpy has two origins (Figure 3.3A), then it may be hypothesized, although only under ACCTRAN (Figure 3.4A), that the form of pleurocarpy independently derived in the major pleurocarpous clade was primitively associated with the presence of subperichaetial innovations. Figure 3.5 shows optimization of pleurocarpous perichaetial module position onto tree C. Under ACCTRAN (Figure 3.5A), the production of perichaetial modules distally on primaries (the state found in all higher pleurocarps) is synapomorphic for the clade that includes all pleurocarps except Hymenodon. Both Rhizogonium and Pyrrhobryum sect. Pyrrhobryum represent independent reversals to basal production of perichaetial modules. As the character is only applicable to pleurocarpous taxa and states dichotomize basally, the condition at the ancestral node of grade R remains ambiguous. Under delayed transformation (Figure 3.5B), this ambiguity perpetuates to more distal branches, and the condition of all deeper nodes outside of the clade that includes Mesochaete, most of Pyrrhobryum sect. Bifariella and the higher pleurocarps cannot be unambiguously reconstructed. Under DELTRAN, therefore, the character must be polarized in order for optimization to be meaningful. Figure 3.6 shows the results of optimizing perichaetial module position onto tree C under DELTRAN, with the character alternatively polarized by the addition of an artificial root to assume that either distal (Figure 3.6A) or basal (Figure 3.6B) module position is primitive. In the former case, basal perichaetial module production is independently derived three times in Rhizogonium, Pyrrhobryum sect. Pyrrhobryum and Hymenodon. If basal module production is plesiomorphic (Figure 3.6B), then the equally parsimonious scenario of an independent origin of distal module production in Pyrrhobryum dozyanum, Goniobryum subbasilare and the clade that includes Mesochaete, most of Pyrrhobryum sect. Bifariella and the higher pleurocarps must be assumed. Polarization does not affect ACCTRAN optimization other than to determine the state of the basal node, and thus which branch of the initial dichotomy is apomorphic. None of these optimizations are altered if Leptotheca is assumed to be sister to Hymenodon, as in Figure 3.3A.

3.4 DISCUSSION The results demonstrate that the pleurocarpous taxa currently classified in the Rhizogoniaceae represent a number of distinctly different architectures that exploit the key innovation of pleurocarpy sensu stricto, i.e., the production of perichaetia on specialized, highly reduced secondary modules. These take the form of alternative combinations of secondary pleurocarpous traits, such as position of fertile modules, form and position of vegetative branching, and presence or absence of subperichaetial innovations. By contrast, the Hypnidae and the hypnodendroid pleurocarps are relatively conservative in terms of pleurocarpous architecture, being based on a much more restricted range of fundamental modular structures. Optimization of pleurocarpy and associated traits onto current

FIGURE 3.3 (A) Optimization of pleurocarpy/non-pleurocarpy onto tree A.

A Non-Pleurocarpous Pleurocarpous

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare Hedwigia ciliata Rhacocarpus purpurascens Bartramia halleriana Philonotis fontana Pohlia nutans Mnium hornum Plagiomnium Bryumalpinum Ulota crispa Dicranum scoparium Schistostega pennata Funaria hygrometrica

Continued. Pleurocarpy in the Rhizogoniaceous Grade

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Non-Pleurocarpous Pleurocarpous

ACCTRAN

FIGURE 3.3 (B) Optimization of pleurocarpy/non-pleurocarpy onto tree B under accelerated transformation (ACCTRAN).

B

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare Hedwigia ciliata Rhacocarpus purpurascens Bartramia halleriana Philonotis fontana Pohlia nutans Mnium hornum Plagiomnium Bryumalpinum Ulota crispa Dicranum scoparium Schistostega pennata Funaria hygrometrica

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Subpericaetial innovations on pleurocarpous perichaetial modules

FIGURE 3.4 Optimization of presence/absence of subperichaetial innovations on pleurocarpous perichaetial modules onto tree C. (A) Under accelerated transformation (ACCTRAN). Continued.

A Subpericaetial innovations on pleurocarpous perichaetial modules not observed

ACCTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

Pleurocarpy in the Rhizogoniaceous Grade

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Subpericaetial innovations on pleurocarpous perichaetial modules

FIGURE 3.4 Optimization of presence/absence of subperichaetial innovations on pleurocarpous perichaetial modules onto tree C. (B) under delayed transformation (DELTRAN).

B Subpericaetial innovations on pleurocarpous perichaetial modules not observed

ACCTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

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Equivocal

Pleurocarpous perichaetial modules produced distally

FIGURE 3.5 Optimization of perichaetial module position onto tree C. (A) Under accelerated transformation (ACCTRAN).

A Pleurocarpous perichaetial modules produced basally

ACCTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

Continued. Pleurocarpy in the Rhizogoniaceous Grade

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Equivocal

FIGURE 3.5 Optimization of perichaetial module position onto tree C. (B) under delayed transformation (DELTRAN).

B Pleurocarpous perichaetial modules produced distally

Pleurocarpous perichaetial modules produced basally

DELTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

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Pleurocarpous perichaetial modules produced distally

FIGURE 3.6 Optimization of perichaetial module position onto tree C under delayed transformation (DELTRAN). (A) Distally produced perichaetial modules assumed to be plesiomorphic. Continued.

A Pleurocarpous perichaetial modules produced basally

DELTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare ROOT

Pleurocarpy in the Rhizogoniaceous Grade

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Pleurocarpous perichaetial modules produced distally

FIGURE 3.6 Optimization of perichaetial module position onto tree C under delayed transformation (DELTRAN). (B) basally produced perichaetial modules assumed to be plesiomorphic.

B Pleurocarpous perichaetial modules produced basally

DELTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare ROOT

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hypotheses of phylogeny reveals a limited set of alternative evolutionary scenarios for the initial development of pleurocarpy within grade R.

3.4.1 CODING STRATEGIES

AND

PRIMARY HOMOLOGY

Due to the close association between characters such as, for example, extreme reduction of perichaetial modules and lack of subperichaetial innovations, there are several different ways in which characters relating to pleurocarpy may be coded, and character definitions may carry assumptions of primary homology that require justification. When optimizing characters onto a preexisting phylogeny, however, the effects of different coding strategies are more transparent than in phylogeny reconstruction. Also, as coded here, position of perichaetial modules and the presence or absence of subperichaetial innovations are properties of pleurocarpous fertile modules that are not applicable to acrocarps, and hence are subject to theoretical problems associated with missing data in phylogeny reconstruction (Maddison, 1993; Hawkins et al., 1997; Lee and Bryant, 1999; Strong and Lipscomb, 1999). The presence or absence of subperichaetial innovations on pleurocarpous fertile modules might be considered equally applicable to non-pleurocarpous fertile modules. As perichaetial branches in pleurocarps are secondary modules, however, it is not clear whether innovations could be considered homologous to those on acrocarpous primary modules. More significantly, due to the highly reduced nature of pleurocarpous perichaetial modules, it is not possible to state whether innovations are apical (i.e., truly subperichaetial, initiated in association with module growth termination), basal or nonspecific, and thus they cannot be homologized with, for example, subperichaetial innovations in cladocarps. Similarly, in the case of position of perichaetial module production on the primary module, given the highly specialized form and function of the pleurocarpous perichaetial module it is questionable if this character could be identified with the position of the elongated fertile module in cladocarps. An alternative coding strategy would be to treat one or more of the various forms of pleurocarpy found in grade R as separate states of a single character in which acrocarpy and “conventional pleurocarpy” were also states. This would inappropriately link characters that appear to vary independently, however, such as pleurocarpy sensu stricto and production of subperichaetial innovations. The result would be a highly artificial character with a large number of states, in which transformational independence would be compromised (Lee and Bryant, 1999).

3.4.2 SCENARIOS Conflict between optimizations, especially under accelerated versus delayed transformation, as well as sensitivity to topological uncertainty, result in more than one equally plausible scenario for the early evolution of pleurocarpy. Rather than adopt a universal preference for, say ACCTRAN over DELTRAN a priori, it is useful to examine conflicting scenarios individually in the light of the nature of the morphological transformations they require. The results are consistent with pleurocarpy sensu stricto either being independently derived in Hymenodon or having a single origin at the base of grade R (Figures 3.3A and 3.3B). The single origin hypothesis requires that the acrocarpous Leptotheca gaudichaudii not be sister to Hymenodon. This is at odds with the most parsimonious tree in Bell and Newton (2004) but not with their maximum likelihood tree, and there is no support for the clade with Hymenodon and Leptotheca under parsimony. Furthermore, although the optimization algorithms favour loss and gain of characters equally, it is clearly more plausible to assume a single loss of pleurocarpy in a hypothetical Leptotheca–Orthodontium clade than the independent origin of such a distinctive key innovation in two closely related taxa, especially as other reversals to acrocarpy are known to occur elsewhere within grade R. Arguably, this may be true even if the most parsimonious topology is preferred

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and a single extra step assumed. Thus, it is hypothesized that pleurocarpy sensu Newton and De Luna (1999) is a synapomorphy for the clade that includes grade R and all higher pleurocarps. Assuming the above, the plesiomorphic form of pleurocarpy is characterized by a lack of subperichaetial innovations on fertile modules (Figure 3.4), which is the state found in nearly all of the higher pleurocarps. The production of subperichaetial innovations giving rise to further perichaetial modules is an adaptation found in a small number of early diverging pleurocarpous lineages, and is either a synapomorphy for the clade that includes Rhizogonium and Pyrrhobryum sect. Pyrrhobryum, or a parallelism in Pyrrhobryum sect. Pyrrhobryum and the Goniobryum–Rhizogonium clade (Figure 3.4). Pleurocarpy potentially confers a competitive advantage by decoupling vegetative growth and sporophyte production. Whereas acrocarps and cladocarps must invest time and physical resources in producing an elongated leafy shoot for each perichaetium, pleurocarps may produce many perichaetia for an equivalent investment in vegetative growth. Where perichaetial modules are exclusively basal, however, physical space on the primary module and/or availability of branch primordia may be limiting factors in the number of perichaetia that may be produced. Reiteration by means of subperichaetial innovations circumvents this problem, just as reiteration of vegetative modules basally circumvents limitations on horizontal propagation imposed by an upright, tufted habit. It therefore seems plausible that subperichaetial innovations could be an adaptive response to the limitations inherent in the production of pleurocarpous perichaetial modules in an exclusively basal position. Conflict between ACCTRAN and DELTRAN optimizations of this character derives from the anomalous position of Pyrrhobryum dozyanum, a member of Pyrrhobryum sect. Bifariella having distinctly distal perichaetial modules that lack innovations. The position of this taxon as well as that of Goniobryum, in which perichaetial modules are distal but subperichaetial innovations are sometimes present, also confounds optimization of the character representing perichaetial module position. Although the earliest diverging pleurocarpous lineage, Hymenodon, produces perichaetial modules basally, only under DELTRAN optimization is it most parsimonious to assume that this state is plesiomorphic in the clade that includes the rest of the pleurocarps (Figures 3.5 and 3.6). Furthermore, this is ambiguous unless the character is artificially polarized (Figure 3.6). Of the available scenarios for the evolution of this character, the least credible is that deriving from DELTRAN optimization where distal modules are assumed to be primitive (Figure 3.6A). This would require three independent origins of basal perichaetial modules from ancestors with distal modules, unlikely given that basally produced fertile modules are unique to the Rhizogoniaceae and appear never to have arisen among the higher pleurocarps. More plausible is that the first pleurocarpous mosses produced perichaetial modules basally, and that either (1) distal modules arose in the ancestor of the clade that includes Rhizogonium and the higher pleurocarps with reversals to basal module production in Rhizogonium and Pyrrhobryum sect. Pyrrhobryum (Figure 3.5A), or (2) there were three independent origins of distal modules, in the clade that includes Mesochaete and the higher pleurocarps, in Pyrrhobryum dozyanum and in Goniobryum (Figure 3.6B). As distal perichaetial module production appears to be a highly successful strategy, as witnessed by the large number of species in the Hypnidae, the latter scenario is marginally preferable. Bringing all of these strands together, a general hypothesis can be proposed, in which there is a single origin of pleurocarpy associated with highly reduced basal perichaetial modules that lack subperichaetial innovations in the ancestral lineage of grade R and the higher pleurocarps. Having developed from acrocarps or cladocarps, these plants would have been adapted in a number of different ways to an upright or tufted existence with determinate primary module growth, even if pleurocarpy theoretically permitted continuous growth of vegetative modules. Basal production of pleurocarpous fertile modules would confer an advantage in terms of maximizing sporophyte production, although this would be limited by availability of primordia at the base of the primary module. In the Rhizogonium–Pyrrhobryum sect. Pyrrhobryum clade, subperichaetial innovations developed as an adaptive strategy for further maximizing sporophyte production, one particularly

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suited to the tufted pleurocarpous growth form. This was usually associated with exclusively basal vegetative module reiteration and often with a preference for terrestrial substrates or dead wood. An alternative strategy, involving acquisition of the ability to produce pleurocarpous perichaetial modules in nonbasal positions, probably developed independently in the ancestor of the clade that includes Mesochaete and the higher pleurocarps, in Pyrrhobryum dozyanum and in Goniobryum. Usually associated with this was the development of distal reiteration of primary modules and in some cases production of vegetative secondary modules, although with the retention of distinctly basal vegetative reiteration. Pyrrhobryum dozyanum may, like the common ancestor of the Mesochaete–higher pleurocarp clade, have evolved from a lineage that had not developed subperichaetial innovations, or it may have lost them in response to the acquisition of distal module production. In Goniobryum this structural type is not fully developed, with perichaetial modules usually produced on the lower sections of primaries, subperichaetial innovations retained and distal vegetative branching not present. This form of pleurocarpous architecture (Figure 3.2B, C and E), i.e., an upright or horizontal to pendulous, determinate growth form coupled with distal perichaetial module production and vegetative reiteration from distal and usually also basal positions, is remarkably successful and characterizes most of the earlier pleurocarpous lineages, including many of the earliest diverging Hypnidae, such as the Ptychomniaceae and the Hypopterygiaceae (although the primary module in Hypopterygium is initially stoloniferous; Kruijer, 2002). It perhaps finds its ultimate expression in the large dendroid mosses of the Hypopterygiaceae and the hypnodendroid pleurocarps. A subsequent novel architectural exploitation of the potential offered by pleurocarpy was the abandonment of forms based on determinate vegetative growth in favour of a prostrate, creeping habit with continuous primary module growth and often extensive secondary vegetative branching. This occurred independently in the Racopilaceae (Bell and Newton, 2005) and in the higher Hypnidae and is outside the scope of this study. Although this architecture is often regarded as characteristic of pleurocarpy (e.g., Buck et al., 2000), it is better seen as the latest and most successful in a line of adaptive strategies based on pleurocarpy sensu stricto, and the one that is most removed from the constraints of plesiomorphic acrocarpous forms.

ACKNOWLEDGMENTS The majority of the work for this study was conducted as part of the lead author’s Ph.D. research at the Natural History Museum (NHM), London and the Department of Plant Sciences at the University of Reading, funded by the Botany Department at the NHM. Production of the published version of the manuscript took place at the Botanical Museum of the University of Helsinki and was funded by the Academy of Finland, initially under Jaakko Hyvönen’s “Bryosphere” project (No. 50620) and latterly the project (No. 108629) “Polytrichales: towards a modern phylogenetic monograph and the development of a model of sporophyte evolution”.

REFERENCES Argent, G. C. G. (1973) A taxonomic study of African Pterobryaceae and Meteoriaceae. Journal of Bryology, 7: 353–378. Bell, N. E. and Newton, A. E. (2004) Systematic studies of non-hypnanean pleurocarps: Establishing a phylogenetic framework for investigating the origins of pleurocarpy. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 290–319. Bell, N. E. and Newton, A. E. (2005) The paraphyly of Hypnodendron and the phylogeny of related nonhypnanaean pleurocarpous mosses inferred from chloroplast and mitochondrial sequence data. Systematic Botany, 30: 34–51.

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Bridel, S. E. (1826–1927) Bryologia universa seu Systematica ad Novam Methodum Dispositio, Historia et Descriptio omnium Muscorum Frondosorum Hucusque cognitorum cum Synonymia ex Auctoribus Probatissimis. Vols. 1, 2. J. A. Bartholomew, Leipzig. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL-trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Hawkins, J. A., Hughes, C. E and Scotland, R. W. (1997) Primary homology assessment, characters and character states. Cladistics, 13: 275–283. Hedenäs, L. (1994) The basal pleurocarpous diplolepidous mosses — A cladistic approach. Bryologist, 97: 225–243. Hedenäs, L. (1998) Cladistic studies on pleurocarpous mosses: Research needs, and use of results. In Bryology for the Twenty-First Century (ed. J. Bates, N. Ashton and J. Duckett). Maney Publishing and the British Bryological Society, Leeds, pp. 125–141. Koponen, T. (1988) The phylogeny and classification of Mniaceae and Rhizogoniaceae. Journal of the Hattori Botanical Laboratory, 64: 37–46. Koponen, T., Touw, A. and Norris, D. H. (1986) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XIV. Rhizogoniaceae (Musci). Acta Botanica Fennica, 133: 1–24. Kruijer, H. (2002) Hypopterygiaceae of the world. Blumea, Supplement 13: 1–388. La Farge-England, C. (1996) Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99: 170–186. Lee, D. and Bryant, H. N. (1999) A reconsideration of the coding of inapplicable characters: Assumptions and problems. Cladistics, 15: 373–378. Maddison, D. R. and Maddison, W. P. (2001) MacClade 4: Analysis of Phylogeny and Character Evolution, Version 4.03. Sinauer Associates, Sunderland, Massachusetts. Maddison, W. P. (1993) Missing data versus missing characters in phylogenetic analysis. Systematic Biology, 42: 576–581. Manuel, M. G. (1980) Miscellanea bryologica. II. Classification of Rhizogonium Brid., Penzigiella hookeri Gangulee, and some nomina nuda. Cryptogamie: Bryologie, Lichenologie, 1: 67–72. Mishler, B. D. and De Luna, E. (1991) The use of ontogenetic data in phylogenetic analyses of mosses. Advances in Bryology, 4: 121–167. Nees von Esenbeck, C. G., Hornschuch, F. and Sturm, J. (1823) Bryologia germanica, oder Beschreibung der in Deutschland und in der Schweiz wachsenden Laubmoose. J. Sturm, Nürnberg. Newton, A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Patterson, C. (1982) Morphological characters and homology. In Problems of Phylogenetic Reconstruction (ed. K. Joysey and A. Friday). Academic Press, London, pp. 21–74. Sainsbury, G. O. K. (1955) A handbook of the New Zealand mosses. Royal Society of New Zealand Bulletin, 5: 1–490. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution, 57: 2226–2241. Strong, E. E. and Lipscomb, D. (1999) Character coding and inapplicable data. Cladistics, 15: 363–371. Swofford, D. L. and Maddison, W. P. (1987) Reconstructing ancestral character states under Wagner parsimony. Mathematical Biosciences, 87: 199–229. Touw, A. (1971) A taxonomic revision of the Hypnodendraceae (Musci). Blumea, 19: 211–354. White, J. (1984) Plant metamerism. In Perspectives on Plant Population Ecology (ed. R. Dirzo and J. Sarukhán). Sinauer Associates, Sunderland, Massachusetts, pp. 15–47.

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of the 4 Reevaluation Phylogeny of the Hypopterygiaceae (Bryophyta) Based on Morphological and Molecular Data Hans (J.D.) Kruijer and Rolf Blöcher CONTENTS Abstract ............................................................................................................................................65 4.1 Introduction.............................................................................................................................66 4.2 Historical Background............................................................................................................70 4.3 Reevaluation of the Phylogeny ..............................................................................................81 4.3.1 Taxon and DNA Sampling .........................................................................................81 4.3.2 Phylogenetic Analyses................................................................................................86 4.4 Results.....................................................................................................................................94 4.5 Discussion...............................................................................................................................99 4.5.1 Clade Composition and Character State Evolution ...................................................99 4.5.2 Evolution of Morphological Characters...................................................................103 4.5.3 Systematic Implications............................................................................................104 Acknowledgments ..........................................................................................................................106 References ......................................................................................................................................106

ABSTRACT The pleurocarpous moss family Hypopterygiaceae comprises 21 species distributed among 7 or 8 genera. This chapter gives an overview of systematic studies in the family and presents a phylogenetic study on the relationships within the family using a combination of morphological and molecular data (rps4 gene and trnL–trnF region of cpDNA, ITS2 of nr ribosomal DNA; 15 species of Hypopterygiaceae and 9 species of related families). The results lend support to the monophyly of the Hypopterygiaceae and indicate that Catharomnion and Canalohypopterygium, the Lopidium species, and Dendrocyathophorum and Cyathophorum africanum form well-supported monophyletic clades, that Cyathophorum and Dendrohypopterygium s. lat. are polyphyletic, and that Cyathophorum hookerianum is nested in a Hypopterygium grade. The high amount of homoplasy indicates that a new view on morphology is necessary for understanding evolutionary history. A different generic classification of the Hypopterygiaceae is nearing, but a final decision awaits more data.

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FIGURE 4.1 Colony of Dendrohypopterygium arbuscula (Brid.) Kruijer growing in a moist and shaded habitat on the forest floor of a native forest between Petrohué and Cayutué at Lago Todos los Santos, Llanquihue Province, Chile. (Photograph by permission of Hans Kruijer.)

4.1 INTRODUCTION The Hypopterygiaceae Mitt. are a family of usually attractive pleurocarpous mosses of humid, temperate to tropical forests of, in particular, the Southern Hemisphere (Figure 4.1). The family has a mainly Gondwanic distribution. The highest diversity is found in Indo-Malaysia and Australasia; occurrences in subtropical and temperate areas of the Northern Hemisphere are restricted to the Indian subcontinent, the Pacific Rim, Central America, and the Caribbean. The family is morphologically well defined and characterized by the following combination of character states: (1) a distally or entirely complanate foliate shoot axis, (2) a dorsi-ventrally oriented, three-ranked leaf arrangement in the parts of shoot axes with complanate foliation, where (3) the leaves are arranged in two rows of asymmetrical lateral leaves and one ventral row of smaller symmetrical amphigastria (“heterophylly”, Figure 4.2). The family Hypopterygiaceae was revised recently by Kruijer (2002) and comprises 21 species distributed among 7 or 8 genera: Canalohypopterygium W. Frey and Schaepe, Catharomnion Hook. f. and Wilson, Cyathophorum P. Beauv., Dendrocyathophorum Dixon, Hypopterygium Brid., Lopidium Hook. f. and Wilson, and Dendrohypopterygium Kruijer, of which Arbusculohypopterygium Stech, T. Pfeiffer, and W. Frey has been split off (Stech et al., 2002). The splitting of Dendrohypopterygium s. lat. is one of the subjects of this study and, for reasons of clarity, we follow Kruijer’s (2002) circumscription of Dendrohypopterygium unless otherwise indicated. Since the 1970s, and especially the last decade of the twentieth century, the Hypopterygiaceae have received special attention from bryologists (below), including the authors of this chapter. This interest may partly be explained by the beauty of the plants, but from a scientific point of view it is in particular the family’s predominantly Gondwanic distribution and its probably late Mesozoic Gondwanic origin (e.g., Kruijer, 2002) combined with the high amount of morphological diversity (Figures 4.3 to 4.6) that attracts the attention. Since Blöcher (the second author) started a molecular study on Hypopterygiaceae in 1999 as part of his master’s degree study in biology under the supervision of Ingrid Capesius (Ruprecht-Karls Universität Heidelberg), he has developed a great interest in the phylogeny of the family and he continued to do molecular work on this family during his PhD study in the Bryology Department of the Nees Institute for Biodiversity of Plants at the University of Bonn. Kruijer (the first author) has been hooked on Hypopterygiaceae since 1989,

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FIGURE 4.2 Leaf arrangement in Cyathophorum bulbosum (Hedw.) Müll. Hal. (ventral view). Epiphytic plant from densely shaded, living roots of a tree near a streamlet in remnant of native forest, White Pine Bush, Hawke’s Bay, North Island, New Zealand (Van Zanten 73.12.68, GRO). (Photograph courtesy and by permission of Ben van Zanten.)

FIGURE 4.3 Colony of Hypopterygium tamarisci (Sw.) Brid. ex Müll. Hal. growing on a piece of lava boulder on a balcony in Leiden, the Netherlands. (Photograph courtesy and by permission of Cris Hesse and Hans Kruijer.)

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FIGURE 4.4 Colony of Lopidium concinnum (W. Hook) Wilson growing in a shaded and moist habitat on a small tree in native forest at Punta Huano, Lago Todos los Santos, Llanquihue Province, Chile (Van Zanten & Kruijer 86.01.987, GRO). (Photograph courtesy and by permission of Ben van Zanten.)

FIGURE 4.5 Colony of Cyathophorum bulbosum (Hedw.) Müll. Hal. growing on densely shaded roots in a native forest near Lake Mahinapoua, Westland, South Island, New Zealand (Van Zanten 74.02.886, GRO). (Photograph courtesy and by permission of Ben van Zanten.)

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A B 1 mm 1 cm

E

C D 1 mm 1 mm 1 mm

FIGURE 4.6 Habit variation in Hypopterygiaceae, examples from dendroid to simple. (A) Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Hamlin 2266, WELT); (B) Hypopterygium didictyon Mull. Hal. (Streimann 51282, L); (C) Lopidium concinnum (W. Hook) Wilson (dorsal view, Telford 4207, L); (D) Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (dorsal view, Meijer B7598, L); and (E) Cyathophorum africanum Dixon (ventral view, Pócs & Harris 6158/B, L). (From Kruijer, J.D. (H.), Blumea Supplement, 13: 106, 147, 257, 286 and 332, 2002. With permission. Drawings by Joop Wessendorp.)

when, in what is now the Leiden University branch of the Nationaal Herbarium Nederland (NHN), he started his PhD study preparing a systematic revision of the Hypopterygiaceae based on morphological data and cladistic analyses — a few years before molecular techniques became widely used in systematic studies (cf. Hedenäs, Chapter 12 in this volume). In this chapter, we joined our skills in order to present a “total evidence” phylogeny of the Hypopterygiaceae, based on our DNA sequences and morphological data. We intend to demonstrate why the Hypopterygiaceae, despite the low number of species, are a moss family of special systematic interest and include an overview of the systematic studies on Hypopterygiaceae, performed by us and other bryologists, such as the researchers in Wolfgang Frey’s research group at the Freie Universität Berlin (e.g., Frey et al., 1999; Pfeiffer, 2000; Pfeiffer et al., 2000; Stech et al., 1999), and the significant progress that has been made in unravelling the systematics of the family.

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Other Genera

Cyathophorum

Cyathophorella

Dendrocyathophorum

Hypopterygium

Lopidium

Canalohypopterygium

Catharomnion

TABLE 4.1 Schematic Overview of Nineteenth and Early Twentieth Century Classifications of Hypopterygiaceae Mitt. sensu Kruijer (2002) by Various Authors

Bridel (1827)

Hypopterygiaceae

Hypopterygiaceae + R.

Müller (1851)

Hypopterygiaceae

Hypopterygiaceae + R. & H.

Wilson (1855)

Hypopterygiaceae

Mitten (1859)

Hypopterygiaceae

Hypopt. Hypopterygiaceae

Jaeger (1876)

Hypopterygiaceae

Kindberg (1898, 1899, 1900)

Hypopterygiaceae

Cyathophoraceae

Brotherus (1907)

Hypopterygiaceae

Hypopterygiaceae

Fleischer (1908)

Hypopterygiaceae

Hypopterygiaceae

Brotherus (1925)

Hypopterygiaceae

Hypopterygiaceae + R. & S.

Hypopterygiaceae

Note: R. = Racopilum P. Beauv.; H. = Helicophyllum Brid.; S. = Schimperobryum Margad. Cells with grey background refer to classification in, respectively, the Cyathophoraceae Kindb. or the subfamilial inclusion of this taxon within the Hypopterygiaceae.

4.2 HISTORICAL BACKGROUND The Hypopterygiaceae are nested in the core of the pleurocarpous mosses, i.e., the superorder Hypnanae W.R. Buck et al. (Buck and Goffinet, 2000; Buck et al., 2005), which accommodates the Hookeriales (M. Fleisch.) M. Fleisch. and the Hypnales (M. Fleisch.) W.R. Buck and Vitt (sensu Buck et al., 2000a). The Hypopterygiaceae are closely related to the Hookeriales, either as a sister to the Hookeriales s. str. or as a basal family within the Hookeriales (Buck et al., 2000a, 2000b, 2005; Cox et al., 2000; Hedenäs, 1994, 1995; De Luna et al., 1999, 2000; Goffinet and Buck, 2004; cf. Blöcher and Capesius, 2002). However, the relationships within the family are less clear. The morphological diversity in Hypopterygiaceae has led to various theories on the classification of the family and its representatives. Before the 1970s the Hypopterygiaceae were usually treated as a single family placed systematically in the Hookeriales (Table 4.1 and references therein). By the late nineteenth and early twentieth centuries, mainly as a result of Kindberg’s work (Kindberg, 1898, 1899, 1901), the idea evolved that cyathophoroid and hypopterygioid genera should be classified into separate groups that are distinct on the subfamilial level (Brotherus, 1907, 1925; Fleischer, 1908). This idea was based mainly on differences in the direction of the sporophyte and the seta length (Figure 4.7).

Hookeriaceae

Hypopterygiaceae

Cyathophorum

Cyathophorella H.

Daltoniaceae

Hookeriaceae

D.

Cyathophoraceae

Lopidium

Canalohypopterygium ← Hypopterygiaceae

Hypopterygiaceae

Hypopterygiaceae

Hypopterygiaceae

Cyathophorella

Dendrocyathophorum

Catharomnion

a

Robinson (1971) presents only the family names in his classification scheme.

Note: D. = Daltoniaceae; H. = Hookeriaceae. Cells with grey background refer to classification in other families. The arrow indicates Whittemore and Allen’s (1989) presumption of relationship (see text).

Whittemore & Allen (1989)

Buck (1987, 1988)

Buck & Vitt (1986)

Crosby (1974) (followed by Walther [1983])

Robinson (1971)a

Miller (1971)

D.

Catharomnion

Hypopterygiaceae

Canalohypopterygium

Noguchi (1951, 1952)

Lopidium Hypopterygiaceae

Dendrocyathophorum

Dixon (1929, 1936, 1937)

Hypopterygium

Bryales

Hypopterygium

Hookeriales

Cyathophorum

TABLE 4.2 Schematic Overview of Mid- and Late Twentieth Century Classifications Until the 1990s of Hypopterygiaceae Mitt. by Various Authors

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1 cm

A

1 cm

B

0

FIGURE 4.7 Examples of differences in sporophyte orientation and seta length. (A) Dendrohypopterygium arbuscula (Brid.) Kruijer (Van Zanten & Kruijer 86.02.1137, GRO) and (B) Cyathophorum bulbosum (Hedw.) Müll. Hal. (ventral view, Streimann 51671, L). (From Kruijer, J.D. (H.), Blumea Supplement, 13: 112 and 298, 2002. With permission. Drawings by Joop Wessendorp.)

Since the 1970s, the monophyly of the family and its systematic position within the pleurocarpous mosses have been the subject of debate (Table 4.2 and references therein). Crosby (1974) classified the genera with poorly developed peristomes (Catharomnion and Cyathophorella (Broth.) M. Fleisch.; Figure 4.8) in the Daltoniaceae Schimp., and the genera with a well-developed peristome (Cyathophorum, Dendrocyathophorum, Lopidium and Hypopterygium, including Canalohypopterygium and Dendrohypopterygium s. lat.; Figure 4.9) in the Hookeriaceae Schimp. Both families belong to the Hookeriales. Buck and Vitt’s (1986) and Buck’s (1987, 1988) familial classifications of the pleurocarpous mosses, on the other hand, were based on both sporophytic and gametophytic characters, which included organization of the leaf costa, stem anatomy, axillary hair morphology, presence or absence of scale leaves, and calyptral ornamentation and anatomy. Examples of the variability within the Hypopterygiaceae in some of these characters are presented in Figures 4.10 to 4.13. Buck transferred the Hypopterygiaceae s. str. to the Bryales and placed the remaining genera Cyathophorum, Cyathophorella and Dendrocyathophorum in the Hookeriaceae (Hookeriales), but it should be remarked that Buck’s classification of the hypopterygiaceous genera is mainly based on the study of Hypopterygium and Cyathophorum. Whittemore and Allen’s (1989) study on relationships within the Hookeriales was based on Buck’s (1987) classification, but they considered Dendrocyathophorum to be a representative of the Hypopterygiaceae s. str. Whittemore and Allen also classified Cyathophorum and Cyathophorella in the Hookeriales, but transferred them to the Daltoniaceae. They remarked, however,

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D

B

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C

E

FIGURE 4.8 Examples of Hypopterygiaceae with a poorly developed peristome. (A) Detail of the processes of the endostome of Catharomnion ciliatum (Hedw.) Wilson (Beever 70-26, CBG); (B) exostome of Cyathophorum parvifolium Bosch and Sande Lac. (Meijer B9095, L); (C) basal part of exostome tooth of Cyathophorum adiantum (Griff.) Mitt. (Decoly & Schaul, BL 2571, S); (D) exo- and endostome of Cyathophorum africanum Dixon (Pócs & Harris, 6158/B, EGR); (E) exo- and endostome of Cyathophorum adiantum (Griff.) Mitt. (Decoly & Schaul, BL 2571, S). (A) and (C): scale bar equals 10 μm; (B), (D) and (E): scale bar equals 50 μm. (Compiled from Kruijer, J.D. (H.), Blumea Supplement, 13: 48, 50 and 51, 2002. With permission. SEM photographs by Hans Kruijer and Ben Kieft.)

that the resemblance of several representatives of the Hypopterygiaceae s. str. (Dendrocyathophorum in particular) to Cyathophorum and Cyathophorella is striking and suggested that the traditional classification of the Hypopterygiaceae in the Hookeriales might be correct. Whittemore and Allen pointed, furthermore, to the striking resemblance between Dendrocyathophorum and Canalohypopterygium (as Hypopterygium commutatum Müll. Hal.) in stem anatomy. Both monotypic taxa have stem cavities, which are always central in Dendrocyathophorum (Noguchi, 1936; Kruijer, 2002; Figure 4.13), but cortical in stem and branches and only central in the rudimentary branches in Canalohypopterygium (Reimers, 1953; Frey et al., 1983; Frey and Schaepe, 1989; Kruijer, 2002; Figure 4.13). Central and cortical cavities occur in several other representatives of the Hypopterygiaceae (Kruijer, 1995b, 2002; Magill and Van Rooy, 1998; Noguchi, 1936; Whittemore and Allen, 1989; Figure 4.13) and often contain solid or liquid inclusions (Noguchi, 1936; Kruijer, 1995b; Figure 4.13). Central cavities are present in stems and branches of Lopidium struthiopteris (Brid.) M. Fleisch., the distal part of stem and branches of Dendrohypopterygium arbuscula (Brid.) Kruijer, D. filiculiforme (Hedw.) Kruijer and Hypopterygium sandwicense Broth., and occasionally in stems of Cyathophorum africanum Dixon. Cortical cavities are present in stems and branches of L. concinnum (W. Hook.) Wilson and Catharomnion ciliatum (Hedw.) Wilson. The cavity system is most complex in the New Zealand endemics and monotypic genera Canalohypopterygium and Catharomnion (Reimers, 1953; Frey et al., 1983; Frey and Schaepe, 1989; Kruijer, 1995b, 2002), which differ considerably in gametophytic and sporophytic characters, in particular in habit (Figure 4.14), leaf dentation and morphology of the peristome (Frey and Schaepe, 1989; Kruijer, 2002; compare Figures 4.8A and 4.9E). They share, however, a character unique for mosses, i.e., short, usually leafless rudimentary branches, which are mainly located in the frond (Figure 4.15) and were misinterpreted in the past by Kindberg (1901), Brotherus (1907, 1925), and Sainsbury (1955) as being bristle-like amphigastria or metamorphosed leaves. The rudimentary branches of

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FIGURE 4.9 Examples of Hypopterygiaceae with a well-developed peristome. (A) Peristome of Cyathophorum bulbosum (Hedw.) Müll. Hal. (Van Zanten 1285, L); (B) peristome of Lopidium concinnum (W. Hook.) Wilson (Beckett 854, L); (C) detail of exostome tooth of Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (Meijer B7598, L); (D) peristome of Hypopterygium tamarisci (Sw.) Brid. ex Müll. Hal. (Herzog 2730, L); and (E) peristome of Canalohypopterygium tamariscinum (Hedw.) Kruijer (Visch s.n., ‘19.11.1972’, L). (A), (D) and (E): scale bar equals 100 μm; (B): scale bar equals 50 μm; (C): scale bar equals 10 μm. (Compiled from Kruijer, J.D. (H.), Blumea Supplement, 13: 48 and 50, 2002. With permission. SEM photographs by Hans Kruijer and Ben Kieft.)

Catharomnion and Canalohypopterygium are similar in morphology and anatomy, but are arranged in three rows in Catharomnion and in eight and three rows in Canalohypopterygium. Each rudimentary branch is associated with a single, superposed leaf and contains a central cavity, which continues in the cortex of the axis bearing the rudimentary branch (Reimers, 1953; Frey et al., 1983; Kruijer, 1995b, 2002; Figures 4.13 and 4.15). The cavities are usually filled with oil droplets, which are colourless to pale yellow in Catharomnion and pale yellow to brownish in Canalohypopterygium (Frey and Schaepe, 1989; Reimers, 1953; Kruijer, 1995b; Figure 4.15). Pelser et al. (2002) attempted to reveal the biological function of the rudimentary branches of Canalohypopterygium and the oil within. They calculated that Canalohypopterygium contains approximately 25 to 35 nl of oil per gametophore. The oil is more or less evenly distributed among the cavities of the rudimentary branches and those of the stipe and branches. It consists mainly of apolar hydrocarbons, some of them alkanes and fatty acids; evidence for the presence of compounds with an aromatic ring moiety was also found. However, Pelser et al. (2002) did not find evidence for a biological function of the rudimentary branches and the oil in the cavity system and pointed to the possibility that the rudimentary branches of Canalohypopterygium and Catharomnion are historical relics. Although field studies in New Zealand on possible biological functions of the cavity system and the oil within are very much needed before Pelser et al.’s (2002) hypothesis can be accepted or rejected, support for their hypothesis is found in the phylogeny reconstruction of the Hypopterygiaceae by Kruijer (2002), which shows reduction of ramification as a general pattern in the evolutionary history of the family. Many, if not all, of the morphological characters used in the systematic studies and classification proposals presented here show variability within the family, much of which has only been recognized since the mid-1990s. This variability is the underlying problem that hampered — and

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A B

1 mm

C D

E

F

FIGURE 4.10 Examples of morphological and anatomical variation in leaves of Hypopterygiaceae. (A) Stipe and rachis leaves of Dendrohypopterygium arbuscula (Brid.) Kruijer (Van Zanten & Kruijer 86.02.1137, GRO); (B) rachis and branch leaves of the “normal” variant and the dwarfish “Northern New Zealand” variant of Hypopterygium didictyon Mull. Hal. (Streimann 51282, L; the ventral and two lateral leaves in the central row and the second dorsal leaf and the second amphigastrium at the top in the right row at the corner are drawn from Fleischer B76, a representative of the “Northern New Zealand” variant); (C) rachis and branch leaves of Lopidium concinnum (W. Hook.) Wilson (Telford 4207, L); (D) stipe, rachis and branch leaves of Catharomnion ciliatum (Hedw.) Wilson (Beever 70-26, CBG); (E) leaves of Cyathophorum hookerianum (Griff.) Mitt. (left lateral leaf and central amphigastrium at top: Norkett 7398, BM; the lateral leaf left at bottom: s. coll., s.n., “Fruct. Neckera hookeriana Griff.”!, NY); the two amphigastria to the right: Burkill 37737, BM); (F) leaves of Cyathophorum bulbosum (Hedw.) Müll. Hal. (Streimann 51671, L). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 114, 134, 148, 270, 306 and 351, 2002. With permission. Drawings by Hans Kruijer and Jan van Os.)

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F

A

B

C

G

D

E

J M

I

L

H

K

O

N

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FIGURE 4.11 Examples of axillary hairs of Hypopterygiaceae. (A) Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Hamlin 2266, WELT); (B) D. arbuscula (Brid.) Kruijer (Van Zanten & Kruijer 86.02.1137, GRO); (C) Canalohypopterygium tamariscinum (Hedw.) Kruijer (Martin 274.9, CHR); (D) Catharomnion ciliatum (Hedw.) Wilson — axillary hairs are rare in this species (Van Zanten 7401243, L); (E) Hypopterygium didictyon Müll. Hal. — the terminal cell of the axillary hairs in this species are frequently covered with white, waxy substances (the three axillary hairs to the left, Streimann 51282, L, a representative of the “normal” variant of the species; the two to the right, Fleischer B76, L, a representative of the dwarfish “Northern New Zealand” variant); (F) H. flavolimbatum Mull. Hal. (Igbal 646, L); (G) H. sandwicense Broth. (Hoe 704.0, NICH); (H) Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (the two axillary hairs to the left, Bor 95, BM; the ones to the right, Boeken 81.03.2587, GRO); (I) Lopidium concinnum (W. Hook.) Wilson (Telford 4207, L); (J) L. struthiopteris (Brid.) M. Fleisch. (Van der Wijk 453, L); (K) Cyathophorum africanum Dixon (Crosby & Pócs 8711, L); (L) Cyathophorum hookerianum (Griff.) Mitt. (left: Williams 1671, NY; central: Norkett 7398, BM; right: Elmer 8544, S); (M) Cyathophorum parvifolium Bosch and Sande Lac. (left, Touw 18479, L; the two axillary hairs to the right, Meijer B9095, L); (N) Cyathophorum tahitense Besch. (left, Vesco s.n., PC; the two axillary hairs to the right, Whittier 2501, BM); (O) Cyathophorum adiantum (Griff.) Mitt. (left and top right, Chen, MSE 92, S; central, Griffith 185/509?, BM; right, Touw 9198, L); (P) Cyathophorum bulbosum (Hedw.) Müll. Hal. (left, Streimann (field no 1), L; right, Van Balgooy 217, L); and (Q) Cyathophorum spinosum (Müll. Hal.) H. Akiyama (the two axillary hairs to the left, Brass 12934, FH; the one to the right, Brass 25066, FH). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 116, 126, 134, 148, 176, 248, 272, 288, 308, 324, 334, and 352. With permission. Drawings by Hans Kruijer and Jan van Os.)

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FIGURE 4.12 Examples of morphological variation of calyptrae in Hypopterygiaceae. (A) Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Ruinard 98.10.31.02, L); (B) Canalohypopterygium tamariscinum (Hedw.) Kruijer (Martin 274.9, CHR); (C) Catharomnion ciliatum (Hedw.) Wilson (Beever 70–26, CBG); (D) Hypopterygium didictyon Mull. Hal. – (Weymouth s.n., hb. Bartram sub no 6457, FH); (E) Lopidium struthiopteris (Brid.) M. Fleisch. (Streimann 2396, L); (F) Lopidium concinnum (W. Hook.) Wilson (Streimann 30553, L); (G) Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (Boeken 81.03.2587, GRO); (H) Cyathophorum bulbosum (Hedw.) Mull. Hal. (left: Streimann 51671, L); (I) Cyathophorum africanum Dixon (Pócs & Harris 6158/B, L); (J) Cyathophorum hookerianum (Griff.) Mitt. (left: mitrate calyptra of Burkill 37737, BM; right: cucullate calyptra of Kanai et al. s.n., ‘Nov. 15, 1963’, NICH); and (K) Cyathophorum parvifolium Bosch and Sande Lac. (Meijer B9095, L). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 108, 126, 134, 148, 270, 288, 306, 334 and 351, 2002. With permission. Drawings by Hans Kruijer and Jan van Os.)

still hampers — the delimitation of separate groups of species within the family and the determination of their mutual evolutionary relationships. That is actually what can be seen; there was no consensus among bryologists on the classification of the Hypopterygiaceae up to about 1990 (e.g., Table 4.2). Since 1989 Kruijer has tried to unravel the phylogeny of the Hypopterygiaceae using morphological characters of both generations in the life cycle, starting with a critical evaluation of the characters that could be used to clarify the question whether the Hypopterygiaceae are monophyletic or polyphyletic. After the evaluation of approximately 150 characters, more than 50 characters were selected that could be used in phylogenetic analyses, some of which were shown above (Figures 4.6 to 4.13 and 4.15). However, selecting the useful and informative characters, finding the best coding for the character states in the data matrices, and finding a well-balanced selection of outgroup species turned out to be problematic. In addition, the phylogenetic analyses were hampered by the high amount of homoplasy in the dataset. In 1995, Kruijer (1995a, 1995b) tentatively suggested that the Hypopterygiaceae are polyphyletic, because Cyathophorum seemed to be closely related to the Hookeriaceae (Figure 4.16). The analyses in 1995 resulted in 234 most parsimonious trees, which differed mainly in the topology of the paraphyletic genus Hypopterygium. Dendrocyathophorum, Lopidium and Cyathophorella were placed in a single monophyletic clade. The results of the analyses in 1995 were the best that could be obtained with the (morphological) data at that date, but the phylogeny of the Hypopterygiaceae was neither reliably nor completely satisfactorily resolved. The selection of Hypnodendron diversifolium Broth. and Geh. in the outgroup proved to be a disturbing source of homoplasy. In addition, the relationship between Hypopterygium filiculiforme (Hedw.) Brid. and the other Hypopterygiaceae (the base of the Hypopterygiaceae clade) needed further study. The outcome that Cyathophorella and Cyathophorum were shown as distantly related was also strange, considering their strong resemblance in morphology in both generations, with the exception of calyptra and peristome characters. These problems led to a critical evaluation of outgroup sampling, character selection and coding of the character states, whereby adjustments in the original dataset were tested each time against the objective criterion that each adjustment should result in more reliable phylogenetic signal; i.e., the phylogenetic analyses should result in more stable, shorter trees with higher support values. In 1996, Kruijer’s phylogenetic analyses based on 59 characters and 32 species of Hypopterygiaceae and representatives

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FIGURE 4.13 Examples of stem anatomical variation in Hypopterygiaceae. (A) Central strand in rachis and central cavity with and without droplet of oil in ultimate branches of Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Hamlin 2266, WELT); (B) central strand in rachis and central cavity in process of formation with degenerating strand cells in branch of Hypopterygium sandwicense Broth. with droplets of oil (still) mainly kept in strand cells; (C) central strand and cortical cavities in rachis and branch and central cavity in rudimentary branches of Canalohypopterygium tamariscinum (Hedw.) Kruijer with droplets of oil trapped in cavities or still kept in the “epithelium cells” of the cavities (Visch s.n., ‘19.11.1072’, L); (D) central strand and cortical cavities in rachis and branch and central cavity in rudimentary branches of Catharomnion ciliatum (Hedw.) Wilson with droplets of oil trapped in cavity or still kept in the “epithelium cells” of the cavities (Beever 70–26, CBG); (E) cortical cavities in rachis of Lopidium concinnum (W. Hook.) Wilson (Telford 4207, L); (F) central cavity in rachis of Lopidium struthiopteris (Brid.) M. Fleisch. (Van der Wijk 453, L); (G) central cavity with trapped droplet of oil in rachis of Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (Meijer B7598, L); (H) central cavity in process of formation and with droplets of oil probably just released from degenerating strand cells in stem of Cyathophorum africanum Dixon (Pócs & Harris 6158/B, L). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 108, 126, 134, 248, 270, 288 and 334, 2002. With permission. Drawings by Hans Kruijer and Jan van Os.)

of potentially related families eventually resulted in better resolved trees with slightly better support values, in which the Hypopterygiaceae were monophyletic and Cyathophorella closely related to Cyathophorum (Kruijer, 1996). Although the results of the analyses were more reliable than the ones obtained in 1995, two problems remained. The analyses were still hampered by a high amount of homoplasy and the circumscription of a few species of the Hypopterygiaceae, in particular Hypopterygium flavolimbatum Müll. Hal. and H. tamarisci (Sw.) Brid. ex Müll. Hal., was not completely clear. After completion of his revision, Kruijer (2002) conducted a series of phylogenetic analyses based on 57 morphological characters and 34 species including representatives of the Hypopterygiaceae and potentially related families (Figure 4.17). However, the topology of the base of the Hypopterygiaceae clade to some extent remained unclear. The high number of equivocal character

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FIGURE 4.14 Habit of two New Zealand related endemics. (A) Canalohypopterygium tamariscinum (Hedw.) Kruijer (Visch s.n., ‘19.11.1972’, L); (B) and (C) Catharomnion ciliatum (Hedw.) Wilson. (B) Female plant (dorsal view); (C) male plant (ventral view) (both from Beever 70–26, CBG). (From Kruijer, J. D. (H.), Blumea Supplement, 13: 124, 132 and 133, 2002. With permission. Drawings by Joop Wessendorp.)

FIGURE 4.15 Oil trapped in the cavity system of (A) branch of Canalohypopterygium tamariscinum (Hedw.) Kruijer (Allison KW 2935, CHR; ventral view); and (B) branch of Catharomnion ciliatum (Hedw.) Wilson (Van Zanten 7401562, GRO; dorsal view). (Photographs courtesy of Cris Hesse.)

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Daltoniaceae Hookeriaceae Cyathophorum Racopilum Hypnodendron Hypopterygium filiculiforme Hypopterygium arbuscula Canalohypopterygium Catharomnion Hypopterygium didictyon Hypopterygium elatum Hypopterygium flavolimbatum tristichous Hypopterygium species Hypopterygium sandwicense Dendrocyathophorum Lopidium Cyathophorella

FIGURE 4.16 Phylogeny of the Hypopterygiaceae based on Kruijer’s (1995a, 1995b) analyses of morphological data. (From Kruijer, J.D. (H.), Buxbaumiella, 38: 32, 1995b. With permission.)

states at the base of the clade led to the conclusion that the underlying problem might be that the Hypopterygiaceae are more distantly related to the non-hypopterygiaceous species used in the analyses than expected. Blöcher and Capesius (2002) tried to unravel the phylogeny of the Hypopterygiaceae using rps4 cpDNA sequence data (26 species of Hypopterygiaceae and potentially related families; Figures 4.18 and 4.19). The topology of their trees is intriguingly different from Kruijer’s (2002) trees based on morphological data. Blöcher and Capesius’ (2002) trees show that the core of the Hypopterygiaceae is monophyletic, as in Kruijer’s trees, but provide evidence that Dendrohypopterygium s. lat. is actually polyphyletic (Figure 4.19) and show that the position of Cyathophorum bulbosum (Hedw.) Müll. Hal. and C. adiantum (Griff.) Mitt. is ambiguous (Figure 4.18). The latter two species are both grouped in a single clade, which is either placed in a basal position in the Hypopterygiaceae s. str. or in a basal position in the “pleurocarpous mosses.” Stech et al. (2002) performed phylogenetic analyses using trnLUAA intron cpDNA, and ITS2 nrDNA sequence data (Figures 4.20 and 4.21). Their trees differ in topology from the ones presented by Blöcher and Capesius (2002), but also provide evidence for the polyphyly of Dendrohypopterygium s. lat. (mainly based on trnL data) and also show an ambiguous position for the Cyathophorum bulbosum–C. adiantum clade. An intriguing difference is the position of the monotypic genus Dendrocyathophorum, which in Blöcher and Capesius’s (2002) trees is nested in a clade consisting of the Catharomnion–Canalohypopterygium clade in a terminal position, and Dendrohypopterygium arbuscula or D. filiculiforme in a basal position. In the Stech et al. (2002) trees, Dendrocyathophorum is either grouped in a clade with the Lopidium clade in a terminal position, or in a clade with the Lopidium clade in a terminal position and Dendrohypopterygium arbuscula (as Arbusculohypopterygium arbuscula [Brid.] Stech, T. Pfeiffer & W. Frey) in a basal position, or in a terminal or inconclusive position in a clade with D. arbuscula and Cyathophorum adiantum.

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The trees obtained by Buck et al. (2005; not shown), based on phylogenetic analyses using trnL–trnF, rps4 cpDNA, nad5 mtDNA and 26S nrDNA sequence data, presents the Hypopterygiaceae, including Cyathophorum, as a monophyletic taxon and sister to the remainder of the Hookeriales. Within the Hypopterygiaceae, the Cyathophorum bulbosum–C. adiantum clade is placed in a basal position as sister to the core of the Hypopterygiaceae. In this core, the Lopidium clade is placed in a basal position to the remaining species, where this clade has a terminal position in the trees obtained by Blöcher and Capesius (2002) and most of those obtained by Stech et al. (2002). In the Buck et al. (2005) trees, as in those of Blöcher and Capesius (2002), Dendrocyathophorum is nested in a clade with Dendrohypopterygium arbuscula in a basal position and the Catharomnion–Canalohypopterygium clade in a terminal position. Most interesting in the Buck et al. (2005) trees is the clade sister to these four taxa, which comprises Hypopterygium tamarisci and Cyathophorum hookerianum (Griff.) Mitt. The remarkable position of Cyathophorum hookerianum in the core of the Hypopterygiaceae, well separated from the Cyathophorum bulbosum–C. adiantum clade, is most intriguing. We obtained a similar position for Cyathophorum hookerianum in the results of the phylogenetic analyses preliminary to our present study that are based on molecular sequence data and those of the preliminary phylogenetic analyses that are based on a combination of morphological and molecular data, albeit with low support in the latter. Despite the obvious differences in tree topology, the recent morphological and molecular studies provide supporting evidence for the monophyly of the Hypopterygiaceae. Within the family two clades are well supported, one formed by the monotypic genera Catharomnion and Canalohypopterygium, the other by the two Lopidium species. The phylogenies in the morphological study present Hypopterygium and Dendrohypopterygium s. lat. as paraphyletic grades with low levels of support. The molecular studies, however, indicate that Hypopterygium is presumably monophyletic and Dendrohypopterygium s. lat. in all probability polyphyletic. Stech et al. (2002) proposed the genus Arbusculohypopterygium to accommodate the South American species of Dendrohypopterygium s. lat. The studies based on molecular data indicate that Cyathophorum in Kruijer’s (2002) circumscription is polyphyletic. The incongruences between these recent morphological and molecular studies led to our initiative to reevaluate the phylogeny of the Hypopterygiaceae by conducting a series of phylogenetic analyses with a combination of morphological and molecular data.

4.3 REEVALUATION OF THE PHYLOGENY In our present study, we try to get new insights into the evolutionary history of the Hypopterygiaceae through a “total evidence” approach using a combination of morphological and molecular sequence data (rps4, trnL–trnF region of cpDNA, and ITS2 of nr ribosomal DNA). Our study focuses on the ancestral origin of the family, the relationship between Dendrocyathophorum and the other genera, in particular Cyathophorum, Catharomnion and Canalohypopterygium, and the relationships within Cyathophorum. Of particular interest are the position of Cyathophorum hookerianum and the relationship of Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer with the African species Cyathophorum africanum — the only Cyathophorum species that occasionally has a central stem cavity, which contains conspicuous inclusions and shows a remarkable resemblance to that of Dendrocyathophorum (Figure 4.13). In contrast to the earlier phylogenetic analyses of morphological data, we included a representative of the Ptychomniaceae M. Fleisch., Ptychomnion cygnisetum (Müll. Hal.) Kindb., since it has recently become clear that the Ptychomniales W.R. Buck, C. Cox, A. J. Shaw and B. Goffinet represents the sister of the Hypnales and the Hookeriales (e.g., Buck et al., 2005; Shaw et al., 2003).

4.3.1 TAXON

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FIGURE 4.17 Four phylogenies of the Hypopterygiaceae based on Kruijer’s (2002) analyses of morphological data. Figures 4.17A–C represent (combined majority rule with superimposed strict) consensus trees; Figure 4.17D represents the single MPT of an analysis solely with Hypopterygiaceae. Numbers under branches refer to bootstrap values and, between parentheses, decay values. Kruijer’s (2002) generic classification of the Hypopterygiaceae is based on these trees. Symbols * and ° refer to the classification previously of the marked species in, respectively, Hypopterygium Brid. and Cyathophorella (Broth.) M. Fleisch. Cyathophorella spinosa (Müll. Hal.) M. Fleisch. was the first Cyathophorella species that was transferred to Cyathophorum P. Beauv. (Akiyama, 1988, 1992). (From Kruijer, J. D. (H.), Blumea Supplement, 13: 68, 2002. With permission.) Continued.

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FIGURE 4.18 Strict consensus tree of 15 MPTs obtained by Blöcher and Capesius (2002) based on rps4 gene sequences of 26 representatives of the Hypopterygiaceae, Hookeriales, Hypnales, Bryales, Splachnales, Funariales and Timmiales. Numbers above branches refer to bootstrap values; numbers under branches refer to decay values. Capitals refer to clades discussed in the original paper. (From Blöcher, R. and Capesius, I., Cryptogamie, Bryologie, 23(3): 199, 2002. With permission.)

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FIGURE 4.19 Single MPT obtained by Blöcher and Capesius (2002) based on rps4 gene sequences of nine representatives of the Hypopterygiaceae and the outgroup species Hookeria lucens (Hedw.) Sm., Schimperobryum splendidissimum (Mont.) Margad., Hypnum cupressiforme Hedw., and Neckera crispa Hedw. Numbers above branches refer to bootstrap values; numbers under branches refer to the numbers of characters supporting each branch (left) or decay values (right). Capitals refer to clades discussed in the original paper. (From Blöcher, R. and Capesius, I. Cryptogamie, Bryologie, 23(3): 202, 2002. With permission.)

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Cyathophorum bulbosum Cyathophorum adiantum Hookeria lucens Distichophyllum crispulum

FIGURE 4.20 Single MPT obtained by Stech et al. (2002) based on trnL intron sequences of 22 specimens from 13 species of the Hypopterygiaceae and two specimens of the outgroup species Distichophyllum crispulum (Hook. f. and Wilson) Mitt. and Hookeria lucens (Hedw.) Sm. Numbers above branches refer to bootstrap values. Stech et al. (2002) placed Dendrohypopterygium arbuscula (Brid.) Kruijer in the monotypic genus Arbusculohypopterygium Stech, T. Pfeiffer, and W. Frey. (From Stech et al., New Zealand Journal of Botany, 40: 216, 2002. With permission.)

selection was based on earlier sampling for a morphological data set by the first author (Kruijer, 2002) and limited by the availability of sequences from the cpDNA and nrDNA regions for these taxa. Sequence data available from GenBank of the trnL–trnF region, the rps4 gene and ITS2 were used. The rps4 and trnL–trnF region were newly sequenced for Ptychomnion cygnisetum and Cyathophorum africanum. Sequences of the trnL–trnF and ITS2 region of Schimperobryum splendidissimum (Mont.) Margad. were kindly provided by Dietmar Quandt (Technical University of Dresden). DNA isolation, polymerase chain reactions (PCR) and sequencing reactions were carried out as described in Blöcher and Capesius (2002) for the rps4 gene and Quandt et al. (2000) for the trnL–trnF region. Table 4.3 presents a list of the sampled species and the GenBank accession numbers of the sequences used in the analyses. Vouchers of the newly sequenced species are preserved in L. Table 4.4 presents the definition of morphological characters and coding of character states used by Kruijer (2002). Table 4.5 presents the morphological dataset for the species sampled for the present study. The data was extracted from Kruijer’s (2002) original dataset; for Ptychomnion cygnisetum, new morphological data was obtained by the examination of herbarium specimens following Kruijer’s (2002) character state coding.

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80

Hypopterygium tamarisci South Africa Hypopterygium tamarisci Bolivia

98

Hypopterygium tamarisci Malaysia

76

Hypopterygium discolor

94

Hypopterygium flavolimbatum Hypopterygium didictyon New Zealand 66

81

74

Dendrocyathophorum decolyi Arbusculohypopterygium arbuscula Cyathophorum adiantum

100

Lopidium concinnum New Zealand Lopidium concinnum Chile Hookeria lucens Distichophyllum crispulum

FIGURE 4.21 One out of three MPTs obtained by Stech et al. based on combined trnL intron/ITS2 sequences of 11 specimens from 8 species of the Hypopterygiaceae and 2 specimens of the outgroup species Distichophyllum crispulum (Hook. f. and Wilson) Mitt. and Hookeria lucens (Hedw.) Sm. Numbers above branches refer to bootstrap values. (From Stech et al., New Zealand Journal of Botany, 40: 218, 2002. With permission.)

4.3.2 PHYLOGENETIC ANALYSES Ptychomnion cygnisetum was selected as the outgroup. All analyses were carried out using the complete dataset, which consists of morphological data and sequence data of the trnL intron and trnL 3-exon, trnL–trnF spacer, ITS2 region, rps4–trnS spacer and rps4 gene. This combined dataset amounts to a total of 1847 characters (Table 4.6). Sequences were aligned manually with the manual sequence alignment editor Align (Hepperle, 2002). Heuristic searches under the parsimony criterion were carried out under the following options: all characters unweighted and unordered, gaps coded as missing data, performing a tree bisection reconnection (TBR) branch swapping, collapse zero branch length branches, MulTrees option in effect, random addition sequence with 1000 replicates. Furthermore, the datasets were analysed using winPAUP 4.0b10 (Swofford, 2002) executing the command files generated by PRAP (Parsimony Ratchet Analyses using PAUP; Müller, 2004), employing the implemented parsimony ratchet algorithm (Nixon, 1999). For the parsimony ratchet the following settings were employed: 10 random addition cycles of 200 iterations each with a 40% upweighting of the characters in the PRAP iterations. Decay values (Bremer, 1988; Donoghue et al., 1992) were also calculated with PRAP with the same settings as for the parsimony ratchet analyses without additional random addition cycles. Heuristic bootstrap searches (Felsenstein, 1985) under parsimony criterion were performed with 1000 replicates, 10 random addition cycles per bootstrap replicate and the same options in effect as the heuristic search for the most parsimonious tree (MPT). The consistency index (CI, Kluge and Farris, 1969), retention index (RI), and rescaled consistency index (RC, Farris, 1989) were calculated to assess homoplasy. In addition to our MP analyses we performed Bayesian inferences with MrBayes 3.0 (Huelsenbeck and Ronquist, 2001). Modeltest 3.5 (Posada, 2004) was used to select DNA substitution models for the molecular dataset (gamma shape distribution, six substitution types). Six data

AY306853 AY306856 AJ 269694 AJ269695 AJ315872 AJ862340 AJ269693 AY306890 AJ271645 AJ252293 AJ252290 AY306902 AJ269689

Achrophyllum dentatum Adelothecium bogotense Canalohypopterygium tamariscinum

Catharomnion ciliatum

Cyathophorum adiantum

Cyathophorum africanum Cyathophorum bulbosum

Cyathophorum hookerianum Dendrocyathophorum decolyi

Dendrohypopterygium arbuscula

Dendrohypopterygium filiculiforme

Distichophyllum pulchellum Hookeria lucens

rps4

AF152380

AF134638 AY306736

AF134637

AF363280

AF134634 AY306724

AF363281 AJ876600

AF134633

AF134632

AY306687 AY306690

trnL

AJ252137

AY091478

AY091480

AY091481

ITS2

Germany

Chile NZ

Kenia NZ NZ Thailand Japan

Japan

New Zealand

New Zealand

Australia

Origin

Blöcher 980328/1 Stech B880404.8

Frey & Frey 95-17 Frahm 31-17 Frey 94-76

Solga s.n., (‘22.09.2003’) Frahm 1-1a Frey 1-4901 Akiyama Th-39 Matsui s.n.

Frahm 9-1 Frey 94-79 Frey & Pfeiffer 98-Z 132 B van Zanten 7401243 Yamaguchi s.n.

Voucher

Shaw et al. 2003 Shaw et al. 2003 Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) This chapter Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL) Shaw et al. 2003 Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL) Shaw et al. 2003 Blöcher & Capesius 2002 (rps4) Stech et al. 1999 (trnL) Continued.

Reference

TABLE 4.3 GenBank Accession Numbers for the Regions Sequenced and, Respectively, Voucher Information and Literature References for Samples Included in the Molecular Analyses

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Reevaluation of the Phylogeny of the Hypopterygiaceae 87

AJ252292

AJ252291 AJ269688 AJ252289

AJ252288 AJ269692 AJ862331 AJ315873

Hypopterygium didictyon

Hypopterygium discolor Hypopterygium flavolimbatum Hypopterygium tamarisci

Leucodon sciuroides

Lopidium concinnum

Lopidium struthiopteris

Neckera crispa

Ptychomnion cygnisetum Schimperobryum splendidissimum AJ507770

AY050280 AJ862681

AF363283

AF033233

AF397786

AF265217

AF363282 AY098638

AF170592

AF472483

trnL

AJ862692

AY050296

AY029369

AF403634

AY091475

AY091473 AY091476 AY091477

ITS2

Chile Chile

Ireland

Germany Russia NZ

Australia China South Africa

New Zealand

Germany

Origin

Blöcher 130 & 131 Blöcher 01-09-1

Blöcher 990705/2

O’Shea 99C14b

Blöcher 961115/7 Huttunen & Wahlberg 819 Frahm 1-1b Frey 92-72

Streimann 52819 Tan 99-143 O’Shea 99E28a

Frahm 9-7 (‘NZ-9’)

Capesius 95-12

Voucher

Blöcher & Capesius 2002 (rps4) Pedersen & Hedenäs 2002 Blöcher & Capesius 2002 (rps4) Pfeiffer 2000 (trnL) Stech et al. 2002 (ITS2) Stech et al. 2002 (trnL + ITS) Stech et al. 2002 (trnL + ITS) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS) Blöcher & Capesius 2002 (rps4) Huttunen & Ignatov 2004 Blöcher & Capesius 2002 (rps4) Frey et al. 1999 Stech & Frahm 2001 (ITS) Blöcher& Capesius 2002 (rps4) Stech et al. 2002 (trnL) Blöcher & Capesius 2002 (rps4) Stech et al. 2003 (trnL + ITS2) This chapter Blöcher & Capesius 2002 (rps4) D. Quandt (unpublished)

Reference

88

Note: Cyathophorum africanum Dixon and Ptychomnion cygnisetum (Müll. Hal.) Kindb. were newly sequenced for the analyses presented here; the remaining sequences were obtained from Dietmar Quandt, earlier studies by the second author, and GenBank.

AJ269690

Hypnum cupressiforme

rps4

TABLE 4.3 (Continued) GenBank Accession Numbers for the Regions Sequenced and, Respectively, Voucher Information and Literature References for Samples Included in the Molecular Analyses

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TABLE 4.4 Definition of Morphological Characters and Coding of Character States, after Kruijer (2002) Characters of the Gametophore 1. Ramification: sympodial: state 1; monopodial: state 2. 2. Habit: strictly palmate or umbellate: state 1; pinnate, bipinnate, or flabellate to palmate or umbellate: state 2; pinnate to bipinnate or flabellate (occasionally somewhat dendroid): state 3; usually simple, less often set with a few innovations or weakly branched (branches may function as new shoots): state 4. 3. Phyllotaxis of the basal part of the stem (stipe): 3/8: state 1; 5/13: state 2; 2/5: state 3; 1/3 or nearly so (i.e., 4/11, or 8/21): state 4. 4. Phyllotaxis of the distal parts of the stem (distal parts of the rachis and branches): 3/8: state 1; 5/13: state 2; 2/5: state 3; 1/3 or nearly so (i.e., 4/11, or 8/21): state 4. 5. Foliation of the basal part of the stem (stipe): not or weakly complanate: state 1; distinctly complanate: state 2. 6. Foliation of the distal parts of the stem (distal parts of the rachis and branches): not or weakly complanate: state 1; distinctly complanate: state 2. 7. Foliation of the basal part of the stem (stipe): homophyllous: state 1; heterophyllous: state 2. 8. Foliation of the distal parts of the stem (distal parts of the rachis and branches): homophyllous: state 1; heterophyllous: state 2. 9. Orientation of the foliation: not orientated in any direction or dorsi-ventral: state 1; dorsal: state 2; ventral: state 3. 10. Compression of the non-gemmiferous parts of the stem (stipe and rachis): entirely dorsi-ventral or partly uncompressed: state 1; mainly dorsi-ventral, but partly lateral (near the stipe base) in a few specimens of the species at least: state 2; lateral: state 3. 11. Central strand cells (in cross sections without central cavities): present: state 1; occasionally present: state 2; absent: state 3. 12. Axial cavities in the basal and middle parts of the stem (the stipe and the basal and middle parts of the rachis): absent: state 1; central: state 2; cortical: state 3. Species for which the character state of this character is coded as state 2 or 3 do not necessarily possess cavities in every cross section. 13. Axial cavities in ultimate branches: absent: state 1; present: state 2. This character state is coded as unknown for species lacking ultimate branches, viz. for species lacking any ramification, for species usually lacking ramification in which the rare branches are similar to the main axis or show indeterminate growth, and for species with indeterminate growth of branches. 14. Rudimentary branches: absent: state 1; present, not gemmiferous but naked or only set with a few scaly leaves: state 2; present, gemmiferous: state 3. 15. Scaly leaves at primordia: occasionally present at least: state 1; absent: state 2. 16. Intermediate cells of axillary hairs (at stipe, rachis, or branches): present: state 1; occasionally present: state 2; absent: state 3. 17. Outline of terminal cell of axillary hairs (at stipe, rachis, or branches): short-linear to linear and rectangular: state 1; short-elliptic to elongate-rectangular: state 2; short and elliptic, subcircular, or circular: state 3. 18. Margin of lateral leaves in the distal part of the frond: entire or truly serrate: state 1; entire or serrate-dentate: state 2; dentate: state 3; partly dentate-ciliate at least: state 4. 19. Border of lateral leaves (above the leaf base) in the distal part of the frond: absent or interrupted: state 1; interrupted or continuous, but never absent and interrupted in a few leaves at least: state 2; always continuous: state 3. 20. Border of lateral leaves (above the leaf base) in the distal part of the frond: up to 2 cells wide at most: state 1; at least partly more than 2 cells wide: state 2. 21. Costa of frond leaves: single: state 1; double or forked at base: state 2. 22. Costa of lateral leaves in the distal part of the frond: reaching 4/5 of the length of the leaf at least: state 1; reaching 1/2–4/5 of the length of the leaf: state 2; reaching up to 1/2 of the length of the leaf at most: state 3. 23. Costa of amphigastria (or ventral leaves) in the distal part of the stem (rachis) and branches: reaching 1/2 of the length of the amphigastrium and at least occasionally percurrent or nearly so: state 1; reaching 1/3 of the length of the amphigastrium at least, but never percurrent: state 2; reaching up to 1/2 of the length of the amphigastrium at most and at least occasionally shorter than 1/3 of the length of the leaf: state 3. Continued.

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TABLE 4.4 (Continued) Definition of Morphological Characters and Coding of Character States, after Kruijer (2002) 24. Laminal cells in frond leaves: cell walls thin or weakly incrassate (prosenchymatous or in parts of the leaf parenchymatous): state 1; cell walls distinctly incrassate (collenchymatous): state 2. 25. Gemmae: absent: state 1; not common, present in only a few specimens: state 2; common: state 3. 26. Sexuality: strictly dioicous: state 1; partly or strictly monoicous: state 2. 27. Paraphyses in perigonia: always present: state 1; present or absent: state 2; always absent: state 3. 28. Paraphyses in perichaetia: present: state 1; present or absent (either in perichaetia prior to sporogone development or in full grown ones): state 2; absent: state 3. 29. Leaf-like paraphyses in full grown perichaetia: absent: state 1; occasionally present: state 2. 30. Stalk of full grown perichaetia: at least occasionally set with rhizoids: state 1; glabrous: state 2. 31. Vaginula length: short, 0.8 mm long at most: state 1; intermediate in length, both shorter and longer than 0.8 mm present: state 2; long, 0.8 mm long at least: state 3. Characters of the Sporophyte and the Calyptra 32. Direction of the sporogone: usually projecting above the gametophore: state 1; usually projecting beneath the gametophore: state 2. 33. Seta: 10.0 mm long at least: state: 1; intermediate in length, between 4.5 mm and 10 mm long: state 2; short, 4.5 mm long at most: state: 3. 34. Seta base: narrow: state 1; narrow or widened: state 2; widened: state 3. 35. Seta surface: smooth or nearly so: state 1; weakly to moderately mammillate: state 2; coarsely mammillate: state 3. 36. Capsule: subglobose to barrel-shaped, never cylindrical: state 1; (occasionally) cylindrical: state 2. Character state 1 includes ovoid, ellipsoid, and turbinate capsules. 37. Angle of the capsule with the direction of the seta: variable, erect to pendulous: state 1; erect to horizontal: state 2; horizontal to pendulous: state 3. 38. Capsule neck: smooth or nearly so: state 1; pustulose: state 2. 39. Annulus: (occasionally) present: state 1; absent: state 2. 40. Orifice: always transverse: state 1; transverse or oblique: state 2. 41. Number of IPL-cells in the peristome: strictly 4: state 1; variable, 4–8(–10): state 2; several, 6–10: state 3. 42. Exostome teeth: present: state 1; absent: state 2. 43. Exostome teeth: 70 μm wide at least: state 1; 70 μm wide at most: state 2. 44. Exostome teeth: partly or entirely bordered above the base: state 1; not bordered or slightly bordered: state 2. 45. Median line: not furrowed: state 1; not or interruptedly furrowed: state 2; distinctly furrowed: state: 3. 46. Ornamentation of the dorsal plates in the basal third of the exostome teeth: conspicuously striate (striae set with papillae or not): state 1; smooth, papillose, or weakly striate near the tooth base: state 2. 47. Papillae on the dorsal plates of the exostome: strictly low: state 1; (occasionally) high: state 2. 48. Trabeculae in the middle parts of the exostome teeth: short to strongly protruding and closely set: state 1; very short to short and distant: state 2. 49. Height of the basal membrane of the endostome beyond the orifice: projecting 1/3 of the length of the exostome teeth at least: state 1; projecting c. 1/3 of the length of the exostome teeth: state 2; projecting 1/3 of the length of the exostome teeth at most: state 3. 50. Endostomial cilia: (occasionally) present and parts of several plates long: state 1; absent or present as a part of single plate: state 2. 51. Operculum: long-rostrate: state 1; short-rostrate: state 2. 52. Rostrum: oblique: state 1; oblique or straight: state 2; straight: state 3. 53. Calyptra: cucullate: state 1; cucullate to mitrate: state 2: mitrate: state 3. 54. Calyptra: completely covering the operculum: state 1; partly or completely covering the operculum: state 2; partly covering the operculum: state 3. 55. Colour of the calyptra below the apex: white, or pale ochraceous to pale brown: state 1; ochraceous or pale brown to brown: state 2; brown to dark brown: state 3.

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TABLE 4.4 (Continued) Definition of Morphological Characters and Coding of Character States, after Kruijer (2002) 56. Paraphyses on the calyptra: absent: state 1; present and short: state 2; present and long: state 3. 57. Texture of the calyptra: entirely membranous: state 1; membranous and slightly fleshy near the apex: state 2; membranous in the basal part and at some distance from the base becoming fleshy in the distal part: state 3; entirely fleshy: state 4. Note: For the present study, morphological data is newly sampled from Ptychomnion cygnisetum (Müll. Hal.) Kindb. Remarks In Catharomnion ciliatum, the peristome is endostomial only. Therefore, the states of exostome characters 43–49 are coded as unknown for this species. Ptychomnion cygnisetum is a nanandrous species; hence character state coding of characters 1–25 refers to female plants only. Ramification type of P. cygnisetum could not be determined with certainty. Ramification seems to be monopodial, but in the material examined the older parts of the (female) plants are usually damaged or not collected. Occasionally, ramification shows some resemblance with sympodial branching. Hattaway’s (1984) description of ramification is, unfortunately, inconclusive. Hence, the state of character 1 is coded as unknown for this species. Hattaway did not mention the existence of paraphyses in P. cygnisetum. However, they can be observed in both perigonia and perichaetia of this species, although in perichaetia presence or absence of paraphyses is often difficult to ascertain due to the thin-walled cells of the paraphyses. In our study, the presence of paraphyses could be ascertained in all perigonia (dwarf males) examined. Paraphyses were also observed in full-grown and sometimes in immature perichaetia. Although perichaetial paraphyses may easily be overlooked, we observed that paraphyses are truly absent from several perichaetia. Hence, the state of character 28 is coded as state 2, and that of character 29 is coded as state 1. The seta of P. cygnisetum is ± straight with a broadly to cygneously curved top. The direction of the curved capsule is ± horizontal to pendulous; hence the state of character 37 is coded as state 3. The operculum is rostrate. Despite a somewhat asymmetrical implantation on the conical base, the rostrum is best described as being straight; hence the state of character 52 is coded as state 3. The morphological data obtained for P. cygnisetum is based on the examination of herbarium specimens of this species that are preserved in L and hb. Blöcher. All specimens examined come from Chile. Selected specimens are: Crosby 11682 (L), 12155 (L), Deguchi BSE 994 (L), Neger s.n. (L, c. 1897, “Anden von Villarica”; dwarf males), Blöcher 236 (hb. Blöcher; dwarf males). See Kruijer (2002) for an explanation of the method of character state coding and the sources used, and for an evaluation of the choices in character state coding that have been made for other species.

partitions were set for the combined dataset: morphological data, trnL intron and 3-exon, trnL–trnF spacer, rps4–trnS spacer and the rps4 gene. Substitution models were set separately for the morphological and sequence data. Each partition was allowed to have its own set of parameters and the overall rate to be different across partitions. The Markov Chain Monte Carlo (MCMC) analyses were run for 2,000,000 generations with four simultaneous MCMCs and one tree per 100 generations was saved. The “burn-in” values were determined empirically from the likelihood values. The analyses were repeated four times; the burn-in trees of each run were excluded before the trees were combined to construct a majority rule tree in PAUP to assess the representative posterior probability (PP) of the clades. The program Treegraph (Müller and Müller, 2004) was used to edit trees directly from the tree files. Morphological characters were optimized using Winclada version 1.000.08 (Nixon, 2002), assuming accelerated transformation (ACCTRAN). Character state changes were evaluated using MACCLADE version 3.0.8 (Maddison and Maddison, 1992).

1

1

1

2

2

2

? 3 1 1 2 2 1 1 1

1 4 3 3 2 2 1 1 1

Canalohy1 2 1 4 1 2 1 2 3 popterygium tamariscinum

1 2 4 4 2 2 2 2 3

1 4 4 4 2 2 2 2 3

1 4 4 4 2 2 2 2 3

1 4 4 4 2 2 2 2 3

Catharomnion ciliatum Cyathophorum adiantum

Cyathophorum africanum

Cyathophorum bulbosum

2

1

1

2 4 1 1 2 2 1 1 3

2 3 1 1 1 1 1 1 1

2

2 4 1 2 2 2 1 1 1

Hookeria lucens Hypnum cupressiforme

1

1

1

1

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3

1

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3

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4

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Outgroup 2 1 1

2

2

2

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2

2

2

1

2

2

2

1

2

2

2

2

1

1

2

1

1

1

2

1

2

2

1

1

1

1

1

3

1

1

3

3

1

1

1

2

2

1

?

3

3

3

1

3

3

3

3

1

1

1

3

3

3

3

1

3

1

3

1

1

1

1

1

1

1

1

1

1

1

3

1

3

2

1

1

1

1

1

1

2

1

1

3

1

1

1

1

1

1

1

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1

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2

1

1

4

1

4

2

2

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1

1

1

4

2

3

4

1

92

Leucodon sciuroides Neckera crispa Schimperobryum splendidissimum

1

3

1

Distichophyl- 2 4 1 1 1 2 1 1 1 lum pulchellum

1

1

Achrophyl1 4 1 1 1 1 1 1 3 lum dentatum 2 4 2 2 2 2 1 1 1 Adelothecium bogotense

3

1

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57

? 4 1 1 1 1 1 1 1

Ptychomnion cygnisetum

Character No.

TABLE 4.5 Morphological Data Matrix, Extracted from Kruijer (2002)

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1

2

2

1 2 1 4 1 2 1 2 3

1 2 4 4 1 2 1 2 3

1 3 4 4 1 2 2 2 3

1 3 4 4 1 2 2 2 3

Hypopterygium flavolimbatum

Hypopterygium tamarisci

Lopidium concinnum Lopidium struthiopteris 2

3

1

1

1

1

2

3

1

1

1

1

1

1

2

1

2

2

1

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2

?

1

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Note: Only the data for the taxa that are sampled for the final phylogenetic analyses of the present study is shown. The morphological data for Ptychomnion cygnisetum (Müll. Hal.) Kindb. was newly sampled for the present study. A question mark indicates unknown character states. Character numbers refer to characters listed in Table 4.4.

2

1

1

1 1 4 4 1 2 1 2 3

1

1

Dendrohy1 1 1 4 1 2 1 2 3 popterygium filiculiforme 1 1 1 4 1 2 1 2 3 Hypopterygium didictyon

Hypopterygium discolor

1

1

1 1 1 4 1 2 1 2 3

Dendrohypopterygium arbuscula

1

1

1 3 4 4 2 2 2 2 3

1

Dendrocyathophorum decolyi

2

1 4 4 4 2 2 2 2 3

Cyathophorum hookerianum

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TABLE 4.6 Total Number of Aligned Characters; Variable Characters and Number of Parsimony Informative Sites of the Data Subsets Used in the Combined Analyses (Sub)set No.

Dataset

Total No. of Characters

No. of Variable Characters

No. of Parsimony Informative Characters

1 2 3 4 5 6 7

Morphological characters trnL intron and 3-exon (partial) trnL–trnF spacer ITS2 region rps4–trnS spacer rps4 gene Combined dataset

57 479 128 481 107 595 1847

57 142 22 158 42 240 661

56 92 19 111 27 163 468

Note: The total number of characters in the combined dataset used in all analyses is 1847.

4.4 RESULTS The topology of the trees obtained from the MP analyses of the morphological dataset closely resemble those obtained by Kruijer (2002) and are not shown here. The trees obtained from the MP analyses of the molecular dataset are similar to the ones obtained from the MP analyses of the combined dataset. The analyses of the combined dataset, however, resulted generally in better supported branches and a higher resolution of, e.g., the Hypopterygiaceae clade and the results of these analyses are therefore presented here. The MP analyses of the complete dataset of morphological and sequence data resulted in six MPTs with a length of 1028 steps, CI of 0.571, RI of 0.533, and RC of 0.305, of which the consensus tree is shown in Figure 4.22. Several clades (e.g., Cyathophorum bulbosum–C. adiantum; the two Lopidium species, Catharomnion–Canalohypopterygium, and Dendrocyathophorum decolyi–Cyathophorum africanum) are well supported by high decay values (Figure 4.22) and bootstrap values (Figure 4.23). A phylogram of one of the six MPTs is shown in Figure 4.24. The 50% majority rule consensus cladogram resulting from the Bayesian inference analyses of the complete dataset is presented in Figure 4.25. The topology of the tree closely resembles those of the MP analyses, but is better resolved within the Hypopterygiaceae. All but one clade in the MP analyses with bootstrap support >70 % (Figure 4.23) received high (100%) PP, the exception being the Hypnales clade, with 82% bootstrap support and 79% PP. In most trees resulting from the MP analyses (e.g., Figure 4.24) and the trees resulting from the Bayesian inference analyses (Figure 4.25), the Hypopterygiaceae is presented as being monophyletic. However, support for this is weak (bootstrap 59%, PP 76%), which is also demonstrated by the strict consensus tree of the MP analyses (Figure 4.22). In most trees of both types of analyses, the first dichotomy within the Hypopterygiaceae splits the family in a Cyathophorum bulbosum–C. adiantum clade (99% bootstrap support, 100% PP) and the remainder of the Hypopterygiaceae (76% bootstrap support, 100% PP). The topology of the strict consensus tree resulting from the MP analyses (Figure 4.22, see also Figure 4.23) shows a polytomy for the remainder of the Hypopterygiaceae, in which are nested (1) the two Dendrohypopterygium species, (2) a weakly supported, polytomous clade (decay value 2, 58% bootstrap support) formed by Cyathophorum hookerianum and the representatives of Hypopterygium, and (3) three distinct clades: Catharomnion–Canalohypopterygium (decay value 6, 97% bootstrap support), Dendrocyathophorum decolyi–Cyathophorum africanum (decay value 12, 97% bootstrap support), and the two Lopidium species (decay value 18, 100% bootstrap support). In the 50% majority rule consensus tree resulting from the Bayesian inference analyses (Figure 4.25) the

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Ptychomnion cygnisetum

95

Ptychomniales

outgroup

Hypnum cupressiforme Leucodon sciuroides

d3

Hypnales

Neckera crispa Achrophyllum dentatum Adelothecium bogotense

d1 d3

Distichophyllum pulchellum

Hookeriales

Hookeria lucens Schimperobryum splendidissimum Canalohypopterygium tamariscinum d6

Catharomnion ciliatum Cyathophorum africanum

d12

Dendrocyathophorum decolyi Cyathophorum hookerianum

Hypopterygium discolor

d2

d4

d2

Hypopterygium tamarisci Hypopterygium flavolimbatum

d1

Hypopterygiaceae

Hypopterygium didictyon

Lopidium concinnum d18

Lopidium struthiopteris Dendrohypopterygium arbuscula Dendrohypopterygium filiculiforme Cyathophorum adiantum

d10

Cyathophorum bulbosum

FIGURE 4.22 Strict consensus of six MPTs (length 1028, CI: 0.571, RI 0.533, RC 0.305) found during the parsimony ratchet of the combined dataset (morphological and sequence data). Values under branches (“dvalue”) are decay values.

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Ptychomnion cygnisetum

Ptychomniales

outgroup

Hypnum cupressiforme 82 57

Leucodon sciuroides

Hypnales

Neckera crispa Canalohypopterygium tamariscinum

97

Catharomnion ciliatum Cyathophorum africanum

98

Dendrocyathophorum decolyi 58

Cyathophorum hookerianum

76

58 74

Hypopterygium discolor Hypopterygium tamarisci Hypopterygium flavolimbatum

Hypopterygiaceae

Hypopterygium didictyon

Dendrohypopterygium arbuscula 59

Dendrohypopterygium filiculiforme 100

Lopidium concinnum Lopidium struthiopteris Cyathophorum adiantum

99

Cyathophorum bulbosum Achrophyllum dentatum 64 98

Adelothecium bogotense Distichophyllum pulchellum

Hookeriales

Hookeria lucens Schimperobryum splendidissimum

FIGURE 4.23 Cladogram of a bootstrap analysis (1000 iterations) with PAUP. Numbers above branches are bootstrap values (%).

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Ptychomnion cygnisetum Hypnum cupressiforme 31

Leucodon sciuroides 12

Neckera crispa Canalohypopterygium tamariscinum 21

Catharomnion ciliatum

11 17

Dendrohypopterygium arbuscula Dendrohypopterygium filiculiforme

20 36

Cyathophorum africanum 36

Dendrocyathophorum decolyi Cyathophorum hookerianum

23

Hypopterygium didictyon

19

14

Hypopterygium flavolimbatum 12

Hypopterygium discolor

19

8

29

Hypopterygium tamarisci

14

Lopidium concinnum 32

Lopidium struthiopteris Cyathophorum adiantum 46

Cyathophorum bulbosum 70

Achrophyllum dentatum 21

Adelothecium bogotense 11 18

Distichophyllum pulchellum Schimperobryum splendidissimum Hookeria lucens

1

100

FIGURE 4.24 Phylogram of one of the six MPTs (length 1028, CI: 0.571, RI 0.533, RC 0.305). Length of the scale bar equals 100 characters.

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Ptychomnion cygnisetum

Ptychomniales

outgroup

Hypnum cupressiforme 79 69

Leucodon sciuroides

Hypnales

Neckera crispa 100

Catharomnion ciliatum

97 100

100

Canalohypopterygium tamariscinum

Cyathophorum africanum Dendrocyathophorum decolyi

49

Dendrohypopterygium arbuscula

Hypopterygium flavolimbatum

100

100

100

100

Cyathophorum hookerianum

Hypopterygium discolor Hypopterygium tamarisci

89

Hypopterygiaceae

93

Hypopterygium didictyon

76

Lopidium concinnum

100

77

Lopidium struthiopteris Dendrohypopterygium filiculiforme Cyathophorum adiantum

100

Cyathophorum bulbosum Achrophyllum dentatum 88 100 60

Adelothecium bogotense Distichophyllum pulchellum

88

Hookeriales

Hookeria lucens Schimperobryum splendidissimum

FIGURE 4.25 Fifty percent majority rule consensus cladogram resulting from a Bayesian inference analysis of the complete dataset. Numbers above branches indicate the posterior probabilities as a percentage value.

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remainder of the Hypopterygiaceae is split in two subclades. One subclade (100% PP) comprises Dendrohypopterygium arbuscula in a basal position and Catharomnion–Canalohypopterygium (100% PP) and Dendrocyathophorum decolyi–Cyathophorum africanum (100% PP) as terminal clades. The other (77% PP) comprises Dendrohypopterygium filiculiforme in a basal position and a grade consisting of the Lopidium clade as sister to a grade of representatives of Hypopterygium with Cyathophorum hookerianum in a terminal position. The topology of the “total evidence” trees resulting from the phylogenetic analyses of the complete dataset fits best with the topology of the trees obtained by the analyses of molecular data by Blöcher and Capesius (2002), but shows also a partial resemblance to the trees based on molecular data obtained by Stech et al. (2002) and, in particular, Buck et al. (2005). However, the “total evidence” trees differ significantly in topology from the trees resulting from the analyses of morphological data by Kruijer (2002) and our own study (not shown), which explains why the majority of the morphological character states are homoplasious in the results of the phylogenetic analyses of the complete dataset. This is shown in Figure 4.26, which presents the optimization of the morphological characters and character state changes on the 50% majority rule consensus tree resulting from the Bayesian inference analyses given in Figure 4.25.

4.5 DISCUSSION 4.5.1 CLADE COMPOSITION

AND

CHARACTER STATE EVOLUTION

The present study does not give a clear answer to the taxonomic position of the Hypopterygiaceae in the “true” pleurocarpous mosses, because it was not designed to do so: our primary objective was to evaluate the relationships of the Hypopterygiaceae. Only a small selection of non-hypopterygiaceous “true” pleurocarpous mosses was used in the analyses. The weak support for the monophyly of the Hypopterygiaceae in our results might, therefore, be due to unbalanced taxon sampling outside the Hypopterygiaceae; i.e., the representatives that we thought a priori would be closely related to the Hypopterygiaceae are in fact distantly related. The high number of equivocal states for the morphological characters at the base of the Hypopterygiaceae clade (not shown) also suggests a distant relationship. The ambiguous position of the Cyathophorum bulbosum–C. adiantum clade in the MP analyses (Figure 4.22) is also an indication for such distant relationship. The results of the recent study by Buck et al. (2005) with broad taxon sampling among the “true” pleurocarpous mosses also give some indication for an unbalanced taxon sampling. Buck et al. (2005) obtained strong support for the monophyly of the Hypopterygiaceae and found them to be the sister to the remainder of the Hookeriales. We found — with weak support — the Hypopterygiaceae to be sister to a clade consisting of the selected representatives of the Hypnales in our results from the Bayesian inference analyses, while our results from the MP analyses are inconclusive whether the Hypopterygiaceae are sister to the Hookeriales or the Hypnales. Apart from unbalanced taxon sampling among non-hypopterygiaceous “true” pleurocarpous mosses, differences in basal topology within the Hypopterygiaceae clade between our trees from the MP analyses and the Bayesian inference analyses and between our trees and those of Buck et al. (2005) suggest that the closest extant relative of the Hypopterygiaceae as a distinct family is still unknown. The clade comprising the Hypopterygiaceae is defined by three synapomorphic character states as evolutionary novelties (two substitutions, one indel) in the ITS2 region, but we found no support for this clade in the trnL region and the rps4 gene. However, the value of synapomorphies based on the ITS2 sequence data is limited due to the limited number of taxa for which ITS2 sequences were available, viz. eight species of Hypopterygiaceae and four species of possibly related taxa; see Table 4.3. Despite the weak support for the monophyly of the Hypopterygiaceae, we are convinced that the family actually forms a monophyletic group. Buck et al. (2005) obtained strong support for the monophyly of the Hypopterygiaceae in a phylogenetic study based on molecular data with broad taxon sampling among the “true” pleurocarpous mosses. In addition to this, we

1 2 3 3

Ptychomnion cygnisetum

19 20 26 28 45 52 55 57 3 2 2 3 3 1 2 2

5 11 2 3

31 3 19 27 52 2 2 1

Dendrocyathophorum decolyi

25 28 2 3

3 31 57 4 2 3

2 17 28 38 41 49 1 1 3 2 3 2

11 12 19 26 27 33 37 3 3 3 2 3 3 1 17 25 36 43 49 56 3 3 2 2 3 3

Lopidium struthiopteris

Lopidium concinnum

26 38 41 57 2 2 3 3

Hypopterygium flavolimbatum

2 41 1 3 Hypopterygium discolor 10 17 26 54 2 3 2 2 Hypopterygium tamarisci 2 3 5 7 10 15 17 18 19 22 23 25 30 32 33 36 37 39 43 44 46 47 48 49 50 52 53 54 57 4 4 2 2 2 2 3 1 1 3 3 3 2 2 2 2 2 2 2 2 2 2 2 3 2 2 2 2 1

Hypopterygium didictyon

2 3 7 10 11 12 18 22 24 29 33 35 37 48 49 50 57 3 4 2 2 2 2 1 1 2 2 2 2 2 2 2 2 3

13 19 27 1 3 3

Cyathophorum hookerianum

Cyathophorum africanum

28 38 41 49 1 2 3 2 Canalohypopterygium tamariscinum 3 5 7 10 19 27 37 40 41 42 50 55 4 2 2 2 2 2 1 2 1 2 2 2 Catharomnion ciliatum

22 23 31 33 54 3 2 3 1 3

2 10 18 31 32 33 36 37 39 41 43 44 46 47 48 49 50 51 4 2 1 1 2 3 2 2 2 1 2 2 2 2 2 3 2 2

Dendrohypopterygium filiculiforme

12 14 18 31 52 53 3 2 4 1 3 3 2 18 20 28 38 56 1 1 1 1 2 2

12 2

2 3 5 7 26 27 28 30 52 57 3 4 2 2 2 3 3 2 1 1

Dendrohypopterygium arbuscula

Cyathophorum bulbosum

100

FIGURE 4.26 Optimization of the 57 morphological characters presented in Table 4.3 on the cladogram of Figure 4.25. Boxes represent apomorphies: black boxes indicate evolutionary novelties; white boxes indicate homoplasious character states. The numbers in the boxes indicate the character state of the apomorphy. For plotting character state changes the configuration of the character optimization was followed for equivocal character states.

2 13 16 17 22 23 37 39 2 2 3 2 2 1 3 1

33 2

16 34 39 52 2 3 1 3 2 19 22 28 30 31 38 52 1 3 1 1 2 3 2 3

Cyathophorum adiantum

Leucodon sciuroides

27 28 41 43 44 46 48 49 50 52 2 3 1 2 2 2 2 3 2 1

Neckera crispa

6 15 18 24 25 33 36 39 40 45 47 51 1 2 1 2 3 2 2 1 2 3 2 2

3 5 7 10 15 25 30 32 33 34 53 54 55 57 4 2 2 2 2 3 2 2 3 2 3 3 3 4

2 17 30 31 41 43 46 48 49 50 52 3 2 2 3 1 2 2 2 3 2 1

Adelothecium bogotense

Distichophyllum pulchellum

3 4 5 14 17 23 24 25 32 33 35 36 38 56 2 2 2 3 3 1 2 3 2 3 2 2 2 2

Hypnum cupressiforme

1 11 18 27 48 2 3 1 3 2

1016 17 18 21 26 2834 37 57 2 2 2 1 2 2 3 3 3 4 Hookeria lucens 4 11 25 28 32 3341 48 49 5152 3 3 3 1 2 3 1 2 3 2 1 Schimperobryum splendidissimum 6 9 16 18 25 28 30 33 37 38 39 44 45 52 57 1 3 3 3 3 3 2 3 3 2 1 2 3 3 4 Achrophyllum dentatum

5 9 18 40 41 51 2 3 1 2 3 2

17 22 23 41 45 2 1 2 1 3

4 8 9 20 57 4 2 3 2 2

1 21 28 2 2 1

31 50 53 57 1 2 3 3

4 5 2 2

6 11 21 31 36 37 41 45 52 55 1 3 2 3 2 3 3 3 3 3

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found that the “traditional” features that define the Hypopterygiaceae as a distinct group, i.e., tristichous phyllotaxy of distal stem, rachis or branch parts in combination with heterophyllous foliation (characters 4 and 8, Table 4.4), are synapomorphic character states and evolutionary novelties in morphology for the family (Figure 4.26). Finding the Cyathophorum bulbosum–C. adiantum clade as the sister to the remainder of the Hypopterygiaceae confirms the earlier molecular analyses by Blöcher and Capesius (2002), Buck et al. (2005), and some of our preliminary analyses. This clade is defined by three synapomorphic genetic character states, viz. one substitution in the trnL region and two in the rps4 gene. The basal position of the clade is in sharp contrast with the results obtained by Kruijer’s (2002) phylogenetic analyses based solely on morphological data, in which the two Cyathophorum species are nested in a terminal clade consisting of the remainder of Cyathophorum. Buck et al. (2005) proposed to resurrect the Cyathophoroideae (Kind.) Broth. for this core of Cyathophorum, but recognition of subfamilies within such a small family as the Hypopterygiaceae is in our opinion, even in the present cladistic configuration, superfluous. Comparing the results of our present study with those of the earlier studies based on molecular data (Blöcher and Capesius, 2002; Buck et al., 2005; Stech et al., 2002) and those based on morphological data (i.e., Kruijer, 1995a, 1995b, 2002) as metadata indicates that the core of Cyathophorum, viz. the species centred around the Cyathophorum bulbosum–C. adiantum clade, is probably monophyletic. Not all species have been used in the molecular studies so far, but if we take the outcome of earlier analyses based on morphological data (Kruijer, 1993, 1995b) into consideration, we predict that this core consists of the following four species: Cyathophorum bulbosum, C. tahitense Besch., C. spinosum (Müll. Hal.) H. Akiyama and C. adiantum. A widened seta base (character 34, state 3) is presumably the morphological synapomorphy for this group of species (cf. Figure 4.26, where in the present configuration, viz. a clade consisting of two species, the state of character 34 is presented as state 2). The short, mitrate calyptra represents two homoplasious synapomorphic character states for this clade (character 53, state 3; character 54, state 4; Figures 4.12 and 4.26). Our trees from both the MP analyses (e.g., Figure 4.23) and the Bayesian inference analyses (Figure 4.25) indicate that the remainder of the Hypopterygiaceae is monophyletic. This core of Hypopterygiaceae is defined by morphological synapomorphies such as, e.g., a habit with a broad amplitude of plasticity ranging from pinnate to palmate or umbellate (character 2, state 2), the presence of axial cavities in ultimate branches (character 13, state 2), and the costa of the lateral leaves in the distal part of the frond ranging in length from 1/2 to 4/5 of the length of the leaf (character 22, state 2; Figure 4.26). The core of the Hypopterygiaceae is also defined by three synapomorphic character states (three substitutions of 1 bp each) in the rps4 gene. The trees from the MP analyses are inconclusive concerning the basal subdivision of the core of the Hypopterygiaceae, but those from the Bayesian inference analyses reveal that this clade is divided in two sister clades, in each of which one of the two Dendrohypopterygium species has a basal position. A similar division of the core of the Hypopterygiaceae in two subclades was also found in some of the MP analyses performed by Blöcher and Capesius (2002), but was not found by Kruijer (2002), whose attempts to resolve the basal topology of the Hypopterygiaceae clade in phylogenetic analyses based on morphological data was hampered by a high number of equivocal ancestral character states. Comparing basal tree topology of the core of the Hypopterygiaceae with the results obtained in the molecular studies by Buck et al. (2005) and Stech et al. (2002) is limited by differences in taxon sampling. Nevertheless, the configuration of the trees of Buck et al. (2005) lends support to a subdivision of the core of the Hypopterygiaceae in two subclades, as we found in our Bayesian inference analyses. The first subclade comprises Dendrohypopterygium arbuscula, Dendrocyathophorum decolyi, Cyathophorum africanum, Canalohypopterygium tamariscinum (Hedw.) Kruijer and Catharomnion ciliatum. It is genetically defined by five substitutions (1 bp each) and two indels (2 to 3 bp) in ITS2 (note the reservations about the ITS2 synapomorphies expressed above, and that also apply below)

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and two synapomorphic substitutions in the rps4 gene (1 bp each), and morphologically weakly defined by the homoplasious synapomorphy of the intermediate seta length (character 33, state 2; Figure 4.26). The second subclade consists of Dendrohypopterygium filiculiforme, the Lopidium and Hypopterygium species, and Cyathophorum hookerianum. It is genetically defined by two synapomorphic substitutions in the rps4 gene and one in the trnS–rps4 spacer (1 bp each) and is morphologically weakly defined by the homoplasious synapomorphy of the intermediate vaginula length (character 31, state 2; Figure 4.26). The results obtained by the molecular studies performed since 2002 and the subdivision of the core of the Hypopterygiaceae in two subclades found in the Bayesian inference analyses of our “total evidence” study confirm the polyphyly of Dendrohypopterygium s. lat. and support the recognition of Arbusculohypopterygium as a separate, monotypic genus (Stech et al., 2002) that accommodates Kruijer’s (2002) second Dendrohypopterygium species (D. arbuscula). The presence of the unique rudimentary branches (character 14, state 2) in Catharomnion ciliatum and Canalohypopterygium tamariscinum serves, as expected, as a good synapomorphic morphological character state for the well-supported Catharomnion–Canalohypopterygium clade; another such character state for this clade is the, at least partial, presence of cilia at the margin of the leaves (character 18, state 4; Figure 4.26). The transition of the axial cavities from central to cortical in the stipe and the basal and middle parts of the rachis is shown to be a homoplasious synapomorphy for this clade (character 12, state 3, Figure 4.26). The straight rostrum (character 52, state 3) and the mitrate calyptra (character 53, state 3) are two other homoplasious synapomorphies for this clade (Figures 4.12 and 4.26). Genetically, the Catharomnion–Canalohypopterygium clade is defined by four synapomorphic substitutions, viz. three in the trnL region and one in the rps4 gene (each 1 bp in length). Blöcher and Capesius (2002) and Stech et al. (2002) found evidence for a relationship between Dendrohypopterygium [Arbusculohypopterygium] arbuscula, Dendrocyathophorum, and the Catharomnion–Canalohypopterygium clade, which is confirmed by Buck et al.’s (2005) work. The configuration of the results of our Bayesian inference analyses corresponds with such a relationship, but also indicates that the evolutionary history of this group of species was more complex. In the results of our MP analyses as well as our Bayesian inference analyses, Dendrocyathophorum decolyi and Cyathophorum africanum are grouped in a well-supported monophyletic clade with a terminal position as sister to the Catharomnion–Canalohypopterygium clade. This finding is one of the more original findings of this study. The clade consisting of Dendrocyathophorum decolyi and Cyathophorum africanum is defined by three substitutions (1 bp each) and one indel (9 bp) in the trnL region and a single substitution of 1 bp in the rps4 gene as synapomorphies. The central axial cavity that Dendrocyathophorum decolyi and Cyathophorum africanum have in common is shown to be a homoplasious synapomorphy for the clade comprising Dendrocyathophorum decolyi, Cyathophorum africanum, Catharomnion ciliatum and Canalohypopterygium tamariscinum and is a plesiomorphy for the Dendrocyathophorum decolyi–Cyathophorum africanum clade (character 12, state 2; Figure 4.26). Cyathophorum africanum may either be accommodated in its own monotypic genus or be transferred to Dendrocyathophorum. The series of homoplasious autapomorphies (Figure 4.26) that separates Cyathophorum africanum from Dendrocyathophorum decolyi, including character states arising from peristome reductions, favours initially the first option. The systematic implications are further discussed below. Dendrohypopterygium filiculiforme is placed in a basal position in the second subclade of the core of the Hypopterygiaceae, which also includes the Lopidium clade and a terminal clade consisting of four Hypopterygium species and Cyathophorum hookerianum (Figure 4.25). The clade comprising the Lopidium species, the Hypopterygium species and Cyathophorum hookerianum is supported with two synapomorphic substitutions in ITS2. The Lopidium clade is defined by six substitutions (1 bp) and one indel (3 bp) in the rps4 gene and one substitution (1 bp) in the trnL intron as genetic synapomorphies, and by a high number of homoplasious morphological synapomorphies. The, at least occasional, presence of leaf-like paraphyses in full-grown perichaetia serves as a single

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morphological synapomorphy for the Lopidium clade (character 29, state 2; Figure 4.26). The frequent absence of a central strand from stems and branches (character 11, state 2) also represents a synapomorphy for this clade (Figure 4.26), but evaluation of the character state changes showed that the character state is actually equivocal. The four Hypopterygium species included in our phylogenetic analyses are grouped in a terminal paraphyletic grade together with the Indo-Malaysian species Cyathophorum hookerianum. The clade comprising the Hypopterygium species and Cyathophorum hookerianum is defined by six genetic synapomorphies, viz. four substitutions (1 bp each) in the rps4 gene, one substitution (1 bp each) and one indel (14 bp) in the trnL intron, as well as four synapomorphic substitutions in the ITS2. The confirmation of the remarkable position of C. hookerianum in a clade comprising Hypopterygium species and placed far away from the core of Cyathophorum is another marked finding of our study. Our finding corresponds not only with the results obtained in our preliminary phylogenetic analyses and by Buck et al. (2005), but also with the results obtained by Shaw and co-workers, who found Cyathophorum hookerianum grouped with its Indo-Malaysian sister species C. parvifolium Bosch and Sande Lac. in a clade with a similar position (Shaw, personal communication). The clade consisting of Cyathophorum hookerianum and Hypopterygium flavolimbatum Müll. Hal. is defined by a synapomorphic substitution in the trnL of 1 bp as sole genetic evolutionary novelty. Cyathophorum hookerianum is separated from Hypopterygium flavolimbatum by a series of homoplasious autapomorphies (Figure 4.26), among which character states arising from peristome reductions and the circular to elliptic outline of the short terminal cell of the axillary hairs (character 17, state 3; Figure 4.11.L). This character state may well be synapomorphic for a clade consisting of the sister species Cyathophorum hookerianum and C. parvifolium, but it should be remarked that axillary hairs with a short and circular to elliptic terminal cell also occur in Hypopterygium tamarisci and Hypopterygium sandwicense Broth. (not sampled for the present analyses; Kruijer, 2002), albeit that the outline of the terminal cell in the two Cyathophorum species is generally more circular than in those species. Cyathophorum hookerianum and C. parvifolium may either be transferred to Hypopterygium or the former genus Cyathophorella might be resurrected for these two species. The systematic implications of the position of Cyathophorum hookerianum (and C. parvifolium) are further discussed below.

4.5.2 EVOLUTION

OF

MORPHOLOGICAL CHARACTERS

It is evident that the recent findings in phylogeny reconstruction lead to new insights in the evolutionary history of the Hypopterygiaceae. Kruijer (2002) summarized the general pattern of character state changes within the Hypopterygiaceae as shifting from complex to simple, but our present results show that the evolutionary history of morphology within the Hypopterygiaceae is actually more complex. In marked contrast with Kruijer’s (2002) hypothesis that the Hypopterygiaceae is derived from the presumably terrestrial dendroid ancestor of Dendrohypopterygium filiculiforme, D. arbuscula, or both, these characteristic terrestrial dendroid species are indicated as being derived from ancestors with simple or weakly branched gametophores (character 2: state 4→1). These ancestors were presumably epiphytic or saxicolous species or species with a broad amplitude for substrate type, ranging from terrestrial to epiphytic, similar to the extant Cyathophorum species. The state of character 2 (habit) at the base of the core of the Hypopterygiaceae is given in the character optimization (Figure 4.26) as ranging from pinnate to dendroid (character 2, state 2), but character state evaluation gives this state as being equivocal (character 2, state 1 or 4). Whether the transition from simple or weakly branched gametophores to dendroid with a stipe and a strongly branched frond originated once or twice, or occurred via an intermediate transition state consisting of a habit with a broad amplitude ranging from fan to dendroid, it came presumably with a shift towards a more strict occupation of the terrestrial habitat and might have been induced by the specific conditions of the forest floor (e.g., more stable and constantly high humidity, ample space, litter). Species with facultative fans or dendroids (character 2: state 2; e.g., Catharomnion ciliatum, Hypopterygium flavolimbatum, H. tamarisci) and with obligate fans (character 2: state 3; e.g., Dendrocyathophorum decolyi, Lopidium

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species) are scattered throughout the Hypopterygiaceae and may have either retained the plesiomorphic condition of the core of the Hypopterygiaceae or gained a new character state for the character “habit,” with obligate fans most likely representing an evolutionary novelty. Species with simple or weakly branched gametophores, i.e., Cyathophorum species and some male plants of Catharomnion ciliatum (Figure 4.14.C), also occur scattered throughout the Hypopterygiaceae (Figure 4.26; the features of the male plants of Catharomnion ciliatum were not used in the analyses), indicating that several descendents of the basal Hypopterygiaceae regained the plesiomorphic habit condition. Tristichous phyllotaxy and heterophyllous foliation of the distal parts of the stem or rachis and branches (character 4, state 4; character 8, state 2) are synapomorphies for all Hypopterygiaceae (Figure 4.26). Homophyllous foliation of the basal part of the stem or stipe (character 7, state 1) is a plesiomorphic condition for the Hypopterygiaceae, but the state of the phyllotaxy of the basal part of the stem or stipe is equivocal (character 3, state 1 or 4). In our character optimization (Figure 4.26) octostichous phyllotaxy of the basal part of the stem (stipe) is assumed to be a plesiomorphy for the Hypopterygiaceae. If so, the shift towards tristichous phyllotaxy (character 3: state 1→4) has occurred, at least, six times independently (Figure 4.26). In the reverse situation, the shift from tristichous to octostichous phyllotaxy (character 3: state 4→1) must have occurred at least four times independently. It should be remarked here, however, that the occurrence of tristichous phyllotaxy of the stipe of tiny plants of Hypopterygium flavolimbatum, in which the phyllotaxy is often difficult to ascertain, was not used in the analyses (cf. Kruijer, 2002). Within the Hypopterygiaceae, heterophyllous foliation is restricted to axes or parts of axes with tristichous phyllotaxy, whereas homophyllous foliation may not only occur in axes or parts of axes with octostichous phyllotaxy, but also in those with tristichous phyllotaxy, as on the stipe of Hypopterygium discolor (Kruijer, 2002). The combination of heterophylly and tristichous phyllotaxy in the basal part of the stem may be correlated with epiphytic or saxicolous growth: all plants of obligate epiphytic and saxicolous species — the fans — have an entirely tristichous phyllotaxy (Kruijer, 2002) and almost all of them have entirely heterophyllous foliation. The only exception in this respect is a minority of the plants within the mainly epiphytic and saxicolous species Lopidium concinnum, in which entirely homophyllous foliation is combined with entirely tristichous phyllotaxy (Kruijer, 2002). The presence of cygneous or uncinate sporophytes projecting above the gametophores (character 32: state 1; Figure 4.7.A) represents a plesiomorphic character state for the Hypopterygiaceae. The transition towards straight or curved spore capsules that are projecting beneath the gametophore (character 32: state 2; Figure 4.7.B) is a homoplasious synapomorphy for the Cyathophorum bulbosum–C. adiantum clade, and a homoplasious autapomorphy in C. africanum and in C. hookerianum (Figure 4.26). A well-developed, complete peristome (Figure 4.9) is the plesiomorphic condition for the Hypopterygiaceae. Peristome reductions (character 43, state 2; character 44: state 2; character 46: state 2; character 48, state 2; character 49, state 3; character 50, state 2) are scattered throughout the Hypopterygiaceae (Figures 4.8 and 4.26), but are found only in epiphytic and saxicolous plants. However, in other epiphytic and saxicolous species reduced peristome structures are absent, for example in the obligate epiphytic species Dendrocyathophorum decolyi and the facultative epiphytic and saxicolous species Cyathophorum bulbosum, Hypopterygium tamarisci, H. flavolimbatum and Lopidium concinnum. The peristome of the latter is partly reduced, with plesiomorphic reductions in characters 48 to 50.

4.5.3 SYSTEMATIC IMPLICATIONS The phylogenetic relationships between the species of the Hypopterygiaceae obtained in our analyses (Figures 4.22 to 4.26) make classification at the generic level complicated. A strictly cladistic classification into truly monophyletic groups for the generic subdivision of the Hypopterygiaceae based on the classification that is in current use is premature, because not every species

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of this family could be sampled for the phylogenetic analyses. This is especially relevant for the classification of Cyathophorum hookerianum and C. africanum and the taxa to which they are closely related. For a good insight into the position of Cyathophorum hookerianum and the previously unexpected relationships of this species with Hypopterygium species, the sampling of Hypopterygium vriesei Bosch and Sande Lac. for a new series of phylogenetic analyses is absolutely essential. Equally important is the sampling of Hypopterygium sandwicense to get a good insight into the position of Cyathophorum africanum and related taxa, This is especially so because H. sandwicense shows a remarkable, but perhaps plesiomorphic, resemblance in stem anatomy to C. africanum and its sister species Dendrocyathophorum decolyi by having a central cavity with inclusions in the distal part of the frond axes. However, sequencing material of Hypopterygium sandwicense will be a challenge. There are only a few and old herbarium specimens of this Hawaiian endemic species preserved. Kruijer (2002) could examine only thirteen specimens including duplicates for his revision and there are only three specimens housed in the Bishop Museum (Brandon Stone, personal communication). The most recent collection known to us is the one made by Hoe near Kulani Honor Camp on Hawaii in 1966. It is not known where in the Hawaiian Islands populations of H. sandwicense are present today. A few years ago, Hawaiian and Dutch bryologists visited the locations where H. sandwicense had been collected a few decades ago, i.e., the Saddle Road and Kulani Honor Camp areas, but the species has not been found there, nor has it been found elsewhere (Brandon Stone and Joop Kortselius, personal communication). Nevertheless, almost regardless of the outcome of an eventual new series of phylogenetic analyses including the remaining species of the Hypopterygiaceae (i.e., Cyathophorum parvifolium, C. tahitense, C. spinosum, Hypopterygium sandwicense, H. vriesei and H. elatum Tixier), classification for the generic subdivision of the Hypopterygiaceae will remain problematic. The tremendous discontinuous morphological diversity that is present within the family has resulted in the recognition of five monotypic genera — that is quite a lot within such a small family of mosses. In the results of all recently performed phylogenetic studies, Canalohypopterygium tamariscinum and Catharomnion ciliatum are found to be placed in a well-defined clade. Despite the fact that they are unambiguously each other’s closest relatives, both species were previously kept separate in monotypic genera because they differ significantly from each other in many qualitative and quantitative gametophytic and sporophytic features (Frey and Schaepe, 1989; Kruijer, 2002; Stech et al., 1999, 2002). In addition, there are no extant intermediate species or groups of species that fill the morphological gaps between the two species (Kruijer, 2002). If we follow this policy for our present findings, Cyathophorum africanum will inevitably have to be accommodated in its own monotypic genus. However, the results of our study clearly show that most morphological characters sampled for the analyses have limited value in the recognition of taxonomic groups beyond the level of species and closely related allies (Figure 4.26). Only few morphological characters reveal information on the deep evolutionary history of the family. The morphological characters studied are probably more representative of adaptations of the sampled taxa to similar ecological conditions in similar habitats than of characters providing information on their deep evolutionary history. Furthermore, at the specific and supraspecific levels, morphology probably shows more plasticity in an evolutionary-adaptive sense than previously thought, which in turn implies that the significance of morphological characters has to be reevaluated in a new perception of morphology to understand and unravel the deep evolutionary history of the Hypopterygiaceae, and perhaps of the entire pleurocarpous mosses (cf. Hedenäs, 1998). That is, of course, if our present findings and those by Buck et al. (2005) and Shaw and co-workers (Shaw, personal communication) are confirmed by new studies based on broader taxon sampling among the Hypopterygiaceae and using sequence data of other regions of the genome. In this respect, it is of utmost importance to include complete ITS2 sequence data for all taxa used in the analyses, in particular the Hypopterygiaceae, and to include markers that are more variable than the trnL and rps4 regions (Table 4.6), e.g., the nad5 region from the mtDNA. We have little doubt, however, that in such studies with broader sampling our present findings will be confirmed.

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The important consequence of such confirmation will be that the arguments to keep Canalohypopterygium tamariscinum and Catharomnion ciliatum in separate genera are no longer valid. The morphological differences between these two species are in that case nothing more than differences between species. If so, there are no morphology-related objections to a classification of the Hypopterygiaceae into two genera, a classification which will be close to the ones proposed by mid-nineteenth century authors like Müller (1851) and Hooker (1867), or even against the merger of all the species of this family into a single genus.

ACKNOWLEDGMENTS We thank Volker Buchbender (University of Koblenz), Eberhard Fischer (University of Koblenz) and Andreas Solga (University of Bonn) for providing us fresh material of Cyathophorum africanum from Kenya. Special thanks are due to Conny Löhne (University of Bonn) for the introduction to the computer program WinClada and her assistance with the construction of Figure 4.26 and Pieter Pelser (Miami University, Oxford, Ohio) for his valuable comments on the manuscript. We very much appreciate the kind help by Dietmar Quandt (Technical University of Dresden), who provided us various DNA sequences and performed the alignment. Permission to use material in the following figures is gratefully acknowledged: Nationaal Herbarium Nederland: Figures 4.6, 4.7, 4.8, 4.9, 4.10, 4.11, 4.12, 4.13, 4.14, 4.15, 4.17; Dutch Bryological and Lichenological Society: Figure 4.16; Association des Amis des Cryptogames: Figures 4.18 and 4.19; Royal Society of New Zealand: Figures 4.20 and 4.21.

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Huttunen, S. and Ignatov, M. S. (2004) Phylogeny of the Brachytheciaceae (Bryophyta) based on morphology and sequence level data. Cladistics, 20: 151–183. Jaeger, A. (1876) Genera et species muscorum systematice disposita seu Adumbratio florae muscorum totius orbis terrarum. Bericht über die Thätigkeit der St. Gallischen naturwissenschaftlichen Gesellschaft, 1874–75: 85–188. Kindberg, N. C. (1898) Studien über die Systematik der pleurokarpischen Laubmoose. Botanisches Centralblatt, 76: 84–87. Kindberg, N. C. (1899) Studien über die Systematik der pleurokarpischen Laubmoose 3. Botanisches Centralblatt, 77: 385–395. Kindberg, N. C. (1901) Grundzüge einer Monographie über die Laubmoos-Familie Hypopterygiaceae. Hedwigia, 40: 275–303. Kluge, A. G. and Farris, J. S. (1969) Quantitative phyletics and the evolution of anurans. Systematic Zoology, 18: 1–32. Kruijer, J. D. (H.) (1993) De systematiek van de Cyathophoroideae: een introduktie (Abstr.). Buxbaumiella, 31: 31–37. Kruijer, J. D. (1995a) Systematics of the moss family Hypopterygiaceae Mitt. (Abstr.). Acta Botanica Neerlandica, 44: 492. Kruijer, J. D. (H.) (1995b) Systematiek van de Hypopterygiaceae (Abstr.). Buxbaumiella, 38: 26–32. Kruijer, J. D. (H.) (1996) Phylogeny of the Hypopterygiaceae Mitt. (Abstr.). The British Bryological Society Centenary Symposium, Glasgow (4–8 August), University of Glasgow, Glasgow, pp. 23. Kruijer, J.D. (2002) Hypopterygiaceae of the World. Blumea Supplement, 13: 1–388 (PhD thesis, Leiden University). Maddison, W. P. and Maddison, D. R. (1992) A user manual for MacClade (Analysis of Phylogeny and Character Evolution), xi + 398 pp. Sinauer Associates, Sunderland, Massachusetts. Magill, R. E. and Van Rooy, J. (1998) Bryophyta, Part 1, Musci. In Flora of Southern Africa (ed. O. A. Leistner). National Botanical Institute, Pretoria, pp. 1–622. Miller, H. A. (1971) An overview of the Hookeriales. Phytologia, 21: 243–252. Mitten, W. (1859) Musci Indiae orientalis; an enumeration of the mosses of the East Indies. Journal of the Proceedings of the Linnaean Society, Supplement to Botany, 1: 1–171. Müller, C. (1851) Synopsis muscorum frondosorum. 2. Alb. Foerstner, Berlin, pp 1–736. Müller J. and Müller, K. (2004) TreeGraph: Automated drawing of complex tree figures using an extensible tree description format. Molecular Ecology Notes, 4: 786–788. Available from http://www.botanik.unibonn.de/system/downloads/ Müller, K. (2004) PRAP — calculation of Bremer support for large data sets. Molecular Phylogenetics and Evolution, 31: 780–782. Available from: http://www.botanik.uni-bonn.de/system/downloads/. Nixon, K. C. (1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics, 15: 407–414. Nixon, K. C. (2002) WinClada. Version 1.00.08. Published by the author, Ithaca, NY. Noguchi, A. (1936) Studies on the Japanese mosses of the orders Isobryales and Hookeriales. I. Journal of Science of Hiroshima University, Series B, Division 2 (Botany), 3: 11–26, pl. 1–2. Noguchi, A. (1951) Musci japonici (1) Hypopterygiaceae. Journal of the Hattori Botanical Laboratory, 6: 24–32. Noguchi, A. (1952) Musci Japonici (1). Hypopterygiaceae (2). Journal of the Hattori Botanical Laboratory, 7: 1–22. Pedersen, N. and Hedenäs, L. (2002) Phylogeny of the Plagiotheciaceae based on molecular and morphological evidence. Bryologist, 105: 310–324. Pelser, P. B., Kruijer, H. (J. D.) and Verpoorte, R. (2002) What is the function of oil-containing rudimentary branches in the moss Canalohypopterygium tamariscinum? New Zealand Journal of Botany, 40: 149–153. Pfeiffer, T. (2000) Relationships and divergence patterns in Hypopterygium “rotulatum” s. l. (Hypopterygiaceae, Bryopsida) inferred from trnL intron sequences. Studies in austral temperate rain forest bryophytes 7. Edinburgh Journal of Botany, 57: 291–307. Pfeiffer, T., Kruijer, H. (J. D.), Frey, W. and Stech, M. (2000) Systematics of the Hypopterygium tamarisci complex (Hypopterygiaceae, Bryopsida): Implications from morphological and molecular data. Studies in austral temperate rain forest bryophytes 9. Journal of the Hattori Botanical Laboratory, 89: 55–70.

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Posada, D. (2004) Modeltest 3.5, Free software. Available at http://darwin.uvigo.es/software/modeltest.html. Quandt, D., Tangney, R. S., Frahm, J.-P. and Frey, W. (2000) A molecular contribution for understanding the Lembophyllaceae (Bryopsida) based on noncoding chloroplast regions (cpDNA) and ITS2 (nrDNA) sequence data. Journal of the Hattori Botanical Laboratory, 89: 71–92. Reimers, H. (1953) Über die “dimorphen” Amphigastrien von Hypopterygium setigerum. Berichte der deutschen botanischen Gesellschaft, 66: 409–420. Robinson, H. (1971) A revised classification for the orders and families of mosses. Phytologia, 21: 289–293. Sainsbury, G. O. K. 1955. A handbook of the New Zealand mosses. Royal Society of New Zealand Bulletin, 5: 1–490, pl. 1–76. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution, 57: 2226–2241. Stech, M. and Frahm, J.-P. (2001) The systematic position of Ochyraea tatrensis (Hypnobartlettiaceae, Bryopsida) based on molecular data. Bryologist, 104: 199–203. Stech, M., Pfeiffer, T. and Frey, W. (1999) Molecular systematic relationships of temperate austral Hypopterygiaceae (Bryopsida): Implications for taxonomy and biogeography. Studies in austral temperate rain forest bryophytes 3. Hausknechtia Beiheft, 9: 359–367. Stech, M., Pfeiffer, T. and Frey, W. (2002) Molecular generic classification of the Hypopterygiaceae (Bryopsida), with the description of a new genus, Arbusculohypopterygium gen. nov. Studies in austral temperate rain forest bryophytes 10. New Zealand Journal of Botany 40: 207–221. Stech, M., Quandt, D., Lindlar, A. and Frahm, J.-P. (2003) The systematic position of Pulchrinodus inflatus (Pterobryaceae, Bryopsida) based on molecular data. Studies in austral temperate rain forest bryophytes 21. Australian Systematic Botany, 16: 561–568. Swofford, D. L. (2002) PAUP* 4b10. Phylogenetic Analysis Using Parsimony (*and other Methods). Sinauer Associates, Sunderland. Walther, K. (1983) Bryophytina. Laubmoose. In A. Engler’s Syllabus der Pflanzenfamilien. Kapitel, Vol. 2 (ed.. J. Gerloff and J. Poelt). Gebrüder Borntraeger Verlag, Berlin, pp. 1–108. Whittemore, A. and Allen, B. (1989) The systematic position of Adelothecium Mitt. and the familial classification of the Hookeriales (Musci). Bryologist, 92: 261–271. Wilson, W. (1855) Musci. In The Botany of the Antarctic Voyage. 2. Flora Novae-Zelandiae. Part 2. Flowerless Plants (ed. J. D. Hooker). Lovell Reeve, London, pp. 57–125.

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Patterns in 5 Growth Calyptrochaeta Desv. (Daltoniaceae) Boon-Chuan Ho and Hans (J.D.) Kruijer CONTENTS Abstract ..........................................................................................................................................111 5.1 Introduction...........................................................................................................................111 5.2 Growth Patterns in Calyptrochaeta ......................................................................................112 5.3 Discussion.............................................................................................................................114 5.4 Conclusions...........................................................................................................................115 Acknowledgments ..........................................................................................................................115 References ......................................................................................................................................115

ABSTRACT Calyptrochaeta Desv. is a small genus of pleurocarpous mosses. Malesian Calyptrochaeta species show striking differences in habit, which result from differences in growth pattern. Orthotropic and plagiotropic types of growth pattern can be distinguished. Species showing the first type form ± equally long, simple or sparingly forked, orthotropic axes with determinate growth and sympodial orthotropic innovations, which also show determinate growth. Species showing the second type form long plagiotropic axes with monopodial, indeterminate growth. Branches are few and also show indeterminate growth. The most important underlying difference between the orthotropic and plagiotropic type of growth pattern is whether the axes remain erect or become prostrate in a later ontogenetic stage. Hence, striking differences in habit should not be overestimated in phylogenetic and taxonomic research on Calyptrochaeta.

5.1 INTRODUCTION Calyptrochaeta Desv. (Eriopus (Brid.) Brid., nom illeg.; Daltoniaceae Schimp. sensu Buck & Goffinet, 2000; cf. Buck et al., 2004) is a small genus of small to large pleurocarpous mosses and comprises approximately 30 species (Streimann, 2000). The genus is mainly distributed in the tropical regions of the world, where the plants grow mainly on humus, decaying wood or tree bases in wet tropical mountain forests. Calyptrochaeta is characterized by having complanately foliated and frequently gemmiferous stems, distinctly bordered leaves with a short, forked costa, thick and spiny setae, and fringed calyptrae. Preliminary results of the forthcoming revision of Calyptrochaeta species reported from Malesia and adjacent areas by the first author reveal that seven species can be recognized. Members of the genus, at least the Malesian ones, demonstrate several morphological features remarkable for mosses, e.g., two-celled teeth at leaf margins that are composed of the proximal and the distal part 111

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FIGURE 5.1 Habit of a typical plant of Calyptrochaeta remotifolia (Mull. Hal.) Z. Iwats., B.C. Tan & Touw (orthotropic type of growth pattern) showing a bundle of ± equally long, radiating axes connected at the base by a dense tomentum (De Vriese s.n., L).

of two curved, adjacent margin cells (cf. Ninh, 1981), filiform gemmae with a peculiar, obliquely downwards directed branching and with a specialized thin-walled abscission cell at the base (Correns, 1899; Goebel, 1898), and rhizoids sprouting from the seta base (Fleischer, 1908; Goebel, 1898). This chapter, however, focuses on another interesting aspect of Calyptrochaeta morphology: the striking differences in habit that occur between Malesian species resulting from two seemingly different growth patterns. For the present study, herbarium specimens from the following herbaria were examined (abbreviations follow Holmgren et al., 1990): B, BM, CAHUP, CBG, FH, G, GRO, H, KLU, KYO, L, NICH, NMW, NY, PC, S, SING, SINU and UKMB.

5.2 GROWTH PATTERNS IN CALYPTROCHAETA There are two main types of growth pattern among the species that occur in the Malesian region, the orthotropic type and the plagiotropic type. Neither type shows a differentiation into axes of different hierarchical levels; i.e., the difference between stem and branches is indistinct or does not exist. Species showing the first type of growth pattern form plants with simple or sparingly forked orthotropic axes and sympodial, often basal, innovations. The axes are determinate and about equally long. This frequently results in plants that consist of bundles of radiating axes, which are interconnected at the base by dense tomentum (Figure 5.1). Where such tufts aggregate in large colonies, e.g., in Calyptrochaeta microblasta (Broth.) B.C. Tan & H. Rob., they may form rough mats. When orthotropic foliate axes topple over onto the substrate, new orthotropic shoots may sprout from the older ones. Species showing the second type of growth pattern typically form wefts of plants essentially consisting of long plagiotropic axes of variable length with rhizoids distributed along the axes for a considerable length (Figure 5.2). These axes show monopodial, indeterminate growth. Branches are few and sprout irregularly. They also show indeterminate growth and may become disconnected and independent from each other with age when the older parts of shoots disintegrate. All newly formed axes have a plagiotropic growth form from the outset and may form new plagiotropic shoots. The morphological differences between the orthotropic and the plagiotropic growth pattern are summarized in Table 5.1.

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FIGURE 5.2 Habit of a typical plant of Calyptrochaeta ramosa (M. Fleisch.) B.C. Tan & H. Rob. (plagiotropic type of growth pattern) showing irregularly branched, long, indeterminate axes (Schiffner CE 3685, NY).

TABLE 5.1 Morphological Differences between the Orthotropic and Plagiotropic Types of Growth Pattern in Calyptrochaeta Species from the Malesian Region Including a List of Species for Both Types of Growth Pattern Orthotropic Type ± Equally long orthotropic axes Sympodial growth Determinate axes, axes often sprouting from a single point Tufts of radiating axes interconnected by strong tomentum Axes may form rough mats when aggregating in large colonies Axes presumably disintegrate with age and are replaced by new orthotropic innovations sprouting from the base, or Axes may form new orthotropic innovations after toppling over onto the substrate Species: Calyptrochaeta remotifolia (Mull. Hal.) Z. Iwats., B.C. Tan & Touw C. flaccida (Broth.) Z. Iwats., B.C. Tan & Touw C. microblasta (Broth.) B.C. Tan & H. Rob. Two new species

Plagiotropic Type Long plagiotropic axes of variable length Monopodial growth Indeterminate axes without any fixed branching pattern Weft forming axes with few rhizoidal attachments

Axes may become disconnected with age when older parts of shoots disintegrate Axes retain plagiotropic growth and may form new plagiotropic shoots Species: Calyptrochaeta ramosa (M. Fleisch.) B.C. Tan & H. Rob. C. parvireta (M. Fleisch.) Z. Iwats., B.C. Tan & Touw

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Two Malesian Calyptrochaeta species (C. ramosa [M. Fleisch.] B.C. Tan & H. Rob. and C. parvireta [M. Fleisch.] Z. Iwats., B.C. Tan & Touw) show the plagiotropic type of growth pattern, whereas the other five Malesian species show the orthotropic type (Table 5.1). It is interesting that both species showing the plagiotropic type occur mainly in Java. Only a few specimens of C. ramosa are reported to come from Sumatra (Meijer 7671, 7893; both in L) and Flores (Schmutz 5379F, Touw & Snoek 23093, 23126, 23274; all in L), while a single specimen of C. parvireta is possibly a dubious record for Borneo (Korthals s.n., L pro parte). According to Fleischer (1908), C. ramosa and C. parvireta are terrestrial species which often grow intermingled with liverworts on humus and decaying litter. Fleischer reported both species from wet habitats. He observed C. ramosa growing on very wet places and described C. parvireta as a species from the high montane belt. Calyptrochaeta remotifolia (Mull. Hal.) Z. Iwats., B.C. Tan & Touw is the most common and widespread Calyptrochaeta species in Malesia and shows the orthotropic type of growth pattern. Fleischer (1908) reported it growing on rotting bark and dead branches, on soil, and rarely on rocks. Fleischer’s habitat description indicates that C. remotifolia occurs in drier habitats than C. ramosa or C. parvireta, but the first author of this paper observed occasionally herbarium specimens of C. remotifolia intermingled with C. ramosa, C. parvireta, or both.

5.3 DISCUSSION The observation that two distinctly different types of growth pattern coexist in Malesian Calyptrochaeta is intriguing. Within forests, gradients of light, temperature, air currents and humidity produce differences in microclimate (e.g., Richards, 1984). Differences in type of growth pattern may reflect adaptations to different microclimates, but field studies would be necessary to demonstrate this and would be a prerequisite for ecophysiological studies. Two correlated factors constitute the type of growth pattern, namely the direction of growth and the duration of growth. Our observations suggest that inheritance is probably not the primary factor in determining the duration of growth of axes in Calyptrochaeta species. In a few herbarium specimens of C. remotifolia, a species with orthotropic growth, it has been observed that toppledover orthotropic foliate axes continue to grow orthotropically — presumably away from the substrate and towards the direction of light. This seems to imply that (1) growth of foliate axes is potentially indeterminate and that (2) the determinacy of growth is dependent upon the direction of growth. However, further experimental testing is necessary to test these hypotheses. The determinacy of growth, in turn, controls the type of branching pattern. When branching occurs, determinate growth of axes will inevitably result in a sympodial branching pattern. Conversely, indeterminate growth of axes produces a monopodial branching pattern. Branch position, on the other hand, may be dependent upon the direction of growth. In Calyptrochaeta species with the plagiotropic type of growth pattern, in which almost every part of the plant is close to the substrate, branches sprout irregularly from various parts of the stem. In C. remotifolia, like in the other orthotropic Calyptrochaeta species, branches usually sprout from the basal (proximal) part of the stem, which is usually the only part of the plant that is close to the substrate. We observed, however, that toppled-over stems form new orthotropic innovations in those stem parts that are in close proximity to the substrate. This suggests that branch initiation is partly controlled by direct contact with or close proximity to the substrate, but other, presumably plant architecture-related, factors are likely to be involved as well. Taken together, the above-mentioned observations indicate that the two different types of growth pattern in Malesian Calyptrochaeta are essentially different in the direction of growth of the axes, this being orthotropic or plagiotropic. However, it is still unknown which one of the two growth types is most derived. Fleischer (1908) observed that plants of Calyptrochaeta ramosa, a species with plagiotropic growth, grow erect at first and become prostrate later. We observed in some herbarium specimens of this species that juvenile plants have long, creeping, foliate axes that seemingly originate from a single point. Although the direction of growth is difficult to determine in herbarium material, these juvenile

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plants resemble the plagiotropic type of growth pattern in habit, whereas they resemble the orthotropic type in the origin of the axes. The observations suggest that the plagiotropic type of growth pattern represents a character state that is derived from the orthotropic one. However, more field observations and further experimental testing are necessary to test this hypothesis.

5.4 CONCLUSIONS In conclusion, the most important fundamental difference between the orthotropic and plagiotropic type of growth pattern in Calyptrochaeta is whether the axes remain erect or become prostrate in a later ontogenetic stage. Hence, the striking differences in habit should not be overestimated in phylogenetic and taxonomic studies of Calyptrochaeta. Secondarily derived characters such as monopodial versus sympodial and determinate versus indeterminate growth should be given much less weight or should be totally excluded from phylogenetic studies, in particular those based solely on morphological data. The limitations in reconstructing the ontogeny and the direction of growth based on the examination of herbarium specimens emphasize the importance of additional field observations and experimental studies of living plants. Future studies of living plants are essential to develop a better understanding of ramification in Calyptrochaeta and, especially, its ontogeny.

ACKNOWLEDGMENTS The research project presented is a spin-off from a forthcoming taxonomic revision of Malesian Calyptrochaeta. This taxonomic revision was conducted at the Nationaal Herbarium Nederland (NHN) by the first author as the major research project in the study programme of his master’s degree in biology at Leiden University, which was financed by the ASEAN Regional Centre for Biodiversity Conservation (ARCBC) Research Scholarship RDR 02-1059. The photographs were prepared by Ben Kieft (NHN). Special thanks are due to Dr. Dries Touw for the inspiring discussions and his useful comments on an earlier draft of the manuscript. We are grateful to the directors and curators of the following herbaria for the loan of specimens: B, BM, CAHUP, CBG, FH, G, GRO, H, KLU, KYO, NICH, NY, PC, S and UKMB. We greatly appreciate the kind hospitality of the directors, curators and staff during herbarium visits of KLU, PC, SING and SINU by the first author, and GRO and NMW by both authors.

REFERENCES Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 77–123. Buck, W. R., Cox, C. J. and Shaw, A. J. (2004) Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematics and Biodiversity, 2: 121–145. Correns, C. (1899) Untersuchungen über die Vermehrung der Laubmoose durch Brutorgane und Stecklinge. Verlag von Gustav Fisher, Jena, pp. 235–236. Fleischer, M. (1908) Die Musci der Flora von Buitenzorg (Zugleich Laubmoosflora von Java), Vol. 3. E. J. Brill, Leiden, pp. 999–1011 (as Eriopus). Goebel, K. I. E. (1898) Organographie der Pflanzen inbesondere der Archegoniaten und Samenpflanzen. 2. Specielle Organographie. 1. Bryophyten. Verlag von Gustav Fischer, Jena. Holmgren, P. K., Holmgren, N. H. and Barnett, L. C. (1990) Index Herbariorum. Part I: The Herbaria of the World. Ed. 8. Regnum Vegetabile, 120: i–x, 1–693. Nihn, T. (1981) Mosses of Vietnam, II. Acta Botanica Academiae Scientiarum Hungaricae, 27: 151–160. Richards, P. W. (1984) The ecology of tropical forest bryophytes. In New Manual of Bryology, Vol. 2 (ed. R.M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 1233–1270. Streimann, H. (2000) Taxonomic studies on Australian Hookeriaceae (Musci). 3. The genera Calyptrochaeta, Daltonia, Hookeriopsis and Sauloma. Journal of the Hattori Botanical Laboratory, 88: 101–138.

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in Knowledge of the 6 Advances Brachytheciaceae (Bryophyta) Sanna Huttunen, Anastasia A. Gardiner and Michael S. Ignatov CONTENTS Abstract ..........................................................................................................................................117 6.1 Introduction and the Current State of Studies of the Brachytheciaceae.............................118 6.2 Molecular Synapomorphies in the Alignment .....................................................................121 6.3 Structure of the trnL Intron and its Variation in the Brachytheciaceae ..............................127 6.4 Phylogenetic Analyses Including Additional Taxa ..............................................................129 6.4.1 Brachythecioideae and Homalothecioideae.............................................................130 6.4.2 Sciuro-hypnum brotheri............................................................................................130 6.4.3 Scleropodium ............................................................................................................130 6.4.4 “Rhynchostegiella” durieui ......................................................................................135 6.4.5 Platyhypnidium austrinum Clade .............................................................................135 6.4.6 Oxyrrhynchium–Donrichardsia Clade .....................................................................137 6.4.7 “Brachythecium” percurrens ...................................................................................138 6.4.8 Platyhypnidium .........................................................................................................138 6.4.9 Platyhypnidium cf. muelleri from Australia.............................................................139 6.4.10 Eurhynchiella ............................................................................................................139 6.4.11 Eriodon .....................................................................................................................140 6.4.12 Bryhnia .....................................................................................................................140 6.4.13 Brachytheciastrum cf. trachypodium........................................................................140 6.5 Concluding Remarks ............................................................................................................140 Acknowledgments ..........................................................................................................................142 References ......................................................................................................................................142

ABSTRACT Although the backbone phylogeny of the Brachytheciaceae has been worked out (Huttunen and Ignatov, 2004; Vanderpoorten et al., 2005), problems with some particular groups still remain. New data are presented for their solution, utilizing three different methods: (1) evaluation of the POY alignment; (2) analysis of the secondary structure of the trnL intron; and (3) phylogenetic analysis with inclusions of additional species. Rhynchostegiella durieui is found to be closely related to a group of tropical and temperate epiphytes (Aerolindigia, Clasmatodon, Helicodontium, Homalotheciella, Remyella) and Platyhypnidium austrinum to sympatric Rhynchostegiella muricatula. Hawaiian specimens referred to Platyhypnidium muelleri are found to be an undescribed species of Donrichardsia. The Madeiran endemic Brachythecium percurrens belongs to subfamily Helicodontioideae, being found in the basal position of the Helicodontioideae clade. Eurhynchiella and Eriodon are found nested in Rhynchostegium s. lat. Platyhypnidium was found to be still not monophyletic but species were found nested in Rhynchostegium in the subfamily Eurhynchioideae or in the 117

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Helicodontioideae. The substitution events in the trnL intron are quite uneven within the family, being especially high in groups of Oxyrrhynchium + Donrichardsia and also in Sciuro-hypnum.

6.1 INTRODUCTION AND THE CURRENT STATE OF STUDIES OF THE BRACHYTHECIACEAE The Brachytheciaceae is one of the largest families of pleurocarpous mosses. It includes no less than 350 species and about 40 genera (520 species according to Crosby et al., 1999, with subsequent corrections). The size of the family has been considerably clarified since the cladistic studies based on morphology (Hedenäs, 1987, 1989, 1992), and later it was defined by a morphological synapomorphy in the pattern of the arrangement of pseudoparaphyllia around branch primordia (Ignatov, 1999). More recently it received support from molecular phylogenetic data, first in analyses of a relatively few taxa within big datasets (Buck et al., 2000; Goffinet et al., 2001; Tsubota et al., 2002), and then in an expanded analysis by Huttunen and Ignatov (2004), based on trnL, psbT and ITS2 sequences and 63 morphological characters. Infrafamilial classification of the Brachytheciaceae has remained quite unclear until the recent past. The previous worldwide revision of Brachytheciaceae was undertaken by Brotherus (1925), who borrowed the concept of the three largest genera of the family from Bruch et al. (1851–1855). Based on combined analysis of morphological and molecular datasets, Ignatov and Huttunen (2002) found Eurhynchium (with its broadest circumscription in the second half of the twentieth century and one of these three largest genera), to be badly polyphyletic, requiring that it be split into at least six genera (Eurhynchium, Plasteurhynchium, Oxyrrhynchium, Eurhynchiadelphus, Kindbergia and Eurhynchiastrum). Brachythecium is also polyphyletic and had to be split into at least three genera (Brachythecium, Sciuro-hypnum and Brachytheciastrum). The third of three largest genera of the family, Rhynchostegium, was paraphyletic with Platyhypnidium nested within it. Ignatov and Huttunen (2002) suggested a new classification of the Brachytheciaceae, subdividing the family into four subfamilies: Rhynchostegioideae, Rhynchostegielloideae, Homalothecioideae and Brachythecioideae (Figure 6.1). They overlooked, however, that the name of the subfamily Rhynchostegielloideae is superfluous, because the subfamily Helicodontioideae M. Fleisch. was described at the same rank in the Fabroniaceae. The Helicodontioideae thus has to substitute for the Rhychostegielloideae, because the genus Helicodontium is found in the same clade as Rhynchostegiella in most of the analyses (Buck et al., 2000; Ignatov and Huttunen, 2002; Huttunen and Ignatov, 2004, Figures 1, 2 and 4). Rhynchostegioideae is also superfluous, and must be substituted by Eurhynchioideae (Milde, 1869). Subsequent analysis of a slightly reduced dataset combined with more Meteoriaceae and Lembophyllaceae taxa (Huttunen et al., 2004) resulted in almost the same tree topology (Figure 6.2), thus supporting in general the previous classification (Ignatov and Huttunen, 2002). Most recently, the analyses of Vanderpoorten et al. (2005), based on a reduced set of taxa, concentrating especially on Brachytheciastrum and Scleropodium, and involving mostly other gene regions (rps4, atpB–rbcL, and ITS 1 and 2), also confirmed the general topology of the Brachytheciaceae tree, although they found Eurhynchiastrum more closely related to Rhynchostegiella than to Brachytheciastrum. Vanderpoorten et al. (2005) also found that the separation of Brachythecioideae and Homalothecioideae is unsatisfactory because such a topology makes the Brachythecioideae paraphyletic. Many of the problems in the traditional morphological classification of the Brachytheciaceae were due to an overestimation of the reliability of the sporophytic characters, a fact that now has been revealed to be widespread in the pleurocarpous mosses (e.g., Vanderpoorten et al., 2002; Goffinet and Buck, 2004). The parallel morphological changes corresponding to adaptation to life on tree trunks occur in all four subfamilies of the Brachytheciaceae and are found in no less than ten independent lineages within the family (Huttunen et al., 2004; Ignatov and Huttunen, 2002). There are many characters that are highly correlated with epiphytic habitats and are often considered

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Rozea Lembophyllaceae Hylocomiaceae

Meteoriaceae

Palamocladium Eurhynchium

Rhynchostegium

Oxyrrhynchium II Donrichardsia clade Oxyrrhynchium I Aerolindigia clade Rhynchostegiella

Brachytheciastrum Eurhynchiastrum Homalothecium

HOMALOTHECIOIDEAE

Cirriphyllum clade

RHYNCHOSTEGIELLOIDEAE

Squamidium

RHYNCHOSTEGIOIDEAE

Scorpiurium

North Eurasiatic Bryhnia Kindbergia

Sciurohypnum

Chinese Bryhnia novae-angliae Brachythecium rivulare clade

BRACHYTHECIOIDEAE

Brachythecium I

Brachythecium II

Unclejackia Brachythecium III

FIGURE 6.1 Strict consensus of three most parsimonious trees from direct optimization analyses of combined morphological and molecular data including 124 terminals (based on Huttunen and Ignatov, 2004).

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Scorpiurium

Eurhynchium

Rhynchostegium

RHYNCHOSTEGIOIDEAE

Palamocladium

Squamidium clade

Oxyrrhynchium I

Aerolindigia clade

Rhynchostegiella Cirriphyllum clade

Brachytheciastrum Eurhynchiastrum

Homalothecium

HOMALOTHECIOIDEAE

Kindbergia

RHYNCHOSTEGIELLOIDEAE

Platyhypnidium austrinum Oxyrrhynchium II Donrichardsia

Sciurohypnum

Brachythecium rivulare clade North Eurasiatic Bryhnia

BRACHYTHECIOIDEAE

Brachythecium

Unclejackia

FIGURE 6.2 The Brachytheciaceae clade from the single most parsimonious tree based on direct optimization analyses of molecular (cp psbT–H and trnL–F, and nr ITS2) and morphological data (based on Huttunen et al., 2004).

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as adaptations, such as capsule shape, peristomial structure and characteristic teeth movements along a humidity gradient, and spore size and ornamentation. Besides epiphytes, the delimitation of aquatic and subaquatic groups have also often led to unnatural groupings in the previous classifications, as this kind of environment seems to result in a strongly uniform general appearance of many taxa in different groups of pleurocarps. The genus Platyhypnidium was found to be polyphyletic: three species analysed by Huttunen and Ignatov (2004) were found within three clades unrelated to each other. Platyhypnidium s. str. was found nested in Rhynchostegium (subfamily Eurhynchioideae), Platyhypnidium patulifolium forming a highly supported clade with Donrichardsia, and both nested in the Oxyrrhynchium clade (subfamily Helicodontioideae), and, finally, “Platyhypnidium austrinum” was found in subfamily Helicodontioideae, but not related to the Oxyrrhynchium–Donrichardsia clade. The systematics of these aquatic and subaquatic taxa is discussed in more detail below. Once the main clades within the Brachytheciaceae had become more or less stabilized, our main goal was to elucidate the position of taxa not included or not well represented in the previous analyses, and also to find additional arguments for generic and subfamilial placement of some particular taxa. Three methods are involved here: (1) evaluation of the molecular synapomorphies in POY alignment, i.e., characteristic indel events and substitutions; (2) analysis of the secondary structure of the trnL intron; and (3) phylogenetic analysis of a reduced dataset from previous analyses, with some additional taxa.

6.2 MOLECULAR SYNAPOMORPHIES IN THE ALIGNMENT For evaluation of synapomorphies in the POY alignment we used the same alignment as used for the tree construction by Huttunen and Ignatov (2004). POY utilizes the direct optimization method (Wheeler, 1996), which requires no separate alignment step prior to analysis, but the search for optimal tree topology and character transformations are combined into one process. Traditionally, alignment of DNA sequences is an independent step preceding phylogenetic analysis, a step that attempts to identify homologous nucleotide positions between sequences from different taxa. The true homologies (i.e., synapomorphies originating from a unique transformation event in the cladogram) in this alignment can be distinguished by running cladistic analyses (De Pinna, 1991), but this information is not used for improving the homology statements in the original alignment. In direct optimization, a separate alignment step is lacking, and “alignment,” meaning the matrix presenting optimal transformations between DNA sequences, is obtained only as a result of analyses. In this matrix, only shared synapomorphies are presented in each column, which distinguishes it from traditional alignments. The synapomorphies presented in alignments are thus always connected to the certain tree topology, which is given as the most parsimonious cladogram in POY analyses. The alignment from the earlier analyses of the Brachytheciaceae consisted of 124 terminals, including 98 Brachytheciaceae (87 species of approximately 30 genera) and 9 Meteoriaceae, and 3 genomic regions: two chloroplastic, trnL and psbT, and one nuclear, ITS2. Details of the analysis are discussed by Huttunen and Ignatov (2004). One of the most parsimonious trees is shown in Figure 6.1. The alignment resulting from this topology is available on the supplemental CD, Appendix 6 and some its parts are shown in Table 6.1. For better visualization, terminals in the alignment are arranged according to the order in which they were found in the phylogenetic tree and empty rows are used to separate outgroup taxa Meteoriaceae and the four accepted subfamilies of Brachytheciaceae: Eurhynchioideae, Helicodontioideae, Homalothecioideae, and Brachythecioideae. If sequences of some taxa are difficult to align, it is possible that different alignment methods in phylogenetic analyses will lead to different positions in a cladogram. Looking through the POY alignment (CD, and Table 6.1), it is easy to see some synapomorphic substitutions which give support to certain genera of subfamilies. In most cases, however, these synapomorphies do not represent the same character state in all taxa within the monophyletic group, raising difficulties in their usage for taxon delimitation. Usually only unique, totally unambiguous substitutions and

TABLE 6.1 Part of POY Alignment, Including Parts of trnL Intron (Positions 112–170), psbT-H Region (Positions 706–792) and ITS2 (Positions 1280–1453)

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122 Pleurocarpous Mosses: Systematics and Evolution

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Continued.

Advances in Knowledge of the Brachytheciaceae (Bryophyta)

TABLE 6.1 (Continued) Part of POY Alignment, Including Parts of trnL Intron (Positions 112–170), psbT-H Region (Positions 706–792) and ITS2 (Positions 1280–1453)

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indels are taken into account and presented as characteristic alignments in publications. However, the bigger the dataset, often the fewer are the unique substitutions. At the same time, there are many substitution patterns that mark certain subfamilies quite clearly (cf. Table 6.1), and which according to POY analyses give support for some monophyletic groups. An example from Eurhynchiastrum will be used here for evaluating the synapomorphies which POY has suggested to support the placement of this taxon. Based on the earlier studies, the position of the genus Eurhynchiastrum is controversial. According to the analysis of Vanderpoorten et al. (2005), it is more related to Rhynchostegiella of the Helicodontioideae than to the Homalothecioideae, which was suggested earlier by Huttunen and Ignatov (2004). Most of the parsimony-informative positions of Eurhynchiastrum in the alignment do not help in clarifying its placement in phylogenies, but some provide evidence for one of the two hypotheses mentioned. The names of subfamilies below are abbreviated as follows: BRA, Brachythecioideae; HEL, Helicodontioideae; HOM, Homalothecioideae. The evidence in POY alignment can either be unambiguous or show a more complex pattern. For example: (1) position 746: all HEL have A, all HOM, T, Eurhynchiastrum has T, thus position 746 provides unambiguous evidence for a closer relationship of Eurhynchiastrum to HOM than to HEL. This will be marked here as HOM>>HEL. (2) In position 121 there is a slightly more complex pattern: all HOM have G (except H. philippeanum (Spruce) Bruch et al. with C), Eurhynchiastrum has G, most of HEL have A, but G is present in Squamidium brasiliense, Cirriphyllum koponenii and all three species of Rhynchostegiella s. str.: HOM >HEL. (3) In position 1338 there is some evidence supporting a closer relationship to Helicodontioideae than Homalothecioideae: most species have A or G, Eurhynchiastrum has C, and C is also found in HEL in all three species of Cirriphyllum and also in all three species of Rhynchostegiella s. str., but never found in HOM (though it is not rare in BRA); thus HOMHEL and HOM
TABLE 6.2 Positions in the POY Alignment that Support the Placement of Eurhynchiastrum in the Homalothecioideae (HOM), Helicodontioideae (HEL), or in the Brachythecioideae (BRA) The Interpretation of Alignment Positions HOM>>HEL HOM>HEL HOM>BRA HOM>BRA HOM
Positions in POY Alignment 123, 743, 744, 748, 749, 947, 1230, 1303, [1298–1323], 1354, 1355, 1360, 1361, 1377, 1381, 1392, 1412, 1414, 1438, 1445, 1506, 1508, 1511, 1513, 1516, 1536, 1541 115, 121, 610, 626, 836, 907, 1220, 1234, 1237, 1247, 1295, 1297, 1394, 1397, 1446, 1698, 1898 480, 1338, 1779 1167 [477, 478, 480, 1167, 1453, 1473, 1934] 907, 1349, 1377, 1438, 1824 1453, 1473 480, 1508 1167, 1338, 1739, 1744, 1745, 1779

Note: See text for details. In bold are positions from chloroplast trnL and psbT regions, in normal font those from nuclear ITS2. In square brackets are positions for the affinities of Eurhynchiastrum with HEL, based on comparison of the reduced set, which includes just three species: Eurhynchiastrum pulchellum, Rhynchostegiella tenella and Brachytheciastrum collinum.

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the Homalothecioideae is obviously much greater. Lines 1 to 4 present the evaluation of alignment positions based on the whole alignment. Interestingly, POY has suggested relatively little support for the close relationship of Eurhynchiastrum to HEL. However, if we compare this genus with one representative of HEL (Rhynchostegiella tenella) and one representative of HOM (Brachytheciastrum collinum), the amount of evidence for HEL>>HOM will be much greater (Table 6.2, line 5). In addition to the different alignment method and different sequence regions used, this might explain why Eurhynchiastrum was found in the analysis of Vanderpoorten et al. (2005) to be closer to HEL, which in that study was represented by only two species: Rhynchostegiella tenella and Clasmatodon parvulus. Note also that species of Rhynchostegiella s. str. are somewhat exceptional within the Helicodontioideae (cf. Table 6.1, positions 115 and 121, and also Appendix 6.1 on supplemental CD). This example once more underlines the sensitivity of phylogenetic analyses to incomplete representation of a group. Another example of the same phenomenon can be found when comparing these same two articles: contrary to Huttunen and Ignatov (2004), who studied only three species of Brachytheciastrum, the analysis by Vanderpoorten et al. (2005) included eight accessions of this genus and found it to be a well-supported clade, whereas Huttunen and Ignatov (2004) found it as a paraphyletic grade. However, in addition to taxon sampling, the alignment method might also affect the position of Eurhynchiastrum. In analyses presented in this chapter (Figure 6.4), Eurhynchiastrum was resolved neither in Homalothecioideae nor in Helicodontioideae, but in a basal group of the Brachythecioideae (sensu Vanderpoorten et al., 2005) without significant support. Visual evaluation of the POY alignment for the delimitation of Homalothecioideae and Brachythecioideae (Table 6.2) gives almost equal amounts of supporting synapomorphies for both hypotheses, thus indirectly confirming the very weak delimitation between these two subfamilies, supporting their unification (Vanderpoorten et al., 2005).

6.3 STRUCTURE OF THE trnL INTRON AND ITS VARIATION IN THE BRACHYTHECIACEAE The trnLUAA–trnFGAA region contains the sequence of the intron I group of the trnLUAA gene. Group I introns are self-splicing ribozymes that catalyze their own excision from an RNA molecule and share conservative sequenced motifs (P, Q, R, S) and secondary structure, containing the paired elements P1–P9 (Cech et al., 1994). Group I introns are distributed broadly in eukaryotes, bacteria and bacteriophages (Rudi and Jakobsen, 1999). The most characteristic features for these tRNA group I introns are: (1) an unusually short exon-intron interaction in P1 (3 bp); (2) a 7-bp P2 stem with A-rich loop; and (3) a T-shaped P9 region. The stability of the secondary structure is often retained in areas where changes in the sequences have occurred. This can be accomplished by a compensating base change on the base-pairing strand in the secondary structure or by changes that allow base pairing of the G-U type. Different parts of the intron also have different degrees of variability, with the catalytic core (PQRS regions) remaining virtually invariable, while some peripheral parts show more changes (such as highly variable regions corresponding to the P8 domain in moss sequences). Figure 6.3 illustrates the trnL intron structure of Brachythecium cirrosum, a species that, according to by-eye evaluation, has minimum changes, in comparison with the majority of the 98 Brachytheciaceae included in the previous analysis. Synapomorphic substitution/indels in the trnL intron of the Brachytheciaceae are mapped onto this structure (Figure 6.3) based on the same POY alignment (see supplemental CD), using the position numbers from that alignment. There are 49 (counting by positions in alignment) or 37 (counting by number of places in the intron) positions where substitution/indel events can be considered as “synapomorphies” for some Brachytheciaceae groups (see also Appendices 6.1 and 6.2 on the supplemental CD). The conservative PQRS regions have very few substitutions (paired nucleotides are underlined, variable ones are in bold): the P region has none; S has only one, in Rhynchostegium serrulatum;

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U U

Pleurocarpous Mosses: Systematics and Evolution

U AU U

UA A A G A U–A U–A P5 G+U G–A A–U 62 U–A U–A C–G A C A A A A G•U P G–C G–C Q A–U C–G P4 U–A UAG

A U A U A U A U U G U G U A A U U A U A U A 173 A U A U C G U G U A U U A

U G GU U A A U U A 3'

5'

124 123

U

P6 121 117 115

U U

U

U -U AA U

81 82

IGS

U+G G–C G–C A A U A

A A A U A A G U UA U A A–U A–U A–U G–C U • G U U

114

A A U U–A U–A U–A 1 G N A N G N 5'

S

97 102–104 106

P2

C G AUGCUA U +G U– A A –U 37 33 G– C U– A A –U G+ U 27 A C A A AA

A U A G A A

284

U U

U U

P1

GCA

A A

A

trnL – intron of Brachythecium cirrosum

U

Donrichardsia macroneuron A

U C 323 A•U A–U U–A P9 U+G G–C A A C A A U UU U •A A AU G U U A A C– G 337 A– U U– A U+ G U– A U– A A G A A A A 3' A A

69

A U

Oxyrrhynchium hians

173 A U A U A U C G U A U

G

U G

U A

U A A U

5'

U

A

272 U

U

3'

278 276 275

U

269–270 267 260–263 253–257 252 212–214

C– GA C– G U– A G– C A– U G– C A A A– U – G C U• G U– A U– A C– G G– C

P7 R 140

P3

A– U U– A A– U G– C G– C A– U A A G–C C–G G A A A A–U U–A U–A P8 A–U U–A A–U G•U U U A–U U–A U–A U–A U–A U U U–A U A–U U U U U U A A AA

41

152

169 170

188 191

FIGURE 6.3 The secondary structure of the trnL intron of Brachythecium cirrosum and secondary structures of P8 regions of Oxyrrhynchium hians and Donrichardsia macroneuron. Numbers indicate positions in POY alignment where substitutions/indels occur (see supplemental CD).

Q has AAUCCUGAGC in all species except part of the Helicodontioideae (Aerolindigia and Cirriphyllum clades), which have GAUCCUGAGC; and the R region has one substitution in most species of Eurhynchioideae and in Homalothecium laevisetum (most species have GCAGAGACUCAA, substitution: GCAGAGACUCGA). In all cases substitutions occur in the unpaired part, close to the end and in the conservative region. The genera of Brachytheciaceae are quite diverse with respect to the level of substitution/indel events within the trnL intron (Appendices 6.1 and 6.2). Very few (0 to 3) substitution/indel events are observed in all members of the Homalothecioideae, most members of the Brachythecioideae (with the exception of Sciuro-hypnum and four species closely related to Brachythecium salebrosum, which have a long insertion), as well as basal groups of the Helicodontioideae (Squamidium clade),

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and basal groups of the Eurhynchioideae (Bryoandersonia, Scorpiurium, Pseudoscleropodium). This low level of variation is obviously one of the reasons in the phylogenetic analyses some of these groups, such as the Bryoandersonia, Squamidium clade, basal members of Brachythecioideae (Kindbergia, Scleropodium, Myuroclada) were found in different subfamilies after the minor changes of analysis parameter (Huttunen and Ignatov, 2004). The well-proved phylogenetic relationships can probably be resolved only after analysis of a more extensive selection of taxa and more molecular markers. The highest rate of substitutions was found in Donrichardsia (18 common substitutions in both species studied) and in four specimens of three species of Oxyrrhynchium: O. hians, O. savatieri and O. vagans (14 substitutions — and 10 of them common with Donrichardsia). This unusually high rate of variability can be considered as additional evidence for the very close relationship of two local endemics, the American Donrichardsia macroneuron and Chinese D. patulifolia, despite their quite different habit. Interestingly, this very high rate of substitutions was found not in an especially isolated lineage, but rather in a group quite ordinary in other respects, thus calling for at least a hypothetical explanation of this fact. One of the possible answers for this question can be linked to the secondary structure of the trnL intron in this group, especially to P8, the most variable region, shown in Figure 6.3. The proportion of paired to unpaired nucleotides in the distal part of P8 region in O. hians (“typical Oxyrrhynchium”) has a proportion of 26:18, whereas in Donrichardsia macroneuron it is 38:14. Within the Oxyrrhynchium–Donrichardsia clade all other species in the Donrichardsia clade except D. patulifolia share the same structure in this distal region. Although all Oxyrrhynchium species (except O. pumilum) and D. patulifolia have a characteristic GGATATTT-insertion in this region, D. macroneuron, D. pringlei and the Hawaiian Donrichardsia specimen have this insertion duplicated (Figure 6.3; positions 195 to 210 in D. macroneuron). It seems that the transition from the less paired and therefore more variable pattern to the more paired pattern results in a number of supplementary substitutions for complementation, making the overall number of substitutions somewhat higher. Another group with a high rate of substitutions is Sciuro-hypnum, which has four substitutions for all eight species (and three more species of this group, S. plumosum, S. populeum and S. flotowianum, have three additional substitutions, two of them in a paired parts of the intron). This substitutional level looks especially high compared with the very low level of substitution within the Homalothecioideae + Brachythecioideae (most species have 0 or 1 substitution). As in the case with Donrichardsia, this is additional evidence for placing S. flotowianum in this genus (suggested by Ignatov and Huttunen [2002], but never previously proposed). Contrary to Oxyrrhynchium, Sciuro-hypnum has almost no substitution in the P8 region. It remains unclear if there are any environmental factors responsible for such a high level of substitutions in the Oxyrrhynchium–Donrichardsia clade and in the Sciuro-hypnum clade. The only correlation we could notice is that both groups are quite rich in eutrophic species, common on humus and decaying wood, which is somewhat less characteristic for other genera of Brachytheciaceae.

6.4 PHYLOGENETIC ANALYSES INCLUDING ADDITIONAL TAXA After the previous analysis of Huttunen and Ignatov (2004), new sequence data for 28 specimens of Brachytheciaceae were obtained. Similar to the previous analysis, ITS2 and trnL–F regions were studied, but, in addition, a nuclear ITS1 was sequenced from the same DNA extraction. Protocols of molecular studies were the same as described by Huttunen and Ignatov (2004). Data on Platyhypnidium mutatum and P. riparioides from Germany were taken from GenBank. ITS sequences of two specimens of Brachytheciastrum, “Brachythecium percurrens” and Platyhypnidium fuegianum were kindly provided to us by Alain Vanderpoorten. The trnL–F sequence for P. fuegianum was obtained using the DNA extraction from the same voucher specimen as for the ITS sequence in Vanderpoorten et al. (2005). Thus, the new dataset for 86 terminals was compiled (see Table 6.3

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for specimen details). Sequences were aligned manually, and the alignment consisted of 1506 positions (ITS1: 514; ITS2: 489; trnL–F: 503). Phylogenetic analyses were done with the parsimony ratchet method in Winclada in connection with Nona. The 50% majority rule of 1000 most parsimonious trees is shown in Figure 6.4. Jackknife support was calculated by Nona based on 1000 replications with gaps treated as missing data. The general topology of the tree (Figure 6.4) is similar to those found by Huttunen and Ignatov (2004) and Vanderpoorten et al. (2005). The strict consensus tree (not shown — see Figure 6.4; branches present in the strict consensus topology are marked with 100 above the branch), however, is fairly unresolved within Eurhynchioideae. Even in other clades the jackknife and Bremer support is low or lacking for most of the clades. Subfamilies Eurhynchioideae and Helicodontioideae received high support, 89% and 96%, respectively. Homalothecium and Brachytheciastrum were found in one clade, although with a low support (jackknife support 74%; Bremer support 3). On a genus level the groups that were fairly well supported included the Oxyrrhynchium–Donrichardsia clade (82%; 3), Sciuro-hypnum (92%; 3), Scleropodium (98%; 6) and Rhynchostegiella (99%; 7). Topology of some particular groups is considered below, within their appropriate sections.

6.4.1 BRACHYTHECIOIDEAE

AND

HOMALOTHECIOIDEAE

The poor delimitation between the Brachythecioideae and the Homalothecioideae was obvious in the earlier analyses. Ignatov and Huttunen (2002) decided, however, to separate them and segregated Brachytheciastrum + Homalothecium in the latter subfamily, including also Eurhynchiastrum. Vanderpoorten et al. (2005) considered that a better solution would be to unite the Homalothecioideae and Brachythecioideae. In the present analysis they are found again as two monophyletic groups but without any significant support. The general topology of the tree, however, remains largely the same (Figures 6.1 and 6.4). As only very few representatives of some genera are still included, an analysis with more taxa of these groups is obviously needed for a final conclusion of the subdivision of the genera within the Homalothecioideae–Brachythecioideae group.

6.4.2 SCIURO-HYPNUM

BROTHERI

As has been assumed since the early treatments of the Brachytheciaceae (Brotherus, 1925; Takaki, 1955), this Japanese subendemic species is closely related to Sciuro-hypnum reflexum. The current analysis resolved it within the Sciuro-hypnum clade with a high support (Figure 6.4).Thus, according to the nomenclature of Ignatov and Huttunen (2002) it belongs to the genus Sciuro-hypnum. This relationship has been doubted mostly due to the much larger size of S. brotheri, which is almost as large as Rhytidiadelphus species. This is not an exception in Sciuro-hypnum, where two other species are also markedly larger than the others: S. oedipodium and S. hylotapetum. The former has proved to be a polyploid (n = 20), differing in this respect from most of the other small-sized species of Sciuro-hypnum, which have mostly n = 10. Thus, we predict that S. brotheri will also be found to be a polyploid species.

6.4.3 SCLEROPODIUM The position of this genus was not well resolved in the analysis by Huttunen and Ignatov (2004), as the only species included in their analysis was found in a fairly unstable position dependent on the analysis parameters used. Thus, the inclusion of this genus in the Brachythecioideae (Ignatov and Huttunen, 2002) was largely based on morphology. Later on, Vanderpoorten et al. (2005) found the genus Scleropodium to be monophyletic and to belong to the Brachythecioideae–Homalothecioideae clade. The present analysis confirms this: the three analysed species were found to be sister to Brachythecioideae + Homalothecioideae, although this placement is lacking any support.

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TABLE 6.3 GenBank Accession Numbers and Voucher Specimens Used for Sequences Species

trnL-F

ITS1

ITS2

Trachypus bicolor Reinw. & Hornsch.

AY044060

Outgroup DQ200118

Aerolindigia capillacea (Hornsch.) M. Menzel

AY044072

Brachytheciastrum collinum (Schleich. ex Müll. Hal.) Ignatov & Huttunen 1 Brachytheciastrum collinum (Schleich. ex Müll. Hal.) Ignatov & Huttunen 2 Brachytheciastrum falcatulum (Broth.) Ignatov & Huttunen Brachytheciastrum leibergii (Grout) Ignatov & Huttunen

AY184776

DQ336896

AY166440

DQ336923

DQ200954

DQ200071

AF397774

DQ336897

AF403662

—

AY737462

AY737462

Brachytheciastrum trachypodium (Funck ex Brid.) Ignatov & Huttunen 1 Brachytheciastrum trachypodium (Funck ex Brid.) Ignatov & Huttunen 2 Brachytheciastrum trachypodium (Funck ex Brid.) Ignatov & Huttunen 3 Brachytheciastrum velutinum (Hedw.) Ignatov & Huttunen 1 Brachytheciastrum velutinum (Hedw.) Ignatov & Huttunen 2 Brachythecium frigidum (Müll. Hal.) Besch. Brachythecium novae-angliae (Sull. & Lesq.) A. Jaeger

DQ336924

DQ200955

DQ200072

DQ336925

DQ200956

DQ200073

—

DQ200957

DQ200074

AF397832

—

AF403667

DQ352071

—

AY737464

AF397874

DQ336898

AF403638

AF397843

DQ336899

AF403665

Brachythecium novae-angliae (Sull. & Lesq.) A. Jaeger Brachythecium percurrens Hedenäs

DQ208198

DQ336900

DQ200959

—

AY737469

AY737469

Brachythecium rivulare Bruch et al.

AF397866

DQ200076

AF403651

Brachythecium rivulare Bruch et al.

—

DQ200077

DQ200977

Brachythecium rutabulum (Hedw.) Bruch et al.

AF397867

DQ200078

AF403644

AF395624

Brachytheciaceae DQ200070 AF395634

Voucher Specimen for Sequences

China, Hunan Prov., T. Koponen, S. Huttunen, S. Piippo & P.-C. Rao 50721, 2. Oct. 1997 (H)

Ecuador, Loja Prov., D. H. Norris 92175 & M. Bolivar, 18. Dec. 1997 (H) Russia, Volgorad Prov., M. Ignatov, 7. Aug. 1999, (MHA) Russian Far east, Kamchatka, Czernyadievk £532, 1. June 2003 (MHA) Russia, Altai, M. Ignatov #0/1680, 26. June 1989 (MHA) (Sequences from GenBank,Vanderpoorten et al., 2005) Russia, Altai., M. Ignatov 31/229, 1992 (MHA) Russia, Yakytia (East Siberia), M. Ignatov 00-1055, 6. Sept. 2000 (MHA) Russia, Caucasus, E. Ignatova, 2. Aug.1986 (MHA) Finland, M. Kiirikki, 23. Aug. 1988 (H) Sequences from GenBank (Vanderpoorten et al. 2005) U.S.A, California, Duell, 23. April 1981 (H) China, Hunan Prov., T. Koponen, S. Huttunen & P.-C. Rao 52900, 11. Oct. 1997 (H) U.S.A., North Carolina, L. E. Anderson 25183 10. April 1988 (H) (Sequences from GenBank, Vanderpoorten et al., 2005) Finland, A. Parnela, 19. May 1996 (H) Germany, J.-P. Frahm, 29. June 1999 (BONN) Finland, S. Huttunen 1415, 16. April 2000 (H) Continued.

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TABLE 6.3 (Continued) GenBank Accession Numbers and Voucher Specimens Used for Sequences Species

trnL-F

ITS1

ITS2

Voucher Specimen for Sequences

Brachythecium salebrosum (F. Weber & D. Mohr) Bruch et al. Bryhnia scabridens (Lindb.) Kaurin

AF397857

AF403648

AF397826

DQ336901 (partial) DQ200079

AF403588

Bryhnia scabridens (Lindb.) Kaurin

AY184779

DQ336902

AY166442

Cirriphyllum crassinervium (Taylor) Loeske & M. Fleisch. Cirriphyllum piliferum (Hedw.) Grout Clasmatodon parvulus (Hampe) Sull.

AF397868

—

AF4036682)

AF397799

DQ200081

AF403608

AF397813

DQ200082

AF403614

Donrichardsia macroneuron (Grout) H. A. Crum & L. E. Anderson

AY009848

AF167350

AF167350

Donrichardsia patulifolia (Cardot & Thériot) Ignatov & Huttunen

AF397850

—

—

Donrichardsia pringlei (Cardot) Huttunen & Ignatov comb. nov. Donrichardsia sp. nov.

DQ336929

DQ336913

DQ336913

DQ208199

DQ200083

DQ200962

Eriodon conostomus Mont.

DQ336926

DQ336903

DQ336903

Eurhynchiadelphus eustegia (Besch.) Ignatov & Huttunen Eurhynchiastrum pulchellum (Hedw.) Ignatov & Huttunen Eurhynchiella acanthophylla (Montagne) M. Fleisch.

AF397790

—

AF395635

AY044069

DQ200084

AF395635

DQ336927

DQ336904

DQ336904

Eurhynchiella zeyheri (Müll. Hal.) M. Fleisch. Eurhynchium angustirete (Broth.) T. J. Kop. Helicodontium capillare (Hedw.) A. Jaeger

DQ208200

DQ200085

DQ200960

AF397825

DQ200086

AF403621

AF397855

DQ200087

DQ336905

AF397860

DQ200088

AF403658

AF397842

—

AF403597

AF397805

DQ336906

AF403587

AF397804

DQ336907

AF403591

Finland, S. Laaka 1835, 18. Oct. 1987 (H) European Russia, Kostroma Province, S. Popov 26, 11. May 1999 (MHA) Russia, Altai, M. Ignatov 34/227 (MHA) Russia, Caucasus, M. Ignatov, 23. Aug. 1999 (MHA) Finland, T. Koponen & S. Huttunen 1324, 24. May 1999 (H) U.S.A., Missouri, P. L. Redfearn, Jr. & B. Allen, 23. April 1992 (H) U.S.A., P. L. Redfearn, Jr. 27208 (Sequences from GenBank, Vanderpoorten et al. 2002) China, Hunan Prov., T. Koponen, S. Huttunen, S. Piippo & P.-C. Rao 53920, 1. Oct. 1998 (H) Mexico, Michoacan, C. Delgadillo M. 12. Sept. 1996 (H3114221) Hawaii, Maui, W. J. Hoe 4296, 28. June 1976 (H sub Platyhypnidium muelleri) Chile, Ancud, Juan Larrain 288, 22. Jan. 2003 (NY, H) China, Jilin Prov., T. Koponen 36592, 20. Sept. 1981 (H) Finland, T. Koponen & S. Huttunen 1321, 24. May 1999 (H) Chile, Prov. Arauco, R. R. Irland & G. Bellolio 31187, 19. Sept. 2001 (NY, H) South Africa, Cecilia Ravine, K. Hylander 10885, 1. Jan. 2001 (S) Russia, Moscow Prov., M. Ignatov, 3. July 1998 (MHA) Colombia, Departamento del Valle, S. Churchill, A. E. Franco & N. Hollaender, 4. May 1990 (H) U.S.A., Missouri, B. Allen & P. L. Redfearn, Jr., 29. March 1995 (NY) U.S.A, Oregon, A. Newton 5206, 6. Aug. 2000 (BM) Finland, T. Koponen & S. Huttunen 1322, 24. May 1999 (H) China, Hunan Prov., T. Koponen, S. Huttunen, S. Piippo & P.-C. Rao 50467, 7. Oct. 1998 (H)

Homalotheciella subcapillata (Hedw.) Broth. Homalothecium megaptilum (Sull.) H. Robinson Homalothecium sericeum (Hedw.) Schimp. Kindbergia praelonga (Hedw.) Bruch et al.

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TABLE 6.3 (Continued) GenBank Accession Numbers and Voucher Specimens Used for Sequences Species

trnL-F

ITS1

Okamuraea brachydictyon (Cardot) Noguchi

AY184789

DQ200090

AF503537

Oxyrrhynchium hians (Hedw.) Loeske

AF397815

DQ336908

AF403603

Oxyrrhynchium pumilum (Wilson) Schimp. Oxyrrhynchium savatieri (Schimp. ex Besch.) Broth.

AY184790

DQ336909

DQ336909

AF397859

DQ336910

AF403659

Oxyrrhynchium speciosum (Brid.) Warnst. Oxyrrhynchium vagans (A. Jaeger) E. B. Bartram

DQ208201

DQ336911

DQ336911

AF397878

—

AF403645

Palamocladium euchloron (Müll. Hal.) Wijk & Margad. Platyhypnidium aquaticum (A. Jaeger) M. Fleisch.

AF397851

DQ336912

AF403623

DQ208202

DQ200091

DQ200961

‘Platyhypnidium’ austrinum (Hook. & Wilson) M. Fleisch. Platyhypnidium fuegianum (Cardot) Vanderpoorten, Ignatov, Huttunen & Goffinet Platyhypnidium hedbergii (P. Varde) Ochyra & Sharp Platyhypnidium muelleri (A. Jaeger) M. Fleisch. Platyhypnidium mutatum Ochyra & Vanderpoorten Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon

AY184791

DQ200095

AY166449

DQ336928

AY737450

AY737450

DQ208203

DQ336915

DQ200965

DQ208204

DQ200096

DQ200966

AF260909

AF230982

AF230997

DQ336930

DQ336914

DQ336914

—

DQ333437

DQ333437

AF260908

AF230981

AF230996

AF397847

DQ200099

DQ200967

DQ208205

DQ336918

DQ200968

DQ336931

DQ336916

DQ200969

DQ208206

DQ200097

DQ200963

Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon

ITS2

Voucher Specimen for Sequences China, Hunan Prov., T. Koponen, S. Huttunen, & P.-C. Rao 48969, 26. Sept. 1997 (H) China, Hunan Prov., T. Koponen, S. Huttunen, S. Piippo & P.-C. Rao 53740, 28. Sept. 1998 (H) Georgia, Caucasus, M. Ignatov, 8. Aug. 1987 (MHA) China, Hunan Prov., T. Koponen, S. Huttunen & P.-C. Rao 51775, 8. Oct. 1997 (H) Malta 1992 (BM) China, Hunan Prov., T. Koponen, S. Huttunen, S. Piippo & P.-C. Rao 49717, 28. Sept. 1998 (H) Russia, Caucasus, M. Ignatov, 23. Aug. 1999 (MHA) Colombia, Departamento de Boyacá, S. P. Churchill, P. Franco & J. D. Parra, 28. Jan. 1995 (H) Australia, Victoria, H. Streimann 49544, 2. May 1992 (H) Goffinet 8440 (ITS sequences from GenBank,Vanderpoorten et al., 2005) Kenya, Pocs et al., 11.-27. Jan. 1992, (H3204025) Malaysia, Pahang, L. Hedenäs MY92-394, 22. March 1992 (S) (Ochyra & Vanderpoorten, 1999) Kenya, Pocs et al., 11.-27. Jan. 1992 (H3204269) Russia, Altai, Yurga, Ignatov 21/10 (MHA). (Sequences from GenBank, Ochyra & Vanderpoorten, 1999) China, Hunan Prov., T. Koponen, S. Huttunen, & P.-C. Rao 51843, 9. Oct. 1997 (H) U.S.A. Kentucky, W. R. Buck 20775, 15. Sept. 1991 (H3114472) Finland, S. Huttunen 1683, 29. Aug. 2002 (H) China, Hunan Prov., V. Virtanen, 23. Sept. 2000 (H) Continued.

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TABLE 6.3 (Continued) GenBank Accession Numbers and Voucher Specimens Used for Sequences Species

trnL-F

ITS1

ITS2

Voucher Specimen for Sequences

Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium riparioides (Hedw.) Dixon Platyhypnidium sp nov. 1

DQ208207

DQ200100

DQ200970

—

DQ200098

DQ336917

DQ208208

DQ200101

DQ200971

DQ208209

DQ200102

DQ200972

DQ208210

DQ200103

DQ200973

Platyhypnidium sp. nov. 2

DQ208211

—

—

Platyhypnidium subrusciforme (Müll. Hal.) A. Jaeger Remyella brachypodia (M. Fleisch.) Ignatov & Huttunen

DQ208212

DQ336919

DQ200974

AF397854

DQ336920

AF403600

Rhynchostegiella durieui (Mont.) S. Allorge & Perss. Rhynchostegiella macilenta (Renauld & Cardot) Cardot Rhynchostegiella muricatula (Hook. & Wilson) Broth.

DQ208213

DQ200104

DQ200975

AF397781

DQ200105

AF403570

DQ208214

DQ200106

DQ200976

Rhynchostegiella tenella (Dicks.) Limpr. Rhynchostegiella teneriffae (Mont.) Dirkse & Bouman

AY044070

DQ200107

AF395633

AF397783

DQ200108

AF403569

Rhynchostegium arcticum (I. Hag.) Ignatov & Huttunen Rhynchostegium confertum (Dicks.) Bruch & al. Rhynchostegium pallidifolium (Mitt.) A. Jaeger

AF397775

DQ336921

AF403661

AF397837

DQ200109

AF403622

AF397807

DQ200110

AF403618

Rhynchostegium psilopodium Ignatov & Huttunen

AF397861

—

AF403643

Rhynchostegium rotundifolium (Brid.) Bruch & al. Rhynchostegium serrulatum (Hedw.) A. Jaeger Sciuro-hypnum brotheri (Par.) Ignatov & Huttunen Sciuro-hypnum plumosum (Hedw.) Ignatov & Huttunen

AF397809

DQ200111

AF403611

AF397829

DQ200112

AF403620

DQ336932

DQ200113

DQ200958

Georgia, Caucasus, M. Ignatov, 8. August 1987 (MHA) Spain, Cantabria, M. Acón & E. Fuertes, 18. Sept. 1996 (H) Portugal, Madeira, L. Hedenäs MA90-250, 14. April 1990, (S) Portugal, Azores, L. Hedenäs, 29. Sept. 2000 (S) Australia, N. Queensland, A. Cairns & D. Meagher 11043, 4. Nov. 2004 (S) New South Wales, Gloucester River, H. Streimann 1585, 25. Jan. 1975 (H) Mexico, C. Delgadillo, 23. Oct. 1990, (H3114503) Papua New Guinea, Morobe Prov., T. Koponen 33007, 11. July 1981 (H) Portugal, Azores, L. Hedenäs, 28. Sept. 2000 (S) Portugal, Madeira, L. Hedenäs, 13. May 1993, (B4503; S) Australia, Norfolk island, H. Streimann 49628, 15. June 1992 (H) Georgia, Caucasus, M. Ignatov, 2. Oct. 1997 (MHA) Portugal, Madeira, S. Fontinha, L. Hedenäs, M. Nobrega, 10. June 1991, (B9121; S) Russia, Perm Prov., A. G. Bezgodov #222, 30. Jun. 1999 (MHA) Georgia, Caucasus, M. Ignatov, 27. Aug. 1987 (MHA) China, Hunan Prov., T. Koponen, S. Huttunen, & P.-C. Rao 51301, 3. Oct. 1997 (H) China, Hunan Prov., T. Koponen, S. Huttunen & P.-C. Rao 51803, 8. Oct. 1997 (H) Russia, Caucasus, V. Onipchenco, 31. Aug. 1999 (MHA) USA, New Jersey, B. C. Tan, 12. Sept. 1992 (H) Japan, S. Huttunen 1432, 1999 (H)

AF397814

DQ336922

AF403586

China, Hunan Prov., T. Koponen, S. Huttunen, S. Piippo & P.-C. Rao 56777, 14. Oct. 1998 (H)

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TABLE 6.3 (Continued) GenBank Accession Numbers and Voucher Specimens Used for Sequences Species

trnL-F

ITS1

Sciuro-hypnum populeum (Hedw.) Ignatov & Huttunen Sciuro-hypnum reflexum (Starke) Ignatov & Huttunen Scleropodium caespitans (Wilson ex Müll. Hall.) L. F. Koch Scleropodium obtusifolium (Mitt.) Kindb. Scleropodium touretii (Brid.) L. F. Koch Scorpiurium circinatum (Brid.) M. Fleisch. & Loeske

AF397873

DQ200114

AF403640

AF397858

—

AF403655

—

DQ200115

DQ200978

AF397793

DQ200116

AF403615

—

DQ200117

DQ200979

AF397834

—

AF403598

6.4.4 “RHYNCHOSTEGIELLA”

ITS2

Voucher Specimen for Sequences Finland, J. Pykälä 7029, 30. Sept. 1990 (H) Finland, S. Huttunen 1195, May 1997 (H) France, Loire, J.-P. Frahm,7. April 2002 (BONN) U.S.A., California, M. Ignatov & D. H. Norris, 13. Aug. 1989 (MHA) Corse, Marsiglia, A. Wahnke ID x10271 (D.Quandt) Georgia, Caucasus, M. Ignatov, 8. Aug. 1987 (MHA)

DURIEUI

Ignatov and Huttunen (2002) did not discuss this species because it was not studied for the earlier analyses. Hedenäs (1992) found that this species has warty papillose rhizoids, which never occur in northern Brachytheciaceae, and suggested its position in the Amblystegiaceae. Previously this species was often attributed to the genus Orthothecium (e.g., Limpricht, 1904; Sergio and Hebrard, 1982). Sequence level data (Figure 6.4) indicate the position of this species in the clade composed of several mono- and oligospecific epiphytic genera, mainly with tropical and warm-temperate distribution: Clasmatodon, Helicodontium, Homalotheciella, Aerolindigia, Remyella, and also Oxyrrhynchium pumilum, but without obvious relation to any of them by the available data. Morphologically and phytogeographically “Rhynchostegiella” durieui is no less peculiar than other representatives of this clade and apparently the species has to be placed in its own genus. We leave it, however, still undescribed because the sporophyte is still unknown in this species. The present analysis also found Oxyrrhynchium pumilum within this clade, whereas in the previous analysis it was resolved as a basal in the Oxyrrhynchium clade without any significant support. Interestingly, this controversial position is somewhat parallel to traditional taxonomic treatments: many authors of the twentieth century classified O. pumilum in Rhynchostegiella (as R. pallidirostris (Brid.) Loeske). Besides “Rhynchostegiella” durieui, Aerolindigia capillacea and Oxyrrhynchium pumilum are the only other species in this clade that are distributed in Africa and Europe (Figure 6.5A).

6.4.5 PLATYHYPNIDIUM

AUSTRINUM

CLADE

As was already noted above, Platyhypnidium in the traditional sense was found in at least three unrelated groups: (1) Platyhypnidium, which form a monophyletic group together with Rhynchostegium; (2) Donrichardsia, which is nested within Oxyrrhynchium; and (3) “Platyhypnidium austrinum,” which was found without obvious relatives in the previous analyses by Huttunen and Ignatov (2004). In the present analysis we found, however, that sympatric Rhynchostegiella muricatula exhibits a high similarity in sequence level data with P. austrinum and these two species together form a well-supported monophyletic group (Figure 6.4). Obviously, these two taxa can be segregated into a separate genus (Huttunen and Ignatov, in preparation), which probably would include also the East-Asian and Malesian group of Rhynchostegiella with thick-walled laminal cells, such as Rhynchostegiella mindorensis (Broth.) Broth., R. opacifolia Dixon, R. papuensis E. B. Bartram, R. santaiensis Broth. & Paris, and R. sinensis Broth. & Paris. Unfortunately, fresh

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Trachypus bicolor Scorpiurium circinatum Eurhynchium angustirete Palamocladium euchloron Rhynchostegium pallidifolium Rhynchostegium serrulatum Platyhypnidium riparioides Altai 100 100 100 Platyhypnidium muelleri Malaysia 1 1 1 Platyhypnidium sp nov1 Australia QUE Eriodon conostomus 100 Platyhypnidium sp nov2 Australia NSW 1 100 Platyhypnidium riparioides USA 54 1 Platyhypnidium subrusciforme Mexico 62 Rhynchostegium arcticum Rhynchostegium psilopodium Platyhypnidium aquaticum Columbia Platyhypnidium riparioides China 1 Platyhypnidium riparioides China 2 Eurhynchiella zeyheri Eurhynchiella acanthophylla Platyhypnidium fuegianum Rhynchostegium confertum Rhynchostegium rotundifolium Platyhypnidium mutatum Platyhypnidium riparioides Germany Platyhypnidium riparioides Caucasus 100 100 Platyhypnidium riparioides Azores 2 100 Platyhypnidium riparioides Madeira Platyhypnidium riparioides Spain 2 100 61 Platyhypnidium hedbergii Kenya 2 Platyhypnidium riparioides Finland Brachythecium percurrens Oxyrrhynchium speciosum 100 Oxyrrhynchium savatieri Oxyrrhynchium hians 3 100 100 Oxyrrhynchium vagans China 82 5 1 Donrichardsia sp nov Hawaii 52 100 96 Donrichardsia patulifolia 2 100 Donrichardsia macroneuron 72 Donrichardsia pringlei Mexico 1 100 Platyhypnidium austrinum Australia 5 Rhynchostegiella muricatula 92 Okamuraea brachydictyon 100 100 100 Cirriphyllum crassinervium 100 2 5 Cirriphyllum piliferum 52 2 1 100 99 Rhynchostegiella tenella 100 Rhynchostegiella macilenta 7 100 99 3 Rhynchostegiella teneriffae 1 94 Rhynchostegiella durieui 100 100 Homalotheciella subcapillata 2 100 Clasmatodon parvulus 52 89 1 Aerolindigia capillacea Oxyrrhynchium pumilum Helicodontium capillare Remyella brachypodia Scleropodium caespitans France 100 Scleropodium obtusifolium 6 100 98 1 Scleropodium tourettii Corse Brachytheciastrum collinum 2 Brachytheciastrum falcatulum 100 Brachytheciastrum collinum 1 1 100 100 Homalothecium sericeum 2 Homalothecium megaptilum 3 76 74 Brachytheciastrum leibergii Brachytheciastrum trachypodium 1 Brachytheciastrum trachypodium 2 Brachytheciastrum velutinum 1 Brachytheciastrum velutinum 2 Brachytheciastrum trachypodium 3 Eurhynchiastrum pulchellum Sciuro-hypnum reflexum 100 Sciuro-hypnum brotheri 3 100 92 2 100 Sciuro-hypnum plumosum 83 9 100 Sciuro-hypnum populeum 99 Kindbergia praelonga China 5 Brachythecium salebrosum Finland 100 100 Brachythecium rutabulum 1 100 2 Brachythecium riparium Germany 5 100 96 1 100 Brachythecium rivulare Finland 63 2 Brachythecium frigidum 100 56 Brachythecium novae-angliae China 3 100 100 78 8 Brachythecium novae-angliae N America 99 3 Eurhynchiadelphus eustegia 70 100 3 100 Bryhnia scabridens Altai 88 3 Bryhnia scabridens Europe 100 3 89 100 1 52

91

FIGURE 6.4 Fifty percent majority rule consensus tree of 2348 most parsimonious trees (L = 808, CI = 54, RI = 79) of analysis of 86 terminals. Jackknife (in italics) and Bremer support values are shown below branches; those clades that appear also in the strict consensus topology are shown with 100 above the branch.

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A

B

C FIGURE 6.5 (A) Distribution of some genera of the Aerolindigia clade: Remyella (circles), Aerolindigia (diamonds), Homalotheciella (simple crosses), Clasmatodon (squares), Helicodontium (only H. capillare included) (drops), and “Rhynchostegiella” durieui (Maltese crosses). (B) Five groups of Platyhypnidium specimens found in five different clades (see Figure 6.4); map represents localities where sequenced specimens were collected; South African Eurhynchiella is included, as it was found related to North American Platyhypnidium fuegianum. (C) Origin of specimens used for sequence studies of Bryhnia scabrida (circles) and Brachythecium novae-angliae (squares).

material of these species was not available for molecular study. Morphological circumscription of these species is briefly discussed by Ignatov et al. (2005).

6.4.6 OXYRRHYNCHIUM–DONRICHARDSIA CLADE This group continues to bring surprises. After Huttunen and Ignatov (2004) found that the Chinese Platyhypnidium patulifolium is closely related to the enigmatic North American endemic Donri-

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chardsia macroneuron, it became clear that superficially similar aquatic and subaquatic Brachytheciaceae, segregated traditionally to Platyhypnidium, are not all derived from Rhynchostegium, but also from Oxyrrhynchium. The present analysis revealed two more representatives of Donrichardsia: a specimen from Hawaii, which was misidentified as Platyhypnidium muelleri, to which it is morphologically most similar (Huttunen and Ignatov, in preparation), and Platyhypnidium pringlei (Cardot) Broth. from Mexico. Interestingly, Oxyrrhynchium speciosum, another subaquatic moss of the Oxyrrhynchium–Donrichardsia clade, obviously represents an independent line of evolution to this type of habitat. According to the present analysis, it does not belong to the Donrichardsia clade. As the position of Eurhynchium pringlei in Donrichardsia is quite well supported here, we suggest a new combination: Donrichardsia pringlei (Card.) Huttunen & Ignatov comb. nov. — Rhynchostegium pringlei Card., Revue Bryologique 37: 70. 1910.

6.4.7 “BRACHYTHECIUM”

PERCURRENS

In its original description, this species was compared with Brachytheciastrum velutinum. The plant has a similar size and appearance, but its costa is percurrent to excurrent, strongly spinose at back, and the distal laminal cells are very short, with a length to width ratio of 1.2–2:1. Vanderpoorten et al. (2005) found this species to be closely related to Eurhynchiastrum pulchellum and Rhynchostegiella tenella. The present analysis found it in a basal position in the Helicodontioideae clade. There are not many morphological characters providing corroborative evidence for this placement of Brachythecium percurrens. Both Eurhynchiastrum and Oxyrrhynchium were traditionally referred to the same genus, Eurhynchium. However, the relatively short one-celled apical part of the axillary hairs of “Brachythecium” percurrens is a rare character state in the Brachytheciaceae but rather is in agreement with Oxyrrhynchium, not with Eurhynchiastrum.

6.4.8 PLATYHYPNIDIUM In the previous analysis only one specimen of Platyhypnidium riparioides was included, and it was found nested within the Rhynchostegium clade (Huttunen and Ignatov, 2004). In the present analysis we expanded the number of representatives of Platyhypnidium, which, however, did not clearly answer the question if it is better to include this genus in Rhynchostegium or if it is better to consider it as an independent genus. Our analysis suggests (Figure 6.4) that there is probably more than one lineage of subaquatic species within the Rhynchostegium clade, although in a strict consensus topology this clade was almost totally unresolved. We hope that additional sequence data will, in the future, confirm the following five phytogeographically limited clades: (1) European, Macaronesian and African Platyhypnidium populations form a clade; (2) Chinese P. riparioides and South American P. aquaticum form another independent lineage; (3) Malesian P. muelleri, Altaian “P. riparioides” and a still undescribed species from North Australia, similar to P. muelleri but with almost ecostate leaves, form a third clade; (4) Mexican P. subrusciforme and North American “P. riparioides” form a fourth clade; and (5) Southern South American P. fuegianum is found closely related to Eurhynchiella zeyheri from South Africa and E. acanthophylla from Chile. The relationship and geography of Platyhypnidium species (Figures 6.4 and 6.5) suggest a somewhat similar pattern to the results by Shaw and Allen (2000) on the Fontinaliaceae. They found the phylogenetic relationships to correlate more with geographical range than with the current taxonomic concepts, which were based on morphological peculiarities of populations. The morphologically most peculiar species in the Platyhypnidium, P. mutatum from Germany and P. hedbergii from Kenya, were found not only within the clade with European and Macaronesian P. riparioides, but they were also most similar to the geographically closest of the P. riparioides specimens sequenced (Figure 6.4; P. riparioides from Germany). ITS and trnL–F sequences revealed P. hedbergii to be identical with P. riparioides from Kenya, and thus only P. hedbergii was included in the phylogenetic analyses. At the same time, North American and European material identified

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as P. riparioides and invariably treated before as a single species, might not only be non-conspecific, but if a narrow generic concept is applied to the Rhynchostegium clade (see below), they might even be in different genera. Thus, it can be concluded that aquatic habitats in this group favour rapid morphological evolution without big changes in even the most variable parts of the genome. Regarding practical taxonomy, and if the ongoing studies confirm our results, it would be simplest to combine Platyhypnidium and Rhynchostegium in one genus (see, however, discussion below under Eriodon). Alternatively, Rhynchostegium s. lat. could be split into several genera: (1) Rhynchostegium for R. confertum (type of genus Rhynchostegium) and R. riparioides and related taxa in Europe, West Asia and Africa; (2) Eurhynchiella for E. zeyheri (type of genus Eurhynchiella), E. acanthophylla and “Rhynchostegium” fuegianum; (3) Platyhypnidium for Malesian P. muelleri (the type of genus Platyhypnidium), and some Platyhypnidium from Asia and Australia and (4) Steerecleus for tropical large-sized and whitish plants, like S. serrulatus (the type of genus Steerecleus), Rhynchostegium pallidifolium, R. javense, R. tenuifolium and maybe also R. megapolitanum. The present analysis left Steerecleus unresolved within Rhynchostegium in the strict consensus topology, and additional analyses with more “Steerecleus” taxa are needed to define its delimitation. These narrower genera, however, will be fairly heterogeneous and currently the unresolved topology makes discussion about their details somewhat speculative. Transitions from terrestrial to aquatic or subaquatic habitats seem to occur in several lineages within Rhynchostegium s. lat., and, thus, retention of Platyhypnidium s. lat. for all aquatic and subaquatic derivates of terrestrial Rhynchostegium s. lat. will be no better a solution than the retaining of Drepanocladus and Hygrohypnum in the circumscriptions of authors of the middle twentieth century.

6.4.9 PLATYHYPNIDIUM

CF. MUELLERI FROM

AUSTRALIA

In the revision of the Brachytheciaceae of the Huon Peninsula, Papua New Guinea, Ignatov et al. (1999) reported Platyhypnidium muelleri from Australia based on a sterile specimen collected by H. Streimann (#1585) in New South Wales, as they found the specimen morphologically to be within the range of Malesian P. muelleri. Hedenäs (2002), however, left this specimen in Platyhypnidium austrinum, the only species of that genus confirmed by him in Australia, as the range of variation of this species was found by him to include the Streimann specimen. As the sporophyte is lacking (P. muelleri has smooth seta, P. austrinum a strongly roughened one), and most of the characters of the two species are very variable, it is a difficult task to find reliable morphological differences between these two taxa. Fortunately we were able to sequence trnL from this specimen. Both shared substitutions and phylogenetic analyses suggest that the Australian specimen is likely more closely related to P. muelleri than to “P. austrinum” (which occurs in a completely different clade). The phylogenetic analysis (Figure 6.4; Platyhypnidium sp. nov 2 Australia NSW), however, shows that this specimen probably does not belong to P. muelleri either, and most probably represents an undescribed species of Rhynchostegium s. lat. As we failed to sequence ITS, more studies are needed to confirm the position of this species.

6.4.10 EURHYNCHIELLA The type species of this genus, E. zeyheri, and E. acanthophylla were found nested within the Rhynchostegium–Platyhypnidium clade, being especially close to Platyhypnidium fuegianum (Figure 6.4). Although Eurhynchiella was originally placed in subfamily Helicodontioideae (Ignatov and Huttunen, 2002), morphological characteristics of E. zeyheri do not contradict the present concept of Rhynchostegium. The differences from the more common form of Rhynchostegium include mostly small size of plants, short hyaline axillary hairs, and the costa ending in a spine. However, none of these characters is totally unknown in Rhynchostegium s. lat. Considering the remaining problems within the Rhynchostegium clade discussed above, Eurhynchiella could be synonymized with Rhynchostegium if one would prefer to accept the latter in a broad sense including

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Platyhypnidium, or otherwise the concept of Eurhynchiella can be expanded to include Platyhypnidium fuegianum. This should, however, be done only after additional, more expanded study, as in this case Eurhynchiella will be morphologically very heterogeneous.

6.4.11 ERIODON This genus was placed in Eurhynchioideae by Ignatov and Huttunen (2002) following some rather inconclusive evidence from gametophyte morphology. Sporophyte structure of Eriodon is one of the most peculiar in the Brachytheciaceae and in pleurocarps in general: the teeth are narrow, long and spirally twisted. The present analysis found E. conostomus, the type of the genus, well nested in the Rhynchostegium–Platyhypnidium clade. If this position of Eriodon gets further support, as we expect, this situation will cause some difficulties for nomenclature, as the genus Eriodon is one of the earliest generic names in Brachytheciaceae. The solution can be either conservation of Rhynchostegium, 1852 against Eriodon 1845, or an acceptance of paraphyletic genera, as discussed in the section “Concluding Remarks” below.

6.4.12 BRYHNIA The taxonomy of this genus is one of the most controversial within the Brachytheciaceae. Takaki (1956) recognized 15 species in the genus in Japan and adjacent areas. Subsequently, due to the presence of morphologically transitional plants, most were reduced to the synonymy of Bryhnia novae-angliae (cf. Noguchi, 1991). The concept of this species was then expanded to consider it a widespread circumboreal taxon. Our previous data (Figure 6.1) show that European + South Siberian and East Asian plants, referred to just one species, Bryhnia novae-angliae, are not only non-conspecific, but probably even non-congeneric. Our new data confirm this (Figure 6.4). Eastern North American and East Asian plants form a well-supported clade sister to Brachythecium frigidum, a common species of wet habitats in western North America. Thus, we suggest the placement of Bryhnia novae-angliae in Brachythecium (cf. Goffinet et al., 2001). However, Siberian and European plants belong to another lineage, for which the genus Bryhnia can be retained, with one to two species, Bryhnia scabrida and probably also Bryhnia hultenii E. B. Bartram. Interestingly, the geographic separation of the two lineages of the former “Bryhnia novae-angliae”, i.e., Europe + Siberia versus China + North America, is somewhat similar to that found in Platyhypnidium (cf. Figures 6.5C and 6.5B, where most species represent two clades, distributed in Europe + Africa and East Asia + North America).

6.4.13 BRACHYTHECIASTRUM

CF. TRACHYPODIUM

We failed to get fresh material of B. trachypodium from central Europe, from where this species was described, and instead included in the analysis two specimens from southern and eastern Siberia. As was already stated by Ignatov (1998), specimens from Altai and other parts of Siberia are probably not conspecific with central European material, but represent a slender form of B. velutinum. In the present study of “B. trachypodium” Siberian specimens are close to western North American B. leibergii, although the Brachytheciastrum clade remained totally unresolved in a strict consensus topology. Certainly this group needs further studies. This is one more example of the fact that morphologically almost identical phenotypes might have independent origins in geographically separated areas, being derived from close, but not the same, species (Shaw and Allen, 2000).

6.5 CONCLUDING REMARKS The Brachytheciaceae is a diverse group of mosses, and most of its representatives are mesic plants of forest floor, tree bases, fallen logs, rocks in forest, etc. The Brachytheciaceae have colonized two extreme habitats: tree trunks, which led to many morphological parallelisms in sporophyte structure,

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discussed by Huttunen et al. (2004), and subaquatic habitats. Almost all major groups of Brachytheciaceae have lineages leading to subaquatic taxa: in the Oxyrrhynchium group these are Oxyrrhynchium speciosum and Donrichardsia; in the Rhynchostegium group, Platyhypnidium; in the Brachythecium group, Brachythecium rivulare, B. frigidum + B. novae-angliae and Bryhnia scabrida; in the Scleropodium group, Scleropodium obtusifolium and S. caespitans; in Rhynchostegiella s. lat.., “Platyhypnidium austrinum”; in Rhynchostegiella s. str., R. teneriffae and R. macilenta. It seems that the change to a wetter environment leads to a number of common changes in morphology: leaves become more shortly and broadly acute, and in aquatic plants leaves at the top of the shoot become reflexed, becoming star-like from the apical view. A very broad costa is not a common character in the Brachytheciaceae, and is found in the family only in aquatic to subaquatic species: Donrichardsia macroneuron, Rhynchostegiella macilenta, Nobregaea latinervis and Platyhypnidium mutatum. The more dependent the species are on aquatic environments, the more similar they are: aquatic lineages of Platyhypnidium, some Donrichardsia (Hawaiian and Chinese) and “Platyhypnidium austrinum” are especially similar in overall morphology, exhibiting also similar variation patterns. The less strictly specialized hygrophytes that only rarely grow totally flooded, e.g., Bryhnia, Brachythecium (B. rivulare-group), and Scleropodium, are less alike. The problem for classification is how to treat these ecologically and morphologically specific groups, which originate from widespread genera including several species. This problem was previously discussed for Unclejackia (Ignatov and Huttunen, 2002). This genus includes two species, alpine tree-fern epiphytes, growing at 3000 to 3300 m elevation in New Guinea (Ignatov et al., 1999). Unclejackia was described as a separate genus, but later it appeared well nested within Brachythecium in molecular analysis. However, numerous morphological differences precluded its inclusion in Brachythecium itself (Ignatov and Huttunen, 2002; Huttunen and Ignatov, 2004). Some authors continue to keep it even outside the Brachytheciaceae, in the Symphyodontaceae (Tan, 2000; Goffinet and Buck, 2004), as this genus has been segregated from Chaetomitrium, a member of the Symphyodontaceae. The disadvantage of including Unclejackia (ecostate pendent plants) in Brachythecium is that it will make morphological circumscription of the genus Brachythecium almost limitless, while the disadvantage of generic recognition of Unclejackia while following cladistic standards of classification will split Brachythecium into about 10 genera. Both alternatives seem much more problematic than the retention of Unclejackia as a genus leaving Brachythecium paraphyletic. Parallel situations appear not to be unique in the Brachytheciaceae. Donrichardsia is clearly nested in Oxyrrhynchium and their close affinity continues to receive more support from molecular evidence. However, these two genera have clear morphological distinctions in axillary hairs, laminal cells and costa structure (Huttunen and Ignatov, in preparation). From the phytogeographic point of view Donrichardsia is an old genus, represented in the world by a few highly isolated populations with classical Arcto-Tertiary disjunctions between East Asia and eastern North America (“Liriodendron-disjunction”) and also with tropical localities. A similar distribution pattern covering East Asia, eastern North America and the tropics is well known for mosses, such as Brothera, Herpetineuron and Rauiella. Should Donrichardsia thus be included in Oxyrrhynchium for the reason that the latter will otherwise be paraphyletic? Eriodon represents the third case. As also seen in this genus, a shift to epiphytic habitats is often associated in pleurocarpous mosses with a remarkable modification in peristome, which has obscured the familial placement of some genera such as Anacamptodon in the Amblystegiaceae (Vanderpoorten et al., 2002), Struckia in the Plagiotheciaceae (Pedersen and Hedenäs, 2002), and Okamuraea and Clasmatodon in the Brachytheciaceae (Tsubota et al., 2002; Goffinet et al., 2001). Eriodon conostomus represents probably the only epiphytic lineage of the large Rhynchostegium–Platyhypnidium clade. This situation is in many ways parallel to Unclejackia. Both genera occur at the limit (if not “corners” — Eriodon occurs in southern South America; Unclejackia in high mountains of New Guinea) of distribution of their ancestral groups, i.e., Brachythecium and Rhynchostegium. Both genera are pendent epiphytes with erect capsules, straight perichaetial leaves, modified peristomes and large spores. The implication to practical taxonomy is also parallel.

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Inclusion of Eriodon in Rhynchostegium (which probably can be retained after being conserved, see above) expands the latter genus drastically: the genus will include both pendent epiphytes, widespread mesophytes and many aquatic “Platyhypnidium” species. On the other hand, division of the Rhynchostegium into smaller units will lead to many small genera that will also be very heterogeneous (see above, discussion under Platyhypnidium). Thus, our suggestion will be the same as in the case of Unclejackia: to keep Eriodon as a separate genus despite its position nested in the Rhynchostegium–Platyhypnidium clade. These kinds of problems will probably repeatedly appear when populations of widespread species more or less rapidly adapt to contrasting ecological environments. Disagreements between morphological and ecological and, on the other hand, genetic characteristics in cases of rapid speciation are, and probably always will be, difficult to solve. Thus, the nomenclatural decisions in similar paraphyletic groups should be as conservative as possible (which, however, is not applicable to polyphyletic groups). TAXONOMIC AND NOMENCLATURAL CHANGES: Donrichardsia pringlei (Card.) Huttunen & Ignatov comb. nov. — Rhynchostegium pringlei Card., Revue Bryologique 37: 70. 1910.

ACKNOWLEDGMENTS This work was partly supported by Jaakko Hyvönen’s project “Bryosphere” by the Academy of Finland, by the Finnish Society for Study of Flora and Fauna, the program Biodiversity of the Russian Academy of Sciences, Scientific School program NS-1712.2003.4 and RFBR grants 0304-48960 and 04-04-48774. In addition, the research was supported by a Marie Curie IntraEuropean Fellowship within the 6th European Community Framework Programme. We are very grateful to Lars Hedenäs for specimens of rare species for sequencing and to Alain Vanderpoorten for supplying us with some sequence data.

REFERENCES Brotherus, V. F. (1925) Musci. In Die natürlichen Pflanzenfamilien, Vol.11, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp.1–522. Bruch, P., Schimper, W. P. and Gümbel, T. (1851–1855) Bryologia Europaea seu genera muscorum Europaeorum monographice illustrata, Vols. 5–6. Sumptibus Librariae E. Schweizerbart, Stuttgartiae. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Novel relationships in pleurocarpous mosses as revealed by cpDNA sequences. Bryologist, 103: 774–789. Cech, T. R., Damberger, S. H. and Gutell, R. R. (1994) Representation of the secondary and tertiary structure of group I introns. Structural Biology, 1: 273–280. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (1999) A Checklist of the Mosses. Missouri Botanical Garden, St. Louis. De Pinna, M. C. C. (1991) Concepts and tests of homology in cladistics. Cladistics, 7: 367–394. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes. Monographs in Systematic Botany, No. 98 (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Goffinet, B., Cox, C. J., Shaw, A. J. and Hedderson, T. J. (2001) The Bryophyta (mosses): Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Annals of Botany, 87: 191–208. Hedenäs, L. (1987) On the taxonomic position of Tomentypnum Loeske. Journal of Bryology, 14: 729–736. Hedenäs, L. (1989) On the taxonomic position of Conardia Robins. Journal of Bryology, 15: 779–783. Hedenäs, L. (1992) Flora of Madeiran pleurocarpous mosses (Isobryales, Hypnobryales, Hookeriales). Bryophytorum Bibliotheca, 44: 1–165. Hedenäs, L. (2002) An overview of the family Brachytheciaceae (Bryophyta) in Australia. Journal of the Hattori Botanical Laboratory, 92: 51–90.

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Huttunen, S. and Ignatov, M. S. (2004) Phylogeny of Brachytheciaceae (Bryophyta), based on morphology and sequence level data. Cladistics, 20: 151–183. Huttunen, S., Ignatov, M. S., Müller, K. and Quandt, D. (2004) Phylogeny and evolution of epiphytism in the three moss families: Meteoriaceae, Brachytheciaceae, and Lembophyllaceae. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R.Magill). Missouri Botanical Garden Press, St. Louis, pp. 328–361. Ignatov, M. S. (1998) Bryophyte flora of Altai Mountains. VIII. Brachytheciaceae. Arctoa, 7: 85–152. Ignatov, M. S. (1999) Bryophyte flora of the Huon Peninsula, Papua New Guinea. LXIII. On the pseudoparaphyllia in Brachytheciaceae and Meteoriaceae (Musci). Acta Botanica Fennica, 165: 73–83. Ignatov, M. S. and Huttunen, S. (2002 [2003]) Brachytheciaceae (Bryophyta) — a family of sibling genera. Arctoa, 11: 245–296. Ignatov, M. S., Ando, H. and Ignatova, E. A. (1996) Bryophyte flora of Altaian mountains. VII. Hypnaceae and related pleurocarps with bi- or ecostate leaves. Arctoa, 6: 21–112. Ignatov, M. S., Koponen, T. and Norris, D. H. (1999) Bryophyte flora of the Huon Peninsula, Papua New Guinea. LXII. Brachytheciaceae (Musci), excluding Homalothecium and Palamocladium. Acta Botanica Fennica, 165: 23–73. Ignatov, M. S., Huttunen, S. and Koponen, T. (2005) Bryophyte flora of Hunan Province, China. 5. Brachytheciaceae (Musci), with an overview of Eurhynchiadelphus and Rhynchostegiella in SE Asia. Acta Botanica Fennica, 178: 1–56. Limpricht, K. G. (1904) Die Laubmoose. In Kryptogamen-Flora von Deutchlands, Oesterreiches und der Schweiz. 2 Aufl., Bd. 4, Abt. 3. (ed. L. Rabenhorst). Eduard Kummer, Leipzig. Milde, J. (1869) Bryologia Silesiacea. Verlag von Arthur Felix, Leipzig. Noguchi, A. (1991) Illustrated Moss Flora of Japan, Vol. 4. Hattori Botanical Laboratory, Hiroshima. Ochyra, R. and Vanderpoorten, A. (1999) Platyhypnidium mutatum, a mysterious new moss from Germany. Journal of Bryology, 21: 183–189. Pedersen, N. and Hedenäs, L. (2002) Phylogeny of the Plagiotheciaceae based on molecular and morphological evidences. Bryologist, 105: 310–324. Rudi, K. and Jakobsen, K.S. (1999) Complex evolutionary patterns of tRNAUAALeu group I introns in cyanobacterial radiation. Journal of Bacteriology, 181: 3445–3451. Sergio, C. and Hebrard, J. P. (1982) Orthothecium durieui (Mont.) Besch. Étude systematique, écologique and phytogéographique. Collectanea Botanica (Barcelona), 13: 247–255. Shaw, A. J. and Allen, B. (2000) Phylogenetic relationships, morphological incongruence, and geographic specialization in the Fontinaliaceae. Molecular Phylogenetics and Systematics, 16: 225–237. Takaki, N. (1955) Researches on the Brachytheciaceae of Japan and its adjacent areas. II. Journal of the Hattori Botanical Laboratory, 15: 1–69. Takaki, N. (1956) Researches on the Brachytheciaceae of Japan and its adjacent areas. III. Journal of the Hattori Botanical Laboratory, 16: 1–71. Tan, B. C. (2000) Additions of the moss floras of Mt. Wilhelm nature reserve and Mt. Gahavisuka Provincial Park, Papua New Guinea. Journal of the Hattori Botanical Laboratory, 89: 173–196. Tsubota, H., Arikawa, T., Akiyama, H., De Luna, E., Gonzales, D., Higuchi, M. and Deguchi, H. (2002) Molecular phylogeny of hypnobryalean mosses as inferred from the large scale dataset of chloroplast rbcL, with special reference on the Hypnaceae and possibly related families. Hikobia, 13: 645–665. Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002) Circumscription, classification, and taxonomy of the Amblystegiaceae (Bryopsida) inferred from nuclear and chloroplast DNA sequence data and morphology. Taxon, 51: 115–122. Vanderpoorten, A., Ignatov, M., Huttunen, S. and Goffinet, B. (2005) A molecular and morphological recircumscription of Brachytheciastrum (Brachytheciaceae, Bryopsida). Taxon, 54: 369–376. Wheeler, W. (1996) Optimization alignment: The end of multiple sequence alignment in phylogenetics? Cladistics, 12: 1–9.

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Relationships 7 Phylogenetic within the Moss Family Meteoriaceae in the Light of Different Datasets, Alignment and Analysis Methods Sanna Huttunen and Dietmar Quandt CONTENTS Abstract ..........................................................................................................................................145 7.1 Introduction...........................................................................................................................146 7.1.1 History of the Meteoriaceae.....................................................................................146 7.2 Material and Methods ..........................................................................................................149 7.3 Results and Discussion.........................................................................................................150 7.3.1 Delimitation of the Meteoriaceae.............................................................................150 7.3.2 Effect of Taxon Selection, Alignment and Analysis Methods on Phylogenetic Relationships within Meteoriaceae ..........................................................................150 7.3.3 Morphological Evolution within Meteoriaceae .......................................................153 7.3.4 Taxonomic Treatment and Phylogenetic Relationships between Genera................154 7.3.4.1 Subfamily Meteorioideae Broth., Nat. Pfl. 2(9): 154. 1925. ...................154 7.3.4.2 Subfamily Meteoriopsoideae subfam. nov................................................157 7.4 Conclusions...........................................................................................................................160 Acknowledgments ..........................................................................................................................161 References ......................................................................................................................................161

ABSTRACT In this chapter we compare the results from four earlier phylogenetic analyses of the moss family Meteoriaceae. Based on our previous studies we review the current state concerning the generic relationships within the family. Phylogenies are used to evaluate the views of morphological evolution within the family and to pinpoint the synapomorphies of the major clades. However, due to limited sampling size for most of the genera, phylogenies can be used in only a few cases to detect the generic synapomorphies and the monophyly of the genera. In the majority of the analyses the family Meteoriaceae was divided in two stable clades, which we recognize here as subfamilies: Meteorioideae Broth., including Chrysocladium M. Fleisch., Diaphanodon Renauld & Cardot., Meteorium (Brid.) Dozy & Molk., Papillaria (Müll. Hal) Lorentz and Trachypus Reinw. & Hornsch.; and Meteoriopsoideae subfam. nov., with Aerobryidium M. Fleisch. ex Broth., Aerobryopsis M. Fleisch., Barbella M. Fleisch. ex Broth., Barbellopsis Broth., Duthiella Müll. 145

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Hal. ex Broth., Floribundaria M. Fleisch., Meteoriopsis M. Fleisch. ex Broth., Neodicladiella (Nog.) W.R.Buck, Neonoguchia S.H.Lin, Pseudospiridentopsis (Broth.) M. Fleisch., Pseudotrachypus P. de la Verde & Thér., Sinskea W.R.Buck, Trachycladiella (M. Fleisch.) M. Menzel and Trachypodopsis M. Fleisch.

7.1 INTRODUCTION The Meteoriaceae consist of mainly epiphytic mosses occurring in humid tropical and warm temperate forests. Most of the Meteoriaceae are easy to recognize in the field as members of this family by their pendent habit, a character earlier regarded as important for the delimitation of this family (Brotherus, 1925; Noguchi, 1976). Other gametophytic characters shared by most of the Meteoriaceae species include papillose leaf cells, monopodial growth and a specific pattern of leaf-like pseudoparaphyllia that surround young branch primordia (Ignatov, 1999). Otherwise, the morphological variation is fairly wide. Shoots may either be terete or complanate, and even in one plant, foliage and appearance of the shoots is plastic depending on the position of the shoot relative to the substrate. Leaf laminal cell shape varies from linear to rhomboidal and the leaf cell papillosity from uni- to pluripapillose. In the latter case, papillae may be either scattered over the cell lumen or arranged in rows over the lumen or cell walls. Both the number of papillae as well as their arrangement and position on cells are usually regarded as important diagnostic characters, such as in generic keys of the Meteoriaceae (e.g., Buck, 1994; Huttunen, 2004a; Menzel, 1992; Noguchi, 1976; Spessard-Schueth and Crum, 1994; Streimann, 1991), although the papillosity pattern has been shown to vary even within some species (Buck, 1994; Streimann, 1992). In sporophytes, seta length ranges from 1 mm to 2–3 cm. Capsules are most often erect and cylindrical to oblong, but in some cases inclined and almost globose. Meteoriaceae peristomes are usually described as “isobryoid,” but character states such as ornamentation of the outer surface of the exostome, height of the trabecula, height of the endostomial cilia and basal membrane, structure of endostome segments and the hygroscopic movements of the peristome still show a considerable variation within the family. For example, despite the fact that those genera with the most distinctively hypnalian peristome structure have already been transferred to other families (e.g., Aerobryum and Meteoridium to the Brachytheciaceae, Weymouthia to the Lembophyllaceae), several species with strongly cross-striate exostome are still present in Meteoriaceae, in addition to those with totally papillose or smooth ornamentation. Indeed, the conflict between sporophytic characters and pendent habit was the main topic of discussion in most of the cases when transferring species or genera into or out of Meteoriaceae (Noguchi, 1976). Due to the wide variation in morphological character combinations and plasticity in some characters that are often used in delimiting genera, the delimitation of Meteoriaceae as family and especially relationships within the family have remained unresolved. Even the monophyly of the family has been questioned (Buck, 1998). Although a more detailed phylogenetic study of the Meteoriaceae is still lacking, our recent studies and ongoing projects on the evolution of the Meteoriaceae provide some new taxonomical aspects and insights into the morphological evolution of this family (Huttunen, 2004a; Huttunen et al., 2004; Quandt and Huttunen, 2004; Quandt et al., 2004). In these studies the number of taxa, the information included as well as method of phylogenetic analyses varied, offering the opportunity to evaluate the effect of these factors on the robustness of phylogenetic relationships and to point out the most stable as well as the more poorly supported groupings within the family. Thus, our aim is to revise the current knowledge of phylogenetic relationships within the Meteoriaceae, to point out taxonomical consequences and problems and to discuss topics that need further and more detailed studies.

7.1.1 HISTORY

OF THE

METEORIACEAE

The Meteoriaceae was originally established by Kindberg (1897) including only those species of Meteoriaceae that occur in North America: Papillaria nigrescens Hedw. [= Meteorium nigrescens

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(Hedw.) Dozy & Molk.], P. donnelii Kindb. [= M. nigrescens (Hedw.) Dozy & Molk.] and Meteorium pendulum Sull. [= Neodicladiella pendula (Sull.) W.R. Buck]. Thereafter, Fleischer (1907) added several tropical genera and gave a detailed diagnosis for the family. In the first worldwide revision of the Meteoriaceae by Brotherus (1909), the family consisted of 13 genera, with most of them still treated in the Meteoriaceae in recent classifications (Table 7.1). By the second edition of Die natürlichen Pflanzenfamilien (Brotherus, 1925), active studies on tropical mosses had raised the number of genera to 16. Brotherus (1925) followed Fleischer’s (1907) division of Meteoriaceae and placed the genera in two subfamilies: Pilotrichelloideae and Meteorioideae. The Pilotrichelloideae included species with smooth leaf cells and occasionally with double or without costa, while most of the Meteorioideae species had papillose leaf cells and a single costa which reaches up to mid-leaf. The family-level classification in Brotherus (1925) was strongly affected by Fleischer’s (1907) work on tropical mosses, and especially at higher taxonomical levels it mainly relied on sporophyte characters. After this “Brotherus–Fleischer” classification, the family concept remained fairly stable for decades (Table 7.1). The wide morphological variation within Meteoriaceae and the pendent life form as the most important delimiting character, however, led to doubts about the naturalness of the family (Buck, 1994; Noguchi, 1976; Norris and Koponen, 1985; Quandt and Huttunen, 2004). The first steps to redefine the delimitation of Meteoriaceae were made by Buck (1994), and since then the family concept has gone through some major changes. Buck (1994) synonymized Meteoriaceae with Trachypodaceae M. Fleisch., including six genera, Diaphanodon Renauld & Cardot, Duthiella Müll. Hal., Pseudospiridentopsis (Broth.) M. Fleisch., Pseudotrachypus Thériot, Trachypus Reinw. & Hornsch. and Trachypodopsis M. Fleisch., which still increased the morphological variability of the family. The circumscription of Trachypodaceae was already questioned earlier, and Norris and Koponen (1985) suggested that at least Diaphanodon, Trachypus and Trachypodopsis could be closely related to Meteoriaceae. Along with these family-level rearrangements, Menzel (1992), Buck (1994), and Menzel and Schultze-Motel (1994) suggested some new generic groupings within the Meteoriaceae. Papillaria (Müll. Hal) Lorentz, the largest genus of the family, was split into three, Toloxis W.R.Buck, Cryptopapillaria M. Menzel and Papillaria, and species in the last mentioned group were transferred to Meteorium (Buck, 1994). Similarly, species in Floribundaria M. Fleisch., Barbella M. Fleisch. and Chrysocladium M. Fleisch. were divided into several genera following the sectional divisions. Buck (1994) also excluded genera such as Dolichomitriopsis Okam., Meteoriella Okam., Pilotrichella (Müll. Hal.) Besch., Pseudopilotrichum (Müll. Hal.) W.R.Buck & Allen (= Orthostichella Müll. Hal.), Squamidium (Müll. Hal.) Broth. and Weymouthia Broth. from the family. Brotherus (1925) placed most of these in the subfamily Pilotrichelloideae and Fleischer (1907) in the tribe Pilotrichellaleae. Due to the fact that Buck (1994) assumed that the Meteoriaceae might be a lineage deriving from the Brachytheciaceae, he still retained some doubtful genera such as Aerobryum Dozy & Molk., Meteoridium (Müll. Hal.) Manuel and Zelometeorium Manuel within Meteoriaceae. Despite these rearrangements, the morphological delimitation of Meteoriaceae remained ambiguous, and the monophyly of the newly circumscribed family remained untested. The first phylogenetic analyses, however, challenged the monophyly of the Meteoriaceae. Studies by both Hedenäs (1995) and Buck et al. (2000) revealed the polyphyly of the family as traditionally circumscribed. At the same time as the first molecular phylogenies of pleurocarpous mosses (see Buck et al., 2000) some pendent genera were transferred from Meteoriaceae to other families such as Brachytheciaceae (e.g., Aerobryum, Zelometeorium, Meteoridium) or Lembophyllaceae (Weymouthia, Neobarbella Nog.) (Table 7.1; Buck and Goffinet, 2000; Crosby et al., 1999). The number of Meteoriaceae species in these studies was, however, very low and hence it was impossible to evaluate the phylogenetic relationships within the Meteoriaceae or to confirm the monophyly of the family. The position of some poorly understood monotypic genera such as Ancistrodes Hampe, Lepyrodontopsis Broth., Aerolindigia M.Menzel, Lindigia Hampe and Cryphaeophilum M. Fleisch. also remained uncertain.

Subfam. Pilotrichelloideae Cryphaeophilum Duseniella (= Ancistrodes) Pilotrichella L Squamidium Weymouthia L Subfam. Meteorioideae Aerobryidium Aerobryopsis Aerobryum Barbella Chrysocladium Floribundaria Lindigia Meteoriella Meteoriopsis Meteorium Papillaria

Aerobryidium Aerobryopsis Aerobryum Barbella Duseniella (= Ancistrodes) Floribundaria Lindigia Meteoriopsis Meteorium Papillaria Pilotrichella L Squamidium Weymouthia L

Crosby et al. 1999 Meteoriaceae Aerobryidium Aerobryopsis Ancistrodes Barbella Barbellopsis Bryowijkia Chrysocladium Cryphaeophilum Cryptopapillaria Diaphanodon Dolichomitriopsis L Duthiella Floribundaria Lepyrodontopsis Meteoriopsis Meteorium Neodicladiella Neonoguchia Papillaria Pseudobarbella Pseudospiridentopsis Pseudotrachypus Sinskea Toloxis Trachycladiella Trachypodopsis Trachypus

Vitt 1984 Meteoriaceae Aerobryidium Aerobryopsis Aerobryum Ancistrodes Barbella Barbellopsis Chrysocladium Cryphaeophilum Dolichomitriopsis L Floribundaria Isotheciopsis (=Neobarbella) L Lindigia Meteoriopsis Meteorium Papillaria Pilotrichella L Pseudobarbella Squamidium Weymouthia L Aerobryidium Aerobryopsis Ancistrodes Barbella Barbellopsis Chrysocladium Cryphaeophilum Cryptopapillaria Diaphanodon Duthiella Floribundaria Lepyrodontopsis Meteoriopsis Meteorium Neodicladiella Neonoguchia Pseudospiridentopsis Pseudotrachypus Sinskea Toloxis Trachycladiella Trachypodopsis Trachypus

Buck and Goffinet 2000 Meteoriaceae

Aerobryidium Aerobryopsis Barbella Barbellopsis Chrysocladium Cryptopapillaria Diaphanodon Duthiella Floribundaria Meteoriopsis Meteorium Neodicladiella Neonoguchia “Papillaria” Pseudospiridentopsis Pseudotrachypus Sinskea Toloxis Trachycladiella Trachypodopsis Trachypus

Huttunen and Quandt Meteoriaceae

148

Note: Analyses based on Huttunen et al., 2004; Quandt et al., 2004; Quandt and Huttunen, 2004). Species that, according to current knowledge (Quandt et al., 2006), belong to Lembophyllaceae are marked with L.

Brotherus 1925 Meteoriaceae

Brotherus 1909 Meteoriaceae

TABLE 7.1 Circumscriptions of the Meteoriaceae in Some Classifications of Mosses and New Delimitations for the Family Based on Phylogenetic Analyses

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TABLE 7.2 Datasets and Methods of Alignment and Phylogenetic Analyses in Quandt et al. (2004), Huttunen et al. (2004) and Quandt and Huttunen (2004) Quandt et al., 2004 No. of taxa Total Meteoriaceae Data Morphological Molecular

Alignment method (gap treatment) + method of analyses

Huttunen et al., 2004

Quandt and Huttunen, 2004

66 36

159 36

48 22

— nr ITS2 cp trnL-F cp psbT-H 1. Manual + MP ratchet

60 chars nr ITS2 cp trnL-F cp psbT-H 1. Manual + MP ratchet (incl. only molecular data) 2. DO (incl. only molecular data) 3. DO (incl. morphology + molecular data)

— nr ITS2 cp trnL-F cp psbT-H 1. Manual + MP ratchet

2. DO 3. DO (gaps as ?) + MP ratchet 4. Manual + ML

Note: In Quandt et al. (2004) all alignment–analyses combinations were performed both for combined data, and nrDNA and cpDNA regions separately. For detecting the homologies between DNA sequences, two methods were used: direct optimization (DO) and manual alignment. In DO analyses and “alignment” steps are combined into one dynamic process while in case of manual alignments, static alignments were afterwards analysed with maximum likelihood (ML) or parsimony as an optimality criterion.

7.2 MATERIAL AND METHODS Phylogenies discussed in this paper are based on analyses performed in three of our earlier papers (Huttunen et al., 2004; Quandt and Huttunen, 2004; Quandt et al., 2004). Data included in these analyses and phylogenetic analyses performed in these studies are presented in Table 7.2. Analyses are either based only on molecular data (Huttunen et al., 2004; Quandt et al., 2004; Quandt and Huttunen, 2004) or included both molecular and morphological data (Huttunen et al., 2004). The effect of different homology assessments and statements between DNA sequences was tested by analysing the data both with traditional methods (manual alignment + separate analyses step) and by direct optimization (Wheeler, 1996). For alignment we used the program Alignment Editor Align (Hepperle, 2002) and parsimony and maximum likelihood analyses of static alignments were performed with winPAUP 4.0b10 or UNIXPAUP 4.0b10 (Swofford, 2002). For parsimony analyses the program PRAP (Müller, 2004) enabled the use of parsimony ratchet (Nixon, 1999) in PAUP analyses. For direct optimization analyses we used the program POY (Gladstein and Wheeler, 2001). In direct optimization (DO), the search for the most parsimonious set of homologies between sequences (“alignment”) and the tree reconstruction are combined into one process; thus, no separate alignment step prior to the analyses is needed. However, in DO analyses indel-information is affecting the tree reconstruction in the same way as other base substitutions. Thus, to enable direct comparisons between manual (gaps treated as missing data) and DO method (gaps included as 5. character state), implied alignments from DO were also re-analysed treating gaps as missing data (Table 7.2).

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7.3 RESULTS AND DISCUSSION 7.3.1 DELIMITATION

OF THE

METEORIACEAE

Results from all analyses supported the monophyly of Meteoriaceae, with the exclusion of some smaller genera (Table 7.1; Figure 7.1, Figure 7.2). The family also appeared in all analyses as sister clade to Brachytheciaceae, hence supporting the ideas presented by Buck (1994) and Ignatov (1999) (Figure 7.1). The unique pattern of pseudoparaphyllia (Ignatov, 1999) seemed to be a synapomorphy for the Meteoriaceae–Brachytheciaceae clade, and both can be distinguished from each other by one additional character, leaf cell papillosity (Huttunen et al., 2004; Ignatov and Huttunen, 2002). Meteoriaceae have variously arranged papillae on leaf cells, while in the Brachytheciaceae all species lack true papillae. In some rare cases, such as Barbellopsis trichophora (Montagne) W. R. Buck, however, papillae may be secondarily lost in the Meteoriaceae. In order to retain a monophyletic family some genera such as Ancistrodes (Müll. Hal.) Crosby, Cryphaeophilum (Dusen) M. Fleisch., Lepyrodontopsis (Hedw.) Broth. and Lindigia (Mitt.) A. Jaeger should be excluded from the Meteoriaceae (Table 7.1; Huttunen et al., 2004; Quandt and Huttunen, 2004; Quandt et al., 2004). These all are monotypic, pendent genera from South America. Based on the molecular data, it seems that Ancistrodes should be placed within Hookeriales and Cryphaeophilum in Cryphaeaceae (Quandt et al., 2004), but the phylogenetic position of Lindigia and Lepyrodontopsis remains ambiguous. The species of Trachypodaceae are resolved as a polyphyletic group within Meteoriaceae, thus confirming the synonymization by Buck (1994). Quandt and Huttunen (2004) showed that a pendent growth habit, which in early classifications served to delimit Meteoriaceae, has evolved several times in different lineages among pleurocarpous mosses, and thus cannot be used alone as a diagnostic character for the family. Although the morphological similarities between the Lembophyllaceae and Meteoriaceae are often emphasized (as in Allen and Magill, 2003), these two families are not closely related (Huttunen et al., 2004; Quandt et al., 2004).

7.3.2 EFFECT OF TAXON SELECTION, ALIGNMENT AND ANALYSIS METHODS PHYLOGENETIC RELATIONSHIPS WITHIN METEORIACEAE

ON

The majority of our phylogenetic analyses revealed that the Meteoriaceae consist of two evolutionary lineages, one including, for example, Papillaria and Meteorium and another with the majority of genera in the Meteoriaceae (Figure 7.2). We will treat these groups here as subfamilies Meteorioideae Broth. and Meteoriopsoideae subfam. nov. (see below). Whereas the Meteoriopsoideae were always monophyletic (Figure 7.2), the Meteorioideae were in some analyses using only molecular data, either paraphyletic (Huttunen et al., 2004; Quandt et al., 2004; Quandt and Huttunen, 2004) or unresolved (Quandt et al., 2004) regardless of the alignment or analysis methods. Topological differences between phylogenetic analyses usually concerned weakly supported groups, namely Aerobryopsis longissima, the Cryptopapillaria–Toloxis clade, Duthiella, Pseudotrachypus, Trachypus and Trachypodopsis (Figure 7.2). Some topological differences seemed to depend on alignment/analysis method. For example, DO in all analyses favoured a placement of Trachypus bicolor Reinw. & Hornsch among the Meteorioideae, whereas analyses of manual alignment left it unresolved or placed it within Meteoriopsoideae (Huttunen et al., 2004; Quandt et al., 2004). The Cryptopapillaria–Toloxis clade behaved in phylogenies similarly to Trachypus. Manual alignments favoured its placement basal to the whole family (Huttunen et al., 2004; Quandt and Huttunen, 2004) or this clade remained unresolved (Quandt et al., 2004) contrasting to the position obtained with DO that resolved it within the Meteorioideae (Huttunen et al., 2004; Quandt et al., 2004). The only exception found was in DO analyses of molecular data in Huttunen et al. (2004) where Meteorioideae formed a paraphyletic grade, and the Cryptopapillaria–Toloxis clade appeared basal to the Meteoriopsoideae. Aerobryopsis longissima [as A. wallichii in Huttunen et al. (2004)] in analyses based on manual alignments was

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151

Lembophyllaceae Hylocomiaceae

Meteoriaceae

Brachytheciaceae

FIGURE 7.1 Phylogenetic relationships of the moss family Meteoriaceae according to Huttunen et al. (2004). Phylogeny is based on direct optimization analyses including nuclear ITS2 and plastid psbT–H and trnL–F data and morphology.

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Floribundaria floribunda

>10

Floribundaria pseudofloribunda

100

Duthiella wallichii

9

Aerobryopsis longissima 99 97 1

Aerobryidium filamentosum Meteoriopsis squarrosa

69

76

Meteoriopsoideae

Pseudospiridentopsis horrida

96 4

Trachypodopsis serrulata Sinskea flammea

10 100

60

Sinskea phaea

3 74 >10

>10

Pseudotrachypus martinicensis

100

Pseudotrachypus wallichii Trachycladiella aurea

58 1

100

Barbellopsis trichophora

78 3

Neodicladiella flagellifera

90 >10 100 1 66 >10 100

Neodicladiella flagellifera Neodicladiella pendula Neodicladiella pendula Trachypus bicolor Diaphanodon blandus

>10 99

Chrysocladium retrorsum 8

>10

99

98

99

5

Meteorium deppei Meteorium nigrescens Meteorium polytrichum

97

Meteorioideae

52

8

Meteorium

Meteorium subpolytrichum Meteorium crispifolium

99

Meteorium papillarioides “Papillaria” intricata

>10

Cryptopapillaria fuscescens

100 6 99 >10 100

7 99

Toloxis imponderosa Toloxis semitorta Papillaria penicillata

>10

Papillaria crocea

100 >10

Papillaria leuconeura

100 >10 100

Papillaria

Papillaria flavo-limbata Papillaria nitens

FIGURE 7.2 Phylogenetic relationships within Meteoriaceae. Topology is based on the same analyses as in Figure 7.1 (see Huttunen et al., 2004 for further information.)

sister to Pseudotrachypus, whereas DO, regardless of data included in analyses, placed it within the Aerobryidium–Pseudospiridentopsis–Meteoriopsis clade (Huttunen et al., 2004). The position of Duthiella and Trachypodopsis differed between analyses with and without morphological data, whereas analysis methods had no effect on it (Huttunen et al., 2004). Their position remained, however, without significant support in all analyses. The topological differences obtained with manual alignments and DO were revealed to be independent from different gap treatment in DO and other tree reconstruction methods (Quandt et al., 2004). In analyses of manual alignments, gaps were treated as missing data whereas in DO analyses information from indel events was utilized in phylogenetic reconstructions in the same way as other substitution events. However, when implied alignments from DO analyses were reanalysed and gaps treated as missing data, they gave almost the same topology as the original DO analyses (Quandt et al., 2004). Thus, the differences in topologies based on manual alignments and DO are rather due to different positioning of nucleotides in the alignment than due to the phylogenetic information of gap positions. Due to a lower number of parsimony informative positions after ignoring indel events (i.e., gaps), branch support values were generally lower and some poorly supported groups remained unresolved. This is not surprising, especially as some clades, such as Meteorium and Papillaria, were supported by characteristic indels ranging from 9 to 21 bp (Quandt et al., 2004). In analyses of a 159-taxa dataset (Table 7.2), DO analyses with combined morphological and molecular data revealed an almost identical topology with DO analyses compared to a 66-taxa dataset without

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morphology. Without morphology, however, the larger dataset analysed with DO led to a paraphyly of the Meteorioideae (Huttunen et al., 2004). Thus, it seems that morphological data had an important role in improving the heuristic searches in DO analyses of our largest data matrix. Unlike in molecular data, user-defined homologies in morphological datasets are not affected by direct optimization. Thus one can expect that inclusion of morphological data could reduce the computational demands of DO analyses and increase the speed of the optimization process of DNA sequence data as there is no need to search for most parsimonious homologies between morphological characters. Besides, the Meteorioideae clade, unlike the Meteoriopsoideae, also has distinct morphological characteristics, and thus inclusion of a morphological data matrix is more likely advantageous for recognizing this clade.

7.3.3 MORPHOLOGICAL EVOLUTION

WITHIN

METEORIACEAE

Phylogenetic analyses revealed that most of the speculations on generic relationships in the early taxonomic publications were hampered by homoplasy of morphological characters and lack of taxonomic value of some easily recognizable differences. As questioned by Buck (1994), a special type of papillosity with numerous papillae being arranged in rows “over the cell walls” has probably evolved at least three times within the Meteoriaceae, in Trachycladiella, Trachypus and Cryptopapillaria. Pluripapillose leaf cells were also revealed to be a plesiomorphic character state in the Meteoriaceae (Huttunen et al., 2004), as suggested by Noguchi (1976), although his argument was based on a slightly different view of relationships within the Meteoriaceae. A unipapillose state evolved from this state at least twice, in Meteorium and Diaphanodon as well as in the Meteoriopsoideae clade, for example in Pseudotrachypus or in the clade including Pseudospiridentopsis, Aerobryidium, Meteoriopsis and Duthiella. However, the number of papillae on each cell and their arrangement does not always provide means for distinguishing genera or even species from each other (Buck, 1994). For example, it seems that despite a variety of papillosity patterns in Floribundaria, phylogenetic analyses support the monophyly of the core group of the genus with several different pluripapillose species such as F. walkeri, F. floribunda and F. pseudofloribunda (Huttunen and Quandt, in preparation). In the Meteoriopsoideae, species of the two major lineages differ in their orientation of stems and leaves. Whereas Duthiella, Pseudospiridentopsis, Aerobryidium and Meteoriopsis are terete foliate plants, the majority of species in the other clade, such as Barbellopsis, Trachypodopsis, Pseudotrachypus and Trachycladiella, have complanate foliation at least on pendent branches. In addition, species of the first clade share a tendency to strongly bent axillary hairs with several cells and a long slender uppermost cell, crispate leaf acumen, and a fairly long seta, although all of these characters are also occasionally present in the latter mentioned clade, but only in a few cases combined with terete shoots. Whereas the peristome structure is very similar in Meteorioideae species, within the Meteoriopsoideae the degree of reduction of peristome structure is highly variable. Although in some of the species cross-striate exostomes are most common (for example, Aerobryidium, Duthiella, Floribundaria, Meteoriopsis, Trachycladiella), species with more slender modified peristomes with totally papillose exostome can also be found (for example, Neodicladiella and Sinskea). To trace the evolution of peristome structures in the Meteoriopsoideae, a more detailed phylogenetic analysis, including a wider selection of species and better support for some interesting species, such as Duthiella and Trachypodopsis, is needed. The majority of the Trachypodaceae species are resolved in phylogenetic analyses as a basal grade within most major clades in Meteoriaceae (Figure 7.2), expect Pseudospiridentopsis and Pseudotrachypus in the Meteoriopsoideae. Remembering the wide variation of gametophytic characters among and within Trachypodaceae species, their polyphyly in the resolved phylogenies is not surprising. At least Duthiella and Trachypus could be regarded as less specialized to epiphytic habitats compared to other Meteoriaceae genera, as they commonly occur both in epiphytic as well

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as terrestrial habitats. This might suggest that former Trachypodaceae species represent a kind of transition from terrestrial to epiphytic habitats within the Meteoriaceae. However, due to the unstable placement of some Trachypodaceae species this idea needs further detailed studies. The usefulness of characters derived from axillary hairs in pleurocarpous mosses has been controversial (Buck, 1980; Hedenäs, 1990); however, our studies concerning the Meteoriaceae show that their structure is informative and even useful for generic classifications. Although in most pleurocarpous mosses axillary hairs are fairly simple, in Meteoriaceae species their structure varies from simple, uniseriate hairs three to four cells long to complex, branching or biseriate forms (see also Hedenäs, 1998; Newton and De Luna, 1999). In some groups, such as Papillaria, they might serve as a good diagnostic character (Quandt et al., 2004). Within the Meteoriaceae, axillary hair characters that could be informative on the genus level include: (1) presence/absence of brown basal cells, (2) tendency of forward axillary hairs consisting of numerous cells, (3) shape of cells, and (4) shape of the most apical cell in each axillary hair, which is in some groups, for example, distinctly bent or very long and slender (e.g., Aerobryopsis M. Fleisch., Meteoriopsis, Pseudospiridentopsis).

7.3.4 TAXONOMIC TREATMENT BETWEEN GENERA

AND

PHYLOGENETIC RELATIONSHIPS

Within the Meteoriaceae two clades appear in most analyses: the clade around Meteorium Dozy & Molk. sensu Buck (1994), and the clade containing the majority of the genera of the family (Figure 7.2; Quandt et al., 2004; Huttunen et al., 2004). The taxa with the most uncertain position comprise Trachypus bicolor Renw. & Hornsch. and the Toloxis clade with Toloxis W. R. Buck, Papillaria intricata (Mitt.) Müll. Hal. & Broth. and Cryptopapillaria fuscescens (Hook.) M. Menzel and Trachypus bicolor Reinw. & Hornsch. Despite the somewhat unstable placement of these taxa, we recognize these two major clades as subfamilies. As generic nomenclature and typifications as well as morphological characteristics have been recently dealt with by Buck (1994), we concentrate here on discussion of phylogenetic relationships between genera. 7.3.4.1 Subfamily Meteorioideae Broth., Nat. Pfl. 2(9): 154. 1925. Type: Meteorium (Brid.) Dozy & Molk. Genera included: Chrysocladium M. Fleisch., Cryptopapillaria M. Menzel, Diaphanodon Renauld & Cardot., Meteorium (Brid.) Dozy & Molk., Papillaria (Müll. Hal) Lorentz, Toloxis W. R. Buck, Trachypus Reinw. & Hornsch. In analyses including morphological characters (Huttunen et al., 2004), synapomorphies for the Meteorioideae include a totally papillose exostome outer surface, relatively large spores (>20 μm), black coloration at the base of shoots which is absent only in species of Toloxis and Cryptopapillaria (Figure 7.2), and an only slightly serrulate or subentire leaf margin. Peristomes have hygrocastic movements, a smooth or papillose exostome outer surface, and very low or almost nonexistent trabeculae on the exostome inner surface. In addition, in SEM micrographs, the exostome in Meteorioideae species bends very strongly into the capsule, which we have never seen in any fresh or herbarium specimens. This might be due to extreme drying during preparation for SEM in combination with the low basal membrane and slender segments of the endostome, very low trabeculae at the inner surface of the exostome and shortness of exostome teeth in relation to the width of the capsule mouth. As discussed above, the position of Cryptopapillaria, Toloxis and Trachypus within the Meteorioideae was not supported by all analyses, but it was somewhat dependent on the method for alignment construction of DNA sequence data as well as phylogenetic analyses. However, in all analyses the placement of these genera either in Meteorioideae or Meteoriopsoideae received very low branch support, and thus we currently follow circumscription suggested by analyses of both molecular and morphological data (Figure 7.2; Huttunen et al., 2004). On a morphological basis there are also grounds for this placement. Both Cryptopapillaria and Toloxis have recently been

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separated from Papillaria, and they share with Papillaria species several gametophytic as well as sporophytic characters. Placement of Trachypus was probably harder to predict prior to phylogenetic analyses partly due to the relatively recent synonymization of the Trachypodaceae with the Meteoriaceae. After comparing the morphological character variation in this genus with that in the rest of Meteorioideae, its position within this subfamily seems well founded. Morphological studies on Chrysocladium, Meteorium and Papillaria reveal some novel character combinations, which seem to be present only in these groups (Huttunen, 2004b; Huttunen et al., 2004; Quandt et al., 2004). All species in these three genera have axillary hairs consisting of one to four short brown basal cells and roundish, hyaline apical cells. Shoots are terete, and due to the leaf insertion on a straight line and the broad segment of stem circumference, the basal part of the leaf is erect or appressed to the shoot. Similarities of the peristome structure in Meteorium and Papillaria were also noted by Noguchi (1976), who regarded them as closely related. Similarly, the affinity of Chrysocladium with these two genera was also already suggested by Fleischer (1907) when he established the genus. Division of the Meteorium and Papillaria species into two major clades also seems to reflect their geographical distribution (Quandt et al., 2004). Meteorium is most diverse in warm temperate and tropical south-east Asia, especially southern China, the eastern Himalayas and Indochina, although some South American (M. deppei) and almost pantropical species (M. nigrescens) also exist. In Papillaria, distribution of species is concentrated in Australia, the southern Pacific and South America. 7.3.4.1.1 Meteorium (Brid.) Dozy & Molk. Our findings for relationships within the Meteorium–Papillaria clade support Buck’s (1994) synonymization of Meteorium and Papillaria Lorentz. In our analyses (Huttunen et al., 2004; Quandt et al., 2004), the type species of Meteorium (Meteorium polytrichum Dozy & Molk.) and Papillaria (Meteorium nigrescens (Hedw.) Dozy & Molk.) are resolved in the same clade with all other species of Meteorium (Figure 7.2). Thus, this species, together with Meteorium deppei (Müll. Hal.) Mitt., should be placed in the genus Meteorium, while the majority of Papillaria still can be retained as a genus of its own (see below). This is also supported by morphology as shown in Quandt et al. (2004). The name Meteorium (Brid.) Dozy & Molk. has been misused almost since the establishment of the genus, but these problems, including conflicting synonymization with Aerobryidium M. Fleisch. ex Broth., are to be resolved (Huttunen et al., in preparation). 7.3.4.1.2 Papillaria (Müll. Hal) Lorentz The majority of the Papillaria species, excluding Meteorium nigrescens, M. deppei, P. intricata and Cryptopapillaria fuscescens, form their own, well-supported clade sister to Meteorium (Figure 7.2). These two groups also have some morphological characters that separate them from each other, and thus the Papillaria clade at this stage is in our minds worth recognizing as a genus separate from Meteorium. For example, especially striking are the densely branching and often biseriate axillary hairs, which are diagnostic for Papillaria species. Due to the position of the type species of Papillaria, either a new name or conservation of the name Papillaria (Müll. Hal) Lorentz with a new type is needed (Quandt et al., 2004). The latter choice would avoid a need for any new combinations as all species, according to current knowledge, belong to Papillaria species in some classifications. Papillaria penicillata (Dozy & Molk.) Broth. has recently been placed in genus Cryptopapillaria (Menzel, 1992; Buck, 1994), but both phylogenetic analyses and morphology place it clearly with Papillaria (see Quandt et al., 2004). Despite some morphological differences between Papillaria nitens (Hook. f. & Wilson) Sainsbury and other species in Papillaria, it also should placed in this genus as Streimann (1991) suggested. 7.3.4.1.3 Chrysocladium M. Fleisch. After Buck (1994) transferred several members of section Chrysosquarridium M. Fleisch. to the new genus Sinskea, Chrysocladium has been a monospecific genus including only Chrysocladium

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retrorsum (Mitt.) M. Fleisch. Based on the molecular data, this treatment seems to be justified (Figure 7.2; Huttunen et al., 2004; Quandt et al., 2004). Chrysocladium appears in the phylogenetic analyses as closely related to Meteorium, but, in most analyses, it remained outside Meteorium and Papillaria. However, analyses based solely on molecular data resolve it within Meteorium (Quandt et al., 2004) or Papillaria (Huttunen et al., 2004) which would allow the transfer of the genus to either of these genera. We, however, see this as unnecessary both in the light of morphological differences between Chrysocladium and these genera as well as due to the fact that analyses including all the available data and the largest number of Meteoriaceae taxa (Figure 7.2; Huttunen et al., 2004) support keeping it as its own monotypic genus. 7.3.4.1.4 Diaphanodon Renauld & Cardot Diaphanodon blandus (Harv.) Renauld & Cardot was earlier placed in Trachypodaceae, and in phylogenies it was resolved as a member of the Meteorium–Papillaria clade (Huttunen et al., 2004). Its position was in all analyses within Meteorioideae, either basal to the Meteorium — Chrysocladium clade (Figure 7.2), Papillaria or a clade including all three genera (Huttunen et al., 2004). Buck (1994) suggested a close relationship with Duthiella, but along with phylogenetic analyses, morphological characters such as terete shoots, straight leaf insertion line and peristome structure support the placement within the Meteorioideae. Very regularly pinnate branching and dense foliation in Diaphanodon makes the genus easily recognizable among the Meteoriaceae. In addition to D. blandus, currently two other species are placed in this genus (Crosby et al., 1999). 7.3.4.1.5 Trachypus Reinw. & Hornsch. Currently only one species of Trachypus has been included in phylogenetic analyses, namely Trachypus bicolor Reinw. & Hornsch., the type of the genus. Its position has remained somewhat unstable, but due to morphological similarities and placement in our most recent phylogenetic study (Figure 7.2; Huttunen et al., 2004), we place the genus in subfamily Meteorioideae. Species in Trachypus share the terete shoots, almost entire leaf margins and several sporophytic characters, such as papillose, slender exostome and a somewhat reduced endostome with taxa in this subfamily. In earlier studies (Buck, 1994; Norris and Koponen,1985; Zanten, 1959), similarities in leaf cell papillosity pattern with Cryptopapillaria and Trachycladiella have often been noted, but the pluripapillose cells over the cell walls have evolved several times among Meteoriaceae as suspected also by Buck (1994). Even within Meteorioideae, taxa with this character, Cryptopapillaria and Trachypus, are not closely related (Figure 7.2). 7.3.4.1.6 Toloxis W. R. Buck Toloxis has been segregated from Papillaria by Buck (1994). Several morphological differences distinguish these two genera, such as leaf cell papillosity (Papillaria s. str.) and several characters in axillary hairs. In the phylogenetic analyses, the position of Toloxis as a separate genus from Papillaria s. str. is well supported. However, the latest analyses including morphological data (Figure 7.2; Huttunen et al., 2004) would also allow its inclusion in Papillaria together with Cryptopapillaria. Due to similar leaf insertion, leaf shape and margins Buck (1998) suggested a close relationship between Toloxis and Trachypodopsis, but this was not supported by phylogenetic analyses. 7.3.4.1.7 Cryptopapillaria M. Menzel Cryptopapillaria as originally circumscribed by Menzel (1992) seems to be polyphyletic, as Papillaria penicillata (Dozy & Molk.) Broth. was resolved within Papillaria. However, the position of the type species of the genus, C. fuscescens, as sister to Toloxis was very well supported in all analyses. These two Cryptopapillaria species differ in several morphological characters, such as the axillary hair structure, the papillosity of leaf cells, and the plication and orientation of leaves (see also Quandt et al., 2004). Toloxis and Cryptopapillaria are very closely related and the morphological similarities between C. fuscescens and Toloxis (Papillaria) semitorta, were also stressed by Menzel (1992). It seems that also C. feae (M. Fleisch.) M. Menzel and C. chrysoclada

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(Müll. Hal.) M. Menzel, which morphologically resemble C. fuscescens more than P. penicillata, are resolved within the same clade with the former species (Huttunen and Quandt, in preparation). Although capsules are exerted as in Toloxis and the gametophytes of P. intricata share more similarities with Toloxis than Cryptopapillaria, its position in the phylogenies rather suggests a position in the latter genus. However, the morphological differences between these two genera are not that distinct. Although Noguchi (1985) regards P. intricata as closely related to Toloxis semitorta, Streimann (1991) discusses the difficulties in distinguishing it from a Cryptopapillaria species, C. helictophylla (Mont.) Broth. 7.3.4.2 Subfamily Meteoriopsoideae subfam. nov. Musci epiphytici vel terrestres, saepe formis incrementi pendentibus. Surculi complanate vel terete foliati. Folia erectopatentia vel effusa, interdum squarrosa, subinde ecostata vel costa robusta fere ad acumen attingenti. Cellulae foliorum elongatae vel rhomboideae cum una papilla in centro cellulae vel cum multis papillis seriatim dispositis super luminem vel parietem cellulae. Papillae raro desunt. Filamenta axillaria hyalina in axillis foliorum, vulgo uniseriata, interdum distincte flexuosa in speciebus aliquis. Cellulae filamentorum axillarium rectangulatae vel elongatae, non rotundatae, cellulae basales brunneae desunt, cellula apicalis foliorum specierum aliquorum longa et gracilis. Sporophyta peristomiis variabile deminutis, exostomia vulgo transverse striolata, segmenta endostomii late vel non perforata, cilia desunt vel fere segmentibus endostomii aequilonga. Typus: Meteoriopsis M. Fleisch. ex Broth., Nat. Pfl. 1(3):825, 1906. Genera included: Aerobryidium M. Fleisch. ex Broth., Aerobryopsis M. Fleisch., Barbella M. Fleisch. ex Broth., Barbellopsis Broth., Duthiella Müll. Hal. ex Broth., Floribundaria M. Fleisch., Meteoriopsis M. Fleisch. ex Broth., Neodicladiella (Nog.) W. R. Buck, Neonoguchia S. H. Lin, Pseudospiridentopsis (Broth.) M. Fleisch., Pseudotrachypus P. de la Verde & Thér., Sinskea W. R. Buck, Trachycladiella (M. Fleisch.) M. Menzel, Trachypodopsis M. Fleisch. For subfamily Meteoriopsoideae, no morphological synapomorphies appeared in the phylogenetic analyses (Huttunen et al., 2004). Unlike the species of the Meteorioideae, most species have at least some cross-striolation at the base of the exostome teeth. Complanate leaf arrangement, at least on branches, is also a character state that occurs in the Meteoriaceae only in the Meteoriopsoideae. It is present in Floribundaria, and in all other species in the clade including, for example, Sinskea and Barbella, but not Trachypodopsis serrulata (Figure 7.2). Leaves are mostly loosely arranged on shoots, never appressed, and in some taxa (e.g., Floribundaria and Pseudotrachypus) they are very widely spreading. Certain axillary hair characters, such as long, slender, multicellular axillary hairs with tendency to be flexuous are only present in Meteoriopsoideae. Brown basal cells of axillary hairs are most often lacking. Clades in the Meteoriopsoideae lend support to the generic divisions suggested by Buck (1994) and Menzel and Schultze-Motel (1994), although due to the limited selection of species from some genera we could not confirm their monophyly. 7.3.4.2.1 Aerobryidium M. Fleisch. ex Broth. Phylogenetic analyses have included only one species of Aerobryidium, the type of the genus Aerobryidium filamentosum (Hook.) M. Fleisch. in Broth. It was always resolved close to Pseudospiridentopsis, Meteoriopsis and Aerobryopsis. The close relationship between Aerobryidium and Aerobryopsis has been discussed previously by several authors (e.g., Buck, 1994; Menzel, 1992; Noguchi, 1976; Norris and Koponen, 1985), but it has never before been connected with the two first mentioned genera. 7.3.4.2.2 Aerobryopsis M. Fleisch. Aerobryopsis is usually expected to be very closely related to Aerobryidium, and, for example, Noguchi (1976) assumed that their separation in two independent genera might not be necessary. Morphological characters that have been used to separate these taxa include complanate foliation,

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totally papillose exostomes and thick-walled cells in Aerobryopsis contrasting the terete shoots, cross-striate basal part of the exostome and elongate, thin-walled leaf cells in Aerobryidium. Of these characters, however, gametophytic ones tend to vary within some species making the generic distinction somewhat obscure. For example, in the type species of Aerobryopsis, Aerobryopsis longissima (Dozy & Molk.) M. Fleisch., both complanate and terete forms occur depending on the type of substrate (see Noguchi, 1976; Streimann, 1991), and cell walls in this species are thin compared to those in most of the other Aerobryopsis species. Currently, only a very limited number of species has been included in phylogenetic analyses. Therefore, the relationship between these genera is somewhat open and more species from these genera should be included in order to resolve it. 7.3.4.2.3 Barbella M. Fleisch. ex Broth. After Buck’s (1994) treatment of Meteoriaceae, this genus has been reduced to two species: B. compressiramea, the type of the genus, and B. turgida Nog. Both were the only species placed by Noguchi (1976) in the former section Barbella of the genus. As this section, as well as most of Noguchi’s Barbella sections, has not been represented in any phylogenetic studies, their relationships still remain untested. 7.3.4.2.4 Barbellopsis Broth. This genus was segregated from Barbella by Buck (1994, as Dicladiella), and includes two species, B. trichophora and B. macroblasta. All phylogenetic analyses placed Barbellopsis trichophora with very high support close to Neodicladiella (Figure 7.2; Huttunen et al., 2004), another segregate of Barbella s. lat. 7.3.4.2.5 Duthiella Müll. Hal. ex Broth. In the phylogenetic analyses, Duthiella was resolved basal to the clade including Aerobryopsis, Aerobryidium, Meteoriopsis and Pseudospiridentopsis. However, this position did not obtain any significant support (Huttunen et al., 2004), and thus the stability of this placement needs to be further tested. Earlier it was suggested that this genus is closely related to Meteorium (Buck, 1994) due to its terete shoots and mainly unipapillose, rhomboid leaf cells. Compared to any other Meteoriaceae species, Duthiella matches the idealized perfect hypnalian peristome structure best. The genus comprises seven species (Crosby et al., 1999), of which two are only poorly known. Although only one species was included in the phylogenetic analyses, high DNA sequence level similarity in the ITS2 region between D. wallichii and two other Duthiella species, D. speciosissima and D. flaccida, suggests that they are closely related and probably form a monophyletic unit (Huttunen and Quandt, in preparation). 7.3.4.2.6 Floribundaria M. Fleisch. Floribundaria M. Fleisch. is most often resolved as a basal member of the Meteoriopsoideae (Figure 7.2; Huttunen et al., 2004). However, the genus was not resolved as a monophyletic entity. Surprisingly, the South American Floribundaria flaccida (Mitt.) Broth. appeared in the phylogenetic analyses as a close relative to Aerobryidium (Quandt et al., 2004). The genus has often been regarded as an unnatural taxon mainly due to the inclusion of species in the section Trachycladiella (Noguchi, 1976; Norris and Koponen 1985; Streimann, 1992). Our analyses supported the separation of Trachycladiella species (= Floribundaria sect. Trachycladiella M. Fleisch.) from Floribundaria (Menzel and Schulze-Motel, 1994), after which at least the southeast Asian species (F. floribunda, F. pseudofloribunda, F. walkeri and F. setchwanica) form a monophyletic clade in the phylogenetic analyses including both morphological and DNA sequence data from the trnL–F and ITS2 region for 90 taxa (Huttunen and Quandt, in preparation). 7.3.4.2.7 Meteoriopsis M. Fleisch. ex Broth. Meteoriopsis has been easy to distinguish from other Meteoriaceae by its spreading, squarrose leaves. Phylogenetic analyses resolve it with very high support in the same clade with Pseudospir-

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identopsis and Aerobryidium. It is likely that the delimitation of the genus should be reconsidered. For example, Manuel (1977) excluded M. ancistrodes, transferring it to Pseudobarbella, due to pluripapillose leaf cells, spreading leaves with long piliferous, flexuous leaf acumen. However, Floribundaria flaccida, which is phylogenetically close to Aerobryidium and Meteoriopsis, shares all these characters. Thus, we do not see it as impossible to place M. ancistrodes in Meteoriopsis. In addition, as discussed already in the case of Meteorium and Floribundaria, the value of leaf cell papillosity does not seem to be a taxonomically important character at the generic level in the Meteoriaceae. 7.3.4.2.8 Neodicladiella (Nog.) W. R. Buck Neodicladiella was earlier recognized as a section within the genus Barbella. In connection with his generic revision of Meteoriaceae, Buck (1994) raised it to genus level, but included only one species, Neodicladiella pendula. Both phylogenetic analyses and morphological similarities, however, support the inclusion of at least one other species, Barbella flagellifera. It differs from N. pendula by having only one to two (or three) papillae in each cell, while otherwise they are very similar; both species have well differentiated alar cell regions consisting of small rectangular cells, filiforme ultimate branches often form the majority of the colonies, and the sporophyte characters are almost identical. Due to the limited selection of Barbella species from other of Noguchi’s (1976) sections in the phylogenetic studies the monophyly of Neodicladiella has not been sufficiently studied. Neodicladiella flagellifera (Cardot) Huttunen & Quandt comb. nov. — Meteorium flagelliferum Cardot, Beih. Bot. Centr. 19: 120, 1905. Type: Kushaku, no.199, Faurie 1903. 7.3.4.2.9 Neonoguchia S. H. Lin This monotypic genus has recently been separated from Aerobryopsis (Lin, 1988). The phylogenetic affinities, however, are still unknown. Noguchi (1976) compares the appearance of Neonoguchia (Aerobryopsis) auriculata with Barbella, Aerobryidium, Papillaria and Meteoriopsis, while Buck (1994) regards it as a close relative of Meteoriopsis and Pseudospiridentopsis. Indeed, these two genera appear in our analyses within the same very stable clade including also Aerobryidium (Figure 7.2; Huttunen et al., 2004; Quandt et al., 2004). The DNA sequence data we have currently been able to obtain from Neonoguchia also suggests the close relationship with Meteoriopsis (Huttunen and Quandt, in preparation). Thus, lacking further evidence, we place this genus in the Meteoriopsioideae where we expect it to group together with Aerobryidium, Meteoriopsis and Pseudospiridentopsis. 7.3.4.2.10 Pseudospiridentopsis (Broth.) M. Fleisch. Monospecific Pseudospiridentopsis was originally established by Brotherus (1909) who placed it as a section of its own in the genus Trachypodopsis. However, Zanten (1959) stressed the differences between this genus and other Trachypodaceae genera, and Buck (1994) suggested that it is closely related to Meteoriopsis and Neonoguchia. The phylogenetic analyses resolved Pseudospiridentopsis with very high support in the same clade as Aerobryidium and Meteoriopsis (Huttunen et al., 2004; Quandt et al., 2004). It shares with Meteoriopsis the strongly squarrose leaves, a character that thus could have evolved in the Meteoriaceae only once in the clade including Meteoriopsis, Aerobryidium and Pseudospiridentopsis. All three genera have the distinctly bent axillary hairs, terete shoots with dense foliage and unipapillose leaf cells. 7.3.4.2.11 Pseudotrachypus P. de la Verde & Thér. Circumscription of Pseudotrachypus was redefined by Buck (1994). He transferred species belonging to Pseudobarbella Nog. and Barbella sections Aerobryella M. Fleisch. and Elongata Nog. to this genus, and currently the naturalness of this group has not been studied using phylogenetic methods. At least the South American P. martinicensis and south-east Asiatic P. wallichii (= Pseudobarbella attenuata), the type of Pseudobarbella, are closely related (Huttunen et al., 2004)

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which indicated that synonymization of these two genera is very likely. Norris and Koponen (1985) suggested a close relationship with Trachypus, whereas Buck (1994) sees it as possibly closely related to Aerobryidium. In the phylogenies its position was dependent on data included in analyses. Manual alignments (Huttunen et al., 2004) placed it sister to Aerobryopsis in the same clade with Aerobryidium, Pseudospiridentopsis and Meteoriopsis, direct optimization analyses of sequence data resolve it with only low support among the basal taxa in Meteoriopsoideae (Huttunen et al., 2004) and with morphological data DO resolves it in the same clade with Sinskea, Trachycladiella, Barbellopsis and Neodicladiella (Figure 7.2). Thus, to confirm the monophyly of this genus as well as its position within Meteoriaceae further analyses are still needed. 7.3.4.2.12 Sinskea W. R. Buck Species in this genus were earlier placed in Chrysocladium sect. Chrysosquarridium M. Fleisch., but phylogenetic analyses revealed that they are not closely related to Chrysocladium. Whereas Chrysocladium retrorsum is a close relative of Meteorium (subfamily Meteorioideae), close relatives of Sinskea are Pseudotrachypus, Trachycladiella and Barbella species (Figure 7.2; Huttunen et al., 2004; Quandt. et al., 2004). This position is very stable in all analyses although support is fairly low. The members of Sinskea differ from Chrysocladium retrorsum by having a short seta and pluripapillose leaf cells, and in the structure of the axillary hairs (Huttunen, 2004a). 7.3.4.2.13 Trachycladiella (M. Fleisch.) M. Menzel Trachycladiella is always a sister to Barbellopsis Broth. or to a clade including Neodicladiella W. R. Buck, and Barbellopsis. None of the analyses suggested close relationships with Floribundaria, which supports its segregation in a genus of its own (Buck, 1994). 7.3.4.2.14 Trachypodopsis M. Fleisch. Zanten (1959) suggested that Trachypodopsis is closely related to the Meteoriaceae based on some shared morphological characters, such as auriculate leaves, unipapillose leaf cells, sporophytic characters and occasionally pendent habit. Within the family, Buck (1994) placed it close to Toloxis. In our analyses its position was affected by inclusion of morphological data (see Huttunen et al., 2004), although support was in all analyses very low or even lacking.

7.4 CONCLUSIONS As a result of recent studies (Buck, 1994; Huttunen et al., 2004; Quandt and Huttunen, 2004; Quandt et al. 2004), the Meteoriaceae is well circumscribed and generic divisions are mostly monophyletic groupings. On the generic level, however, much work is still to be done. As phylogenetic studies have included only a rather small number of species from each genus, monophyly has not been critically tested for them. For some genera, for example the newly circumscribed Pseudotrachypus and Barbella (Buck 1994), the major problem for molecular studies is the large number of species for which recently collected material is not available. The largest genera, such as Meteorium and Papillaria, also are in need of worldwide revisions. Papillaria, for example, includes currently approximately 40 names, the majority of which are poorly known South American taxa (Crosby et al., 1999). Morphological plasticity, combined with scattered field observations due to distributions in tropical and subtropical areas where the bryophyte flora are rather poorly known, makes taxonomical conclusions sometimes difficult on a species level. Intraspecific studies combining the molecular methods and reevaluation of morphological characters might bring interesting insights into the morphological evolution of tropical bryophytes, but for this we would need to overcome the problem of availability of recently collected material from areas such as southeast Asia and South America. Taxonomic and nomenclatural changes: Meteoriopsoideae subfam. nov., Neodicladiella flagellifera (Cardot) Huttunen & Quandt, comb. nov.

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ACKNOWLEDGMENTS This study was supported by the Academy of Finland, Finnish Cultural Foundation, the German Academic Exchange Service (DAAD), and the SYS-RESOURCE program which provided the opportunity to work in the Natural History Museum, London. Greatest thanks go to Dr. Teuvo Ahti for help with nomenclatural details and Heino Vänskä for Latin translation. We wish to thank curators in B, BM, FH, JE, L, M, NICH, NY, PC, PE, S, TUNG and W for providing herbarium material for our study.

REFERENCES Allen, B. and Magill, R. E. (2003) A revision of Pilotrichella (Lembophyllaceae, Musci). Acta Academiae Paedagogicae Agriensis, Sectio Biologiae, 24: 43–83. Brotherus, V. F. (1901–1909) Musci. In Die natürlichen Pflanzenfamilien, Vol. 1(3) (ed. A. Engler and K. Prantl). Verlag von W. Engelmann, Leipzig, pp. 277–1246. Brotherus, V. F. (1925) Musci. In Die natürlichen Pflanzenfamilien, Vol. 11. Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–542. Buck, W. R. (1980) A generic revision of Entodontaceae. Journal of the Hattori Botanical Laboratory, 48: 71–159. Buck, W. R. (1994) A new attempt at understanding the Meteoriaceae. Journal of the Hattori Botanical Laboratory, 75: 51–72. Buck, W. R. (1998) Pleurocarpous mosses of the West Indies. Memoirs of the New York Botanical Garden, 82: 1–400. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL–trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (1999) A Checklist of the Mosses. Missouri Botanical Garden Press, St. Louis. Fleischer, M. (1907) Die Musci der Flora von Buitenzorg, Band 3. E. J. Brill, Leiden, pp. 750–847. Gladstein, D. and Wheeler, W. (2001) POY documentation and command summary; available at ftp://ftp.amnh.org/pub/molecular/poy Hedenäs, L. (1990) Axillary hairs in pleurocarpous mosses — a comparative study. Lindbergia, 15: 166–180. Hedenäs, L. (1995) Higher taxonomic level relationships among diplolepidous pleurocarpous mosses — a cladistic overview. Journal of Bryology, 18: 723–781. Hedenäs, L., (1998) Cladistic studies on pleurocarpous mosses: Research needs, and use of results. In Bryology for the Twenty-First Century (ed. J. W. Bates, N. W. Ashton and J. G. Duckett). Maney Publishing and the British Bryological Society, Leeds, pp. 125–141. Hepperle, D. (2002) Align — Manual sequence alignment editor for PCs. http://wwwuser.gwdg.de/~dhepper/software.html Huttunen, S. (2004a) Bryophyte flora of the Hunan Province, China. 9. Meteoriaceae (Musci) I. Chrysocladium, Duthiella, Meteorium, Pseudospiridentopsis, Sinskea, Toloxis, and Trachypodopsis with identification key for Meteoriaceae in Hunan. In Phylogeny and Evolutionary Relationships on the Moss Families Meteoriaceae and Brachytheciaceae. Publications in Botany from the University of Helsinki, 34 Article II; 1–34. Huttunen, S. (2004b) Phylogeny and evolutionary relationships on the moss families Meteoriaceae and Brachytheciaceae. Publications in Botany from the University of Helsinki, 34 Introduction: 1–33. Huttunen, S., Ignatov, M. S., Müller, K. and Quandt, D. (2004) Phylogeny and evolution of epiphytism in the three moss families Meteoriaceae, Brachytheciaceae and Lembophyllaceae. Monographs in Systematic Botany, 98: 328–261. Ignatov, M. S. (1999) On pseudoparaphyllia in Brachytheciaceae and Meteoriaceae (Musci). Acta Botanica Fennica, 165: 73–84.

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Ignatov, M. S. and Huttunen, S., (2002 [2003]) Brachytheciaceae (Bryophyta) — family of sibling genera. Arctoa, 11: 229–244. Kindberg, N. C. (1897) Species of European and North American Bryinae (Mosses). Part 1. Pleurocarpous. Linköping Lithografiska Aktiebolag, Linköping. Lin, S.-H. (1988) List of mosses of Taiwan. Yushania, 5: 1–39. Manuel, M. G. (1977) Monograph on genus Meteoriopsis (Bryopsida; Meteoriaceae). Bryologist, 80: 584–599. Menzel, M. (1992) The bryophytes of Sabah (North Borneo) with special reference to the BRYOTROP transect of Mount Kinabalu. XVII. Meteoriaceae (Leucodontales, Bryopsida). Willdenowia, 22: 171–196. Menzel, M. and Schultze-Motel, W. (1994) Taxonomische Notizen zur Gattung Trachycladiella (Fleisch.) stat. nov. (Meteoriaceae, Leucodontales). Journal of the Hattori Botanical Laboratory, 75: 73–83. Müller, K. (2004) PRAP — Calculation of Bremer support for large data sets. Molecular Phylogenetics and Evolution, 31: 780–782. Newton, A. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Nixon, K. C. (1999) The parsimony ratchet, a new method for rapid parsimony analyses. Cladistics, 15: 407–414. Noguchi, A. (1976) A taxonomic revision of the family Meteoriaceae of Asia. Journal of the Hattori Botanical Laboratory, 41: 231–357. Noguchi, A. (1985) Isobryalean mosses collected by Dr. Z. Iwatsuki in New Caledonia. Journal of the Hattori Botanical Laboratory, 58: 87–109. Norris, D. H. and Koponen, T. (1985) Bryophyte flora of the Huon Peninsula, Papua New Guinea. VII. Trachypodaceae, Thuidiaceae, and Meteoriaceae (Musci). Acta Botanica Fennica, 131: 1–52. Quandt, D. and Huttunen, S. (2004) Evolution of pendent life-forms in bryophytes. Journal of the Hattori Botanical Laboratory, 95: 207–217. Quandt, D., Huttunen, S., Streimann, H., Frahm, J.-P. and Frey, W. (2004) Molecular phylogenetics of the Meteoriaceae s. str.: Focusing on the genera Meteorium and Papillaria. Molecular Phylogenetics and Evolution, 32: 435–461. Quandt, D., Huttunen, S., Tangney, R. and Stech, M. (2006) A generic revision of Lembophyllaceae based on molecular data. Systematic Botany, in press. Streimann, H. (1991) Taxonomic studies on Australian Meteoriaceae (Musci). II. The genera Aerobryopsis, Barbella, Floribundaria, Meteoriopsis, Meteorium, Weymouthia. Journal of the Hattori Botanical Laboratory, 69: 277–312. Streimann, H. (1992) Moss genus Papillaria (Meteoriaceae) in the Pacific. Journal of the Hattori Botanical Laboratory, 71: 83–111. Spessard-Schueth, L. and Crum, H. (1994) Meteoriaceae. In The Moss Flora of Mexico, Vol. II (ed. A. J. Sharp, H. Crum and P. M. Eckel). Memoirs of the New York Botanical Garden, 69: 718–738. Swofford, D. L. (2002) PAUP*4b10. Phylogenetic Analysis Using Parsimony (*and other methods) Ed. 4. Sinauer Associates, Sunderland. Wheeler, W. (1996) Optimization alignment: The end of multiple sequence alignment in phylogenetics? Cladistics, 12: 1–9. Zanten, B. O. (1959) Trachypodaceae, a critical revision. Blumea, 9: 477–575.

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Amblystegiaceae and 8 The Calliergonaceae Lars Hedenäs and Alain Vanderpoorten CONTENTS Abstract ..........................................................................................................................................163 8.1 Introduction...........................................................................................................................163 8.2 Historical Outline .................................................................................................................164 8.2.1 Family Position and Circumscription ......................................................................164 8.2.2 Family Subdivision...................................................................................................167 8.2.3 Species Concepts ......................................................................................................168 8.3 Recent Results and Current Understanding of the Amblystegiaceae and the Newly Separated Calliergonaceae....................................................................................................169 8.3.1 Family Position and Circumscription ......................................................................169 8.3.2 Family Subdivision...................................................................................................170 8.3.3 Species Concepts ......................................................................................................172 8.4 Future Challenges.................................................................................................................173 References ......................................................................................................................................173

ABSTRACT The Amblystegiaceae were traditionally circumscribed by their mostly single and long leaf costa, cylindrical and curved spore capsule, and their preference for humid to wet environments. Generic subdivisions were based on relatively few “key characters.” Towards the end of the twentieth century studies of more complete morphological data suggested (1) radical reclassifications of species and (2) that some taxa do not belong to the Amblystegiaceae. During recent years, phylogenetic studies based on both molecular and morphological data resolved many relationships at the generic level and provided strong evidence that the family should be split into the Amblystegiaceae s. str., with the taxa related to Amblystegium, Campylium, Drepanocladus and Palustriella, and the Calliergonaceae, with the taxa around Calliergon, Scorpidium and Warnstorfia. Many relationships within the two families and their genera are still uncertain. Within Hygroamblystegium morphological and molecular evolution appear to be uncoupled, suggesting that several currently recognized morphospecies should be synonymized.

8.1 INTRODUCTION The Amblystegiaceae, as traditionally circumscribed, consists of between 120 and 170 species. These are most likely the most important mosses in relatively mineral-rich to calcareous wetlands in temperate to polar environments. They are also abundant in many other humid habitats of the temperate zones, as well as in wetlands at high altitudes in tropical and subtropical areas (cf., Hedenäs, 1999, 2003a). Because of their importance and widespread occurrence in wetland habitats

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in Eurasia and North America, they have been subject to a vast number of treatments in various systematic and ecological contexts. It is therefore next to impossible to provide a complete overview of all taxonomic treatments of the members of this family, and the following should be viewed as a synopsis of how concepts regarding the Amblystegiaceae have changed over time rather than as an exhaustive review of all published treatments of the family and its members. In this ever-changing taxonomic context, morphological analyses in a cladistic framework (e.g., Hedenäs, 1995, 1998a; Hedenäs and Kooijman, 1996) and, later, phylogenetic analyses of DNA sequence data (e.g., Buck et al., 2000; Ignatov et al., Chapter 9 in this volume; Hedenäs et al., 2005; Vanderpoorten, 2004; Vanderpoorten et al., 2001, 2002b, 2003; Vanderpoorten and Jacquemart, 2004) offered the possibility of assessing the validity of previous concepts and to propose, within the limits inherent to the different datasets and methods employed, a new classification system. Some relationships are unsupported and remain an area of controversy in the proposed system. Furthermore, most analyses focused on generic relationships, whereas species-level studies are extremely scarce. We therefore briefly summarize the gaps that eventually need to be filled in the coming years before a complete picture of the taxonomy of the Amblystegiaceae is available.

8.2 HISTORICAL OUTLINE The family Amblystegiaceae was first recognized and described in 1885 by the Swedish bryologist Nils Conrad Kindberg, to accommodate the two genera Amblystegium and Apterygium (Kindberg, 1885; Ochyra, 2003). These two genera were then widely circumscribed and included many species that have since been considered members of the Amblystegiaceae, but also taxa that are nowadays placed in several other pleurocarpous moss families. Kindberg’s Amblystegiaceae was forgotten and the family was redescribed by Roth (1899), this time more thoroughly. According to Roth (1899) and in most treatments of pleurocarpous families that were published later in which the Amblystegiaceae were recognized, the family consists of species growing in humid to wet environments that have a cylindrical and curved spore capsule and usually a single and long leaf costa (e.g., Brotherus, 1925; Buck and Vitt, 1986; Crum and Anderson, 1981; Fleischer, 1915–1922; Kanda, 1975, 1976; Noguchi et al., 1991; Nyholm, 1965; Smith, 1978; Walther, 1983; Vitt, 1984). Buck (1998) noted the variability in costa development in West Indian species and suggested that greatly enlarged perichaetia, a relatively long seta and strongly curved spore capsules are the features characterizing species of this family. Additionally, it has been suggested that the meiotic complements of the studied species from this family differ from those of other Hypnales species (Smith, 1978; Smith and Newton, 1966). The family has often been understood as a natural unit (Crum and Anderson, 1981; Fleischer, 1915–1922; Smith, 1978). Table 8.1 provides an overview of the genera that were placed in the family in some global treatments of the family.

8.2.1 FAMILY POSITION

AND

CIRCUMSCRIPTION

In the very beginning the Amblystegiaceae were placed close to the Hypnaceae (Kindberg, 1885), and it was early noted that some taxa were transitional between this family and the Hypnaceae (Roth, 1899). Nishimura et al. (1984) discussed the positions of such transitional taxa in detail and moved Calliergonella, Campylophyllum halleri (Hedw.) M. Fleisch. and Pseudohygrohypnum, the latter a segregate from the heterogeneous Hygrohypnum (cf. Kanda, 1976), to the Hypnaceae. On the other hand, Calliergon, Campylium, Campyliadelphus, Campylophyllum (excl. C. halleri) and most of Hygrohypnum were retained in the Amblystegiaceae. The Hypnaceae of Nishimura et al. (1984) was differentiated from the Amblystegiaceae by a lack of paraphyllia, although paraphyllia occur in Campylophyllum halleri and some Hypnum species, and a short and double costa, which is found also in Serpoleskea, Campylium, some Drepanocladus species, Pseudocalliergon turgescens (T. Jens.) Loeske and Scorpidium scorpioides (Hedw.) Limpr. Obviously, several genera supposedly belonging to the respective families do not fit into the circumscriptions given by

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TABLE 8.1 Circumscriptions of the Amblystegiaceae by Selected Authors who Treated the Family on a Global Scale Brotherus (1925)

Walther (1983)

Vitt (1984)

Goffinet & Buck (2004)

— Amblystegium — — Calliergon Calliergonella Campyliadelphus Campylium Campylophyllum Conardiaa Cratoneuron Cratoneuropsis — Drepanocladus — Hamatocaulis Hygroamblystegium Hygrohypnum — — Leptodictyum — Loeskypnum — Palustriella — Platyhypnidium Platylomella — Pseudocalliergon Sanionia — — Sciaromiopsis Scorpidium Serpoleskea — Straminergon Vittia Warnstorfia

Acrocladium Amblystegium — — Calliergon Calliergonella Campyliadelphus Campylium Campylophyllum Conardia Cratoneuron Cratoneuropsis Donrichardsia Drepanocladus — Hamatocaulis Hygroamblystegium Hygrohypnum — — Leptodictyum — Loeskypnum Ortholimnobium Palustriella — — Platylomella Platydictya Pseudocalliergon Sanionia Sasaokaea — Sciaromiopsis Scorpidium Serpoleskea — Straminergon Vittia Warnstorfia

Acrocladium Amblystegium — — Calliergon Calliergonella Campyliadelphus Campylium Campylophyllum Conardia Cratoneuron Cratoneuropsis — Drepanocladus — Hamatocaulis Hygroamblystegium Hygrohypnum — — Leptodictyum — Loeskypnum Ortholimnobium Palustriella — Platyhypnidium Platylomella — Pseudocalliergon Sanionia — — Sciaromiopsis Scorpidium Serpoleskea Sinocalliergon Straminergon Vittia Warnstorfia

— Amblystegium Anacamptodon Bryostreimannia — — Campyliadelphus Campylium — Conardia Cratoneuron Cratoneuropsis — Drepanocladus Gradsteinia — Hygroamblystegium Hygrohypnum Hypnobartlettia Koponenia Leptodictyum Limbella — — Palustriella Pictus — — — Pseudocalliergon Sanionia Sasaokaea Sciaromiella Sciaromiopsis Scorpidium Serpoleskea Sinocalliergon — Vittia —

a

Only treated by Brotherus (1909).

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Nishimura et al. (1984). Fleischer (1915–1922) suggested that the Amblystegiaceae evolved from the Thuidiaceae, and the positions of these two families in the treatment by Brotherus (1925) suggest that he agreed with this idea. The Amblystegiaceae and Thuidiaceae were both revised thoroughly for Japan and adjacent areas in the 1970s, but problems with the positions and delimitations of the families were not treated in detail (Kanda, 1975, 1976; Watanabe, 1972). Most modern treatments of the Amblystegiaceae place it together with other families in which the species have predominantly long single costae, thus abandoning the original idea that the Hypnaceae may be closely related (e.g., Buck, 1998; Buck and Vitt, 1986; Crum and Anderson, 1981; Nyholm, 1965; Smith, 1978; Vitt, 1984). In their overview of the classification of pleurocarpous mosses, Buck and Vitt (1986) placed the Amblystegiaceae in the superfamily Brachytheciacanae, which was circumscribed by a strong single costa, well marked alar cells, linear leaf lamina cells and lanceolate leaves. They placed the Hypnaceae and Thuidiaceae in two different superfamilies, the Hypnacanae and Leskeacanae, respectively, suggesting that members of these three families are only distantly related to each other. In a series of papers, Ochyra (1985a, 1987a, 1987b, 1989) recognized several families, the Cratoneuraceae, Donrichardsiaceae, Helodiaceae, Hypnobartlettiaceae and Vittiaceae, within the Amblystegiaceae-Thuidiaceae complex. Ochyra (1986) and Ochyra et al. (1991), attempted to redefine the Amblystegiaceae, but unfortunately excluded taxa with paraphyllia, thereby excluding several Hygroamblystegium species that have foliose paraphyllia of the same kind as in Cratoneuron, the type of the Cratoneuraceae. This redefined Amblystegiaceae would also exclude single species from the monophyletic genera Scorpidium and Pseudocalliergon because S. scorpioides and P. turgescens have short and double costae (Hedenäs, 1989a, 1992a). Ochyra (1985a, 1987a, 1987b, 1989) segregated families mostly based on a few striking characters, more or less of a “key character” kind, such as the number of cell layers in the leaf lamina or leaf margin, whereas, for example, many characters of the sporophyte were not considered. As a last example from the period before modern methodology was employed to evaluate the relationships of the Amblystegiaceae, Hedenäs (1989d) showed that there is no sharp morphological limit between some parts of this family and the Thuidiaceae, as these families were traditionally understood. The first cladistic overview of the entire group of pleurocarpous mosses, based on morphology and anatomy (Hedenäs, 1995), suggested that members of the Amblystegiaceae belong to a clade that additionally includes the Thuidiaceae and the temperate members of the Hypnaceae. Characters supporting this clade and its sister relationship with the Plagiotheciaceae are mainly found in the perichaetial branches and sporophytes. Especially important are the orientation of the inner perichaetial leaves, whether these leaves are plicate or not, and, in taxa with unspecialized sporophytes, capsule shape, whether the capsule is constricted below the mouth when dry or not, the shape of the stomatal pore, the appearance of the exostome border, exostome colour, and spore maturation time. The single, long costa does not seem to be as valuable as earlier thought for the delimitation of the Amblystegiaceae from other temperate pleurocarps. Recognition of the families segregated by Ochyra (1985a, 1987a, 1987b, 1989) could not be supported (Hedenäs, 1995). The Hypnobartlettiaceae were suggested to be polyphyletic, whereas Platylomella lescurii and Vittia pachyloma were suggested to possibly be specialized Amblystegium or Hygroamblystegium species, with adaptations to growth in running water. In a more detailed phylogenetic study by Hedenäs (1998a) of the Thuidiaceae-Amblystegiaceae-temperate Hypnaceae clade, also based on morphology and anatomy, the Thuidiaceae appeared as monophyletic. However, it was impossible to resolve relationships among taxa referred to the Amblystegiaceae and temperate members of the Hypnaceae. Morphological and anatomical data simply do not support two monophyletic groups corresponding to these two families. On the contrary, the distinctions between the two families appear to become less clear when the morphology of the included taxa is studied more thoroughly. For example, Hedenäs (1998a, 1997b) suggested that Campylophyllum, Hygrohypnum montanum (Lindb.) Broth., H. norvegicum (Schimp.) J. J. Amann, Hypnum pallescens (Hedw.) P. Beauv., and H. recurvatum (Lindb. & Arnell) Kindb., or at least some of these taxa, are closely related.

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In the first study in which relationships of the Amblystegiaceae were addressed with the help of molecular data the results were not quite convincing (Buck et al., 2000). It was here suggested that the family should be split in two, the Amblystegiaceae s. str. and the Campyliaceae, based on chloroplast DNA sequences. However, the voucher for the species representing the Amblystegiaceae s. str. belongs to Leskea obscura Hedw. rather than to Hygroamblystegium tenax (Hedw.) Jenn. as was thought (Buck et al., 2000) when the study was done (voucher checked by A. Vanderpoorten), and therefore the foundation for this division of the family no longer exists.

8.2.2 FAMILY SUBDIVISION Neither Fleischer (1915–1922) nor Brotherus (1925) provided subdivisions of the Amblystegiaceae above the genus level. Their generic subdivisions were clearly based on a few, easily observable characters, such as leaf orientation and shape, development of the vegetative leaf costa and leaf border, leaf lamina cell shape, the presence or absence of paraphyllia, and the habitat of the species (cf., Brotherus, 1925). Loeske (1907) studied in detail numerous features of both the gametophyte and sporophyte in the genus Drepanocladus and other members of the Amblystegiaceae. Among other things, he thought that the short double costa in the vegetative leaves was due to a reduction that has occurred repeatedly among the “Hypneen” and that the appearance of the costa has therefore been overrated as evidence for generic relationships among these. Among the species he placed in Limprichtia he found differences concerning the epidermal cells and central strand of the stem, but thought such characters reflected direct adaptations to the habitat rather than being evidence of joint ancestry. In the sporophyte he noted that some species lack a separating annulus, and that some species do not have cross-striolate lower exostome outer surfaces. In summary, Loeske (1907) found that all traditional members of Drepanocladus are unlikely to be closely related to each other and distributed the species of this genus and Scorpidium among the six genera Drepanocladus, Limprichtia, Pseudocalliergon, Sanionia, Scorpidium and Warnstorfia. Although the circumscriptions of those of these genera that are still recognized deviate in details, this was the first important step towards the understanding of the Amblystegiaceae we have today. Among recent authors, the most extensive subdivision was made by Kanda (1975, 1976) in his revision of the Japanese Amblystegiaceae. His generic concepts were mostly traditional, but he distributed the genera among five subfamilies. The Amblystegioideae included members of what are today called Amblystegium, Hygroamblystegium, Serpoleskea, Cratoneuron, Palustriella and Leptodictyum. The Campylioideae included Campylium, Campyliadelphus, Campylophyllum and Drepanocladus polygamus (Schimp.) Hedenäs. The Drepanocladoideae consisted of Drepanocladus, Hamatocaulis, Sanionia, Sasaokaea, Scorpidium and Warnstorfia. The Calliergonoideae included Calliergon, Calliergonella, Loeskypnum, Pleurozium, Straminergon and Warnstorfia sarmentosa (Wahlenb.) Hedenäs. Finally, the Hygrohypnoideae consisted of Hygrohypnum s. lat. The subfamilies were separated mainly by continuously variable quantitative characters, such as leaf orientation, leaf lamina cell length, and plant size, and taxa that we now know are closely related were placed in different subfamilies (cf., the Calliergonoideae and Drepanocladoideae). This subfamilial subdivision has received little support from later studies and has not been followed extensively by later authors. Tuomikoski and Koponen (1979) continued the studies of Loeske (1907), and added numerous observations on characters that had so far been considered of little relevance to our understanding of the relationships within the Calliergon–Scorpidium–Drepanocladus complex. This led them to conclude that traditional taxonomical treatments of this group, as seen in most flora treatments during the twentieth century (cf., Brotherus, 1923; Churchill and Linares, 1995; Crum and Anderson, 1981; Grout, 1931; Noguchi et al., 1991; Nyholm, 1965; Smith, 1978), are unlikely to reflect the phylogenetic relationships of its species. Based on both gametophytic and sporophytic characters they referred the genera Calliergon, Loeskypnum, Straminergon and Warnstorfia (cf., Hedenäs,

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1993b) to the subfamily Calliergonoideae, and Drepanocladus, Hamatocaulis, Pseudocalliergon, Sanionia and Scorpidium to the Drepanocladoideae. Towards the end of the twentieth century and in the very beginning of the twenty-first century, several groups of the Amblystegiaceae were thoroughly studied and the conclusions of Loeske (1907) and Tuomikoski and Koponen (1979) were partly confirmed. However, further studies, partly of characters that had not been considered by these authors, led to partly novel concepts of the genera within the family. Thus, in a series of papers the genera Calliergon, Calliergonella, Campyliadelphus, Campylium, Campylophyllum, Conardia, Cratoneuron (incl. Callialaria), Donrichardsia, Drepanocladus, Gradsteinia, Hamatocaulis, Koponenia, Loeskypnum, Ochyraea, Palustriella, Platylomella, Sanionia, Sciaromiella, Sciaromiopsis, Scorpidium, Straminergon, Tomentypnum, Vittia and Warnstorfia were treated in some detail, and in some cases described as new (Crum and Anderson, 1979; Hedenäs, 1987, 1989a, 1989b, 1989c, 1992b, 1993a, 1993b, 1996, 1997a, 1997b, 1998b, 2003a, 2003b; Hedenäs and Kooijman, 2004; Ochyra, 1985a, 1985b, 1987a, 1987b, 1987c, 1989, 1990; Vána, 1986). Although some concepts presented by these authors are not universally agreed on, or may even have been rejected by later studies, these studies give a good up-to-date morphological and anatomical overview of most of the taxa belonging to the Amblystegiaceae. Most of the suggestions by these authors that are relevant to Western Europe were also followed in the recently published British moss flora (Smith, 2004). Hedenäs and Kooijman (1996) suggested that Palustriella is sister to a monophyletic group that consists of Calliergon, Conardia, Hamatocaulis, Loeskypnum, Scorpidium, Straminergon, Tomentypnum and Warnstorfia. This conclusion was based on the presence of many character states rare or unique among the Amblystegiaceae s. lat. Finally, the morphology-based cladistic study of Hedenäs (1998a) supported two clades, one with Calliergon, Loeskypnum, Straminergon and Warnstorfia, and one with Hamatocaulis and Scorpidium. In some analyses these clades, and Tomentypnum and Conardia, appeared in the same clade, while in other cases they were found in two (or three) clades at different positions. Several relationships between the genera could thus not be resolved in that study (Hedenäs, 1998a). Although the above-mentioned taxa are rather well understood morphologically, this cannot be said for Amblystegium, Anacamptodon, Cratoneuropsis, Hygroamblystegium, Hygrohypnum and Leptodictyum. The latter genera are treated in several modern floras, and Hygrohypnum was relatively recently revised (Jamieson, 1976) and its Iberian Peninsula species were described in detail by Oliván (2005). However, we still need further in-depth studies of the morphology of many members of these genera.

8.2.3 SPECIES CONCEPTS Among temperate zone taxa, species of the Amblystegiaceae are notorious for their great phenotypic variability, no doubt related to their frequent ability to thrive under varying wetness conditions. Many species are able to grow both submerged and emergent, and some are even able to stand complete desiccation for shorter or longer periods. As was shown for Drepanocladus aduncus (Hedw.) Warnst., species of the Amblystegiaceae occurring in both inundated wetland habitats and in habitats that may dry out more or less completely show strong phenotypic plasticity (Hedenäs, 1996). The same species can form small plants with small, short leaves, short leaf laminal cells, and weak costae under relatively dry growth conditions, and large plants with large, long leaves, long laminal cells, and strong costae when growing wet. This kind of variation is widespread in the family and has caused much confusion regarding the circumscriptions of many species. Especially during the nineteenth and early twentieth centuries many authors recognized a vast number of infraspecific taxa for many species (e.g., Mönkemeyer, 1927; Roth, 1905; Warnstorf, 1904–1906). However, the most extreme example is probably Carl G. Sanio (see Sanio, 1885, 1887a, 1887b, 1887c), where entities such as “Hypnum fluitans δ amphibium c) paludosum ††† pennulosum” were commonly recognized (Sanio, 1885). The great phenotypic plasticity also blurred species

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limits to the degree that taxa currently recognized as species were treated as forms alongside other phenotypes that are now understood as environmentally induced variation only. An example of this is the treatment of Warnstorfia pseudostraminea (Müll. Hal.) Tuom. & T. J. Kop. as one of eight forms under W. fluitans (Hedw.) Loeske var. fluitans (Mönkemeyer, 1927). An even more extreme consequence of the problems associated with the plasticity is the recognition of Drepanocladus longifolius (Mitt.) Par. (syn. D. capillifolius (Warnst.) Warnst.) as separate taxa under both D. aduncus and D. sendtneri (Schimp. ex H. Müll.) Warnst. (Mönkemeyer, 1927).

8.3 RECENT RESULTS AND CURRENT UNDERSTANDING OF THE AMBLYSTEGIACEAE AND THE NEWLY SEPARATED CALLIERGONACEAE 8.3.1 FAMILY POSITION

AND

CIRCUMSCRIPTION

The family relationships of taxa that have been referred to the Amblystegiaceae were recently analysed based on chloroplast (trnL–trnF and atpB–rbcL) and nuclear (ITS) molecular data, as well as morphological and anatomical data (Vanderpoorten et al., 2002b). This study was based on 54 taxa that represent most of the genera that were ever included in the Amblystegiaceae, plus representative Hypnalean members for which relationships with the Amblystegiaceae are suggested by their morphology (Hedenäs, 1995, 1998a; Ochyra and Vanderpoorten, 1999). The analysis resolved two major clades, corresponding to the two families Amblystegiaceae s. str. and Calliergonaceae (Figure 8.1, Table 8.2; cf., Vanderpoorten et al. 2002a). On the other hand, the relationships of several taxa that had earlier been referred to the Amblystegiaceae could not be addressed by this study (Figure 8.1), and information from additional molecular regions is needed for their evaluation. Further studies of the Calliergonaceae (Hedenäs et al., 2005) suggest that Hygrohypnum ochraceum (Turner ex Wilson) Loeske does not belong to the Calliergonaceae. A very different opinion regarding familial relationships of the Amblystegiaceae species was recently offered by Ignatov and Ignatova (2004) who suggested that a third family should be recognized for some of the earlier Amblystegiaceae s. lat.. taxa, the Scorpidiaceae, including Hamatocaulis, Hygrohypnella [segregated from Hygrohypnum; with H. duriuscula (De Not.) Ignatov & Ignatova and H. ochracea (Turn. Ex Wils.) Ignatov & Ignatova], Limprichtia, Sanionia, and Scorpidium. The basis for the recognition of this family, as well as for their split of Hygrohypnum, where different species groups were placed in several different families, is the study by Ignatov et al. (see Chapter 9). Possible reasons for the apparently different results are the less complete molecular (trnL-trnF and ITS versus trnL-trnF, atpB–rbcL, and ITS) and morphological (35 versus 68 characters) datasets in the study by Ignatov et al. (Chapter 9) than in that of Vanderpoorten et al. (2002b), or the different species selections. However, probably due to the substantial ambiguity in the alignment of large portions of the ITS region and the high homoplasy level in the trnL region throughout the Hypnales, the analysis of a sample of Hypnalean taxa resulted in poorly supported trees at a number of several key nodes in the analyses of both Vanderpoorten et al. (2002b) and Ignatov et al. (Chapter 9). Hence, topological conflicts between these different hypotheses are not supported by the data. Although some general patterns emerge from all the analyses, such as a strongly resolved Amblystegiaceae s. str., or the clear polyphyly of large genera such as Hygrohypnum s. lat. (cf., Oliván et al., Chapter 10), the phylogeny of the Hypnales currently remains mostly unresolved due to limited molecular and taxonomic sampling. Due to this instability, it seems that any taxonomic treatment for accommodating the polyphyly of many large Hypnalean genera, as well as the family relationships of the numerous earlier Amblystegiaceae taxa that have not yet been resolved (cf., Vanderpoorten et al., 2002b), such as Calliergonella, Campylophyllum, Conardia, most of the Hygrohypnum species, Sanionia, and Tomentypnum, is highly speculative. We therefore feel that additional species and molecular sampling is necessary to converge towards

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Calliergonaceae Amblystegiaceae s.str.

Hypnum pallescens Platydictya jungermannioides Hygrohypnum montanum Hygrohypnum ochraceum Hamatocaulis vernicosus Loeskypnum badium Straminergon stramineum Warnstorfia fluitans Calliergon giganteum Calliergon cordifolium Warnstorfia exannulata Scorpidium revolvens Scorpidium scorpioides Platygryrium repens Anomodon attenuatus Platyhypnidium riparioides Donrichardsia macroneuron Rhytidium rugosum Abietinella abietina Helodium blandowii Thuidium delicatulum Haplocladium virginianum Leskea gracilescens Campylophyllum halleri Hygrohypnum smithii Tomentypnum nitens Tomentypnum falcifolium Anacamptodon splachnoides Serpoleskea confervoides Hygrohypnum luridum Hygroamblystegium tenax Hygroamblystegium fluviatile Hygroamblystegium varium Amblystegium serpens Hypnobartlettia fontana Campyliadelphus chrysophyllus Campylium stellatum Cratoneuropsis relaxa Drepanocladus aduncus Drepanocladus sendtneri Drepanocladus sordidus Leptodictyum riparium Pseudo-calliergon trifarium Pseudo-calliergon turgescens Cratoneuron filicinum Palustriella falcata Caribaeohypnum polypterum Ptilium crista-castrensis Sanionia uncinata Calliergonella cuspidata Calliergonella lindbergii Conardia compacta Outgroup taxa

FIGURE 8.1 Strict consensus tree of five equally parsimonious trees for selected Hypnales members that have either been placed in the Amblystegiaceae or have been thought to be related to members of this family (adapted from Vanderpoorten et al., 2002b). The tree is based on molecular (ITS, atpB-rbcL, trnL-trnF) and morphological data. The families Amblystegiaceae s. str. and Calliergonaceae are indicated by boxes, and species that have sometimes been referred to the Amblystegiaceae s. lat. are indicated by black dots.

a resolved and supported hypothesis for the Hypnales, which is needed to eventually propose a robust and stable classification system for the pleurocarps.

8.3.2 FAMILY SUBDIVISION Detailed studies of the Amblystegiaceae s. str. or parts of the family (Rosborg, 2004; Vanderpoorten et al., 2002b, 2003) revealed two well-supported major clades within the family (Figure 8.2). One of these includes Anacamptodon, the type of Hygrohypnum [H. luridum (Hedw.) Jenn.], and Serpoleskea in a moderately well-supported subclade, and Campyliadelphus, Campylium and Leptodictyum in a well-supported subclade. The other major clade includes one well-supported subclade with species of Cratoneuropsis, Drepanocladus and Pseudocalliergon, a well-supported one with Hygroamblystegium species, possibly sister to Amblystegium (Vanderpoorten et al., 2002b), and a relatively poorly supported subclade with members of Hypnobartlettia and Vittia. Cratoneuron and Palustriella appeared in a moderately well-supported clade sister to the rest of the Amblystegiaceae (Figure 8.2). In another study, based only on a smaller molecular dataset than the studies just mentioned (trnLUAA intron, ITS2), the Amblystegiaceae, including the genus Gradsteinia, received

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TABLE 8.2 Circumscriptions of the Amblystegiaceae and the Calliergonaceae Amblystegiaceae Amblystegium Anacamptodon Campyliadelphus Campylium Cratoneuron Cratoneuropsis Drepanocladus Hygroamblystegium Hygrohypnum (s. str.) Hypnobartlettia Leptodictyum Palustriella Pseudocalliergon Serpoleskea Vittia/Sciaromiella

Calliergonaceae Calliergon Hamatocaulis Loeskypnum Scorpidium Straminergon Warnstorfia

Data from Vanderpoorten et al., 2002a, 2002b, 2003.

OUTGROUP Cratoneuron Palustriella Hygrohypnum luridum Anacamptodon splachnoides Serpoleskea confervoides Campyliadelphus chrysophyllus Campylium stellatum Leptodictyum riparium Pseudocalliergon Cratoneuropsis Drepanocladus Amblystegium serpens Hygroamblystegium Hypnobartlettia fontana Vittia

FIGURE 8.2 Relationships within the Amblystegiaceae s. str., compiled from information in Vanderpoorten et al. (2002b), Vanderpoorten et al. (2003) and Rosborg (2004). The first study was based on maximum parsimony (MP) and yielded eight equally parsimonious trees, the second one a single most likely tree under maximum likelihood, and the last two most parsimonious trees (MP). The branches with Drepanocladus, Hygroamblystegium, Pseudocalliergon and Vittia represent several species. Nodes with dots received a high or relatively high bootstrap support (80% or higher) in at least one of these analyses.

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OUTGROUP Hamatocaulis Scorpidium Calliergon cordifolium Calliergon giganteum Calliergon megalophyllum Calliergon richardsonii Loeskypnum Warnstorfia fluitans Warnstorfia pseudostraminea Straminergon stramineum Warnstorfia sarmentosa Warnstorfia procera Warnstorfia exannulata Warnstorfia trichophylla Warnstorfia tundrae

FIGURE 8.3 Relationships within the Calliergonaceae, based on information in Hedenäs et al. (2005). The tree is the single one resulting from a maximum parsimony analysis of molecular (ITS, atpB-rbcL, trnL-trnF) and morphological data. The branches with Hamatocaulis, Loeskypnum and Scorpidium represent several species. Nodes with dots received a high or relatively high bootstrap support (80% or higher).

good support, whereas relationships within this family were generally poorly resolved (Stech and Frahm, 2001). The results of Hedenäs et al. (2005) suggest that there is good support for two subclades within the Calliergonaceae (Figure 8.3). One of these subclades consists of the members of Hamatocaulis and Scorpidium in the sense of Hedenäs (1989a), and both genera are well supported. The second subclade includes the species of Calliergon, Loeskypnum, Straminergon and Warnstorfia. Among these, well-supported clades are one including Calliergon cordifolium, C. giganteum and C. megalophyllum and one with all species except those in Calliergon, with two of the subclades in the latter, one with the Loeskypnum species, and one with the autoicous Warnstorfia species W. fluitans (Hedw.) Loeske and W. pseudostraminea (Müll. Hal.) Tuom. & T. J. Kop.

8.3.3 SPECIES CONCEPTS Although a few disagreements still exist concerning which species to recognize, most of the Amblystegiaceae and Calliergonaceae species are today well defined morphologically. Species circumscriptions have been recently summarized throughout monographs providing exhaustive taxon descriptions and identification keys (e.g., Hedenäs, 1989a, 1992a, 1993a, 1993b, 1996, 1997a, 1997b, 1998b, 2003a, 2003b; Ochyra, 1985a, 1985b, 1987b, 1989; Ochyra et al., 1991). Few molecular data are, however, currently available to test those species concepts as most of the phylogenetic studies have so far focused on relationships at higher taxonomic levels (genus or beyond). In a preliminary study of two Hygroamblystegium species, patterns in amplified fragment length polymorphism (AFLP) markers showed that the genetic divergence among specimens assigned to H. tenax based on their morphology was higher than the difference with specimens of H. fluviatile (Hedw.) Loeske (Vanderpoorten and Tignon, 2000). Subsequent phylogenetic investigation using ITS sequences at the family level further confirmed that the several accessions of H. tenax included were not monophyletic (Vanderpoorten et al., 2001). In fact, culture experiments revealed that most of the morphological variation in Hygroamblystegium species resulted from plasticity. Within the remaining, genetically fixed morphological variation, characters tended to evolve fast and independently from the phylogeny. Most characters furthermore evolved in a manner correlated with plant size (Vanderpoorten and Jacquemart, 2004). Because morphological evolution was uncoupled from molecular evolution, and because patterns of molecular evolution were consistent with a scenario of clonal evolution within polyploid lineages, it was pragmatically suggested to synomize all the Hygroamblystegium species (Vanderpoorten, 2004). This example illustrates how our taxonomic concepts can be dependent on the variation in morphological features that can

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be plastic, correlated to each other, or do not exhibit the stability and phylogenetic association that would be required for taxon circumscription. This suggests that other species concepts might need a thorough revision in those aquatic or subaquatic taxa. For example, the reliability of a series of highly intercorrelated size features for recognizing four different species within the Drepanocladus aduncus species complex, as proposed by Zarnowiec (2001), has been questioned (Hedenäs and Bisang, 2002; Hill, 2003; Long, 2003; Vanderpoorten, 2003). Although the availability of sequence markers to address such issues at the species level remains low, unexpected levels of sequence polymorphism can actually be found in some clades of the Amblystegiaceae-Calliergonaceae. In particular, Hedenäs and Eldenäs (unpublished data) using molecular markers, such as ITS, trnL-trnF, rpl16, and tRNA-Gly, found high infraspecific variation within a few Calliergonaceae species (e.g., in Hamatocaulis vernicosus and Warnstorfia exannulata). Hence, it can be expected that species-level phylogenies will become increasingly available in the Amblystegiaceae-Calliergonaceae in the next few years, making it possible to test species concepts and determine whether the causes of conflict with morphology are due to inappropriate morphological circumscriptions or to evolutionary processes such as interspecific hybridization.

8.4 FUTURE CHALLENGES Although recent advances in our understanding of relationships among taxa that were earlier referred to the Amblystegiaceae are substantial, several challenging problems still remain. We see the following as the fields where the primary efforts should be made in the near future: 1. As shown by the results of Vanderpoorten et al. (2002b, 2003) and Ignatov et al. (Chapter 9), additional species and molecular sampling is necessary to resolve a well-supported phylogeny of the Hypnales. Only when this goal is achieved can relationships of earlier Amblystegiaceae taxa that were not resolved within the Amblystegiaceae s. str. or Calliergonaceae be addressed in detail (cf., Figure 8.1). 2. Generic circumscriptions need to be addressed for the Calliergon–Loeskypnum-Straminergon-Warnstorfia clade, and for Hygrohypnum. 3. Species relationships within Campylium, Drepanocladus, Hygroamblystegium and Pseudocalliergon need to be evaluated. 4. Molecular variation within and between morphologically defined species is currently a poorly studied field. The few studies of species and species complexes made so far within the Amblystegiaceae and Calliergonaceae indicate that many of our ideas regarding the species’ circumscriptions will have to be revised in the future.

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Churchill, S. P. and Linares C. E. L. (1995) Prodromus Bryologiae Novo-Granatensis. Introduccion a la flora de musgos de Colombia. Bibliotheca “Jose Jeronimo Triana,” 12: 1–924. Crum, H. and Anderson, L. E. (1979) Donrichardsia, a new genus of Amblystegiaceae (Musci). Fieldania, Botany, New Series, 1: 1–8. Crum, H. and Anderson, L. E. (1981) Mosses of Eastern North America. Columbia University Press, New York. Fleischer, M. (1915–1922) Die Musci der Flora von Buitenzorg. Band 4. E. J. Brill, Leiden. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Grout, A. J. (1931) Moss Flora of North America North of Mexico, Vol. III, part 2, 63–114, plates 15–29. Privately published, Newfane, Vermont. Hedenäs, L. (1987) On the taxonomic position of Tomentypnum Loeske. Journal of Bryology, 14: 729–736. Hedenäs, L. (1989a) The genera Scorpidium and Hamatocaulis, gen. nov., in Northern Europe. Lindbergia, 15: 8–36. Hedenäs, L. (1989b) The genus Sanionia (Musci) in Northwestern Europe, a taxonomic revision. Annales Botanici Fennici, 26: 399–419. Hedenäs, L. (1989c) On the taxonomic position of Conardia Robins. Journal of Bryology, 15: 779–783. Hedenäs, L. (1989d) Some neglected character distribution patterns among the pleurocarpous mosses. Bryologist, 92: 157–163. Hedenäs, L. (1992a) The genus Pseudocalliergon in northern Europe. Lindbergia, 16: 80–99. Hedenäs, L. (1992b) Taxonomic and nomenclatural notes on the genera Calliergonella and Breidleria. Lindbergia, 16: 161–168. Hedenäs, L. (1993a) Field and Microscope Keys to the Fennoscandian Species of the Calliergon–Scorpidium–Drepanocladus Complex, Including Some Related or Similar Species. Biodetektor, Märsta. Hedenäs, L. (1993b) A generic revision of the Warnstorfia–Calliergon group. Journal of Bryology, 17: 447–479. Hedenäs, L. (1995) Higher taxonomic level relationships among diplolepidous pleurocarpous mosses — a cladistic overview. Journal of Bryology, 18: 723–781. Hedenäs, L. (1996) On the interdependence of some leaf characters within the Drepanocladus aduncus–polycarpus complex. Journal of Bryology, 19: 311–324. Hedenäs, L. (1997a) The Drepanocladus s. str. species with excurrent costae (Musci: Amblystegiaceae). Nova Hedwigia, 64: 535–547. Hedenäs, L. (1997b) A partial generic revision of Campylium (Musci). Bryologist, 100: 65–88. Hedenäs, L. (1998a) An evaluation of phylogenetic relationships among the Thuidiaceae, the Amblystegiaceae, and the temperate members of the Hypnaceae. Lindbergia, 22: 101–133. Hedenäs, L. (1998b) An overview of the Drepanocladus sendtneri complex. Journal of Bryology, 20: 83–102. Hedenäs, L. (1999) Altitudinal distribution in relation to latitude, with examples among wetland mosses in the Amblystegiaceae. Bryobrothera, 5: 99–115. Hedenäs, L. (2003a) Amblystegiaceae (Musci). Flora Neotropica Monograph, 89: i–iv, 1–107. Hedenäs, L. (2003b) The European species of the Calliergon–Scorpidium–Drepanocladus complex, including some related or similar species. Meylania, 28: 1–116. Hedenäs, L. and Bisang, I. (2002) Drepanocladus sordidus und D. stagnatus, zwei Sippen für die Schweiz angegeben. Meylania, 23: 15–20. Hedenäs, L. and Kooijman, A. (1996) Phylogeny and habitat adaptations within a monophyletic group of wetland moss genera (Amblystegiaceae). Plant Systematics and Evolution, 199: 33–52. Hedenäs, L. and Kooijman, A. (2004) Habitat differentiation within Palustriella. Lindbergia, 29: 40–50. Hedenäs, L., Oliván, G. and Eldenäs, P. (2005) Phylogeny of the Calliergonaceae (Bryophyta) based on molecular and morphological data. Plant Systematics and Evolution, 252: 49–61. Hill, M. O. (2003) Further observations on Drepanocladus aduncus in Britain. Bulletin of the British Bryological Society, 81: 64–65. Ignatov, M. S. and Ignatova, E. A. (2004) Flora mchov srednej tjacti evropejskoj Rossii. Tom 2. Fontinalaceae–Amblystegiaceae. Arctoa, 11, Suppl. 2: 609–944. Jamieson, D. W. (1976) A monograph of the genus Hygrohypnum (Musci). Doctoral thesis. University of British Columbia, Vancouver. Kanda, H. (1975) A revision of the family Amblystegiaceae of Japan. I. Journal of Science of the Hiroshima University, Series B, Div. 2, 15: 201–276.

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Kanda, H. (1976) A revision of the family Amblystegiaceae of Japan. II. Journal of Science of the Hiroshima University, Series B, Div. 2, 16: 47–119. Kindberg, N. C. (1885) Table analytique des Mousses pleurocarpes européennes. Revue Bryologique, 12: 24–31. Loeske, L. (1907) Drepanocladus, eine biologische Mischgattung. Hedwigia, 46: 300–321. Long, D. G. (2003) Further observations on Drepanocladus aduncus in Britain. Bulletin of the British Bryological Society, 81: 64–65. Mönkemeyer, W. (1927) Die Laubmoose Europas. IV. Band, Ergänzungsband. Andreaeales-Bryales. Leipzig. Nishimura, N., Higuchi, M., Seki, T. and Ando, H. (1984) Delimitation and subdivision of the moss family Hypnaceae. Journal of the Hattori Botanical Laboratory, 27: 20–46. Noguchi, A., Iwatsuki, Z. and Yamaguchi, T. (1991) Illustrated Moss Flora of Japan. Part 4. The Hattori Botanical Laboratory, Nichinan. Nyholm, E. (1965) Illustrated Moss Flora of Fennoscandia. II, Musci. Fasc. 5. C. W. K. Gleerup, Lund. Ochyra, R. (1985a) Hypnobartlettia fontana gen. et sp. nov. (Musci: Hypnobartlettiaceae fam. nov.), a unique moss from New Zealand. Lindbergia, 11: 2–8. Ochyra, R. (1985b) Koponenia, a new pleurocarpous moss genus from Bolivia. Journal of Bryology, 13: 479–486. Ochyra, R. (1986) Sciaromiadelphus A. Abr. & I. Abr.: The relationship between extant and fossil moss specimens. Journal of the Hattori Botanical Laboratory, 61: 309–332. Ochyra, R. (1987a) On the taxonomy and family placement of the moss genus Limbella (C. Müll.) Broth. Journal of Bryology, 14: 465–485. Ochyra, R. (1987b) A revision of the moss genus Sciaromium (Mitt.) Mitt. II. The section Limbidium Dusén, with a description of Vittia gen. nov. (Vittiaceae fam. nov.). Journal of the Hattori Botanical Laboratory, 62: 387–415. Ochyra, R. (1987c) A revision of the moss genus Sciaromium (Mitt.) Mitt. III. The section Platyloma Broth. Journal of the Hattori Botanical Laboratory, 63: 107–132. Ochyra, R. (1989) Animadversions on the moss genus Cratoneuron (Sull.) Spruce. Journal of the Hattori Botanical Laboratory, 67: 203–242. Ochyra, R. (1990) Gradsteinia andicola, a remarkable aquatic moss from South America. Tropical Bryology, 3: 19–28. Ochyra, R. (2003) The first recognition of the family Amblystegiaceae. Journal of Bryology, 25: 135–136. Ochyra, R. and Vanderpoorten, A. (1999) Platyhypnidium mutatum, a mysterious new moss from Germany. Journal of Bryology, 21: 183–189. Ochyra, R., Koponen, T. and Norris, D. H. (1991) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XLVI. Amblystegiaceae (Musci). Acta Botanica Fennica, 143: 91–106. Oliván, G. (2005) Revisión taxonómica y fitogeográfica de algunos géneros de Amblystegiaceae s.l. (grupo Calliergon-Drepanocladius-Scorpidium y géneros afines) en la Península Ibérica. Tesis doctoral. Universidad Complutense de Madrid, Madrid. Rosborg, C. (2004) Morphology and molecules modelling relationships within the genus Pseudocalliergon. Degree project thesis. Stockholms universitet, Stockholm. Roth, G. (1899) Uebersicht über die Familie der Hypnaceen. Hedwigia, Beiblatt, 1: 3–8. Roth, G. (1905) Die europäischen Laubmoose. Zweiter Band. Verlag von Wilhelm Engelmann, Leipzig. Sanio, C. (1885) Beschreibung der Harpidien welche vornehmlich von Dr. Arnell während der schwedischen Expedition nach Sibirien im Jahre 1876 gesammelt wurden. Bihang till Kungliga Svenska VetenskapsAkademiens Handlingar, 10(1): 1–60. Sanio, C. (1887a) Bryologische Fragmente. I. Hedwigia, 26: 99–109. Sanio, C. (1887b) Bryologische Fragmente. II. Hedwigia, 26: 129–169. Sanio, C. (1887c) Bryologische Fragmente. III. Hedwigia, 26: 194–214. Smith, A. J. E. (1978) The Moss Flora of Britain and Ireland. Cambridge University Press, Cambridge. Smith, A. J. E. (2004) The Moss Flora of Britain and Ireland, Ed. 2. Cambridge University Press, Cambridge. Smith, A. J. E. and Newton, M. E. (1966) Chromosome studies on some British and Irish mosses. III. Transactions of the British Bryological Society, 5: 463–522. Stech, M. and Frahm, J.-P. (2001) Palustriella pluristratosa spec. nov. (Amblystegiaceae, Bryopsida), a new aquatic moss species with pluristratose lamina from Switzerland. Botanica Helvetica, 111: 139–150. Tuomikoski, R. and Koponen, T. (1979) On the generic taxonomy of Calliergon and Drepanocladus (Musci, Amblystegiaceae). Annales Botanici Fennici, 16: 213–227.

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Vána, J. (1986) Ochyraea tatrensis gen. et spec. nov., a remarkable pleurocarpous moss from Czechoslovakia. Journal of Bryology, 14: 261–267. Vanderpoorten, A. (2003) Review of: Zarnowiec, J. “A taxonomic monograph of the Drepanocladus aduncus group (Bryopsida, Amblystegiaceae).” Taxon, 52: 397–398. Vanderpoorten, A. (2004) A simple taxonomic treatment for a complicated evolutionary story: The genus Hygroamblystegium (Hypnales, Amblystegiaceae). Monographs in Systematic Botany from the Missouri Botanical Garden, 98: 320–327. Vanderpoorten, A. and Jacquemart, A.-L. (2004) Evolutionary mode, tempo, and phylogenetic association of continuous morphological traits in the aquatic moss genus Amblystegium. Journal of Evolutionary Biology, 17: 279–287. Vanderpoorten, A. and Tignon, M. (2000) Amplified fragment length polymorphism between populations of Amblystegium tenax exposed to contrasting water chemistry. Journal of Bryology, 22: 57–62. Vanderpoorten, A., Shaw, A. J. and Goffinet, B. (2001) Testing controversial alignments in Amblystegium and related genera (Amblystegiaceae: Bryopsida). Evidence from rDNA ITS sequences. Systematic Botany, 28: 470–479. Vanderpoorten, A., Hedenäs, L., Cox, C. and Shaw, A. J. (2002a) Circumscription, classification, and taxonomy of Amblystegiaceae (Bryopsida) inferred from nuclear and chloroplast sequence data and morphology. Taxon, 51: 115–122. Vanderpoorten, A., Hedenäs, L., Cox, C. and Shaw, A. J. (2002b) Phylogeny and morphological evolution of the Amblystegiaceae (Bryopsida). Molecular Phylogenetics and Evolution, 23: 1–21. Vanderpoorten, A., Goffinet, B., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2003) A taxonomic reassessment of the Vittiaceae (Hypnales, Bryopsida): Evidence from phylogenetic analyses of combined chloroplast and nuclear sequence data. Plant Systematics and Evolution, 241: 1–12. Vitt, D. H. (1984) Classification of the Bryopsida. In New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). Hattori Botanical Laboratory, Miyazaki, pp. 696–759. Walther, K. (1983) Bryophytina, Laubmoose. In A. Englers Syllabus der Pflanzenfamilien (ed. J. Gerloff and J. Poelt). Gebrüder Borntraeger, Berlin, pp. I–X, 1–108. Warnstorf, C. (1904–1906) Kryptogamenflora der Mark Brandenburg und angrenzender Gebiete. Laubmoose, Zweiter Band. Verlag von Gebrüder Borntraeger, Leipzig. Watanabe, R. (1972) A revision of the family Thuidiaceae in Japan and adjacent areas. Journal of the Hattori Botanical Laboratory, 36: 171–320. Zarnowiec, J. (2001) A Taxonomic Monograph of the Drepanocladus aduncus Group (Bryopsida: Amblystegiaceae). Lódz Technical University, Bielsko-Biala.

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the Relationships of 9 On Mosses of the Order Hypnales, with Special Reference to Taxa Traditionally Classified in the Leskeaceae Michael S. Ignatov, Anastasia A. Gardiner, Vera K. Bobrova, Irina A. Milyutina, Sanna Huttunen, and Alexey V. Troitsky CONTENTS Abstract ..........................................................................................................................................178 9.1 Introduction...........................................................................................................................178 9.2 Materials and Methods .........................................................................................................179 9.2.1 Taxon Sampling........................................................................................................179 9.2.2 Datasets.....................................................................................................................179 9.2.3 Laboratory Techniques .............................................................................................181 9.2.4 Phylogenetic Analysis ..............................................................................................181 9.2.5 Secondary Structure of the trnL Intron ...................................................................182 9.3 Results...................................................................................................................................182 9.3.1 Overall Topologies of Trees .....................................................................................182 9.3.2 Comparison of Tree Topologies from Different Analyses ......................................185 9.3.2.1 MB135 and MB144 ..................................................................................185 9.3.2.2 MB144 and Nona......................................................................................185 9.3.2.3 POY and Nona ..........................................................................................185 9.3.3 Substitutions in the trnL Intron................................................................................187 9.4 Discussion.............................................................................................................................187 9.4.1 General Comments on Analysis...............................................................................187 9.4.2 General Comments on Tree Topologies...................................................................194 9.4.2.1 Basal Grade O1.........................................................................................194 9.4.2.2 Basal Grade O2.........................................................................................196 9.4.2.3 Main Clades M1 and M2..........................................................................196 9.4.3 Leskeaceae s. lat.......................................................................................................197 9.4.3.1 The Lescuraea Clade (L1) ........................................................................198 9.4.3.2 The Lindbergia Clade (L2) .......................................................................198 9.4.3.3 The Pseudoleskeella Clade (L3)...............................................................198 9.4.3.4 The Leskea + Thuidiaceae Clade (LT) .....................................................199 9.4.4 Other Hypnalean Taxa..............................................................................................199 9.4.4.1 The Hylocomiaceae Clade (O4) ...............................................................199 177

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9.4.4.2 The Brachytheciaceae Clade (O5) ............................................................200 9.4.4.3 The Claopodium Clade (O6) ....................................................................200 9.4.4.4 The Neckeraceae Clade (O7)....................................................................200 9.4.4.5 The Taxiphyllum Clade (O8).....................................................................201 9.4.4.6 The Amblystegiaceae Clade (O9).............................................................201 9.4.4.7 The Ochyraea Clade (O10) ......................................................................201 9.4.4.8 The Pylaisiaceae Clade (O11) ..................................................................202 9.4.4.9 The Scorpidiaceae (O12) and Calliergonaceae Clades (O3) ...................202 9.4.5 Comments on Some Species that Change their Positions.......................................203 9.5 Concluding Remarks ............................................................................................................204 Acknowledgments ..........................................................................................................................204 Appendix 9.1..................................................................................................................................205 References ......................................................................................................................................212

ABSTRACT Parsimony and Bayesian analysis of nrITS and trnL-F for 134 species of Hypnales and 2 from Hookeriales found a basal grade within Hypnales, which includes Plagiotheciaceae, Stereophyllaceae, Habrodontaceae, Leucodon and Hypnum cupressiforme + Eurohypnum (and sometimes also Pterigynandrum and Platygyrium), while the rest of Hypnales are segregated in two main clades. Main clade 1 includes representatives of the Brachytheciaceae, Calliergonaceae, Climaciaceae, Hylocomiaceae, Neckeraceae, Pseudoleskeaceae, Theliaceae, and genera Anomodon, Antitrichia, Claopodium, Conardia, Dolichomitriopsis, Echinodium, Glossadelphus, Heterocladium, Leptopterigynandrum, Neodolichomitra, Pilotrichella, Rhytidiopsis, Taxiphyllum, and Thelia. Main clade 2 includes representatives of Amblystegiaceae, Leskeaceae, Pylaisiaceae, Scorpidiaceae, Thuidiaceae, and genera Breidleria, Calliergonella, Campylophyllum, Drepanium, Entodon, Iwatsukiella, Myrinia, Ochyraea, Platygyrium, Ptilium, Rhytidium, Sematophyllum, Tomentypnum. The Leskeaceae as traditionally circumscribed were not monophyletic but found in both main clades. In the main clade 1 are four groups: (1) Pseudoleskeaceae, which forms a well-supported clade; (2) Leptopterigynandrum, with Taxiphyllum and Glossadelphus; (3) Claopodium, with Anomodon rostratus; (4) Pseudoleskeella serpentinensis, with Heterocladium, and Neckeraceae (incl. Leptodon and Forsstroemia). Main clade 2 includes three groups of Leskeaceae: (1) Pseudoleskeella clade; (2) Lindbergia + Mamillariella clade; (3) Leskea, Haplocladium and Pseudoleskeopsis zippelii were found among Thuidiaceae, not forming a monophyletic group.

9.1 INTRODUCTION Traditional circumscription of the Leskeaceae includes mainly plants with reduced peristomes and short laminal cells (Smith, 1978; Crum and Anderson, 1981; Buck and Crum, 1990). The reduced peristome was considered to be a very important feature in the systematics of pleurocarps during most of the twentieth century, until molecular phylogenetic analyses started to discover individual cases where strong peristome reduction appears in epiphytic lineages within groups where the other, nonepiphytic, species have complete perfect or hypnoid (peristomes). Although certain examples of the correlation between peristome reduction and epiphytism were known for groups with peculiar gametophytic morphology, such as Neckera and Homalia in Neckeraceae, or even within one genus such as Pylaisia (Arikawa, 2004), the universality of this phenomenon was underestimated. It was quite unexpected to most bryologists that plants with strongly reduced peristomes could belong to families which in the traditional systematics of the twentieth century were circumscribed as having complete hypnoid peristomes. For example, Struckia was found in Plagiotheciaceae (Pedersen and Hedenäs, 2002); Anacamptodon in Amblystegiaceae (Vanderpoorten et al., 2002b); Clasmatodon, Squamidium and Zelometeorium in Brachytheciaceae (Buck et al., 2000); Helicodontium in

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Brachytheciaceae (Goffinet et al., 2001), and Okamuraea in Brachytheciaceae (Tsubota et al., 2002). The short laminal cells, another important diagnostic character of Leskeaceae, also exhibit a tendency to associate with epiphytic habitats: the epiphytic genera mentioned above all have laminal cells shorter than nonepiphytic representatives of the respective families. Hypnoid peristomes and elongate laminal cells were considered by Buck and Vitt (1986) as diagnostic for Hypnales in comparison with Leucodontales. These two largest orders of pleurocarps were accepted almost universally during the twentieth century, following Brotherus (1925), until Buck and Goffinet (2000) combined them because molecular phylogenetic data demonstrated no way to separate these orders. A huge intermixture of genera referred traditionally to Leucodontales and Hypnales was shown also by Tsubota et al. (2002, 2004). Thus, the situation in Leskeaceae appears to be similar to that in the Leucodontales, in that the important diagnostic characters are essentially the same and dependent on the epiphytic habitats. As with the polyphyly of the Leucodontales, the family Leskeaceae was hypothesized to be badly polyphyletic, and the results of our previous studies (Gardiner et al., 2005) confirmed this: several genera attributed to the Leskeaceae (Anomodon, Claopodium, Dolichomitriopsis, Habrodon, Iwatsukiella, Leptopterigynandrum, Okamuraea and Thelia) were found not to be related to any other taxa of this family (Figure 9.1). The rest of the Leskeaceae were grouped in three clades. One of these, the Lescuraea clade, was found to be not closely related to the two others. These were shown to be sisters, although one of them included taxa of both the Leskeaceae (Leskea, Haplocladium, etc.) and members of the Thuidiaceae. In this chapter, we present further study that we undertook of relatives of the genera traditionally classified in Leskeaceae by adding more potentially related taxa, especially from families not represented in the previous analysis. Another objective of this study was the analysis of some well-supported clades, which were not recognized previously in systematics based only on morphology.

9.2 MATERIALS AND METHODS 9.2.1 TAXON SAMPLING The present study includes 35 species of genera referred to the Leskeaceae by one or more of the following authors: Buck and Crum (1978, 1990), Buck and Goffinet (2000), Crosby et al. (1999), Crum and Anderson (1981) and Noguchi (1972, 1991). Altogether we studied representatives of 20 such genera for which we were able to find recently collected material for sequencing: Anomodon, Claopodium, Dolichomitriopsis, Habrodon, Haplocladium, Iwatsukiella, Leptopterigynandrum, Lescuraea, Leskea, Leskeella, Lindbergia, Mamillariella, Okamuraea, Pseudoleskea, Pseudoleskeella, Pseudoleskeopsis, Pterigynandrum, Ptychodium, Rigodiadelphus and Thelia. Limpricht (1895) also included Heterocladium, Abietinella, Helodium and Thuidium in the Leskeaceae. Representatives of these four genera (nine species) were also included in the present analysis. We also attempted to include in the analysis representatives of most nontropical families of pleurocarps, as our main hypothesis was that the Leskeaceae is an unnatural group, composed by epiphytic lineages of different families. GenBank accession numbers and specimen data are shown in Appendix 9.1 and on the supplemental CD. Species nomenclature in most cases follows Ignatov and Ignatova (2004) or, for taxa not present in that publication, Crosby et al. (1999).

9.2.2 DATASETS The main dataset (dataset 1) included 144 terminals (136 species), representing part of 25S rDNA (20 bp), ITS1 (220–316 bp), parts of 5.8S rDNA (87–96 bp), ITS2 (245–294 bp), part of trnL intron (230–296 bp), 3-exon trnL (51–52 bp), trnL–trnF spacer (41–66 bp), and part of trnF (13–22 bp). For nine species of these 144 terminals ITS1 or ITS1 +ITS2 data were not available. Preliminary

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analyses indicated that this incompleteness somewhat affected the results of some analyses, thus the smaller dataset (dataset 2) with 135 terminals (127 species) for which the more complete data was available was also used. Datasets 1 and 2 were aligned by eye using BioEdit 7.0.1 software (Hall, 1999). The alignments consisted of 1833 positions and were used in NONA and MrBoyes analysis. Results of the new analyses based on datasets 1 and 2 are compared here with our previous work (Gardiner et al., 2005) which resulted in the POY tree (Figure 9.1). The dataset used for the POY analysis (dataset 3) was slightly different in that it included 139 terminals (134 species), 130 of these terminals being the same as in dataset 1. Nine species (see Figure 9.1) were excluded due to lack of considerable parts of the DNA regions studied and/or difficulties in aligning the ITS data. The dataset 3 alignment was obtained from POY from unaligned sequences (Gladstein and Wheeler, 2001) and includes 3232 positions. In addition to molecular data, dataset 3 also includes morphological data for 35 characters; for the morphological data matrix see Gardiner et al. (2005).

9.2.3 LABORATORY TECHNIQUES DNA extraction, polymerase chain reactions (PCR) and sequencing protocols were as described in Gardiner et al. (2005).

9.2.4 PHYLOGENETIC ANALYSIS There are still numerous discussions about the best methods in phylogenetic studies. Our previous studies, however, demonstrate the strong congruence in results of analyses of the same datasets by methods of direct optimization and parsimony (Huttunen and Ignatov, 2004) and by methods of direct optimization, parsimony and maximum likelihood (Gardiner et al., 2005). We believe that this congruence can serve as additional support for the results obtained. For the new phylogenetic analysis two analytical procedures were implemented: (1) parsimony analysis with NONA (Goloboff, 1994) within the Winclada (Nixon, 1999a) shell; (2) Bayesian analysis using MrBayes 3.04b (Huelsenbeck and Ronquist, 2001). For NONA analysis, a multiratchet option with three sequential parsimony ratchet runs was used (Nixon, 1999b). Each replicate included 200 iterations and 20 trees were held in memory during the iterations. During ratcheting 25% of the characters were resampled. Jackknifing with 1000 replications including 10 searches and 20 starting trees in each replication was performed with NONA within the Winclada shell. This analysis will be referred to as “Nona.” In Bayesian analysis GTR+I+G model of nucleotide substitutions with four rate categories was used. Four Metropolis-coupled MCMC chains were run from randomly chosen starting trees for 3000000 generations, trees were saved once every 10 generations, 114000 first trees were ignored. The other options retained default values. Majority-rule consensus trees were constructed and Bayesian posterior probabilities as branch support values were calculated. This analysis will be referred to as MB144 where based on dataset 1, and as MB135 where based on dataset 2. The results of these analyses are compared here with those obtained in our previous work by direct optimization (Wheeler, 1996) as employed in the program POY (Gladstein and Wheeler,

FIGURE 9.1 (See figure, facing page.) The single most parsimonious tree (L = 7646, CI = 51, RI = 73) from POY analysis of dataset 3. Gaps were treated as a fifth nucleotide. Jackknife and Bremer support values are shown above and below branches, respectively. Species not included in MB144 and Nona analyses are marked with +; species changing their positions in MB and Nona analyses are marked with xx; abbreviations (O1, O2, etc.) given for clades and basal grades are discussed in text; abbreviations with an asterisk mean that the clade does not exactly correspond to those found in Nona and MB analyses, although its main content is the same. (Redrawn from Gardiner et al., Taxon, 54, 653, 2005. With permission.)

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2001). Results of POY analysis are especially interesting for comparison because they are produced without the “subjective” stage of manual aligning. The details of POY analysis are described in Gardiner et al. (2005).

9.2.5 SECONDARY STRUCTURE

OF THE

trnL INTRON

Secondary structure of the trnL intron was estimated using two main approaches (1) for the whole intron of Rigodiadelphus robustus we used the Cech et al. (1994) model for intron group I to identify the overall structure of the intron and conservative regions and then manually and computationally paired up the nucleotides; (2) the secondary structures of the variable regions such as P8 and P6 were estimated using the mfold program to minimize free energy (Mathews et al., 1999; Zuker, 2003). Common substitutions/indels in the intron were mapped on the Rigodiadelphus robustus structure (Figure 9.5) based on the alignment for the dataset 1 (see Appendix 9.2 on the supplemental CD). Special attention was paid to substitutions in conservative S, P-Q, and R parts of the intron. Rigodiadelphus robustus was selected for this procedure because its intron, as far as was possible to evaluate by eye from the alignment, has the minimum of peculiar substitutions observed in other species of Leskeaceae involved in the analysis.

9.3 RESULTS The single most parsimonious tree resulting from direct optimization (Wheeler, 1996) as implemented in POY for dataset 3, the trees produced by Bayesian analysis for dataset 2 (135 terminals: MB 135) and dataset 1 (144 terminals: MB 144) and shown in Figures 9.2 and 9.3 respectively, and the Nona tree for dataset 1 is shown in Figure 9.4. Support for clades and notes on the differences in their composition are shown in Table 9.1. The comparison of the results of different analyses is given below. Many shared substitutions were found in the trnL intron (Figure 9.5 and Table 9.2), both in variable loop regions and in conservative regions. They are commented upon under the corresponding groups, along with their descriptions, in the Discussion section. Part of the alignment of dataset 2 is shown in Figure 9.6, demonstrating the numerous shared substitutions in the ITS1 and ITS2 regions, which are also considered in the discussions of the respective groups.

9.3.1 OVERALL TOPOLOGIES

OF

TREES

Trees were rooted on Hookeria (Hookeriales) and with the other representatives of the Hookeriales included in the analyses (Lopidium in Nona and POY analyses, and Distichophyllum in POY analysis) formed a grade basal to the other taxa included, all members of Hypnales according to Goffinet and Buck (2004). All four trees include a basal grade (O1–O2) and two main clades (M1 and M2). The composition of the basal part of the basal grade (O1) and the general composition of the two main clades were found to be stable in MB135, MB144 and Nona analyses. In the distal part of the basal grade (O2) one species from O2 moved to M1 and one from M1 to O2 as a result of the inclusion of additional taxa in the analysis. In the POY tree, which, however, was based on a somewhat different dataset (as discussed below), most of the differences compared with Nona and MB analyses were in the topology of the distal part of the basal grade, O2. FIGURE 9.2 (See figure, facing page.) The Bayesian majority rule consensus tree MB135 from analysis of manual alignment of the dataset 2. Maximum likelihood branch lengths are shown. The arithmetic mean negative log likelihood score –lnL = 18453.29. Posterior probabilities above 0.7 are indicated near internal nodes. Abbreviations are given for clades and basal grades discussed in text.

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Four groups, formed mostly by Leskeaceae taxa (L1, L2, L3, LT) and ten groups of other hypnalean taxa (O3–O12) were consistently supported as monophyletic in MB144, MB135 and Nona analyses (Figures 9.2 to 9.4), although their position and internal relationships varied. Although support for some of them was moderate (74% to 80% in Nona analysis) these clades agreed with the morphology, and thus are considered worth discussion. Basal grades are marked as O1 and O2, as they also represent some interest for the foregoing discussion. As the POY analysis was based on a slightly different dataset, its clades in many cases are not identical in species composition, although these differences are generally rather small. Thus, we apply the same abbreviation for POY topology, marking clades with slightly different species composition as, for example, O3′, O4′ instead of O3, O4.

9.3.2 COMPARISON

OF

TREE TOPOLOGIES

FROM

DIFFERENT ANALYSES

9.3.2.1 MB135 (Figure 9.2) and MB144 (Figure 9.3) The relationships of taxa in MB135 (dataset 2) were unaltered in MB144 (dataset 1), with the following exceptions: • • •

•

•

Platygyrium repens moved from O2 (grouped with Hypnum/Eurohypnum), to a position sister to Sematophyllum homomallium, which is absent in MB135 Pterigynandrum groups with Hypnum/Eurohypnum in MB144, but in MB135 was found sister to the M1 clade Anomodon rugelii was sister to L1 (that was sister to O7 + O8) in MB135, but in MB144 groups with the newly added Pilotrichopsis, together forming a clade sister to O7 + O8, sister to L1 within L1 the topology was also changed: two species, Rigodiadelphus and Lescuraea secunda, that formed a basal grade within L1 in MB135, form a clade nested among other species of L1 in MB144 the inclusion of Rauiella in MB144 resulted in Leskea polycarpa changing position within LT, moving from a position sister to Haplocladium angustifolium to group with Rauiella, while Pseudoleskeopsis zippellii moved from a basal position in LT to become sister to Haplocladium angustifolium.

9.3.2.2 MB144 (Figure 9.3) and Nona (Figure 9.4) Both analyses used dataset 1. Differences in the topologies are summarized in Table 9.3: most of them involve switching from one basal position to a basal position in the neighboring clade. The position of these species in Nona analysis was never supported above 73%. 9.3.2.3 POY (Figure 9.1) and Nona (Figure 9.4) POY analysis was based on a dataset with 9 species excluded from the subsequent analyses; thus some differences were expected. Nevertheless, the main topology of the tree (O1, O2, M1, M2) was the same, although O2 was expanded by a clade (sister to M1 + M2), that included Callicladium

FIGURE 9.3 (See figure, facing page.) The Bayesian majority rule consensus tree MB144 from analysis of manual alignment of the dataset 1. Maximum likelihood branch lengths are shown. The arithmetic mean negative log likelihood score –lnL = 19178.13. Posterior probabilities are indicated near internal nodes. Species not included in MB135 analysis are marked with +; species with changed positions in comparison with MB135 are marked with #; abbreviations are given for clades and basal grades discussed in text.

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and also Leptopterigynandrum (found in M1 in Nona) and Calliergonella and Stereodon plumaeforme (found in M2 in Nona); jackknife support for this clade was 95%. Most of clades L1, L2, L3, O3, O6, O7, O9, O11 in POY had exactly the same composition in Nona or the same plus the additional taxa of dataset 3 that were absent in dataset 1 (e.g., one more species of Warnstorfia, one more species of Neckera, etc.). Clades O5, O8, O10 were either too incompletely represented, or overlapped with species whose position was found variable in Nona. The most peculiar composition was found for O4, O12 and LT. Species in these clades found by Nona were all found within the corresponding groups in POY, but in addition the terminal positions in groups O4′, O12′ and LT′ in POY included species that are totally unrelated, as far as we can judge from other molecular phylogenetic analyses, both our own and those by other authors, and also from morphology. In POY the group O4′ (Hylocomiaceae + Antitrichiaceae) included Pilotrichella and Thelia forming a well-supported clade with Antitrichia; O12′ (Scorpidiaceae) included Ctenidium, Hypnum and Eurohypnum; and LT′ (Leskeaceae s. str. + Thuidiaceae) included Pterigynandrum (forming a rather well-supported clade with Haplocladium angustifolium).

9.3.3 SUBSTITUTIONS

IN THE

trnL INTRON

Many shared substitutions were found in the trnL intron (Figure 9.5 and Table 9.2); however, some of them belong to variable loop regions, while some belong to the following conservative regions: • • •

• •

Region Q has no substitutions. Region P (position 38) has a shared substitution (A versus G) in Fabronia, Stereophyllum and Platygyrium. Region R (position 137) has a shared substitution (G versus A) in 19 species. These included five of nine members of the LT clade (both species of Leskea, both species of Haplocladium, and Pseudoleskeopsis zippelii); four of seven members of the Lescuraea clade (L1); three of six species of Lescuraea (L. mutabilis, L. saxicola, L. plicata), and Rigodiadelphus. Six additional species with this substitution (Breidleria pratensis (O12), Neodolichomitra yannanensis (O4), Forsstroemia trichomitria (O7), Ochyraea montana (O10), Stereodon vaucheri and S. plicatulus (O11)) were not related to the above groups or to each other (except the two Stereodon species). Region S (position 285) has a shared substitution (G versus A) in two species, Stereodon plicatulus (O11) and Glossadelphus ogatae (O8). Region S (position 289) has a shared substitution (G versus T) in four species, three members of the O7 clade (Heterocladium dimorphum, H. procurrens and Pseudoleskeella serpentinensis) and Leptodictyum riparium (O9).

9.4 DISCUSSION 9.4.1 GENERAL COMMENTS

ON

ANALYSIS

Results from different analyses have some peculiarities, which, however, can probably be used in a complementary way. For example, MB135, which used dataset 2 with species with both ITS1 and ITS2, provides better support for main clades M1 and M2 compared to MB144 where nine species without ITS1 data were included (Table 9.1). Nona analysis showed poorer resolution

FIGURE 9.4 (See figure, facing page.) Strict consensus (L = 3233, CI = 41, RI = 62) of 120 most parsimonious trees (L = 3218) resulting from Nona analyses of manual alignment of the dataset 1. Gaps were treated as missing data. Jackknife support values are shown above branches. Species that differ in position in comparison with the MB144 analysis are marked with @; abbreviations are given for clades and basal grades discussed in text.

Main clade 1, incl. Calliergonaceae

Main clade 1 excl. Calliergonaceae Main clade 2 incl. Scorpidiaceae (incl. Hamatocaulis and Iwatsukiella) Main clade 2 excl. Scorpidiaceae (incl. Hamatocaulis and Iwatsukiella)

Calliergonaceae Hylocomiaceae + Climaciaceae + Antitrichia + Neodolichomitra Hylocomiaceae (Hylocomium + Rhytidiadelphus) Climaciaceae (Climacium + Pleuroziopsis) Antitrichia + Neodolichomitra

Brachytheciaceae + Dolichomitriopsis Anomodon rostratus + Claopodium Neckeraceae + Heterocladiaceae + Echinodiaceae + Pseudoleskeella serpentinensis + Anomodon longifolius Neckera + Forsstroemia + Leptodon + Heterocladium heteropterum + H. macounii Neckera + Forsstroemia + Leptodon

M1

m1 M2

O3 O4+

O5 O6 O7++

O7–

O7+

O4b O4c

Basal Grade 100/3 100/2

100/5

99/7

97/5

100/2 97/2

100/2

Main Clade 1 100/4 100/6

100/3 98/5 100/12

100/3

MB144

55/73 (without Lopidium, but with Platygyrium-clade)

100/3 97/4 100/10

100/2 97/2

100/2

100/4 100/6

97/67

Main Clades 72/45 (incl. 47/46 Pterigynandrum) 98/40 100/42 56/75 47/83

100/3 100/2

MB135

97/5

87/7

97/3 77/4 83/12

98/2 86/2

97/2

POY

100/4 (only Neckera)

90/6

Not studied *83/4 (with Thelia and Pilotrichella nested) *Polyphyletic 98/4 66/9 (Echinodium and Anomodon longifolius Not studied)

99/5 *67/7 (with Thelia and Pilotrichella nested) 86/3

<50

<50/73

99/4 82/6

<50 100/90

<50

Not studied 96/2

<50/42 <50/83

<50/46

97/3 100/2

Nona

188

O4a

m2

Stereophyllum + Entodontopsis + Fabronia Hypnum + Eurohypnum

Groups of Taxa

O1– O2–

No.

TABLE 9.1 Posterior Probabilities (MB135 and MB144) and Jackknife Supports (Nona, POY) for Some Clades

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Leskea + Thuidiaceae + Lindbergia clade Leskea + Thuidiaceae Lindbergia clade Amblystegiaceae s. str. (incl. Hypnum bambergeri) Ochyraea clade (incl. Myrinia) Ochyraea clade (excl. Myrinia)

Pseudoleskeella clade (incl. Rhytidium) Pseudoleskeella clade (excl. Rhytidium) Pylaisiaceae (excl. Calliergonella and Stereodon pallescens) Scorpidiaceae (incl. Hamatocaulis)

Scorpidiaceae (excl. Hamatocaulis)

L2+LT

L3+ L3– O11

O12+

O12– 96/6

59/7

99/6

73/7

100/6 100/4 59/8

62/14 97/12

71/14 94/12

100/6 100/4 <60/7

100/10 100/4 100/21

Main Clade 2 88/14

88/13 100/9 99/4 100/21

100/7

81/4

100/7

84/4

77/6

74/7

89/6 94/4 76/8

89/14 80/12

92/10 83/4 99/21

Unresolved/14

99/7

87/4

*Polyphyletic *89/7 (but Ochyraea tatrensis and Drepanium recurvatum not within the group) *Polyphyletic 99/4 *99/7 (Stereodon plumaeforme outside M2, in O2) *67/11 (incl. Breidleria, Hypnum cupressiforme, Eurohypnum and Ctenidium) <50/6

*80/12 (Pterigynandrum nested) 96/4 99/20

Polyphyletic

100/7

Not studied

Note: Clades are marked as L1, L2, etc. for Leskeaceae in the traditional circumscription, O1, O2, etc. for other Hypnalean taxa; M1, M2, etc. for main clades; + and – are used for larger and smaller size of some clades (usually including or excluding basal taxa). Support and size of clades is shown as probabilities or jackknife above/number of terminals in clade below. As the POY analysis was based on a slightly different dataset, its clades in many cases are not identical; however, as these differences are rather small, we also provide the POY data here, marking nonidentical clades with an asterisk.

O10+ O10–

LT L2 O9

L1

Leptopterigynandrum + Taxiphyllum + Glossadelphus Pseudoleskeaceae

O8

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FIGURE 9.5 Secondary structure of trnL intron of Rigodiadelphus robustus. Splice sites are identified with bold arrows. Variable positions are circled, and those bearing group-specific changes (see Table 9.2) are numbered. Points of insertions are identified with thin arrows. Secondary structures of hairpins P6 for Amblystegium serpens and Cratoneuron filicinum with loops of different lengths are shown below.

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TABLE 9.2 Clade-Specific Substitutions in the trnL Intron Position in Alignment

Most Species

18 24

T A

32 38 54 63 70 89

C G A A A C

95 96 98–101 102 102–105 107

T C

A

110

A

111

A

112

A

115

A

117–119 120

A

137

A

156 159 161

G T A

162 165 219

T T A

230 231

A T

Shared Substitutions C: 6: 2/2 Campylophyllum + 4/6 Ochyraea G: 2: 2/2 Brachytheciaceae (Okamuraea and Homalothecium) T: 6: {2/2 Myrinia + 2/6 Ochyraea} + {2/2 Calliergonella} A: 3: Fabronia, Stereophyllum + Platygyrium G: 3: 2/2 Cratoneuron + Palustriella G: 9: 9/10 (Leskea + Thuidiaceae clade) G: 6: {2/4 Heterocladium + Echinodium} + 3/6 Lescuraea A: 2: 2/2 Brachytheciaceae; T: 8/8 Stereodon–clade s. str. + Stereodon pallescens + 2/2 Calliergonella C: 2: 2/2 Sterophyllaceae T: 8: 6/16 from basal grade + Platygyrium and Sematophyllum 20/21 Amblystegiaceae (incl. Hypnum bambergeri) insertion TTTT 18/21 Amblystegiaceae (incl. Hypnum bambergeri) insertion G 2/2 Cratoneuron insertion TTTT G: 31: {29/42 of main clade I (without Claopodium clade and Hylocomiaceae)} + {Hypnum cupressiforme and Eurohypnum} C: 4: 4/5 Lindbergia clade G: 5: 2/6 Hylocomiaceae clade {Hylocomium + Antitrichia} + 2/7 Scorpidiaceae {Scorpidium + Hamatocaulis} + Breidleria G: basal grade – 3/19; main clade M1 – 9/42 main clade M2 – 52/82 (not including 4/4 Pseudoleskeella, 4/4 Calliergonaceae, 2/2 Calliergonella, 2/2 Entodon, etc.) G: basal grade – 1/19; main clade M1 – 1/42 main clade M2 – 44/82 (including 19/21 Amblystegiaceae, but none from Pseudoleskeella, Calliergonaceae, etc.) G: 17: {5/5 Neckeraceae + Heterocladium macounii, H. heteropterum} + {6/8 Stereodon clade) + {Neodolichomitra + Antitrichia) + {2/2 Isopterygiopsis} Insertion TAA, TAG, or TGA in 6/6 Taxiphyllum clade (Leptopterigynandrum, Glossadelphus, Taxiphyllum, Caribaeohypnum) and Thelia G: 13: {Hookeriaceae + Stereophyllaceae + Fabroniaceae} + {5/5 Neckeraceae + Heterocladium macounii, H. heteropterum} G: 9: {2/2 Leskea + 2/2 Haplocladium + Pseudoleskeopsis zippelii} + {3/6 Lescuraea (mutabilis, saxicola, plicata) + Rigodiadelphus} C: 5: 5/6 Ochyraea G: 5: 5/5 Neckeraceae s.l.(Neckera, Leptodon, Forsstroemia) G: 7: 7/7 Pseudoleskeaceae (i.e., Lescuraea+Rigodiadelphus) C: 2: 2/2 Tomentypnum C: 6: 2/2 Stereophyllaceae + 4/4 Calliergonaceae C: 7: 5/6 Ochyraea + 2/2 Campylophyllum G: 2: Hypnum cuperssiforme + Eurohypnum T: 9: {Platygyrium + Sematophyllum} + {5/6 Ochyraea + 2/2 Campylophyllum} G: 3: Fabronia+ 2/2 Stereophyllaceae G: 21: 21/21 Amblystegiaceae

Exceptions C: 1 G: 1 T: 2

G: 4 G: 1; A: 3; T: 12 C: 1 T: 1

C: 1

G: 1

C: 1; G: 11

G: 4 G: 6 A: 1; C: 2 T: 1; C: 1 C: 1 C: 2 T: 1

1: C; 1: T G: 1 Continued.

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TABLE 9.2 (Continued) Clade-Specific Substitutions in the trnL Intron Position in Alignment

Most Species

251

G

252 255 256–272 278 289 308 313 339

Shared Substitutions

Exceptions

A: 6: 6/21 Amblystegiaceae (6/8 from subclade with Anacamptodon); A: 4; T: 5 T: 3: 2/2 Claopodium whippleanum + Anomodon rostratus A G: 6: 5/5 Hygroamblystegium + Amblystegium G: 1 T C: 2: Lescuraea saxicola + L. mutabilis similar insertion in 4/4 Pseudoleskeella, in 2/2 Thuidium, Abietinella, Rauiella + 5 other speces G A: 2: 2/2 Hylocomiaceae (Hylocomium + Rhytidiadelphus) T G: 3: 2/4 Heterocladium + Pseudoleskeella serpentinensis G: 1 T C: 2: 2/2 Calliergonella C: 1 C A: 10/10 Thuidiaceae + Leskea clade A: 2; T: 3 T: 4/4 Calliergonaceae + {Platygyrium + Sematophyllum + Leucodon} A G: 25: {20/21 Amblystegiaceae} + {5/6 Lescuraea} G: 1

Note: Numbering of intron positions (1–342) is according to the alignment of the intron from 143 species (see Appendix 9.2 on the CD). Ochyraea mollis is omitted since sequence data on trnL is absent for that species. All variable positions are circled in Figure 9.5. In the column “Shared Substitutions” the total number of species and the groups having this substitution are given, shown as number of representatives of groups with substitution above slash/total number of terminals in corresponding group below slash. The column “Exceptions” provides the number of species with the corresponding mutation found in phylogenetically distantly related groups (according to the trees constructed). Occasional point mutations in the phylogenetically distantly related groups (according to the trees constructed) are not listed.

TABLE 9.3 A Comparison of Clades in Nona and MB144 Analyses Nona Lopidium Topology of m1 Topology of m2 Conardia Rhytidiopsis and Thelia

Pilotrichella + Anomodon rugelii clade Breidleria Calliergonella cuspidata + C. lindbergii clade Ptilium

Sister to all Hypnalean taxa (O1+O2+M1+M2) (07+08)+O4+(L1+(O5+O6)) O10+(O9, O10, O11, L2, L3, LT) Sister to L1, that is sister to (O5+O6) Form clade sister to O7 and this broader clade is sister to O8+ (Pilotrichella + Anomodon rugelii) Sister to O8

MB144 Within M2, sister to m2

Sister to (O9 + Calliergonella clade) Sister to O9

(L1+(O7+O8))+O4+(O5+O6) (L2+LT)+((O9+O10)+(O11+L3)) Sister to O4+(O5+O6) Form basal grade in a clade terminated by O8 clade; and this broader clade is sister to O7 Sister to O7+ (O8+Thelia and Rhytidiopsis) Sister to O12 Sister to O11

Sister to O11

Sister to O9+O10

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within the M2 clade when compared with the MB144 analysis (both based on dataset 1), but corrected the obvious artifact of MB144 analysis, the placement of Lopidium (Hookeriales) among Hypnalean taxa. Nona analysis found very low support for main clades M1 and M2, and for other clades the support was generally lower than in MB. However most of the clades found in Nona analysis, even those with moderate support of 73% to 80%, are relatively stable and worth discussion. These clades with moderate support agree, as a rule, with the species morphology and molecular trees obtained by other methods and by other authors (using other genes and sometimes different, though related, species). The changes in position between MB144 and Nona were relatively few and represent mostly displacements from one basal position to a position basal (or at most two nodes) within the neighboring clade, and not affecting the composition of those clades with jackknife support greater than 74% in the Nona tree, which are the main subject of discussion in this chapter. The changes in position between MB135 and MB144 analyses can at least partly be explained by the addition of species. For example, Platygyrium was found in the basal grade in the MB135 analysis probably because the dataset lacks any close relative of this genus, which has a relatively peculiar ITS1 sequence (cf. Figure 9.6). However, when Sematophyllum was included in MB144, Platygyrium formed a clade with it, displacing to M2. The relationship of Sematophyllum and Pylaisiadelphaceae (where Platygyrium belongs, according to Goffinet and Buck, 2004) was also found by Tsubota et al. (2004). Although there are many shared clades in POY (Figure 9.1) and the other analyses (Figures 9.2 to 9.4), the support of Pterigynandrum in a terminal position in the LT clade, and the position of Hypnum cupressiforme, Eurohypnum and Ctenidium molluscum in a terminal position in the Scorpidiaceae clades (O12) are surprising results. Such results were not found in other analyses either by ourselves or by any other authors, and they are most likely due to the fairly complex phylogenetic structure of our data. Due to high length variation in the ITS region and insufficient sampling of taxa in certain clades, the simultaneous search for the most parsimonious tree and synapomorphies in sequence data might have been almost too hard a task with our limited computational capacity. This could have led to the somewhat spurious placements especially in the case of taxa which, on a sequence level, have the highest number of differing positions. The inclusion in the POY analysis of morphological data could have contributed to this. It is, however, unlikely that this is the case, as the taxa under question are quite different morphologically and Nona analysis of morphological dataset alone (not shown) never found them to be related. Inconsistency in the terminal portions of some particular clades in moderately big analyses, like this one, is not a rare event, and may represent a sampling artifact. For example, the Brachytheciaceae are represented in this analysis by two genera, Homalothecium and Okamuraea, which belong to distinct subfamilies (Ignatov and Huttunen, 2002). Lembophyllaceae, one of the closest families to the Brachytheciaceae + Meteoriaceae (cf. Huttunen et al., 2004) is represented by a single genus, Dolichomitriopsis. Nona and MB analyses presented here resolved these three genera as a monophyletic group, but Okamuraea always formed a clade with Dolichomitriopsis, while Homalothecium was found sister to these two genera. However, a series of analyses with 98 species of Brachytheciaceae and several species of Lembophyllaceae invariably resolve Dolichomitriopsis well outside Brachytheciaceae with reasonable support (Huttunen and Ignatov, 2004). Our tests of dataset 1 with three additional Brachytheciaceae and two additional Lembophyllaceae (not shown) also resolved these two families as monophyletic. These observations once more underline the importance of uniform selection of taxa. The small number of Thuidiaceae included in this analysis, for example, does not allow further discussion of the topology of the LT clade, namely the possible separation of Leskea + Haplocladium from the rest of Thuidiaceae found in the NJ analysis of Gardiner et al. (2005). It is worth noting that species whose positions change in different analyses (see Figures 9.1, 9.3 and 9.4 and Tables 9.1 and 9.2) also had no well-supported close relationships in analyses by

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FIGURE 9.6 Two parts of the alignment from ITS1 and ITS2 regions, showing shared substitutions and indels of some groups (shaded). Taxa are arranged in the order of the MB135 tree. Seven species (Eurohypnum leptothallum, Entodon beyrichii, Rhytidium rugosum, Warnstorfia fluitans, Ochyraea alpestris, O. tatrensis, Hygrohypnella duriuscula) are not included due to lack of considerable parts of data in this part of the alignment. Continued.

other authors (for example, Vanderpoorten et al., 2002b; Goffinet et al., 2001; Tsubota et al., 2004.). This especially concerns such genera as Anomodon, Breidleria, Calliergonella, Conardia, Ctenidium, Fontinalis, Hypnum cupressiforme, Pilotrichella, Pterigynandrum and Ptilium. In the following discussion we will not include species and groups with unstable positions.

9.4.2 GENERAL COMMENTS

ON

TREE TOPOLOGIES

9.4.2.1 Basal Grade O1 The basal part of the basal grade, O1, is composed of species of Plagiotheciaceae s. lat., as defined by Hedenäs (1999) (Orthothecium, Platydictya, Herzogiella, Plagiothecium and Isopterygiopsis), Stereophyllaceae (Stereophyllum and Entodontopsis), Fabroniaceae (Fabronia) and Habrodontaceae (Habrodon). The grouping or order of these taxa is somewhat different in the different analyses, but in all of them the composition of this basal grade remains stable. All the members of O1, including Hookeria and Lopidium, and also Leucodon, possess a specific insertion in ITS2 region (Figure 9.6). In both Bayesian and Nona analyses the Stereophyllaceae

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FIGURE 9.6 Continued.

(represented by two species of two genera, Stereophyllum and Entodontopsis) plus Fabronia formed a well-supported clade. The close relationship of Stereophyllaceae and Fabronia is also supported by characteristic substitutions in the trnL intron (positions 38, 120, 230, the first being in the conservative P-region). The position of the Plagiotheciaceae, Fabroniaceae and Habrodontaceae in the basal part of the Hypnales tree was found in our previous publications (Budyakova et al., 2003; Gardiner et al., 2005). Similarly, Tsubota et al. (2004) found in the rbcL gene analysis that Stereophyllaceae (a family considered by some authors, e.g., Fleischer (1923), as a subfamily of Plagiotheciaceae), is one of the most basal in the Hypnales s. lat., while the Plagiotheciaceae is also placed in the basal part of the grade. Budyakova et al. (2003) showed that the species of the basal grade of Hypnales, O1, as well as Hookeria and Lopidium, are characterized by the lack of pseudoparaphyllia, if a somewhat narrowed concept of pseudoparaphyllia is applied, considering only structures remaining on the stem after elongation of branch primordia. Also, most groups in this grade lack regular pinnate branching (with the exception of Herzogiella), often have no rhizoids below the leaf insertion, often produce uniseriate two- to five-celled green propagulae on stems or leaves, and also have rather pale exostome teeth (in taxa with mostly complete double-alternate peristomes). Fabronia shares with Plagiothecium at least one rare morphological character: in both genera rhizoids arise from the adaxial side of the costa (Budyakova et al., 2003). This is also known in the Stereophyllaceae, where rhizoids are formed below the leaf insertion (Ireland and Buck, 1994).

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9.4.2.2 Basal Grade O2 The distal part of the basal grade, O2, invariably includes Leucodon sciuroides and a wellsupported clade formed by Hypnum cupressiforme and Eurohypnum lepthothallum in MB135, MB144 and Nona trees. Analysis of the somewhat reduced dataset in MB135 resulted in displacement of Platygyrium to O2, whereas in MB144 this genus was found in a clade with Sematophyllum, which agreed with the present understanding of its relationships, as discussed above. Analysis of the more complete dataset 1 in MB144 and Nona analysis found Pterigynandrum filiforme in O2. The family Pterigynandraceae was extended by Buck and Crum (1990) to include Habrodon, Heterocladium and Iwatsukiella. However, our current analysis found the two latter genera in a quite distinct position within M1. Habrodon was found in a basal grade not far from Pterigynandrum, but these genera never formed a clade. Due to numerous morphological differences, the two genera are probably better kept in their own monogeneric families, as suggested by Budyakova et al. (2003). 9.4.2.3 Main Clades M1 and M2 Distal to the basal grade (O1 + O2), two main clades (M1 and M2) were found in both Bayesian and Nona analyses. Main clade 1 includes representatives of the Brachytheciaceae, Calliergonaceae (Warnstorfia, Straminergon, Calliergon), Climaciaceae (Climacium and Pleuroziopsis), Hylocomiaceae, Neckeraceae, Pseudoleskeaceae (Rigodiadelphus and Lescuraea s. lat., incl. Ptychodium and Pseudoleskea), and genera Anomodon*, Antitrichia*, Claopodium, Conardia, Dolichomitriopsis, Echinodium*, Glossadelphus, Heterocladium*, Leptopterigynandrum, Neodolichomitra, Pilotrichella, Rhytidiopsis, Taxiphyllum, and Thelia* (taxa marked with asterisks are genera sometimes segregated in their own families, mostly monogeneric). Main clade 2 includes representatives of Amblystegiaceae, Leskeaceae (however, found non-monophyletic), Pylaisiaceae (Homomallium, Pseudohygrohypnum, Pylaisiella, Stereodon), Scorpidiaceae (Scorpidium, Limprichtia, Hamatocaulis, Sanionia, and Hygrohypnella), Thuidiaceae, and genera Breidleria, Calliergonella, Campylophyllum, Drepanium, Entodon*, Iwatsukiella, Myrinia*, Ochyraea, Platygyrium, Ptilium, Rhytidium*, Sematophyllum, Tomentypnum (asterisks as above). The composition of the main clades M1 and M2 was generally constant among trees resulting from different analysis methods, although support was low. This low support, at least partly, is connected with two groups: Calliergonaceae (O3) and Scorpidiaceae (O12). These two groups were found in basal positions of the M1 and M2 clades, respectively, in MB and Nona analyses (Figures 9.2 to 9.4). In the POY analysis Scorpidiaceae was placed in a basal position in M2, while Calliergonaceae was found within M1. In some preliminary analyses (not shown), however, they easily switch their position, occurring as a clade or grade in position basal to M1 or M2 or M1 + M2. The support of main clades M1 and M2 was very weak in Bayesian analyses, but the support values were much higher for “m1”, the main part of M1, excluding Calliergonaceae, and for “m2”, the main part of M2, excluding Scorpidiaceae (Figures 9.2 to 9.4, Table 9.1). Thus, the positions of Calliergonaceae (O3) in M1 and Scorpidiaceae (O12) in M2 probably have a very weak background. Main clades M1 and M2 (and especially m1 and m2) correspond to the content of groups found in cladistic analysis of morphological characters by Hedenäs (1989, 1997a, 1999). M1 corresponds mostly to “Brachytheciaceae + Hylocomiaceae + Ctenidiaceae” and the Isobryales, whereas M2 corresponds to “Thuidiaceae + Amblystegiaceae + temperate Hypnaceae.” The few exceptions include Conardia, which belongs to main clade M1, and Calliergonaceae, which we discuss below under Section 9.4.4.9 (O12 + O3). More roughly M1 and M2 correspond to the two orders of pleurocarps recognized during most of the twentieth century: Leucodontales (Isobryales) and Hypnales (Hypnobryales), correspondingly. This roughness especially concerns groups of Brachytheciaceae, Hylocomiaceae, Hetero-

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cladiaceae, Ctenidiaceae and Pseudoleskeaceae. According to the present analysis, as well as analyses by Hedenäs (1997a), they are more closely related to groups traditionally classified within “Isobryales” (= “Leucodontales”), rather than “Hypnobryales” (= “Hypnales”). Ironically, Hypnum cupressiforme, the type of the genus Hypnum, does not belong in the “Hypnales clade” according to the present analysis, nor according to analyses by other authors based on morphological (Hedenäs, 1989; 1997a) or molecular data (Goffinet et al., 2001; Tsubota et al., 2002, 2004). Several neglected morphological and ecological characters highlighted by Hedenäs (1989) correspond very well to the subdivision into two main clades. 1. All species of main clade m1 have round-pored stomata, whereas stomata are generally long-pored in species of main clade M2 (exceptions are Thuidiaceae and Entodontaceae). 2. Perichaetial leaves in main clade m1 are widely reflexed in taxa with curved capsules, non-plicate, without a costa, or rarely, with a costa, but then the costa less developed than in stem leaves. In contrast to this, the majority of species in main clade M2 have perichaetial leaves straight and more or less appressed to the base of the seta in taxa with curved capsules. Perichaetial leaves are also plicate, and often have a very thin but still discernible costa, which is often present even in species with ecostate vegetative leaves. 3. Most species of the main clade m1 produce spores in the cold half of the year, whereas those of M2 produce spores in the warm half of the year. According to the new definition of paraphyllia, suggested by Ignatov and Hedenäs (Chapter 13), no group of main clade M2 have true paraphyllia, which are arranged on the stem in longitudinal rows. This type of paraphyllia was observed only in Hylocomiaceae, Climaciaceae and Pseudoleskeaceae (main clade M1). There are some less strictly delimited characters that, however, are worth mentioning. Many groups of main clade m1 develop stoloniform branches (sometimes called “primary stems”), which are almost never present in main clade M2; also members of main clade M2 often have dense and regularly pinnate, feather-like branching (Ptilium, Sanionia, Stereodon, Helodium and Palustriella, etc.), whereas non-complanate branching is more characteristic of the main clade M1 (though a number of exceptions exists, for example Hylocomium and Neckera).

9.4.3 LESKEACEAE S.

LAT.

Many taxa that have been referred to Leskeaceae were found scattered among other Hypnalean taxa and unrelated to each other, but three groups (L1, L2, L3), formed solely by Leskeaceae taxa, and one group including both Leskeaceae and Thuidiaceae (LT) were found as monophyletic in both the Bayesian and Nona analyses (Figures 9.2 to 9.4, Table 9.1), although their internal topology and position in the trees had certain differences. These four clades are as follows L1) Rigodiadelphus (one species) and of Lescuraea s. lat. (six species), with Pseudoleskea (three species) and Ptychodium (one species). L2) Lindbergia (two species), Mamillariella and Pseudoleskeopsis imbricata (Hook. and Wilson) Thér. L3) Pseudoleskeella, including Leskeella but not including Pseudoleskeella serpentinensis P. Wilson and Norris (four species). LT) Leskea (two species), Haplocladium (two species), Pseudoleskeopsis zippelii and species of Thuidiaceae. Of these four clades, L1 was invariably found within main clade M1, whereas L2, L3 and LT were found within main clade M2. All four clades were supported, as shown in Table 9.1, and also had

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characteristic shared indels and substitutions in the trnL intron (Table 9.2) and ITS (Figure 9.6). These results support our previous results (Gardiner et al., 2005), and contradict a monophyletic interpretation of the Leskeaceae as traditionally circumscribed by Brotherus (1908, 1925), Noguchi (1972, 1991), Crum and Anderson (1981), Buck and Crum (1990), Buck and Goffinet (2000) and Goffinet and Buck (2004). At least certain groups, especially L1, should be excluded from the Leskeaceae. 9.4.3.1 The Lescuraea Clade (L1) The recognition of L1 as the family Pseudoleskeaceae (Rigodiadelphus and Lescuraea s. lat., including Ptychodium and Pseudoleskea), suggested by Gardiner et al. (2005) and Ignatov and Ignatova (2004), received further support from the present analysis. The circumscription of the family, however, still remains problematic, especially with regard to Conardia, which has numerous morphological dissimilarities with Lescuraea s. lat.. Conardia was found sister to the Pseudoleskeaceae clade in POY and Nona analyses (in the latter with jackknife support of 70%), while the Bayesian analyses found Conardia sister to the clade O4 + O5 + O6 (three nodes away from the position in the Lescuraea clade, L1). The Pseudoleskeaceae is distinct from the members of L2, L3 and LT in having round-pored (versus elongate-pored) stomata and paraphyllia arranged on the stem in longitudinal rows (true paraphyllia in the terminology of Ignatov and Hedenäs, see Chapter 13), in contrast to the lack of true paraphyllia in Leskea and Haplocladium. Lescuraea also differs from Leskea, Haplocladium and other Leskeaceae s. lat., and most of the Thuidiaceae, in having papillae on both surfaces of the leaf. In these other taxa papillae are developed mostly on the dorsal side of the leaf, more rarely on the ventral side on ridges of leaf plicae. Shared substitutions in the trnL intron also clearly differentiate L1 and LT (Table 9.2: positions 63, 70, 171, 313, 339). Preliminary comments on the classification of the Pseudoleskeaceae at the generic level were given by Gardiner et al. (2005). Here we can just repeat that more data are necessary for better evaluation of the status of the separate groups, such as Ptychodium and Pseudoleskea. It seems apparent that taxa with straight capsules and reduced peristomes (Lescuraea mutabilis, L. saxicola) have a derived position among taxa with curved capsules and more-or-less complete double-alternate peristomes. A similar distal position of taxa with reduced peristomes among species with curved capsules and more or less complete peristomes was found in some other families of Hypnales (see introduction). 9.4.3.2 The Lindbergia Clade (L2) Lindbergia, Mamillariella and Pseudoleskeopsis imbricata form a clade sister to the Leskea + Thuidiaceae clade (LT) in MB and Nona analyses (in latter case with jackknife support of 76%, not shown in the strict consensus in Figure 9.4). Morphologically some of these taxa, for example Lindbergia, are poor in characters specific to the genus (except variously modified peristomes), and only Mamillariella has peculiar high mamillae on the seta. The only family in the main clade M2 where some species have mamillose setae is the Thuidiaceae; thus this may be additional evidence for the relationship of L2 and LT. The Australian Pseudoleskeopsis imbricata was not found to be congeneric with east Asian P. zippelii in any of the analyses, and some characteristic parts of ITS1 (Figure 9.6) also demonstrate their distant position. 9.4.3.3 The Pseudoleskeella Clade (L3) The separate position of the Pseudoleskeella clade (L3) was confirmed by the present analysis, with support in Nona (99%) and MB (100%) analyses, and it also had one characteristic insertion in ITS1 (Figure 9.6). Species of this genus differ from most other representatives of the Leskeaceae in having small plants with short leaves, short lamina cells and no paraphyllia. In Nona and Bayesian analyses Rhytidium was found sister to Pseudoleskeellaceae. This observation is difficult to comment on: on the one hand Rhytidium is morphologically very different from Pseudoleskeella; on the other, most

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of the diagnostic characters of the latter genus are those that are commonly associated in pleurocarps with the occurrence in xeric and epiphytic habitats. Small mosses typically have shorter cells, a characteristic which has obscured their real familial placement in the past, as for example in Clasmatodon (Brachytheciaceae), Serpoleskea (Amblystegiaceae) and Platydictya (Plagiotheciaceae). 9.4.3.4 The Leskea + Thuidiaceae Clade (LT) The type genus of the Leskeaceae, Leskea, presents the main problem for classification. Both the previous (Gardiner et al., 2005) and present analysis found two species of Leskea and two species of Haplocladium nested in the Thuidiaceae, usually not forming a clade (although the NeighborJoining analysis by Gardiner et al. (2005) found these four in a monophyletic group). The resolution of relationships in this group needs inclusion of data from more taxa and probably also from more gene regions. Analysis of rps4 sequences (Goffinet et al., 2001) gave essentially similar results, though without support. Note, however, that the substitution in the conservative part of the trnL intron (position 137) was characteristic, among others, for Leskea, and both Haplocladium and Pseudoleskeopsis zippelii, but was never found in taxa of Thuidiaceae. Representatives of other genera studied that were traditionally placed in the Leskeaceae are commented on in the following groups: Anomodon longifolius (O7), A. rostratus (O6), A. rugelii (after O12), Claopodium spp. (O6), Dolichomitriopsis (O5), Habrodon (O1), Iwatsukiella (O3), Leptopterigynandrum (O8), Okamuraea (O5), Pterigynandrum (O2), and Thelia (after O12).

9.4.4 OTHER HYPNALEAN TAXA This section provides comments on groups that have single or no representatives of Leskeaceae. Clades O4 + O5 + O6 and O7 + O8 are grouped in two bigger clades, with support of 70% to 91% (Bayesian analyses) and 67% to 68% (Nona analysis). However, these two groups are rather stable and might be usefully subject to further examination. O3, “Calliergonaceae clade,” is discussed below, together with O12, in Section 9.4.4.9. 9.4.4.1 The Hylocomiaceae Clade (O4) We studied representatives of four genera (Hylocomium, Neodolichomitra, Rhytidiadelphus and Rhytidiopsis) referred to the Hylocomiaceae by Goffinet and Buck (2004). We also included Pleuroziopsis, which was considered as a member of the family by Hedenäs (2004). Hylocomium and Rhytidiadelphus, the representatives of the “core” of the family, were always found in a wellsupported clade (Table 9.1). The larger clade, which also received high support (Table 9.1), included two other clades, Pleuroziopsis + Climacium and Neodolichomitra + Antitrichia. The high support (MB 100%; Nona 98%) of the clade Pleuroziopsis + Climacium confirms the traditional concept of Brotherus (1925), as well as that of Norris and Ignatov (2000), who suggested that these two genera should not be separated into different families, as was proposed by Ireland (1968). However, the result of cladistic analysis based on morphology (Hedenäs, 2004), supports the placement of Climacium and Pleuroziopsis in different families, while in the rbcL analysis of Tsubota et al. (2004) these genera were found not to be closely related. Alignment of ITS and the trnL intron also provides no characteristic substitutions for these two genera. The genus Neodolichomitra was found to be related to Antitrichia, with considerable support (Nona 86%; MB 97%). The relationship of these genera has never been discussed before, as far as we know. Antitrichia was traditionally classified in the Leucodontaceae, although Fleischer (1923) had already noted that it is not closely related to Leucodon and suggested that it needed its own subfamily. Recently Buck (1998) also noted that Antitrichia is not a member of the Leucodontaceae, but “as default” this genus was retained within the Leucodontaceae until Ignatov and Ignatova (2004) put it in a family of its own. In the latter circumscription, Antitrichiaceae was a monogeneric family, but present data suggest the exploration of the possible relationships between

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Antitrichia and genera previously classified in the Hylocomiaceae. Alternatively, all these six genera could be classified in Hylocomiaceae, but this approach would be possible only after additional studies of more representatives of this large family. Hylocomiaceae was traditionally understood as having complete double-alternate peristomes, and if the position of Antitrichia in or near the Hylocomiaceae is established, this will be one more example of an epiphytic lineage with a derived straight capsule with reduced peristome. 9.4.4.2 The Brachytheciaceae Clade (O5) The family Brachytheciaceae was represented by two species, Homalothecium sericeum and Okamuraea brachydictyon, and they were found in a clade with Dolichomitriopsis diversiformis, the only member of the Lembophyllaceae in the present analysis. The latter was sister to Homalothecium, thus making the Brachytheciaceae non-monophyletic. The possible explanation of this fact is probably linked to the under-representing of groups. The previous analysis of numerous Brachytheciaceae and Lembophyllaceae (including the three taxa used here) found Homalothecium and Okamuraea within a monophyletic Brachytheciaceae (Huttunen and Ignatov, 2004; Huttunen et al., 2004). 9.4.4.3 The Claopodium Clade (O6) This interesting and rather well-supported (Nona 77%; MB 97% to 98%) clade is formed by Anomodon rostratus and Claopodium spp. Anomodon rostratus is especially similar to Claopodium whippleanum: plants have similar size, leaf shape and laminal cells that are short and heavily papillose with the exception of the uppermost cells, which form a contrasting pellucid “hair-point.” Their important difference includes unipapillose cells in both Claopodium species studied, and pluripapillose cells in Anomodon rostratus; however, both genera (in their present circumscription) include species with uni- and pluripapillose cells. In addition A. rostratus has a straight capsule and reduced peristome, whereas in Claopodium species the capsules are curved and peristomes are complete, with well-developed cilia. Among Anomodon s. lat., however, A. rostratus has a relatively slightly reduced peristome: the exostome teeth are cross-striolate below, the basal membrane is relatively high, and segments are relatively broad and long. The moderate support precludes at the moment the immediate transfer of Anomodon rostratus to Claopodium, but we anticipate that expanded analysis with more representatives of this group will allow this. 9.4.4.4 The Neckeraceae Clade (O7) Gardiner et al. (2005) found a close relationship between Neckera and Heterocladium, especially with two of the four species studied of the latter genus (Figure 9.1). In order to get better resolution, we added to the present analysis Leptodon, Forsstroemia and Echinodium. They were all found within a clade that includes also Neckera spp., Heterocladium spp., Anomodon longifolius, Echinodium umbratum and Pseudoleskeella serpentinensis. Similar groups were found previously by Tsubota et al., 2004 (many Neckeraceae, Echinodium, Forsstroemia, Anomodon giraldii) and by Goffinet et al., 2001 (Neckeraceae, Forsstroemia, Echinodium). A clade with three species of Neckera, one Leptodon and one Forsstroemia got high support (Nona 97%; MB144 100%, Figure 9.3), but Neckera was found to be non-monophyletic. This, however, may be dependent on the incomplete dataset, since two of the three species of Neckera lack ITS1 data. The close relationship between Leptodon and Forsstroemia was suggested by Stark (1987) based on morphology, but these genera were classified outside the Neckeraceae in a separate family, the Leptodontaceae. The relationship of Heterocladium with the groups of the main clade M1 was found by Hedenäs (1999) based on morphology; however, he thought that they were more closely related to the Brachytheciaceae + Ctenidiaceae + Hylocomiaceae complex. Species of Heterocladium differ markedly from the Neckeraceae in having perfect doublealternate peristomes (versus moderately to strongly reduced), julaceous to slightly complanate

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foliage (versus often strongly complanate), and papillose laminal cells (versus smooth). A certain similarity between Heterocladium and Neckera can be seen in the pseudoparaphyllia. These are linear and quite long in some species, and arranged more or less distant from the branch initial; thus in both groups they were interpreted as paraphyllia by some authors (see also Ignatov and Hedenäs, Chapter 13). Another similarity is the sharp differentiation between acuminate stem leaves and obtuse branch leaves in some Heterocladium species. It is possible that this is an initial stage of a trend to differentiation into acute leaves on “primary” stems and obtuse leaves on “secondary” stems seen in most Neckeraceae. Finally, Pseudoleskeella serpentinensis was found within this clade in all analyses. This species differs from other Pseudoleskeella species in being bigger and having thick-walled cells arranged in more or less firm oblique rows, reminiscent of Neckeraceae. The leaf margin of P. serpentinensis is also remotely but quite prominently serrate, a character never found in other species of Pseudoleskeella, but characteristic of both Neckeraceae and Heterocladium. Thus, the placement of P. serpentinensis in Heterocladium or near it seems more likely than in Pseudoleskeella. 9.4.4.5 The Taxiphyllum Clade (O8) This clade was found only in the course of the present study, and combines groups with rather distinct morphology. It includes Leptopterigynandrum, Glossadelphus and Taxiphyllum. In MB analysis Carribaeohypnum and Thelia were found in a grade basal to this clade, with strong support, but Nona analyses found no support, thus they are not discussed here. However, they could be the focus of further studies, as species of O8 and Carribaeohypnum have a characteristic substitution in ITS1 (Figure 9.6), and they, along with Thelia, also have a characteristic insertion in the trnL intron (Table 9.2). Although the assemblage of mosses of this clade might look strange, the relationship of at least Glossadelphus (same species) and Taxiphyllum (different species) was found by Tsubota et al. (2004) in rbcL analysis. The relationship of these taxa to Leptopterigynandrum looks plausible for the reasons already discussed for Pseudoleskeella. The diagnostic characters of the genus Leptopterigynandrum (small plants with short laminal cells) have appeared many times in epiphytic lineages, for example in Brachytheciaceae (Clasmatodon), Amblystegiaceae (Serpoleskea) and Plagiotheciaceae (Myurella). Interestingly, Leptopterigynandrum has round-pored stomata (He, 2005), supporting its position in the M1 clade, as discussed above, and thus is not related to the Leskeaceae s. str. as suggested by He (2005). 9.4.4.6 The Amblystegiaceae Clade (O9) Taxa in this clade in the present analysis were drawn largely from data on GenBank, obtained by Vanderpoorten et al. (2002b). Incorporated in our alignment, these data resulted in principally the same topology and similar support values as found in the original analysis. The addition is Hypnum bambergeri, which was found sister to the Campylium + Leptodictyum clade. This placement is unexpected and needs further study, but it is supported by the presence in Hypnum bambergeri of numerous indels and substitutions characteristic for Amblystegiaceae (Table 9.2, Figure 9.6). This clade has the highest support among larger clades (more than five species) in Nona analyses (99%), which agrees with the numerous characteristic insertions in the ITS region (Figure 9.6). The secondary structure of the trnL intron in Amblystegiaceae is unusual in the P6 loop (Figure 9.5). In most species studied in the present analysis P6 is 4 nucleotides long, whereas in most Amblystegiaceae it is 9 nine nucleotides long and in Cratoneuron 12 nucleotides. 9.4.4.7 The Ochyraea Clade (O10) This clade includes part of Hygrohypnum (species around H. norvegicum and H. smithii, segregated in the genus Ochyraea by Ignatov and Ignatova [2004]), Campylophyllum, Drepanium (Hypnum) recurvatum, Tomentypnum and Myrinia. The main composition of this clade was found in cladistic

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analysis of morphological data by Hedenäs (1997a, 1997b), who, however, also included in the clade species now classified in Campylidium (“Campylium hispidulum” group) and Hypnum pallescens, which is not supported in the present study. Tomentypnum, found in a basal position in this clade in molecular analysis (Gardiner et al., 2005, and present study) and Myrinia, found external to this clade by Gardiner et al., 2005, but sister to this clade in the present study, were not found related to the “core of Ochyraea-clade” in the morphological analysis of Hedenäs. This clade (excluding Myrinia) had high support (Nona 80%; MB135 94%; MB144 97%) while the whole clade including Myrinia had mostly lower support (Nona 89%; MB 135 71%; MB 144 62%). Characteristic indels in the trnL intron support the close relationship of Campylophyllum and Ochyraea (Table 9.2). The type species of Ochyraea, O. tatrensis was found in a clade with O. smithii with high support (Nona 99%; MB 100%). Relationship of these species was found previously by Stech and Frahm (2001), and some morphological characters, for example pseudoparaphyllia, are very similar in these two species. Interestingly, the opinion of R. Duell (Ochyra, personal communication) on the holotype of Ochyraea tatrensis was that this is just an aberrant form of Hygrohypnum smithii. A clade with Drepanium recurvatum and Tomentypnum nitens was found also by Tsubota et al. (2004). These two species were the only representatives of this clade in that analysis of approximately 600 species of mosses. Our previous analysis did not include Ochyraea (Hygrohypnum) mollis, thus this combination is introduced here as new: Ochyraea mollis (Hedw.) Ignatov, comb. nov.–Hypnum molle Hedw., Species Muscorum Frondosorum 273. 70 f. 7–10. 1801. 9.4.4.8 The Pylaisiaceae Clade (O11) The fact that Hypnum cupressiforme, the type of the genus Hypnum, is not related to most of the other species traditionally classified in this genus was found by Hedenäs (1989) in his morphological analysis of pleurocarps. This conclusion appears to be in agreement with all the molecular phylogenetic analyses that have involved at least a few species of Hypnum s. lat. (e.g., Goffinet et al., 2001; Tsubota et al., 2002, 2004). Gardiner et al. (2005) suggested the separation of the main part of Hypnum in Stereodon, and its placement in the family Pylaisiaceae, together with Pylaisia, Homomallium and Pseudohygrohypnum. Species of the former “Hypnum” found here in the Pylaisiaceae clade (Hypnum procerrimum Mol., from section Pseudostereodon (Broth.) Ando; H. revolutum (Mitt.) Lindb. and H. vaucheri Lesq., from section Revolutohypnum Mönk.; Hypnum plicatulum (Lindb.) Jaeger, from section Hamulosa Bruch et al. and H. plumaeforme Wilson, from section Curvifolia Ando.) represent a wide selection from different groups of this genus (sections according to the classification of Ando, 1976). Tsubota et al. (2004) found three species of Hypnum s. lat. (H. plumaeforme, H. sakurai, H. oldheimii) in the group with Pylaisia. Besides Hypnum cupressiforme, three other species of the former “Hypnum” were found outside the Stereodon group: Hypnum bambergeri, H. recurvatum and H. pallescens. The position of Hypnum bambergeri within Amblystegiaceae and Drepanium (Hypnum) recurvatum in the “Ochyraea-clade” were well supported (see discussion above for O9 and O10). In both Nona and MB144 analyses Stereodon (Hypnum) pallescens was found sister to a clade composed of Sematophyllum, Platygyrium and Entodon, and this combined clade was found sister to O11 in MB144 (not resolved in Nona). One characteristic substitution in the trnL intron (pos. 115, see Appendix 9.2) is shared between clade M2 for Pylaisiaceae (most species) and Sematophyllum, Platygyrium, Entodon and Stereodon pallescens. 9.4.4.9 The Scorpidiaceae (O12) and Calliergonaceae Clades (O3) These two clades were found in basal positions of M2 and M1 clades, respectively, in MB and Nona analyses. In some preliminary analyses (not shown), however, they easily switch their position,

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occurring as a clade or grade in a position sister to or basal in M1 or M2 or M1 + M2. The analysis of Vanderpoorten et al. (2002b) found Hamatocaulis in Calliergonaceae (now found in a basal position in O12 in MB and Nona analyses), and Scorpidium also closely related to the Calliergonaceae s. lat. (i.e., including Hamatocaulis). Thus Scorpidiaceae and Calliergonaceae are probably rather closely related, despite their present positions in different main clades. In comparison with the Calliergonaceae, which were found monophyletic with high support (Nona 99%; MB 100%), the clade of Scorpidiaceae has much lower support (Nona 74%; MB144 73%; MB135 <50%), although the main part of this O12 clade (excluding Hamatocaulis) has higher values (Nona 77%; MB135 99%; MB 144 96%, respectively). From the morphological point of view, the placement of Hamatocaulis in Scorpidiaceae is more likely than in Calliergonaceae for at least two reasons. First, the family Calliergonaceae becomes much more homogeneous, and all its members share the rare morphological characters outlined by Tuomikoski and Koponen (1979) (radial branching pattern; development of rhizoids on leaf apex; rhizoids with scattered distribution on stems; absence of annulus; development of cherry-red pigmentation in habitats exposed to strong sunlight, etc.). Second, Hamatocaulis is probably rather closely related to Limprichtia (Scorpidium pro parte). Some species of these genera look very similar and are sometimes confused in herbarium collections (especially if identification is based mostly on leaf characters), and they occur in similar, rather specific habitats. However, the final decision on the position of Hamatocaulis, as well as the separation of the Calliergonaceae from the Scorpidiaceae, needs the study of all representatives of these two groups. The Scorpidiaceae were resolved in the present analysis as a clade that includes Limprichtia, Sanionia, part of Hygrohypnella (species of the former Hygrohypnum with a hyalodermis, H. ochraceum and H. polare, and also H. duriusculum), Scorpidium (MB 144) and Hamatocaulis (always in a basal position). Most members of this clade are hygrophytes, preferring habitats rich in minerals. Most of them (except Hamatocaulis and Hygrohypnum duriusculum) have a hyalodermis. In this respect they differ from the Amblystegiaceae and most Calliergonaceae (except Warnstorfia, where a hyalodermis is occasionally present). The Scorpidiaceae do not share the specific features of the Calliergonaceae listed above, and most Scorpidiaceae also have a clearly complanate branch arrangement (radial in Calliergonaceae). In common with the Calliergonaceae and in contrast to the Amblystegiaceae, the Scorpidiaceae usually lack a separating annulus. It is worth noting that Iwatsukiella was found sister to the Scorpidiaceae clade in Nona analysis, and the Scorpidiaceae + Breidleria clade in MB analyses. This rather xerophytic moss is unlikely to be closely related to the bog plants of the Scorpidiaceae, which differ in both sporophytic and gametophytic characters. However, further analyses of Scorpidiaceae should probably include this genus, which might be shown to represent an epiphytic lineage of this family, as was Anacamptodon of the Amblystegiaceae or Struckia of the Plagiotheciaceae.

9.4.5 COMMENTS

ON

SOME SPECIES

THAT

CHANGE

THEIR

POSITIONS

The present analysis failed to find anything definite about the relationships of several groups. Ptilium, Calliergonella and Breidleria were always within main clade M2 but changed position in different analyses. Other species of rather indefinite position (Stereodon pallescens, Sematophyllum, Platygyrium and Entodon) were commented on briefly under O11, and Platygyrium and Sematophyllum under “general comments on tree topology.” These species are single representatives of big families, so discussion of their relationships cannot be done on such incomplete data. The genera Conardia, Pilotrichella, Thelia, Rhytidiopsis and Anomodon rugelii were found in variable positions within main clade M1. Anomodon is a very problematic genus. Tsubota et al. (2002, 2004) found species of Anomodon in three remote positions within their phylogenetic tree. We studied three species here, and also found all of them unrelated to each other. Of these, Anomodon rostratus was found closely related to Claopodium (see O6), A. longifolium was a member of a clade with Echinodium and Heterocladium (see O7), while Anomodon rugelii was

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placed with Pilotrichella ampullacea in Bayesian (MB144 82%) and Nona (74%) analyses. The plants are morphologically too different to discuss their relationships. Thelia and Rhytidiopsis formed a clade in Nona analysis without support, and in MB analyses they were found together in the grade basal to O8. Despite being very different morphologically, these genera share a rare character (abundant paraphyllia) and their relationships should probably be a focus of further studies.

9.5 CONCLUDING REMARKS In comparison with analyses based on data from the chloroplast genome only (e.g., Goffinet et al., 2001; Shaw et al., 2003; Tsubota et al., 2004), our analysis obtained better resolution for the Hypnales as a whole, which may be due to the inclusion of one of the most variable loci from the nuclear genome: ITS1 and ITS2. When we started our analysis, we expected mostly to achieve better resolution in the terminal parts of the clades. This, we hoped, would help in determining the position of some genera that, in smaller molecular phylogenetic analyses, were found “nowhere,” that is, not related to any known family, for example Leptopterigynandrum in Gardiner et al. (2005), or Sanionia in Vanderpoorten et al. (2002b). Somewhat unexpectedly, in addition to this the segregation of two larger clades (M1 and M2) was found, and moreover these clades corresponded more or less to those found in cladistic analysis based on morphology (Hedenäs, 1997a) as well as the traditional classification of pleurocarps into Isobryales and Hypnobryales (with a number of emendations commented on under “M1 and M2” in the Discussion section). It is significant that these two main clades (M1 and M2) appeared in analyses of datasets aligned using completely different methods (that is, both direct optimization and manual). More cases of peristome reduction associated with epiphytism were revealed in our analysis. Huttunen et al. (2004) analyzed epiphytism-dependent characters and found 13 to be strongly correlated with occurrence on tree trunks (for example, spore size, hygroscopic exostome movement, height of endostome membrane, hairy calyptra, capsule orientation, seta length, etc.). In addition to that set, two more characters need to be considered — small plant size and short laminal cells. These were not included in the analysis by Huttunen et al.(2004) because the characters are difficult to define, but the examples offered by Serpoleskea, Clasmatodon, Pseudoleskeella, Leptopterigynandrum and Leskea, might illustrate this trend in the evolution of pleurocarps. Thus, our analysis showed that Leskeaceae in the traditional circumscription is rather a concept than a taxon. In the recent past there have been numerous re-evaluations of the circumscription of families that traditionally were based on a single or few “key character(s).” Leskeaceae was probably one of the last in this series.

ACKNOWLEDGMENTS We are grateful to Neil Bell for valuable comments on the manuscript. This work was partly supported by the Biodiversity program of the Russian Academy of Sciences, the Scientific School program NS-1712.2003.4 and RFBR grants 06-04-49493 and 04-04-48774, by the Academy of Finland for Jaakko Hyvönen’s project “Bryosphere”, and the Finnish Cultural Foundation.

Claopodium whippleanum (Sull.) Renauld & Card. (2)

Campylium stellatum (Hedw.) C. Jens. Campylophyllum halleri (Sw. ex Hedw.) M. Fleisch(2) Campylophyllum halleri (Sw. ex Hedw.) M. Fleisch. (1) Caribaeohypnum polypterum (Mitt.) Ando & Higuchi Claopodium crispifolium (Hook.) Renauld & Card. Claopodium whippleanum (Sull.) Renauld & Card. (1)

Campyliadelphus chrysophyllus (Brid.) Kanda Campylidium sommerfeltii (Myr.) Ochyra

Antitrichia californica Card. Breidleria (Hypnum) pratense (J. Koch ex Spruce) Loeske Callicladium haldanianum (Grev.) H. A. Crum Calliergon cordifolium (Hedw.) Kindb. Calliergon giganteum (Schimp). Kindb. Calliergonella cuspidata (Hedw.) Loeske Calliergonella lindbergii (Hedw.) Hedenäs

Abietinella abietina (Hedw.) M. Fleisch. Amblystegium serpens (Hedw.) Bruch & al. Anacamptodon splachnoides (Brid.) Brid. Anomodon longifolius (Brid.) Hartm. Anomodon rostratum (Hedw.) Schimp. Anomodon rugelii (Müll. Hal.) Keissl.

Species

APPENDIX 9.1 Taxon Sampling and GenBank Accession Numbers

GB: (Vanderpoorten & al., 2002): Allen 19816 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield 106313 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield et al. 96592 (DUKE) Caucasus, Ignatov 30.VIII.1999 (MHA) Caucasus, Ignatov 30.VIII.1999 (MHA) GB: (Buck & al., 2000): Buck 32519 (NY) GB: (Chiang T.Y., unpubl.) California, Ignatov s. n. 9.VIII.1989 (MHA) European Russia, Vologda, Ignatov s. n. 22.IX.1990 (MHA) European Russia, Kursk Prov., Ignatov s. n. 14.VIII.1996 (MHA) GB: (Vanderpoorten & al., 2002): Ireland 24198 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield et al. 93733 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield 100768 (DUKE) GB: (Buck & al., 2000): Buck 33459 (NY) GB: (Vanderpoorten & al., 2002): Anderson 27099b (DUKE) GB: (Vanderpoorten & al., 2002): Anderson 26799 (DUKE) European Russia, Kostroma Prov., Braslavskaya s. n. 17.VII.2003 (MW) GB: (Vanderpoorten & al., 2002): Schofield 105981 (DUKE) South Siberia, Kuznetsky Alatau, Pisarenko s. n. 20.VII.2002 (MHA) GB: (Vanderpoorten & al., 2002): Schofield et al. 93995 (DUKE) GB: (Vanderpoorten & al., 2002): Allen 11570 (DUKE) California, Ignatov s. n. 7.VIII.1989 (MHA) GB: (Shaw & al., 2003a) California, Düll, 22C4/2 (H) GB: (Shaw & al., 2003a) California, Düll, 22C4/2 (H)

Sourse/specimen (GB, GenBank — followed by the reference and if available — specimen, as cited)

AY683584

AY683584

AY009832 AY683610 AY009853 AY009846 AY683583

AY009831 AY683609

AY683582 AY683606 AY762372 AY009836 AY009834 AY009859 AF161128

AY009850 AY009827 AY009816 AY683562 AY528896 AF161116

trnL-F

AY009813 AF168150 AY693654

AY009813 AF168150 AY693654

AY173470

Continued.

AY173470

AF168151 AY693655 AF168134 AY009799 AY695778 AY173471

AJ277232 AY693658 AY693659 AY695785 AF168146 AF168144 AF168145

AJ288420 AY693658 AY693659 AY695761 AF168146 AF168144 AF168145

AF168151 AY693655 AF168134 AY009799 AY695739 AY173471

AY009802 AF168152 AY009810 AY695766 AY528899

ITS2

AY009802 AF168152 AY009810 AY695750 AY528899

ITS1

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Relationships of Mosses of the Order Hypnales 205

Glossadelphus ogatae Broth. & Yas. Habrodon perpusillus (De Not.) Lindb.

Eurohypnum leptothallum (Müll. Hal.) Ando Fabronia ciliaris (Brid.) Brid. Fontinalis welchiana B. H. Allen Forsstroemia trichomitria (Hedw.) Lindb.

Entodontopsis leucostega (Brid.) W. R. Buck & R. R. Ireland

(Chiang T.Y., unpubl.) (Buck & al., 2000) (Vanderpoorten & al., 2002): Risk 10846 (DUKE) (Vanderpoorten & al., 2002): Lewis 87262 (DUKE) (Vanderpoorten & al., 2002): Vanderpoorten 769 (DUKE)

Finland, Pykälä 8706 (H) GB: (Stech & al., unpubl.) GB: (Shaw & al., 2003b) Russian Far East, Nedoluzhko s. n. 18.VII.1990 (MHA) Asian Russia, Yakutia, Ignatov 00-528 (MHA) GB: (Vanderpoorten & al., 2002): Schofield 104541 (DUKE) GB: (Vanderpoorten & al., 2002): Hedenäs B39576 (S) GB: (Buck & al., 2000) Norfolk Island, Streimann, 49668 GB: (Majestyk,P., unpubl.) GB: (Majestyk,P., unpubl.) GB: (Majestyk,P., unpubl.) GB: (Chiang T.Y., unpubl.) GB: (Buck & al., 2000) Columbia, Sastre-De Jesus & al., 1440 (H, ex NY) Altai, Ignatov 34/129 (MHA) Urals, Bezgodov 268 (MHA) GB: (Shaw & Allen, 2000): Alabama (Allen: exs. 157) GB: (Buck & al., 2000) China, Zhejiang, Buck 23861 (H) Japan, Deguchi 26.III.1998 (Bryophytes of Asia, # 134) (H) Caucasus, Ignatov & Ignatova, s. n. 9.VIII.2002 (MHA)

GB: GB: GB: GB: GB:

Sourse/specimen (GB, GenBank — followed by the reference and if available — specimen, as cited)

DQ019931 AY527126

AY683563 AY527128 AF191542 AF161099

AF161153

AY255481 AY255490 AY255486

AY306736 AF397777 AY683592 AY009828 AY009868 AF161137

AF161158 AY009865 AY009817

trnL-F

AY999172 AY255494

AY999172 AY255494

AY999175 AY695786 AY528883 AF192133 AY999173 AY999169 AY528880

AY999175 AY695733 AY528883 AF192133 AY999173 AY999169 AY528880

AJ288572

AF403664 AY693660 AF180949 AY009792

AF403632 AY091472

AY009806 AY009812 AF168155

AJ288569

ITS2

AF516159 AY693660 AF180949 AY009792

AY009806 AY009812 AF168155

AJ288355

ITS1

206

Entodon beyrichii (Schwägr.) Müll. Hal. Entodon jamesonii (Taylor) Mitt. Entodon seductrix (Hedw.) Müll. Hal.

Climacium dendroides (Hedw.) F. Weber & D. Mohr Climacium americanum Brid. Conardia compacta (Müll. Hal.) Robins. Cratoneuron filicinum (Hedw.) Spruce (1) Cratoneuron filicinum (Hedw.) Spruce (2) [var. atrovirens (Brid.) Ochyra] Ctenidium molluscum (Hedw.) Mitt. Distichophyllum crispulum (Hook. & Wilson) Mitt. Distichophyllum pulchellum (Hampe) Mitt. Dolichomitriopsis diversiformis (Mitt.) Nog. Drepanium (Hypnum) recurvatum (Lindb. & Arnell) G. Roth Drepanocladus aduncus (Hedw.) Warnst. Drepanocladus sordidus (Müll. Hal.) Hedenäs Echinodium umbrosum (Mitt.) A. Jaeger

Species

APPENDIX 9.1 (Continued) Taxon Sampling and GenBank Accession Numbers

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Pleurocarpous Mosses: Systematics and Evolution

GB: (Vanderpoorten & al., 2002): Piercey-Normore NF57 (DUKE) Asian Russia, Yakutiya, Ignatov 00-9476 (MHA) Mongolia, Ignatov 01-710a (MHA) GB: (Vanderpoorten & al., 2002): Schofield et al.104900 (DUKE) GB: (Stech & Frahm, 2001): Germany, Frey 1-4957 (BONN) GB: (Chiang T.Y., unpubl.) European Russia, Archangelsk Prov., Ignatov s. n. 11.VIII.1988 (MHA) Finland, Ignatov, 17.VIII.1990 (MHA) Finland, Huttenen 1438 (H) Asian Russia, Yakutia, Ignatov 00-298 (MHA) Asian Russia, Yakutia, Ignatov 00-287 (MHA) Russian Far East, Ignatov 97-243 (MHA)

GB: (Vanderpoorten & al., 2002): Hedenäs & Janssens B16968 (S) Japan, Higuchi 13216 (HIRO, dupl. MHA) GB: (Vanderpoorten & al., 2002): Buck 32482 (NY) GB: (Vanderpoorten & al., 2002): Schofield 108637 (DUKE) European Russia, Ryazan Prov., Ignatov s. n. 30.IX.1999 (MHA) GB: (Pedersen & Hedenäs, 2002) Slovakia, Huttunen & Jalkanen VIII.1996 (H3194478) Canada, Vitt 35998 (ALTA, dupl. MHA) Urals, Bezgodov 377A (1995) (MHA) Caucasus, Akatova, s. n. 20.VIII.1999 (MHA) Canada, Schofield 77203 (H) Poland, Ignatov 10.III.1997 (MHA) Altai, Ignatov & Ignatova 11/85 (MHA) GB: (Cox & al., 2000) GB: (Capesius & Blöcher, unpublished) GB: (Vanderpoorten & al., 2002): Allen 16372 (DUKE) GB: (Vanderpoorten & al., 2002): Buck 15943 (DUKE) GB: (Vanderpoorten & al., 2002): Vanderpoorten 4195 (DUKE) GB: (Vanderpoorten & al., 2002): Vanderpoorten 4263 DUKE) GB: (Vanderpoorten & al., 2002): Anderson 27620 Caucasus, Ignatov 8.VIII.1998 (MHA)

AY527138 AY683568 AY527132

AF397812

AY683607

AY009861 AY683566 AY683566 AY009862 AF152385

AY009822 AY009874 AY009820 AY009821 AY009825 AY009870

AY683587 AY683586 AY527130 AY683588 AY683605 AY683564 AF215906

AY009819 AY527129 AF161133 AY009852 AY683585 AF472453

AY528888 AY528882 AY695751 AF516162

AF403607 AY528882 AY695770 AF516157+ Continued.

AJ270021 AY695781

AJ288336 AY695759

AJ252137 AF168154 AF168165 AF168156 AF168157 AF168159 AY695767

AJ252137 AF168154 AF168165 AF168156 AF168157 AF168159 AY695736

AF168138 AY695787 AY762374 AF168137

AY999174 AY695782 AY695771 AY528895 AY695783 AF516155

AY999174 AY695756 AY695757 AY528894 AY695742 AF516160

AF168138 AY695735 AY762375 AF168137

AF315073 AY528885 AF168160 AY009803 AY695764

AF315073 AY528884 AF168160 AY009803 AY695758

Relationships of Mosses of the Order Hypnales

Isopterygiopsis muelleriana (Schimp.) Z. Iwats. Isopterygiopsis pulchella (Hedw.) Z. Iwats. Iwatsukiella leucotricha (Mitt.) W. R. Buck & H. A. Crum

Hypnum cupressiforme Hedw.

Hypnum bambergeri Schimp.

Hygroamblystegium fluviatile (Hedw) Bruch & al. Hygroamblystegium humile (P. Beauv.) Crundw. Hygroamblystegium tenax (Hedw.) C. E. O. Jensen (1) Hygroamblystegium tenax (Hedw.) C. E. O. Jensen (2) Hygroamblystegium varium (Hedw.) Lindb. Hygrohypnella (Hygrohypnum) duriuscula (De Not.) Ignatov & Ignatova Hygrohypnella (Hygrohypnum) ochracea (Wils.) Ignatov & Ignatova Hygrohypnella (Hygrohypnum) polaris (Lindb.) Ignatov & Ignatova Hygrohypnella (Hygrohypnum) polaris (Lindb.) Ignatov & Ignatova Hygrohypnum luridum (Hedw.) Jenn. Hylocomium splendens (Hedw.) Bruch et al.

Heterocladium procurrens (Mitt.) A. Jaeger Heterocladium dimorphum (Brid.) Bruch & al. Heterocladium heteropterum (Hedw.) Bruch et al. Heterocladium macounii Best Homalothecium sericeum (Hedw.) Bruch et al. Homomallium incurvatum (Schrad. ex Brid.) Loeske Hookeria lucens (Hedw.) Sm.

Hamatocaulis vernicosus (Mitt.) Hedenäs Haplocladium angustifolium (Hampe & Müll. Hal.) Broth. Haplocladium virginianum (Brid.) Broth. Helodium blandowii (F. Weber & D. Mohr) Warnst. Herzogiella seligeri (Brid.) Z. Iwats. (1) Herzogiella seligeri (Brid.) Z. Iwats. (2)

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207

GB: (Vanderpoorten & al., 2002): Bowers and Haynes 15869 (DUKE) France, De Sloover 44.843 (H) Mongolia, Ignatov 01-388 (MHA) Altai, Ignatov 36/270 (MHA) Poland, Bednarek-Ochyra & Ochyra 318/90 (KRAM, dupl. MHA: Musci Poloniae Exs. 1162)) Urals, Ignatov & Bezgodov 675 (1994) (MHA) Caucasus, Korotkov s. n. 2.IX.1987 (MHA) Caucasus, Onipchenko s. n. 30.VIII.1998 (MW) Caucasus, Onipchenko s. n. 30.VIII.1998 (MW) Altai, Ignatov 13/28 (MHA) GB: (Vanderpoorten & al., 2002): Buck 30102 (NY) European Russia, Moscow Prov., Ignatov s. n. 18.VI.1996 (MHA) European Russia, Karelia, Huttunen & Wahlberg 819 (H) GB: (Vanderpoorten & al., 2002): Schofield et al. 99517 (DUKE) USA, Churchill 1328 (H) Russian Far East, Ignatov 97-567 (MHA) GB: (Shaw & al., 2003): Holz & Franzaring CH 00-135 (NY) GB: (Stech & Frahm, 2001): Frey 92-72 Russian Far East, Cherdantseva s. n. 21.VII.1988 (MHA) European Russia, Ryazan Prov., Ignatov s. n. 29.IX.1999 (MHA) Asian Russia, Yakutya, Ivanova s. n. 7.X.2002 (MHA) GB: (Quandt & Huttunen, 2004, sub. Homalia besseri) GB: (Stech & al., 2003): Frey 1-4956 GB: (Stech & al., 2003): Frey 1-4955 GB: (Vanderpoorten & al., 2002): Shaw 9354 (DUKE) China, Koponen 54666 (H, dupl.. MHA) GB: (Chiang T.Y., unpubl.)

Sourse/specimen (GB, GenBank — followed by the reference and if available — specimen, as cited)

AY683597 AY527127 AY528897 AF543543 AY050279 AY050280 AF315072 AY683602

AJ288367

AY009809

AY693652 AY528886 AY528898

AF168140 AY695760 AF516170

AY693661 AY695738 AY695746 AF516165 AF516164 AF176277 AY528889

AY683595 AY683601 AY683577 AY683569 AY683576 AF161135 AY527134 AF397786 AY009841 AY683571 AY683572 AY306780

AY527133 AY683596

AF168163 AY999171 AY693656 AF516163 AY695740

ITS1

AY009830 DQ019932

trnL-F

AJ288581

AY029369 AY693652 AY528887 AY528898 AF543544 AY050295 AY050296 AY009809

AY693661 AY695792 AF516149 AY695774 AF516150 AF176277 AF516151 AF403634 AF168140 AY695763 AF516153

AF168163 AY999171 AY693656 AF516158 AY695765

ITS2

208

Mamillariella geniculata Laz. Myrinia pulvinata (Wahlenb.) Schimp. Myrinia rotundifolia (Arnell) Broth. Neckera besseri (Lob.) Jur. Neckera complanata (Hedw.) Huebener Neckera crispa Hedw. Neckera pennata Hedw. Neodolichomitra yunnanensis (Besch.) T.J. Kop.

Leptodictyum riparium (Hedw.) Warnst. Leptodon smithii (Hedw.) F. Web.& D. Mohr Leptopterigynandrum austro-alpinum Müll. Hal. (1) Leptopterigynandrum austro-alpinum Müll. Hal. (2) Lescuraea (Ptychodium) plicata (Schleich. ex F. Weber & D. Mohr) Schimp. Lescuraea incurvata (Hedw.) Lawt. Lescuraea mutabilis (Brid.) I. Hag. Lescuraea patens (Lindb.) Arnell & C. E. O. Jensen Lescuraea saxicola (Bruch & al.) Mol. Lescuraea secunda Arnell Leskea gracilescens Hedw. Leskea polycarpa Hedw. Leucodon sciuroides (Hedw.) Schwägr. Limprichtia revolvens (Sw. ex Anonymo) Rubers Lindbergia brachyptera (Mitt.) Kindb. Lindbergia duthiei Broth. Lopidium concinnatum (Hook.) Wilson

Species

APPENDIX 9.1 (Continued) Taxon Sampling and GenBank Accession Numbers

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Pleurocarpous Mosses: Systematics and Evolution

Pseudoleskeella catenulata (Brid. ex Schrad.) Kindb. Pseudoleskeella papillosa (Lindb.) Kindb. Pseudoleskeella serpentinensis P. S. Wilson & D. H. Norris Pseudoleskeella tectorum (Funck ex Brid.) Kindb. ex Broth. Pseudoleskeopsis imbricata (Hook. & Wilson) Thér. Pseudoleskeopsis zippelii (Dozy & Molk.) Broth. Pterigynandrum filiforme Hedw. Ptilium crista-castrensis (Hedw.) De Not. (1) Ptilium crista-castrensis (Hedw.) De Not. (2) Pylaisia polyantha (Hedw.) Schimp. Rauiella fujisana (Paris) Reimers

Pseudo-calliergon turgescens (C. E. O. Jensen) Loeske Pseudohygrohypnum (Hygrohypnum) eugyrium (Bruch & al.) Kanda Pseudoleskeela nervosa (Brid.) Loeske

Pilotrichella ampullacea (Müll. Hal.) A. Jaeger Plagiothecium denticulatum (Hedw.) Bruch & al. Platydictya jungermannioides (Brid.) H. A. Crum Platygyrium repens (Brid.) Schimp. Pleuroziopsis ruthenica (Weinm.) Britt. Pseudo-calliergon trifarium (F.Weber & D. Mohr) Loeske

Palustriella falcata (Brid.) Hedenäs

Ochyraea (Hygrohypnum) alpestris (Sw. ex Hedw.) Ignatov & Ignatova Ochyraea (Hygrohypnum) cochlearifolia (Venturi) Ignatov & Ignatova Ochyraea (Hygrohypnum) montanum (Lindb.) Ignatov & Ignatova Ochyraea (Hygrohypnum) norvegica (Bruch & al.) Ignatov & Ignatova Ochyraea (Hygrohypnum) smithii (Sw.) Ignatov & Ignatova Ochyraea(Hygrohypnum) mollis (Hedw.) Ignatov Ochyraea tatrensis Váa Okamuraea brachydictyon (Card.) Noguchi Orthothecium rufescens (Brid.) Bruch et al. Altai, Ignatov 7/16 (MHA) Kola Peninsula, Belkina s. n. 22.IX.1995 (MHA) GB: (Vanderpoorten & al., 2002): Schofield et al. 92572 (DUKE) Asian Russia, Yakutiya, Ignatov 00-952 (MHA) GB: (Vanderpoorten & al., 2002): Schofield 104556 (DUKE) Russia, Far East, Bureya, Borisov 21.VIII.1991 (MW) GB: (Stech & Frahm, 2001): Váa s. n. 30.VIII.1987 (BONN) China, Koponsen & al., 48969 (H) GB: (Pedersen & Hedenäs, 2002) Slovakia, Huttunen & Jalkanen 27 (H3194639) GB: (Vanderpoorten & al., 2002): Schofield and Godfrey 97864 (DUKE) GB: (Quandt, unpubl.) Asian Russia, Yakutiya, Ignatov 00-883 (MHA) GB: (Vanderpoorten & al., 2002): Schofield et al. 101911 (DUKE) GB: (Vanderpoorten & al., 2002): Buck 33448 (NY) U.S.A., Alaska, Schofield 110515 (H) GB: (Vanderpoorten & al., 2002): Schofield and Spence 84225 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield et al. 92508 (DUKE) Sweden, Hedenäs, s. n. 3.X.1992 (S, dupl.. MHA) European Russia, Nizhnij Novgorod Prov., Ignatov s. n. 12.IX.1999 (MHA) Urals, Ignatova 12/29 (MHA) Urals, Bezgodov, 1990 (MW) California, Wilson 944 (1986) (H) Altai, Ignatov 23/30 (MHA) Australia, Streimann 54809 (exs. # 509) (H) China, Hainan, Redfearn 36225 (H) Altai, Ignatov 4.VII.1991 (MHA) GB: (Vanderpoorten & al., 2002): Schofield 108705 (DUKE) European Russia, Udmurtia, Munitsina s. n. 21.VII.2000 (MHA) Moskva, Ignatov, s. n. 10.VII.2003 (MHA) Russian Far East, Ignatov 97-464 (MHA) AY683578 AY683598 AY683580 AY683579 AY683581 AY683603 AY526198 AY009847 AY683611 AY527137 AY683600

AY009843 AY683608 AY527135

AF508315 AY527131 AY009857 AF161131 DQ019930 AY009835

AY009829

AF260915 AY184789 AF472464

AY683565 AY683589 AY009863 AY683567 AY009856

AY695747 AY695753 AY695748 AF516168 AY693653 AY695749 AY528890 AY009800 AY693657 AY528881

AY009794 AY695737 AF516167

AY528892 AF168162 AY009798 AY999170 AY009793

Relationships of Mosses of the Order Hypnales Continued.

AF516154 AY695784 AY695775 AY695776 AY693653 AY695777 AY528891 AY009800 AY693657 AY528881

AY009794 AY695790 AF516152

AF508322 AY528893 AF168162 AY009798 AY999170 AY009793

AY999177 AF168158

AY999177 AF168158

AF516161

AY695769 AY695788 AY009804 AY695789 AF168139 AY999178 AF260916 AF503537

AY695752 AY695734 AY009804 AY695753 AF168139 AY999178

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Sanionia uncinata (Hedw.) Loeske Scorpidium scorpioides (Hedw.) Limpr. Sematophyllum homomallum (Hampe) Broth. Serpoleskea confervoides (Brid.) Loeske Stereodon (Hypnum) pallescens (Hedw.) Mitt. Stereodon (Hypnum) plicatulum Lindb. Stereodon (Hypnum) plumaeformis (Wilson) Mitt. Stereodon (Hypnum) procerrimum Baumgartner Stereodon (Hypnum) revolutum Mitt.

Rhytidium rugosum (Hedw.) Kindb. (2) Rigodiadelphus robustus (Lindb.) Nog.

Rhytidium rugosum (Hedw.) Kindb. (1)

Rhytidiopsis robusta (Hook.) Broth.

GB: (Meissner & al., 1998) GB: (Chiang & Shaal, 2000) Canada, Vitt 35999 (ALTA dupl. MHA) GB: (Chiang T.Y., unpubl.) GB: (Vanderpoorten & al., 2002): Schofield and Godfrey 98103 (DUKE) GB: (Stech & Frahm) Japan, Deguchi, s. n. 2.VIII.1998 (MHA ex HIRO: Bryophytes of Asia #164)) GB: (Vanderpoorten & al., 2002): Scholfield 95255 (DUKE) GB: (Vanderpoorten & al., 2002): Hedenäs 20461 (S) GB: (Quandt, unpubl.) GB: (Vanderpoorten & al., 2002): Allen & Risk 4761 (DUKE) European Russia, Vologda, Ignatov s. n. 22.IX.1990 (MHA) Altai, Zolotukhin s. n. 11.VII.1988 (MHA) Hong Kong, Li, s. n. 2003 (MHA) Mongolia, Ignatov 01-439 (MHA) Mongolia, Ignatov 01-39 (MHA)

Sourse/specimen (GB, GenBank — followed by the reference and if available — specimen, as cited)

AY009860 AY009791 AF509540 AY009858 AY683591 AY683594 AY683604 AY683590 AY683599

AF264046 AY762373

AY009849

AY683574

AF071845

trnL-F

AF168142 AY695744 AY695741 AY695743 AY695755 AY695745

AF168148 AY009790

AF516166

AJ288331 AY009801

AJ288328

ITS1

AF168148 AY009790 AF509838 AF168142 AY695772 AY695779 AY695768 AY695780 AY695773

AF516156

AJ288545 AY009801

AJ288542

ITS2

210

Rhytidiadelphus loreus (Hedw.) Warnst.

Species

APPENDIX 9.1 (Continued) Taxon Sampling and GenBank Accession Numbers

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Mongolia, Ignatov 01-3 (MHA) GB: (Cox & Newton, unpubl.) Australia, Streimann 52610 (H) GB: (Vanderpoorten & al., 2002): Fagerstén 5092 (DUKE) GB: (Pedersen & Hedenäs, 2002) Russia, Ural Mts., Ignatova 11/81? (H ex MHA) USA, Tan 92-158 (MHA) GB: (Chiang T.Y., unpubl.) GB: (Vanderpoorten & al., 2002): Buck 32594 (NY) GB: (Zhang & al., 2003) GB: (Cox & Hedderson, 1999) GB: (Vanderpoorten & al., 2002): Schofield and Hedderson 94870 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield 103470 (DUKE) GB: (Vanderpoorten & al., 2002): Schofield & Talbot 99701 (DUKE) GB: (Vanderpoorten & al., 2002): Belland & Schofield 17963 (DUKE) AY009854 AY009839 AY009838

AF023770 AY009855

AF161132

AY527136

AY009833 AF472481

AY683593 AF472484

AY999168

AY999168

AF168161 AF315074 AF168149

AF168136

AF168161 AF315074 AF168149

AF168136

AJ277225 AF176278 Aj416442

AY999176 AF168143

AY999176 AF168143

AJ288413 AF176278 AJ416442

AY695791

AY695762

Note: Distichophyllum (crispulum/pulchellum), Climacium (dendroides/americanum) and Thuidium (philibertii/tamariscinum) were included in analysis using trnL and ITS data from two different species (which we believe are closely related). Expanded version of this table (with references to publications) is on the supplemental CD.

Tomentypnum nitens (Hedw.) Loeske Warnstorfia exannulata (Bruch & al.) Loeske Warnstorfia fluitans (Hedw.) Warnst.

Thuidium delicatulum (Hedw.) Bruch & al. Thuidium philibertii Limpr. Thuidium tamariscinum (Hedw.) Bruch & al. Tomentypnum falcifolium (Renauld ex Nichols) Tuom.

Thelia asprella (Schimp.) Sull. & Lesq.

Straminergon stramineum (Kindb.) Hedenäs Taxiphyllum wissgrillii (Garov.) Wijk & Marg.

Stereodon (Hypnum) vaucheri (Lesq.) Lindb. ex Broth. Stereophyllum radiculosum (Hook.) Mitt.

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REFERENCES Ando, H. (1976) Studies on the genus Hypnum Hedw. (II). Journal of Science of Hiroshima University, Ser. B, Div. 2, Botany, 14: 165–207. Arikawa, T. (2004) A taxonomic study of the genus Pylaisia (Hypnaceae, Musci). Journal of the Hattori Botanical Laboratory, 95: 71–154. Brotherus, V. F. (1908) Musci, in Die natürlichen Pflanzenfamilien, Vol. 1(3) (ed. A. Engler and K. Prantl). Verlag von W. Engelmann, Leipzig, pp. 1009–1152. Brotherus, V. F. (1925) Musci, in Die natürlichen Pflanzenfamilien, Vol. 11, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–522. Buck, W. R. (1998) Pleurocarpous mosses of the West Indies. Memoirs of the New York Botanical Garden, 82: 1–400. Buck, W. R. and Crum, H. (1978) A re-interpretation of the Fabroniaceae with notes on selected genera. Journal of the Hattori Botanical Laboratory, 44: 347–369. Buck, W. R. and Crum, H. (1990) An evaluation of familial limits among the genera traditionally aligned with the Thuidiaceae and Leskeaceae. Contributions from the University of Michigan Herbarium, 17: 55–69. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. Shaw, A. J. and Goffinet, B.). University of Cambridge Press, Cambridge, pp. 71–123. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL–trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Budyakova, A. A., Ignatov, M. S., Yatsentyuk, S. P. and Troitsky, A. V. (2003 [2004]). Systematic position of Habrodon (Habrodontaceae, Musci) as inferred from nuclear ITS1 and ITS2 and chloroplast trnL intron and trnL–trnF spacer sequence data. Arctoa, 12: 137–150. Cech, T. R., Damberger, S. H. and Gutell, R. R. (1994) Representation of the secondary and tertiary structure of group I introns. Structural Biology, 1: 273–280. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (1999) A Checklist of the Mosses. Missouri Botanical Garden, St. Louis. Crum, H. and Anderson, L. E. (1981) Mosses of Eastern North America. Vols. 1, 2. Columbia University Press, New York. Fleischer, M. (1923) Die Musci der Flora von Buitenzorg, Band 4. E. J. Brill, Leiden, pp. 1105–1729. Gardiner, A., Ignatov, M., Huttunen, S. and Troitsky, A. (2005) On resurrection of the families Pseudoleskeaceae Schimp. and Pylaisiaceae Schimp. (Musci, Hypnales). Taxon, 54: 651–663. Gladstein, D. and Wheeler, W. (2001) POY documentation and command summary. Available at ftp://ftp.amnh.org/pub/molecular/poy. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Goffinet, B., Cox, C. J., Shaw, A. J. and Hedderson, T. J. (2001) The Bryophyta (mosses): Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Annals of Botany, 87: 191–208. Goloboff, P. A. (1994) NONA: A Tree Searching Program. Program and documentation, published by the author, Tucumán, Argentina. Hall, T. A. (1999) BioEdit: A user-friendly biological sequence alignment editor analysis program for Windows 95/98/NT. Nucleic Acids Symposium, Ser. 41: 95–98. He, S. (2005) A revision of the genus Leptopterigynandrum (Bryopsida, Leskeaceae). Journal of the Hattori Botanical Laboratory, 97: 1–38. Hedenäs, L. (1989) Some neglected character distribution patterns among the pleurocarpous mosses. Bryologist, 92: 157–163. Hedenäs, L. (1997a [1998]) An evaluation of phylogenetic relationships among the Thuidiaceae, the Amblystegiaceae, and the temperate members of the Hypnaceae. Lindbergia, 22: 101–113. Hedenäs, L. (1997b) A partial generic revision of Campylium (Musci). Bryologist, 100: 65–88. Hedenäs, L. (1999) New views of the relationships among European pleurocarpous mosses. Stuttgarter Beiträge zur Naturkunde, Serie A (Biologie), 589: 1–15.

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Hedenäs, L. (2004) Morphological and anatomical evidence suggest that “Hylocomiaceae” taxa belong to at least two clades. Journal of Bryology, 26: 125–135. Huelsenbeck, J. P. and Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17: 754–755. Huttunen, S. and Ignatov, M. S. (2004) Phylogeny of Brachytheciaceae (Bryophyta), based on morphology and sequence level data. Cladistics, 20: 151–183. Huttunen, S., Ignatov, M. S., Müller, K. and Quandt, D. (2004) Phylogeny and evolution of epiphytism in the three moss families: Meteoriaceae, Brachytheciaceae, and Lembophyllaceae. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 328–361. Ignatov, M. S. and Huttunen, S. (2002 [2003]) Brachytheciaceae (Bryophyta) — a family of sibling genera. Arctoa, 11: 245–296. Ignatov, M. S. and Ignatova, E. A. (2004) Moss Flora of the Middle European Russia. Vol. 2. KMK, Moscow (in Russian). Ireland, R. R. (1968) Pleuroziopsidaceae, a new family of mosses. Journal of the Hattori Botanical Laboratory, 31: 59–64. Ireland, R. R. and Buck, W. R. (1994) Stereophyllaceae. Flora Neotropica, 65: 1–50. Mathews, D. H., Sabina, J., Zuker, M. and Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Biology, 288: 911–940. Nixon, K. C. (1999a). Winclada (BETA) ver. 0.9.9. available at http://www.cladistics.com/about_winc.html. Nixon, K. C. (1999b) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics, 15: 407–414. Noguchi, A. (1972) Musci Japonici. IX. The Leskeaceae. Journal of the Hattori Botanical Laboratory, 36: 499–529. Noguchi, A. (1991) Illustrated Moss Flora of Japan, Part 4. Hattori Botanical Laboratory, Nichinan. Norris, D. H. and Ignatov, M. S. (2000) Observations on stem surface anatomy in Climacium and Pleuroziopsis (Climaciaceae, Musci). Arctoa, 9: 151–154. Pedersen, N. and Hedenäs, L. (2002) Phylogeny of the Plagiotheciaceae based on molecular and morphological evidences. Bryologist, 105: 310–324. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution, 57: 2226–2241. Smith, A. J. E. (1978) The Moss Flora of Britain and Ireland. University of Cambridge Press, Cambridge. Stark, L. R. (1987) A taxonomic monograph of Forsstroemia Lindb. (Bryopsida: Leptodontaceae). Journal of the Hattori Botanical Laboratory, 63: 133–218. Stech, M. and Frahm, J.-P. (2001) The systematic position of Ochyraea tatrensis (Hypnobartlettiaceae, Bryopsida) based on molecular data. Bryologist, 104: 199–203. Tsubota, H., Arikawa, T., Akiyama, H., De Luna, E., Gonzales, D., Higuchi, M. and Deguchi, H. (2002) Molecular phylogeny of hypnobryalean mosses as inferred from a large scale dataset of chloroplast rbcL, with special reference to the Hypnaceae and possibly related families. Hikobia, 13: 645–665. Tsubota, H., De Luna, E., Gonzales, D., Ignatov, M. and Deguchi, H. (2004) Molecular phylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcL sequences of mosses. Hikobia, 14: 149–170. Tuomikoski, R. and Koponen, T. (1979) On the generic taxonomy of Calliergon and Drepanocladus (Musci, Amblystegiaceae). Annales Botanici Fennici, 16: 213–227. Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002a) Circumscription, classification, and taxonomy of the Amblystegiaceae (Bryopsida) inferred from nuclear and chloroplast DNA sequence data and morphology. Taxon, 51: 115–122. Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002b) Phylogeny and morphological evolution of the Amblystegiaceae (Bryopsida). Molecular Phylogenetics and Evolution, 23: 1–21. Wheeler, W. (1996) Optimization alignment: The end of multiple sequence alignment in phylogenetics? Cladistics, 12: 1–9. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 34063415. www.bioinfo.rpi.edu/~zukerm/rna/node3.html.

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of 10 Phylogeny Hygrohypnum Lindb. Based on Molecular Data Gisela Oliván, Lars Hedenäs, and Angela E. Newton CONTENTS Abstract ..........................................................................................................................................215 10.1 Introduction...........................................................................................................................216 10.2 Material and Methods ..........................................................................................................217 10.2.1 Taxon Sampling........................................................................................................217 10.2.2 DNA Extraction and Sequencing .............................................................................217 10.2.3 Sequence Assembling and Alignment......................................................................217 10.2.4 Cladistic Analyses ....................................................................................................219 10.3 Results...................................................................................................................................219 10.4 Discussion.............................................................................................................................220 10.4.1 Discussion of the Main Well-Supported Clades......................................................222 10.4.1.1 Hygrohypnum styriacum to Palustriella decipiens ...................................222 10.4.1.2 Hygrohypnum bestii to H. polare .............................................................222 10.4.1.3 Hygrohypnum eugyrium–H. subeugyrium ................................................223 10.4.1.4 Hygrohypnum montanum to H. smithii ....................................................224 10.5 Conclusions...........................................................................................................................224 Acknowledgments ..........................................................................................................................225 References ......................................................................................................................................225

ABSTRACT The phylogeny of Hygrohypnum is reconstructed based on ITS1–2, trnL–trnF and atpB–rbcL sequences. The analyses were conducted with 15 species of Hygrohypnum and 6 species that were considered to be related to the genus Hygrohypnum on the basis of previous phylogenetic studies of Amblystegiaceae s. lat. Platyhypnidium riparioides was used as outgroup. This study shows >80% bootstrap support for two major clades, one with Hygrohypnum styriacum and H. luridum (the type of the genus) and the two species included as representatives of Amblystegiaceae s. str. (Drepanocladus polygamus and Palustriella decipiens), and the other with the remaining species of the genus, Platydictya jungermannioides, Campylophyllum halleri and the two taxa chosen as representatives of Calliergonaceae (Kanda) Vanderpoorten et al., Calliergon cordifolium and Warnstorfia exannulata. The results support the polyphyly of the genus suggested previously based on morphology and molecular data, and show that the morphological characters traditionally used to circumscribe the genus may reflect convergence.

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10.1 INTRODUCTION Hygrohypnum Lindb. is a medium-sized genus of pleurocarpous mosses associated with aquatic and semiaquatic habitats, traditionally placed in the family Amblystegiaceae Roth. The frequently repeated statement that the genus Hygrohypnum is characterized by having broad and shortly pointed to rounded-obtuse leaves and variously developed costae can certainly be applied to some mosses from other genera (Ochyra, 1999a) and many pleurocarpous mosses were given names under this genus. Thus, Wijk et al. (1962) compiled 60 specific and subspecific taxa published under Hygrohypnum. During the 1970s two works shed light on this obscurely circumscribed genus. Jamieson (1976) carried out an exhaustive worldwide revision of Hygrohypnum, using a large number of morphological and anatomical characters not employed before in this context. He retained only 16 species in Hygrohypnum and synonymized many subspecies and varieties, although he did not relocate most of the excluded taxa. At the same time Kanda (1976), in a revision of the Amblystegiaceae for Japan, split the genus into Hygrohypnum and Pseudohygrohypnum Kanda, on the basis of costa structure and habitat preferences, and placed these in a new subfamily of the Amblystegiaceae, the Hygrohypnoideae Kanda. However, despite these works, the circumscription of Hygrohypnum remained unclear, and many species were later described in this genus or transferred to it (e.g., Crum, 1985; Delgadillo et al., 1995; Frahm, 1996; Nishimura, 1985; Sharp and Crum, 1994; Vohra, 1980). The Checklist of the Mosses (Crosby et al., 1999) lists 33 species remaining in the genus, although many of them, especially those from Central and South America, have been transferred to other genera (e.g., Buck, 1997; Ochyra, 1999a, 1999b; Ochyra and Sharp, 1988). Mostly the species left in the genus are those that were previously recognized by Jamieson (1976), all of them of Holartic distribution, with the exception of Hygrohypnum luridum (cf. Hedenäs, 2003). Jamieson himself, after circumscribing Hygrohypnum, concluded by saying that he believed the genus was polyphyletic. This hypothesis was later confirmed by Hedenäs (1998), who carried out phylogenetic analyses employing 74 morphological and anatomical characters from 93 species representing the Thuidiaceae, the temperate Hypnaceae and the Amblystegiaceae, including 10 species of Hygrohypnum. The polyphyly of Hygrohypnum was also supported by recent molecular studies of the family Amblystegiaceae in the broad sense (Vanderpoorten et al., 2001, 2002a), which showed that this family is polyphyletic and contains the family Amblystegiaceae s. str. and Calliergonaceae (Kanda). These molecular studies included four of the more common species of Hygrohypnum, that were shown to be unrelated: the type species of the genus, H. luridum, belongs to the Amblystegiaceae s. str., H. ochraceum appears as sister to Calliergon–Warnstorfia–Hamatocaulis–Scorpidium (although without support), and H. smithii with Campylophyllum halleri as a clade sister to Tomentypnum. Also included was H. montanum, which appeared with Platydictya jungermannioides in a nonsupported clade sister to that containing the Calliergonaceae as defined in that study. Ignatov and Ignatova (2004) have made substantial nomenclatural changes in the genus Hygrohypnum. Only Hygrohypnum luridum was kept in the genus, while H. alpestre and H. cochlearifolium were transferred to the genus Ochyraea Vána, which had already been placed in the family Amblystegiaceae and suggested to be closely related to Hygrohypnum (Stech and Frahm, 2001a). Two species, H. ochraceum and H. duriusculum, were transferred to a new genus, Hygrohypnella Ignatov & Ignatova, included in a new family, Scorpidiaceae Ignatov & Ignatova, together with Scorpidium, Limprichtia, Hamatocaulis and Sanionia. Hygrohypnum subeugyrium was transferred to Pseudohygrohypnum Kanda, in the family Pylaisiaceae Schimp., along with Breidleria, Calliergonella, Callicladium, Stereodon, Ptilium, Homomallium and Pylaisia. These nomenclatural changes were based on the phylogenetic analyses of molecular data (Ignatov, personal communication, 2004), reported by Ignatov et al. (Chapter 9 in this volume). These analyses show several species of Hygrohypnum in four different clades, which correspond

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to the four genera segregated by Ignatov and Ignatova (2004). Ignatov et al. (Chapter 9) included some species of Hygrohypnum in large-scale analyses. However, the analyses conducted in the present study included all the species widely accepted to belong to the genus Hygrohypnum with the purpose of: (1) establishing the relationships among them and investigating the polyphyly of the genus previously suggested; (2) finding out which species could belong to the new family Calliergonaceae, and which ones to the Amblystegiaceae s. str.; (3) assessing the circumscription of the genus and comparing it with previous classifications.

10.2 MATERIAL AND METHODS 10.2.1 TAXON SAMPLING Fifteen species of Hygrohypnum were included in the analyses out of the 16 species that Jamieson (1976) retained in the genus. Based on the results of Vanderpoorten et al. (2001, 2002a, 2002b), the following species were also included: Calliergon cordifolium and Warnstorfia exannulata as representatives of Calliergonaceae, Drepanocladus polygamus and Palustriella decipiens as representatives of Amblystegiaceae s. str., Campylophyllum halleri as a representative of a well-supported clade with Hygrohypnum smithii, and Platydictya jungermannioides as it was linked with Hygrohypnum montanum in a nonsupported clade sister to the Calliergonaceae (Vanderpoorten et al., 2002b). Platyhypnidium riparioides was used as outgroup. Although the genus Platyhypnidium was sometimes associated with the Amblystegiaceae s. lat. (cf., Hedenäs, 2003), and some members of it were occasionally included in Hygrohypnum (e.g., Hygrohypnum validum Herzog), previous molecular analyses indicated a position of the genus Platyhypnidium in the Brachytheciaceae, and thus a separation from all other 21 taxa of the present study (e.g., Stech and Frahm, 2001b; Huttunen and Ignatov, 2004). Details of specimen vouchers and GenBank accession numbers are listed in Table 10.1.

10.2.2 DNA EXTRACTION

AND

SEQUENCING

DNA was extracted using an adapted protocol of Rogers and Bendich (1994). Double-stranded DNA templates were prepared by polymerase chain reaction (PCR). PCR was performed using a reaction mix of 47 μl (1 μl Taq polymerase, 5 μl buffer, 3 μl MgCl, 5 μl dNTPs, 2 μl of each primer, 30 μl distilled water). Betaine was added to the reaction mix for unsuccessful amplifications of ITS (12 μl betaine 5M for 50 μl of reaction mix). The primer combinations and PCR programs employed are described in Table 10.2. Amplified fragments were cleaned using the GFX PCR DNA and Gel Band Purification Kit (Amersham Biosciences), according to the manufacturer’s protocol, and eluted into 30 μl of distilled water. Cycle sequencing was performed using 5 μl of PCR product + water, 1 μl of each amplification primer in conjunction with 2 μl Big Dye Sequencing Reaction Mix and 2 μl of dilution buffer. The program used for the sequencing reaction was 28 cycles of 30 sec at 95ºC, 15 sec at 48ºC and 2 min at 60ºC. The final reactions were cleaned and sequenced at the sequencing facility in the Natural History Museum in London with a fully automated sequencing Perkin Elmer 377.

10.2.3 SEQUENCE ASSEMBLING

AND

ALIGNMENT

Assembling and editing of the sequences was conducted using SeqMan (Lasergene, DNA Star, Inc.) on a Macintosh computer. The assembled sequences were aligned using MegAlign (Lasergene, DNA Star, Inc.). The default settings for the “Clustal Method” of alignment (Gap opening cost = 10, Gap extension cost = 10) were used to form the alignment, which needed very little refinement by eye. Regions of ambiguous alignment and incomplete data at the beginning and end of sequences were identified and excluded from subsequent analyses. The resulting alignment was exported as a Nexus file.

H. norvegicum (Schimp.) J.J. Amann H. ochraceum (Turner ex Wilson) Loeske H. polare (Lindb.) Loeske H. smithii (Sw.) Broth. H. styriacum (Limpr.) Broth. H. subeugyrium (Renauld & Cardot) Broth. Platydictya jungermannioides (Brid.) H.A. Crum Calliergon cordifolium (Hedw.) Kindb. Warnstorfia exannulata (Schimp.) Loeske Campylophyllum halleri (Sw. ex Hedw.) M. Fleisch. Drepanocladus polygamus (Schimp.) Hedenas Palustriella decipiens (De Not.) Ochyra Platyhypnidium riparioides (Hedw.) Dixon

Hedenäs (S; B81980) Hedenäs (S; B81863) Schofield (S; B81888) Ignatov (S; B81890) Hedenäs (S; B81865) Hakelier (S; B20304) Hedenäs (S; B81975) Allen (S; B81897) Sidenvall, cf. Hedenäs (S; B81884) Sidenvall, cf. Hedenäs (S; B81885) Hedenäs (S; B81898) Hedenäs (S; B818976) Hedenäs (S; B6362) Hedenäs (S; B81869) Hakelier (S; B81902) Hakelier (S; B81904) Hedenäs (S; B63169) Hedenäs & Oliván (MACB88611) Fuertes, Acón & Oliván (MACB; 90035) Hedenäs (S; B39520) Hedenäs & Oliván (MACB; 90036) Hedenäs & Oliván (MACB; 90037) Hedenäs (S; B32421)

Voucher of Reference AY857574 AY857575 AY857576 AY857577 AY857578 AY857579 AY857580 AY857581 — AY857582 AY857583 AY857584 AY857585 AY857586 AY857587 AY857588 AY857589 AY857590 AY857591 AY857592 AY857593 AY857594 AY857595

atpB–rbcL GenBank Accession No. AY857553 AY857554 AY857555 AY857556 AY857557 AY857558 AY857559 AY857560 — AY857561 AY857562 AY857563 AY857564 AY857565 AY857566 AY857567 AY857568 AY857569 AY857570 AY857571 — AY857572 AY857573

trnL–F GenBank Accession No.

AY857596 AY857597 AY857598 AY857599 AY857600 — AY857601 AY857602 AY857603 — AY857604 AY857605 AY857606 AY857607 AY857608 AY857609 AY857610 AY857611 AY857612 AY857613 AY857614 AY857615 AY857616

ITS1–2 GenBank Accession No.

218

Hygrohypnum alpestre (Sw. ex Hedw.) Loeske H. alpinum (Lindb.) Loeske H. bestii (Renauld & Bryhn) Broth. H. cochlearifolium (Venturi) Broth. H. duriusculum (De Not.) D.W. Jamieson H. eugyrium (Schimp.) Broth. H. luridum (Hedw.) Jenn. H. molle (Hedw.) Loeske H. montanum (Lindb.) Broth.

Species

TABLE 10.1 Taxon Sampling and GenBank Accession Numbers

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TABLE 10.2 Primers and Programs Used for PCR Molecular Marker

Primer

Reference

PCR Program Melting step 5 min at 94ºC 30 cycles: 45 sec at 94ºC 1 min 15 sec at 57ºC 1 min 15 sec at 72ºC Final extension 10 min at 72ºC 30 cycles: 15 sec at 94ºC 30 sec at 50ºC 1 min at 72ºC Final extension 5 min at 72ºC Melting step 2 min at 94ºC 30 cycles: 30 sec at 94ºC 30 sec at 50ºC 2 min at 72º C Final extension 5 min at 72ºC

atpB–rbcL spacer

ATPB-1 RBCL-1

Chiang et al. (1998)

trnL (UAA) 5 exon– trnF (GAA) region

trnC trnF

Taberlet et al. (1991)

ITS1–2

AB101F (17SE) ITS4

Sun et al. (1994) Baldwin (1992)

10.2.4 CLADISTIC ANALYSES The data were analysed under equally weighted maximum parsimony criterion using PAUP 4.0b10 (Swofford, 2003). Analyses of all included species were performed with four different datasets: ITS data, trnL–trnF data, atpB–rbcL data, and all molecular data. Heuristic searches were performed with the following settings: all characters unweighted and unordered, random addition sequence with 1000 replicates, gaps coded as missing data, TBR branch swapping. When more than two shortest trees resulted from the analyses a strict consensus tree was constructed. Bootstrap analyses were conducted employing 1000 replicates, 100 random addition replicates per bootstrap replicate.

10.3 RESULTS Separate analyses of the ITS, trnL–trnF and atpB–rbcL sequences showed no conflict between clades resolved with >65% bootstrap support in any of the individual analyses, and the sequences were therefore combined. The combined analysis included 265 parsimony informative characters (Table 10.3). The analysis of the combined ITS, atpB–rbcL and trnL–trnF sequences gave six equally parsimonious trees (length = 1015, CI = 0.769, RI = 0.696). The strict consensus tree with bootstrap values is shown in Figure 10.1. The taxa included are divided into two main clades that are well supported: Hygrohypnum styriacum to Palustriella decipiens (Figure 10.1A), and Platydictya jungermannioides to Hygrohypnum smithii (the rest of the ingroup). The first clade, with 100% bootstrap support, contains four species including Hygrohypnum styriacum and H. luridum, which is the type of the genus Hygrohypnum. It also includes those taxa used as representatives of Amblystegiaceae s. str. (Drepanocladus polygamus and Palustriella decipiens) as defined in previous studies of Amblystegiaceae s. lat. (Vanderpoorten et al., 2001, 2002a, 2002b). The second clade, with 83% bootstrap support, includes the rest of the Hygrohypnum species, Platydictya jungermannioides, Campylophyllum halleri and the two taxa chosen as representatives

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TABLE 10.3 Total Number of Characters and Parsimony Informative Characters of the Genomic Regions Used in the Study Genomic Region

Total No. of Characters

Parsimony Informative Characters

ITS1–2 trnL–trnF atpB–rbcL spacer Combined regions

987 483 760 2230

203 25 37 265

of Calliergonaceae (Vanderpoorten et al., 2002a, 2002b), Calliergon cordifolium and Warnstorfia exannulata. Platydictya jungermannioides is basal in this clade, but the Calliergonaceae are resolved within the ingroup, although without support. Several subclades are supported with bootstrap values of greater than 95%: Hygrohypnum bestii to H. polare (99%; Figure 10.1B), Hygrohypnum eugyrium–H. subeugyrium (95%; Figure 10.1C) and Hygrohypnum montanum to H. smithii (99%; Figure 10.1D), the latter with two clades, Hygrohypnum montanum–Campylophyllum halleri (95%), and Hygrohypnum cochlearifolium to H. smithii, moderately well supported (77%), with seven Hygrohypnum species.

10.4 DISCUSSION The results of the present study show that Hygrohypnum is a polyphyletic genus since Hygrohypnum luridum, the type of the genus, and Hygrohypnum styriacum appear in a very well-supported clade with Amblystegiaceae s. str., while the rest of the genus (13 species) forms a clade that includes Calliergonaceae, Platydictya jungermannioides and Campylophyllum halleri. The polyphyly of the genus was previously suggested by Jamieson (1976). He produced a classification of Hygrohypnum that gave priority to variation in leaf shape, leaf symmetry, alar cell differentiation and the orientation of the leaves upon the stem. Jamieson’s classification system recognized two groups. The most cohesive one, which Jamieson called the “broad leafed” group, included the species with straight, orbicular to ovate and more or less concave leaves, i.e., Hygrohypnum alpinum, H. duriusculum, H. smithii, H. bestii, H. cochlearifolium, H. norvegicum and H. molle. The remaining species constituted a more heterogeneous group with straight or falcate, ovate to lanceolate leaves. Within the latter group Jamieson suggested that Hygrohypnum alpestre, H. luridum, H. styriacum and H. polare have certain affinity with the first group, while the position of Hygrohypnum closteri, H. montanum, H. ochraceum, H. eugyrium and H. subeugyrium in the genus is unclear. In addition, Jamieson carried out a numerical analysis of 24 qualitative morphological characters for 16 Hygrohypnum species, recognizing a total of 89 character states. These data were used to generate a similarity matrix with the percentages of similarity for each species pair, which were later subjected to cluster and ordination analyses (Figure 10.2). The result of these analyses gave some support for Jamieson’s broad leafed group, but the more heterogeneous group, and his idea of relationships amongst these latter species, received less support. Although Jamieson acknowledged the heterogeneity of the genus, he concluded that the result of his study was a better understanding of its morphological characters that would provide the basis on which to integrate new information in the future. Recent studies based on molecular data (Vanderpoorten et al., 2001; Ignatov et al., Chapter 9) and molecular and morphological data (Vanderpoorten et al., 2002a) have also suggested the polyphyly of Hygrohypnum. The resolution of the 15 species included in our study agreed to a large extent with the results of Vanderpoorten (2002a), with the exception that Hygrohypnum

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Platyhypnidium riparioides Hygrohypnum styriacum 100

Hygrohypnum luridum Drepanocladus polygamus

A

Palustriella decipiens Platydictya jungermannioides Hygrohypnum bestii 99

83

Hygrohypnum ochraceum

B

Hygrohypnum polare Calliergon cordifolium 95 Warnstorfia exannulata Hygrohypnum eugyrium 95

C

Hygrohypnum subeugyrium Hygrohypnum montanum 95 Campylophyllum halleri

89

99

Hygrohypnum cochlearifolium Hygrohypnum norvegicum

77

98

Hygrohypnum duriusculum Hygrohypnum molle Hygrohypnum alpestre Hygrohypnum alpinum

D

Hygrohypnum smithii

FIGURE 10.1 Strict consensus tree of six equally parsimonious trees (length = 1015, CI = 0.769, RI = 0.696) for 15 species of Hygrohypnum based on ITS, trnL–trnF and atpB–rbcL sequences. Numbers on branches are bootstrap support percentages (>65%). (A) to (D): Four main clades containing Hygrohypnum species (discussed in the text). Outgroup taxa are underlined.

montanum appears in a very well-supported clade (95% bootstrap) with Campylophyllum halleri, sister to the clade including the majority of species of Hygrohypnum (99% bootstrap) (Figure 10.1, clade D). Differences observed may reflect taxon sampling. Our results agree mostly with those showed by Ignatov et al. (Chapter 9). In both studies the species of Hygrohypnum are grouped in the same way in four main clades, except for Hygrohypnum duriusculum. In the present study H. duriusculum appears in a very well-supported clade (98% bootstrap) with H. molle in the main clade (Figure 10.1D), whereas in some of the analyses by

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Hygrohypnum alpinum Hygrohypnum duriusculum Hygrohypnum smithii Hygrohypnum cochlearifolium Hygrohypnum molle Hygrohypnum bestii Hygrohypnum ochraceum Hygrohypnum norvegicum Hygrohypnum styriacum Hygrohypnum montanum Hygrohypnum eugyrium Hygrohypnum subeugyrium Hygrohypnum luridum Hygrohypnum alpestre Hygrohypnum polare Hygrohypnum closteri

FIGURE 10.2 Cluster diagram resulting from a weighted pair group cluster analysis carried out from a similarity matrix based on 89 morphological character states from 16 species of Hygrohypnum (From Jamieson, D.W., 1976. A Monograph of the Genus Hygrohypnum Lindb. (Musci). Unpublished Ph.D. thesis, University of British Columbia, Vancouver.)

Ignatov et al. (Chapter 9) it is grouped with H. ochraceum and, with moderate support, H. polare. This discrepancy may be due to the taxon sampling, or could be an effect of the larger context of their study. However, although clades A–D (Figure 10.1) appear to be well-supported, neither of these two studies provides unambiguous evidence for the positions of the recognized clades in relation to other taxa.

10.4.1 DISCUSSION

OF THE

MAIN WELL-SUPPORTED CLADES

10.4.1.1 Hygrohypnum styriacum to Palustriella decipiens Clade A, Figure 10.1. In the light of this study and those of Vanderpoorten and coworkers (2001, 2002a) it seems that Hygrohypnum luridum and H. styriacum are the only species in the genus belonging to Amblystegiaceae s. str. These two species had not previously been considered closely related within the genus, except by Nyholm (1965). 10.4.1.2 Hygrohypnum bestii to H. polare Clade B, Figure 10.1. This clade includes Hygrohypnum bestii, H. ochraceum and H. polare, the only three dioicous species of the genus, and appears as sister to a larger clade containing Calliergon and Warnstorfia in a basal position, although without support, and separated from the Amblystegiaceae s. str. clade (containing Drepanocladus). This result agrees with Hedenäs et al. (2005), who reconstructed the relationships within the Calliergonaceae (sensu Vanderpoorten et al., 2002b),

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including H. ochraceum, based on molecular and morphological data. The results of Hedenäs et al. (2005) questioned the position of H. ochraceum in the family, as the inclusion of this species in the ingroup increased tree length and decreased consistency and retention indices as well as the support for the clade containing Hamatocaulis and Scorpidium, its possible closest relatives. Although their analyses show a low support for many suggested relationships, Ignatov and Ignatova, (2004) and Ignatov et al. (Chapter 9) place H. ochraceum and H. polare close not only to Scorpidium and Hamatocaulis, but also to Sanionia and Limprichtia, and suggest a new family for all of them, Scorpidiaceae. In addition H. ochraceum appeared with Sanionia uncinata in the molecular analyses carried out by Stech and Frahm (2001b) and Vanderpoorten et al. (2001). However, this is contradicted by the results obtained by Vanderpoorten et al. (2002a) when combining molecular and morphological data. This difference may be an effect of the inclusion of many morphological characters in the last study, in contrast to the use of no, or a few, morphological characters in the other studies. Traditionally Hygrohypnum bestii has been considered closely related to H. molle and H. duriusculum and has been treated as subspecies of H. molle (Grout, 1931; Crum and Anderson, 1981) due to its apparent morphological similarity. This relationship was contradicted by cluster and ordination analyses performed by Jamieson (1976) (Figure 10.2), which showed that Hygrohypnum bestii was related to H. ochraceum as they share some characters like the dioicous sexuality, the marginal leaf cells >60 μm and the costal and endostomial structure. However, and against this evidence, Jamieson defended the membership of H. bestii in the “broad leafed” group on the basis of characters such as leaf symmetry, leaf shape, leaf concavity, alar cell differentiation and attitude of the leaves upon the stem. The results of the present study support the placement of Hygrohypnum bestii together with the other dioicous species, demonstrating that the traditional morphological characters used to circumscribe the “broad leafed” group, considered the most cohesive group in the genus, may reflect convergence, while other disregarded morphological characters could be taxonomically informative. Hygrohypnum polare has been previously considered to have an isolated position in the genus due to its stout single percurrent costa (only sometimes present in H. luridum), its hyalodermis and dioicous condition. Moreover, although the rest of the species of Hygrohypnum grow always in or beside mountain streams or sometimes lakes, H. polare can be found not only in streams, but also in mountain fens with moving water (Nyholm, 1965), which made Jamieson (1976) suggest a transfer of this taxon to Calliergon or Drepanocladus. However, our results contradict this possibility as H. polare appears with H. bestii and H. ochraceum in a very well-supported clade (99% bootstrap). 10.4.1.3 Hygrohypnum eugyrium–H. subeugyrium Clade C, Figure 10.1. This is one of the clades that appear well supported in all the separate analyses. It is sister to the Hygrohypnum montanum to H. smithii clade (Figure 10.1D), although without support. Kanda (1976) transferred Hygrohypnum eugyrium and H. purpurascens, synonymized with H. subeugyrium by Jamieson (1976), to a new genus, Pseudohygrohypnum, which was recognized by Ignatov and Ignatova (2004) and placed in the family Pylaisiaceae. Our results agree with those of Ignatov et al. (Chapter 9) in separating H. eugyrium and H. subeugyrium from the rest of the species traditionally placed under Hygrohypnum. However, further large-scale analyses including these species seem to be necessary to thoroughly evaluate their taxonomic affinity before possibly transferring them to another genus. Jamieson (1976) found in the cluster analyses (Figure 10.2) that Hygrohypnum eugyrium and H. subeugyrium exhibited the highest degree of similarity between any two species in the genus. In fact, these species have often been confused, and can be separated only on the basis of their alar cells, stem anatomy and the nature of the vegetative leaf apices.

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10.4.1.4 Hygrohypnum montanum to H. smithii Clade D, Figure 10.1. This clade contains most of the species of Hygrohypnum and Campylophyllum halleri, and includes those species transferred to the genus Ochyraea by Ignatov and Ignatova (2004), i.e., Hygrohypnum alpestre and H. cochlearifolium, as well as H. molle, H. alpinum and H. duriusculum. This last species was placed by Ignatov and Ignatova (2004) with H. ochraceum in the genus Hygrohypnella. The close relationship between Hygrohypnum and Ochyraea was suggested by Stech and Frahm (2001a) on the basis of molecular data. They found that O. tatrensis Vána and H. smithii had identical trnLUAA sequences and differed only in two substitutions for ITS2 sequences. However, they decided to keep the genus Ochyraea as separate from Hygrohypnum on the basis of the polyphyly of the latter, and on the presence of a polystratose lamina and paraphyllia in Ochyraea, characters which have never been found in any of the Hygrohypnum species. Clade D appears within the large clade containing Calliergonaceae, and separated from the Amblystegiaceae s. str., which contradicts the placement of Hygrohypnum alpestre and H. cochlearifolium in the Amblystegiaceae by Ignatov and Ignatova (2004). Within clade D there are two well-supported clades: Hygrohypnum montanum–Campylophyllum halleri. This result supports the morphological similarity pointed out by Nyholm (1965) and Hedenäs (1998) between these two species. Both species possess plane or weakly plicate perichaetial leaves and entire to serrulate and recurved leaf margins, and are similar in size, although they live in different habitats. In experimental cultures carried out by Jamieson (1976) H. montanum, which usually has falcate and loosely imbricate leaves, produced straight and distantly spaced leaves, with a resemblance to several species of Campylium s. lat. Hygrohypnum cochlearifolium to H. smithii. This moderately supported clade (77%) includes seven species of the genus: Hygrohypnum cochlearifolium, H. norvegicum, H. duriusculum, H. molle, H. alpestre, H. alpinum and H. smithii. Except for the absence of Hygrohypnum bestii and the presence of H. alpestre, this group is that which Jamieson (1976) called the “broad leafed” group, characterized by possessing straight, orbicular to ovate leaves, which are shallowly to deeply concave, julaceous shoots, alar cells undifferentiated (except in H. alpinum and H. duriusculum), autoicous sexuality and a well-developed central strand. Except for its dioicous sexuality and the lack of a well-developed central strand H. bestii fitted very well in this group. However, as mentioned above, this similarity is only apparent, and other morphological and anatomical characters, less obvious than leaf shape and symmetry, place it closer to H. ochraceum. Hygrohypnum alpestre shares the rest of the characters of the broad leafed group and Jamieson (1976) suggested the likely closeness, but again preferring leaf characters, did not include it because of its oblong to oblonglanceolate leaves. Within this clade there are two well-supported clades, Hygrohypnum cochlearifolium–H. norvegicum and Hygrohypnum duriusculum–H. molle. Hygrohypnum cochlearifolium and H. norvegicum have been traditionally considered as closely related (Nyholm, 1965), and small forms of H. cochlearifolium have been frequently identified as H. norvegicum, as only the size and grade of concavity have been used to differentiate them. The morphological similarity between Hygrohypnum molle and H. duriusculum is also very high, with forms of these species that are very difficult to separate. Many authors have considered H. duriusculum as a subspecies of H. molle. This close relationship is reflected in our analyses where these species had the highest bootstrap support (98%) of any species pair.

10.5 CONCLUSIONS The results of the present study suggest that a revision of the genus is necessary, but we think that further nomenclatural changes would be premature at this point. Inclusion of a large set of mor-

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phological, anatomical and ecological characters, and further sampling especially among closely related taxa (Tomentypnum species, Ochyraea tatrensis, Sanionia species and the rest of the Campylophyllum species) are required to fully develop the implications of this work and to either confirm the nomenclatural changes already made (e. g., Ignatov and Ignatova, 2004) or to establish a new classification of Hygrohypnum.

ACKNOWLEDGMENTS This study was funded by SYS-RESOURCE under the EC-funded IHP program. We thank Steve Russell, manager of the Botany Molecular Laboratory of the Natural History Museum in London.

REFERENCES Baldwin, B. G. (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: An example from the Compositae. Molecular Phylogenetics and Evolution, 1(1): 3–16. Buck, W. R. (1997) Schofieldiella (Hylocomiaceae), a new genus for an old species. Journal of the Hattori Botanical Laboratory, 82: 39–46. Chiang, T. I., Schaal, B. A. and Peng, C.-I. (1998) Universal primers for amplification and sequencing a noncoding spacer between the atpB and rbcL genes of chloroplast DNA. Botanical Bulletin of Academia Sinica, 39: 245–250. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (2000) A Checklist of the Mosses. Missouri Botanical Garden, St. Louis. Crum, H. A. (1985) Two undescribed species of Hygrohypnum from Mexico. Bryologist 88: 22–23. Crum, H. A. and Anderson, L. E. (1981) Mosses of Eastern North America, Vol. 2, Columbia University Press, New York. Delgadillo, M. C., Bello, B. and Cárdenas, S. A. (1995) LATMOSS. A Catalogue of neotropical mosses. Monographs in Systematic Botany from the Missouri Botanical Garden 56: 1–191. Frahm, J. P. (1996) Revision der Gattung Rhacocarpus Lindb. (Musci). Cryptogamie, Bryologie, Lichénologie, 17: 39–65. Grout, A. J. (1931) Moss Flora of North America and North Mexico, Vol. III, Part 2, published by the author, New York. Hedenäs, L. (1998) An evaluation of phylogenetic relationships among the Thuidiaceae, the Amblystegiaceae, and the temperate members of the Hypnaceae. Lindbergia, 22: 101–133. Hedenäs, L. (2003) Amblystegiaceae (Musci). Flora Neotropica, Monograph 89: 1–107. Hedenäs, L., Oliván, G. and Eldenäs, P. (2005) Phylogeny of Calliergonaceae (Bryophyta) based on molecular and morphological data. Plant Systematics and Evolution, 252: 49–61. Huttunen, S. and Ignatov, M. S. (2004) Phylogeny of the Brachytheciaceae (Bryophyta) based on morphology and sequence level data. Cladistics, 20: 151–183. Ignatov, M. S. and Ignatova, E. A. (2004) Flora mkhov srednei chasti evropeiskoi Rossii. Tom 2. Fontinalaceae–Amblystegiaceae. Arctoa, a Journal of Bryology, 11(Supplement 2): 609–960. Jamieson, D. W. (1976) A Monograph of the Genus Hygrohypnum Lindb. (Musci). Unpublished Ph.D. thesis, University of British Columbia, Vancouver. Kanda, H. (1976) [1977] A revision of the family Amblystegiaceae of Japan II. Journal of Science of Hiroshima University, Series B, Division 2 (Botany), 16: 47–119. Nishimura, N. (1985) A revision of the genus Ctenidium. Journal of the Hattori Botanical Laboratory, 58: 1–82. Nyholm, E. (1965) Illustrated Moss Flora of Fennoscandia II, Musci, Fasc. 5, C. W. K. Gleerup, Lund. Ochyra, R. (1999a) The identities of three neotropical species of Hygrohypnum (Musci, Amblystegiaceae). Fragmenta Floristica et Geobotanica, 44 (2): 261–268. Ochyra, R. (1999b) New combinations in neotropical mosses. Fragmenta Floristica et Geobotanica, 44: 255–259. Ochyra R. and Sharp A. J. (1988) Results of a bryogeographical expedition to East Africa in 1968, IV. Journal of the Hattori Botanical Laboratory, 65: 335–377. Rogers, S. O. and Bendich, A. J. (1994) Extraction of total cellular DNA from plants, algae and fungi. In Plant Molecular Biology Manual, D1, Ed. 2 (ed. S. B. Gelvin and R. A. Schilperoort). Kluwer Academic Press, Dordrecht, The Netherlands, pp. 1–8.

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Sharp, A. J. and Crum, H. A. (1994) Amblystegiaceae. In Moss Flora of Mexico (ed. A. J. Sharp et al.). Memoirs of the New York Botanical Garden, 69: 886–909. Stech, M. and Frahm J.-P. (2001a) The systematic position of Ochyraea tatrensis (Hypnobartlettiaceae, Bryopsida) based on molecular data. Bryologist, 104: 199–203. Stech, M. and Frahm J.-P. (2001b) Palustriella pluristratosa spec. nov. (Amblystegiaceae, Bryopsida), a new aquatic moss species with pluristratose lamina from Switzerland. Botanica Helvetica, 111: 139–150. Sun, Y., Skinner, D. Z., Liang, G. H. and Hulbert, S. H. (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theoretical and Applied Genetics, 89: 26–32. Swofford, D. L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4, Sinauer Associates, Sunderland, Massachusetts. Taberlet, P., Gielly, L., Pautou, G. and Bouvet, J. (1991) Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Molecular Biology, 17: 1105–1109. Vanderpoorten, A., Shaw, A. J. and Goffinet, B. (2001) Testing controversial alignments in Amblystegium and related genera (Amblystegiaceae: Bryopsida). Evidence from rDNA ITS sequences. Systematic Botany, 26(3): 470–479. Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002a) Phylogeny and morphological evolution of the Amblystegiaceae (Bryopsida). Molecular Phylogenetics and Evolution, 23(1): 1–21. Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002b) Circumscription, classification, and taxonomy of Amblystegiaceae (Bryopsida) inferred from nuclear and chloroplast DNA sequence data and morphology. Taxon, 51: 115–122. Vohra, J. N. (1980) New taxa of Hypnobryales (Musci) from the Himalayas. Bulletin of the Botanical Survey of India, 22: 115–125. Wijk, R. Van Der, Margadant, W. D. and Florschütz, P. A. (1962) Index Muscorum, volume II (D-Hypno). Regnum Vegetabile, 26: 1–535.

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Characters and 11 Morphological Their Use in Pleurocarpous Moss Systematics Lars Hedenäs CONTENTS Abstract ..........................................................................................................................................227 11.1 Introduction...........................................................................................................................228 11.2 Principles of Pleurocarpous Moss Classification through Time .........................................229 11.2.1 The “Key Morphological Character” Stage.............................................................229 11.2.2 The “All Morphological Characters” Stage .............................................................229 11.2.2.1 Inferring Relationships Based on Overall Similarity ...............................229 11.2.2.2 Inferring Relationships Based on Shared Derived Character States, Synapomorphies.............................................................................230 11.2.3 The Molecular Stage ................................................................................................230 11.2.4 The “Total Evidence” Stage.....................................................................................230 11.3 Changing Classifications Reflect Changing Classification Principles.................................231 11.3.1 The Leucodontales (or Isobryales)...........................................................................231 11.3.2 Calliergon, Campylium, Drepanocladus and Scorpidium .......................................232 11.4 Correspondence between Morphological and Molecular Data ...........................................233 11.4.1 The Brachytheciaceae, Hylocomiaceae, Ctenidiaceae and Heterocladioideae .....................................................................................................233 11.4.2 The Plagiotheciaceae ................................................................................................233 11.4.3 The Amblystegiaceae, Thuidiaceae and Temperate Members of the Hypnaceae.................................................................................................................235 11.4.4 The Hookeriales, Sematophyllaceae and Ptychomniales ........................................236 11.4.5 Some Genus-Level Relationships ............................................................................236 11.5 Problems with the Interpretation of Some Sporophyte Characters.....................................237 11.6 Concluding Remarks ............................................................................................................240 Acknowledgments ..........................................................................................................................240 References ......................................................................................................................................241

ABSTRACT Morphology has been the primary source of information regarding pleurocarpous moss relationships for the past approximately 200 years. Originally, a few “key characters” were used to infer relationships, and only relatively recently have numerous characters been studied systematically in numerous species. During the last 20 years cladistics and the inclusion of molecular data for phylogenetic reconstruction have been revolutionary for our understanding

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of pleurocarpous moss relationships. Since the molecular information used is largely independent of morphology, the reliability of the latter in reconstructing relationships can now be assessed. Relationships that are well supported by molecular data are frequently suggested by morphology. Morphology yields more ambiguous results than molecular data, most likely due to incorrect interpretations of homology. The latter is especially serious for taxa with orthotropous (earlier called “erect”), specialized spore capsules. Morphology sometimes reveals relationships that have not yet been resolved by molecular data, and molecular phylogenies can be fully interpreted only in the light of structural similarities or differences between taxa.

11.1 INTRODUCTION When modern molecular methods were introduced to reconstruct relationships among pleurocarpous mosses, the use of morphology and anatomy in inferring phylogenetic relationships decreased drastically. This is easy to understand because the large amounts of molecular data that quickly accumulated have made it possible to advance our knowledge of pleurocarpous moss relationships at a rate that could not even have been dreamt of as recently as 20 years ago. However, when only molecular data are used in phylogenetic analyses, the meaning of the results is frequently unclear, or makes sense only when the morphology, anatomy or habitats of the included taxa are considered. For this reason the value of morphology for our understanding of how pleurocarps are related to each other and how they function in nature has started to be appreciated again. It is therefore important to review the value of morphological and anatomical characters in assessing the relationships among pleurocarpous mosses. Relatively detailed morphological and anatomical information has been available for studies of pleurocarpous moss relationships since the work of Hedwig (1782, 1785–1787, 1789, 1791–1792, 1797, 1801). For around 200 years after Hedwig, morphological characters were almost the only available sources of evidence regarding relationships. The way characters were studied and interpreted changed only slowly during most of this time. Only recently has the theoretical framework around phylogenetic reconstruction changed from an overall similarity approach to the cladistic method that uses only shared derived character states as evidence of a common descent. Although cladistic methods for phylogenetic reconstruction of bryophyte relationships were first employed more than 35 years ago (Koponen, 1968), it was a long time before bryologists started to use the method more widely (cf. Mishler, 1986). For pleurocarpous mosses, examples of cladistic or semicladistic approaches can be found in a discussion of higher-level relationships among pleurocarpous mosses (Buck and Vitt, 1986), a revision of the Hylocomiaceae (Rohrer, 1985), a treatment of the relationships between Thuidiaceae and Amblystegiaceae species (Hedenäs, 1989c), and a cladistic analysis of relationships among Rigodium species and their relationships to other members of the Leskeacanae (Zomlefer, 1993). Only later were the higher-level phylogenetic relationships among the pleurocarpous mosses more widely addressed using cladistic methods and based on morphological characters (cf. Hedenäs, 1994, 1995, 1996, 1997a, 1998b; Hedenäs and Buck, 1999). During recent years, molecular methods have become widely employed, thus providing much data that are supposedly largely independent from morphology and anatomy. The number of molecular studies assessing pleurocarp relationships at various levels has therefore, not surprisingly, increased enormously during the last few years (for example, Arikawa and Higuchi, 2003; Buck et al., 2000a, 2000b; De Luna et al., 2000; Newton and De Luna, 1999; Pedersen and Hedenäs, 2002; Tsubota et al., 2001, 2002; Vanderpoorten et al., 2002, 2003). In this chapter, the value and use of morphological data for reconstructing relationships among pleurocarpous mosses will be reviewed, keeping in mind both the evidence available and the theoretical framework prevailing at the different time periods.

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11.2 PRINCIPLES OF PLEUROCARPOUS MOSS CLASSIFICATION THROUGH TIME 11.2.1 THE “KEY MORPHOLOGICAL CHARACTER” STAGE Current systems of classification of pleurocarpous mosses, including those employed in many of our modern floras (for example, Crum and Anderson, 1981; Noguchi, 1989, 1991, 1994; Nyholm, 1960, 1965; Smith, 1978), are generally similar to those of Fleischer (1906–1908, 1915–1922) and Brotherus (1924, 1925). These systems of classification are based on relatively few “key characters,” such as the appearance of the costa of the vegetative leaves, the shape of the median leaf lamina cells, the presence or absence of leaf cell papillae, the presence or absence of paraphyllia, and whether the shoots are flattened or not. In the sporophyte, the degree of peristome specialization was considered, but not all the differences that exist between different types of perfect peristomes. Additionally, habitat preferences, for example, whether species occur in dry or wet habitats, were taken into account. It is easy to imagine that these characters were appealing when good microscopes were nonexistent or rare, and because they are easily observed in the field, but their persistent use in many systems of classifications, up to the present, must to some degree be explained by traditionalism. Although “key character”-based reclassifications have become fairly rare during the last decades, the erection of the families Pleuroziopsidaceae (Ireland, 1968) and Hypnobartlettiaceae (Ochyra, 1985) may serve as relatively recent examples of this tradition.

11.2.2 THE “ALL MORPHOLOGICAL CHARACTERS” STAGE 11.2.2.1 Inferring Relationships Based on Overall Similarity Accompanying the accumulation of information about character variation, researchers working with pleurocarpous mosses gradually started to realize that “key character”-based classifications may not reflect the true relationships among taxa. Although a few early bryologists included a relatively complete set of the known morphological and anatomical characters in inferring relationships, especially Loeske (1907) in his paper on Drepanocladus and related or similar taxa, this must be regarded as exceptional. Towards the end of the twentieth century many systematic studies of selected characters were performed across numerous groups of pleurocarpous mosses. Thus, several papers have appeared that discussed rhizoids or rhizoid topography (for example, Crundwell, 1979; Hedenäs, 1987a, 1989c; Tuomikoski and Koponen, 1979), pseudoparaphyllia, and potentially analogous or homologous structures (e.g., Akiyama, 1990a, 1990b; Akiyama and Nishimura, 1993; Ireland, 1971; Nishimura and Matsui, 1990a, 1990b), leaf costa (Kawai, 1968), paraphyllia (Rohrer, 1985), axillary hairs (Hedenäs, 1990), stem structure (Kawai, 1971, 1976, 1977b, 1978; Watanabe and Kawai, 1975), and the ontogeny of various parts (e.g., Frey, 1970, 1972, 1974a, 1974b; Hedenäs, 1987b; Kawai, 1977a). Tuomikoski and Koponen (1979) investigated perichaetial branch characters, such as the presence or absence of paraphyses, or whether the perichaetial leaves are plicate or smooth, and sporophytic characters, such as the presence or absence of a separating annulus, or the ornamentation of the outer surface of the lower exostome, among species of Calliergon, Drepanocladus and Scorpidium. Stomatal pore shape, capsule shape, exostome colour, the appearance of the exostome border, process perforations and spore maturation time were the subjects of other studies (Hedenäs, 1989c; Paton and Pearce, 1957; also cf. Arnell, 1875). As attention was drawn to the usefulness of numerous nontraditional characters in the systematics of pleurocarps, modern revisions have tended to consider more complete sets of characters for classifications of taxa rather than only a few characters that are immediately apparent. Examples at different taxonomic levels include the revisions of Ctenidium (Nishimura, 1985), Gollania (Higuchi, 1985), the Calliergon-Scorpidium-Drepanocladus complex (for example, Hedenäs, 1989a, 1989b, 1992a, 1993; Tuomikoski and Koponen, 1979), Cratoneuron (Ochyra, 1989), the

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Entodontaceae (Buck, 1980), the Hookeriales (Buck, 1988), the Meteoriaceae (Buck, 1994), the Phyllogoniaceae (Lin, 1983a, 1983b), and the Plagiotheciaceae (Buck and Ireland, 1985). 11.2.2.2 Inferring Relationships Based on Shared Derived Character States, Synapomorphies The two major advantages of the cladistic method for phylogenetic reconstruction, compared with the overall similarity approach, are the implicit necessity to clearly state which characters are used and how they are interpreted, and the fact that the hypotheses of common origin are based strictly on shared derived character states, rather than just on similar appearances. Without doubt, the cladistic approach forces the systematists, including those investigating the pleurocarps, to account much more clearly for the reasons behind their system of classification than was the case earlier. Scattered cladistic studies of pleurocarpous mosses that were based on morphological and anatomical characters were published in the 1980s (e.g., Hedenäs, 1989c; Ramsay, 1987; Rohrer, 1985), and after this period the frequency of papers based on cladistic studies increased markedly (e.g., Granzow-de la Cerda, 1992; Zomlefer, 1993; Hedenäs, 1994, 1995, 1996, 1997a, 1998b, 2004; Hedenäs and Buck, 1999; Hyvönen and Enroth, 1994; Pedersen and Hedenäs, 2001). General features of morphology-based cladistic analyses are the relatively poor resolution of relationships and few well-supported clades in terms of bootstrap or jackknife support values. In addition, relatively low values of the consistency index suggest comparatively high levels of homoplasy (Hedenäs, 1998a). These weaknesses imply that the data put into the morphology-based analyses are, to a relatively high degree, incorrectly interpreted. We are simply not yet knowledgeable enough to separate the many analogous similarities from homologous ones. Nevertheless, before molecular data became available, morphology and anatomy provided almost all the data that could be used for reconstructing the phylogeny of the pleurocarps.

11.2.3 THE MOLECULAR STAGE Although molecular data seemingly bypasses many of the problems associated with the interpretation of morphological characters, such as the interpretational biases of the latter, or problems associated with the evolutionary interpretation of complexes of correlated character states, molecular studies based on single coding or noncoding regions are sometimes used uncritically to infer relationships among taxa. Most researchers now realize that molecular data also have weaknesses, especially when limited sets from single genomes are evaluated, and selected examples from a phylogeny of the Hypnales that was suggested by rbcL data will be used to illustrate this (Tsubota et al., 2002). It should be noted that this phylogeny is used only to demonstrate the weakness of single marker molecular phylogenies, not to suggest otherwise poor quality of this particular study. In the cladograms resulting from this study, members of both the Plagiotheciaceae and the Hylocomiaceae are spread among two or several clades (Figure 11.1), and several clades, marked with boxes in Figure 11.1, include taxa of very different appearances. Morphologically some of these results make little sense, even if the support for some of the suggested relationships was moderately strong to strong. This example demonstrates that results from cladistic analyses of limited molecular datasets may not be more reliable than limited morphological and anatomical datasets, and that neither should be used uncritically for suggesting relationships among taxa.

11.2.4 THE “TOTAL EVIDENCE” STAGE The “total evidence” stage is here defined as the stage where morphological, anatomical, habitatrelated, molecular and other characteristics likely to be inheritable (cf. Grandcolas et al., 2001) are considered in order to give us a more complete understanding of the relationships among the organisms. Although there are presently few groups of pleurocarpous mosses for which relatively

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Climacium Pleuroziopsis Stereophyllaceae Neodolichomitra Tomentypnum Brachytheciaceae Plagiothecium Hylocomiastrum Pleurozium Meteoriaceae Myurium hochstetteri Sciaromium tricostatum Ctenidium Hylocomium s.str. Loeskeobryum Rhytidiadelphus Antitrichia formosana Prionodon densus Isopterygium vineale Anomodon rugelii Herzogiella perrobusta Leucodon-Pterobryon-Cryphaea Hypnaceae (mainly temperate) Boulaya Isopterygiopsis Orthothecium Abietinella Thuidium Entodon Sematophyllaceae

FIGURE 11.1 Some of the relationships among Hypnalean taxa suggested by a cladistic analysis of rbcL data (Tsubota et al., 2002).  = moderately well-supported node;  = well-supported node. Vertical double lines indicate portions with several representatives that were summarized in the figure. Taxa that have been suggested to belong to the Hylocomiaceae (Hedenäs, 2004) are in bold and taxa belonging to the Plagiotheciaceae (Pedersen and Hedenäs, 2002) are in italics. Boxes indicate clades with morphologically very diverse taxa.

complete data exist, the aim must be to include at least all kinds of data that are available in order to arrive at the most reliable hypotheses regarding pleurocarpous moss relationships.

11.3 CHANGING CLASSIFICATIONS REFLECT CHANGING CLASSIFICATION PRINCIPLES The improved methodologies have gradually made our classifications of pleurocarpous mosses better in the sense that they more and more reflect what is likely to be true phylogenetic relationships among the taxa. The following two examples serve as illustrations for this.

11.3.1 THE LEUCODONTALES (OR ISOBRYALES) Three “key character” states, namely, an orthotropous capsule (often called “erect,” cf. below and Figure 11.4), the narrow and usually gradually tapered exostome teeth, and a reduced endostome, have long been used to circumscribe the order Leucodontales (e.g., Brotherus, 1924, 1925; Fleischer, 1902–1904, 1906–1908, 1915–1922, 1920). Additional studies using numerous morphological characters obviously did not amass enough evidence to overturn the earlier ideas regarding the circumscription of this order as late as the middle of the 1980s (Buck and Vitt, 1986). Whereas “overall similarity” could not convincingly refute the “key character”-based circumscription of the Leucodontales, cladistic studies based on morphological evidence clearly did not support the recognition of a monophyletic Leucodontales (e.g., Hedenäs, 1995, 1998a). This is most likely due

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TABLE 11.1 The Character States Circumscribing Calliergon, Campylium, Drepanocladus and Scorpidium as These Genera Were Traditionally Defined Character

Calliergon

Campylium

Drepanocladus

Leaf apex Leaf concavity Leaf orientation Costa

Rounded Concave Straight Single, long

Acuminate Concave Squarrose Varying

Acuminate Concave Falcate Single, long

Scorpidium Acute to rounded-apiculate Strongly concave Straight or falcate Short, double

to a combination of an accumulation of additional character data and the use of cladistic methodology that together are better than “overall similarity” for data evaluation. Nowadays it is widely recognized that both morphological (e.g., Hedenäs, 1995, 1998a) and molecular evidence (e.g., Buck et al., 2000a; De Luna et al., 2000; Huttunen et al., 2004; Tsubota et al., 2002) show this order is paraphyletic and should therefore not be recognized.

11.3.2 CALLIERGON, CAMPYLIUM, DREPANOCLADUS

AND

SCORPIDIUM

Several genera from the families Amblystegiaceae and Calliergonaceae provide a good example of a “key character”-based classification. Numerous species were earlier placed in the four genera Calliergon, Campylium, Drepanocladus and Scorpidium according to a few characters of their vegetative leaves (Table 11.1; cf. Crum and Anderson, 1981; Karczmarz, 1971; Nyholm, 1965; Smith, 1978; Wynne, 1944). Even if Loeske (1907) had attempted a broader approach it was only later, when significant amounts of new evidence had accumulated, that numerous studies suggested a radical rearrangement of the species (cf. Hedenäs, 1989a, 1989b, 1992a, 1993, 1997b, 1997c, 1998c, 2003; Tuomikoski and Koponen, 1979). The explanatory power of the new classification became much greater than that based on “key characters” (cf., Hedenäs, 2001b), and made the maintenance of the old genera untenable. The novel classification did, in addition, appear to make more sense from the ecological point of view (Hedenäs and Kooijman, 1996). Whereas the knowledge of the generic placement of members of the four traditionally circumscribed genera only tells us that their habitat is probably wet, the corresponding knowledge for the member of any one of the newly defined genera, in addition, provides information regarding the mineral concentration and/or nutrient status of the habitat. A true cladistic evaluation of the generic concepts based only on morphological data has not been published for the Amblystegiaceae s. lat. However, the result of an analysis based solely on the morphological component of the total data in the Calliergonaceae study of Hedenäs et al. (2005) is instructive. In this case, Calliergon, Hamatocaulis, Loeskypnum and Scorpidium appeared as monophyletic genera, although bootstrap and jackknife support for Scorpidium were absent, and in addition a well-supported clade with Calliergon, Loeskypnum, Straminergon and Warnstorfia members was present. Resolution of the cladogram was thus relatively poor. For the relationships among the Amblystegiaceae s. lat., analyses based on both molecular and morphological data showed unambiguously that the traditional classification of species in the genera Calliergon, Campylium, Drepanocladus and Scorpidium is untenable and that their species should in fact be distributed among two different monophyletic groups that are best recognized as the families Amblystegiaceae and Calliergonaceae, respectively (Vanderpoorten et al., 2003, 2002). Internal relationships in these families are treated in more detail by Hedenäs and Vanderpoorten (in this volume).

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11.4 CORRESPONDENCE BETWEEN MORPHOLOGICAL AND MOLECULAR DATA The value of morphological and anatomical data in systematics can be assessed when the implications from relatively complete sets of such data are compared with those from molecular evidence. In the following a number of suggested systematic treatments based on morphology and anatomy are therefore compared with available results based on molecular data.

11.4.1 THE BRACHYTHECIACEAE, HYLOCOMIACEAE, CTENIDIACEAE AND HETEROCLADIOIDEAE The members of these families appeared to form a non-basal grade in a morphological study of 66 representatives from throughout the pleurocarps (Hedenäs, 1995). Although placed far from each other in most recent treatments (e.g., Buck and Vitt, 1986; Crum and Anderson, 1981; Nyholm, 1960, 1965; Smith, 1978), no doubt due to their different gametophytic characteristics, members of these families that have unspecialized sporophytes actually share numerous features of their sporophytes and perichaetia. Character states that are typical for this grade are described in Table 11.2. The most strikingly similar states are the nonplicate perichaetial leaves with spreading to squarrose upper portions, the typical Brachythecium-like capsule shape, the round-pored stomata, the frequently red or reddish lower exostome in newly dehisced capsules, the exostome border gradually narrowed upwards, the widely split endostome processes, and the spore maturation time during the winter season (late autumn to early spring in species from temperate areas). The few members of Meteoriaceae (including Trachypodaceae; cf. Huttunen et al., 2004) that were included in Hedenäs’ (1995) study were either placed close to members of the Brachytheciaceae, Hylocomiaceae, Ctenidiaceae or Heterocladioideae (Duthiella), or together with “Leucodontales” species that have specialized, orthotropous capsules (Aerobryopsis, Floribundaria). Molecular and morphological evidence combined (Huttunen et al., 2004) support a close relationship of most of the above taxa, including the Meteoriaceae, which were considered problematic in Hedenäs’ (1995) study because species with unspecialized and specialized sporophytes appeared to have different ancestors, even if the characters of their vegetative gametophytes suggested otherwise.

11.4.2 THE PLAGIOTHECIACEAE The circumscription of the Plagiotheciaceae has been repeatedly discussed during the past 20 years, after it was suggested that only Plagiothecium belongs in the family (Buck and Ireland, 1985). Based on overall similarity, it was later shown that numerous unique or almost unique character states indicate a close relationship between Plagiothecium and a number of taxa that have been placed in very different families (Hedenäs, 1987a, 1989c), including the Amblystegiaceae, Catagoniaceae, Entodontaceae, Fabroniaceae, Hypnaceae and Theliaceae. These taxa were placed in such families due to a few “key character” similarities with other taxa. Hedenäs’ results thus indicated that the Plagiotheciaceae should be more widely circumscribed rather than reduced to include only a single genus. Representatives of this more widely circumscribed family formed a clade in the study of Hedenäs (1995) and a phylogeny for these taxa was later proposed, based on analysis of morphology and anatomy (Pedersen and Hedenäs, 2001). In this case numerous characters of both the gametophyte and sporophyte contributed to the circumscription of the family (Table 4.2). Among the gametophytic states, the most important were found in the narrow branching angle and easily detached branches, and in several special rhizoid features. In the perichaetia and sporophyte the most important states were the small, erect and nonplicate perichaetial leaves, the typical cylindrical capsules curved throughout, the long-pored stomata, the pale, whitish yellow lower exostome in recently dehisced capsules, the exostome border gradually narrowed upwards, the narrowly split

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TABLE 11.2 The Most Frequent Character States within Some Important Pleurocarp Clades or Grades

Character Branch attachment Branching angle Alar cells

Leaf costa Rhizoid colour (young) Rhizoid ornamentation (young) Rhizoid insertion

Pseudoparaphyllia Inner perichaetial leaf orientation

Inner perichaetial leaf plication Vaginular paraphyses Seta ornamentation Capsule shape Lid Separating annulus Exothecial cells Stomatal pores Stomata guard cells Stomata on protuberances Exostome colour

Brachytheciaceae, Ctenidiaceae, Heterocladioideae, Hylocomiaceae

Plagiotheciaceae

Amblystegiaceae, Thuidiaceae, temperate Hypnaceae, Rhytidiaceae

Hookeriales, Sematophyllaceae, (Garovagliaceae?), (Ptychomniaceae)

Firmly attached Wide Usually differentiated, mostly oblate to shortly rectangular, few or numerous, rarely inflated Single and long or double and short Red-brown

Easily detached Narrow Mostly poorly differentiated

Firmly attached Wide Differentiated, usually numerous, strongly inflated or not

Firmly attached Wide Well differentiated or not

Mostly double and short Often purplish

Single and long or double and short Red-brown

Smooth

Smooth or often granular-papillose

Smooth or sometimes warty-papillose

Single or double, long or short Red-brown, rarely hyaline Smooth or sometimes warty-papillose

At or just below leaf insertions, in the Hylocomiaceae axillary near branch apices Mostly present and foliose From erect basal portion usually ± spreading

At or just below leaf insertions, occasionally scattered on stem and on leaves a Mostly present and foliose Straight and erect

Straight and erect

Not plicate

Often axillary or some distance up on abaxial costa, sometimes near leaf apex Frequently filiform or lacking Erect and small, sometimes suddenly narrowed to ± recurved acumen Not plicate

Mostly plicate

Mostly smooth

Present Smooth or rough

Present Smooth

Present or absent Smooth or rough

Of Brachythecium kind Conical or rostrate Mostly present Evenly thickened or collenchymatous Round-pored Usually two

Cylindrical, curved

Present or absent Smooth or (especially Thuidiaceae) rough Cylindrical, curved

Mostly conical Mostly present Mostly evenly thickened Long-pored Usually two

Conical or rostrate Mostly present Mostly evenly thickened Mostly long-pored Usually two

No

No

No

Mostly rostrate Mostly absent Mostly collenchymatous Round-pored Frequently three or more Frequently

Mostly red, redbrown, or orangebrown

Pale whitish yellow

Yellow-brown or brownish yellow

Yellow, yellowbrown, or red

At or just below leaf insertions, occasionally axillary or scattered on stem Frequently absent

Cylindrical, straight

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TABLE 11.2 (Continued) The Most Frequent Character States within Some Important Pleurocarp Clades or Grades

Character

Brachytheciaceae, Ctenidiaceae, Heterocladioideae, Hylocomiaceae

Plagiotheciaceae

Amblystegiaceae, Thuidiaceae, temperate Hypnaceae, Rhytidiaceae

Hookeriales, Sematophyllaceae, (Garovagliaceae?), (Ptychomniaceae)

Exostome furrow

No furrow

No furrow

No furrow

Furrowed or split, rarely unfurrowed Not widened

Exostome border at zone of transition in OPL pattern Primary peristomial layer of exostome Endostome cilia Endostome process width Endostome process perforation Spore maturation time

Not widened

Not widened

Normal

Normal

Widened or (sometimes in Thuidiaceae) not Normal

Well developed Normal

Well developed Narrow

Well developed Normal

Mostly strongly developed Mostly short Often narrow

Wide

Narrow

Narrow

Narrow

Winter season

Summer season

Summer season

Not relevantb

Note: States of sporophyte characters refer to the condition in species with unspecialized capsules and peristomes. In orthotropous capsules the character states are partly very different from those given and, in addition, many similarities occur between taxa having such sporophytes in all five groups. a b

The latter present only in the Calliergon-Scorpidium-Drepanocladus complex. Rarely grow in seasonal, temperate zone climates.

endostome processes, and the spore maturation time during the summer season (late spring to early autumn in species from temperate areas). An early molecular phylogenetic study was based only on rbcL and included only members of Plagiothecium (Arikawa and Higuchi, 1999). Because this is only one out of the more than ten genera that are now placed in the family (cf., Pedersen and Hedenäs, 2002), this study was not informative regarding circumscription of the family. Molecular and morphological evidence were later combined in an investigation by Pedersen and Hedenäs (2002), whose results corroborated the circumscription based on morphology and anatomy.

11.4.3 THE AMBLYSTEGIACEAE, THUIDIACEAE OF THE HYPNACEAE

AND

TEMPERATE MEMBERS

Members of these families usually formed a clade sister to the Plagiotheciaceae in Hedenäs’ (1995) analyses. This study also suggested that the Rhytidiaceae belong to this clade. A more detailed study of this clade showed that the Thuidiaceae (excluding the Heterocladioideae) is likely to be monophyletic, deviating from the other members in several gametophytic characteristics (Hedenäs, 1998b). However, the position of the Thuidiaceae in relation to other members of the entire clade could not be decided. As in the earlier examples, these families are usually placed in different positions in the majority of recent treatments (e.g., Buck and Vitt, 1986; Crum and Anderson, 1981; Nyholm, 1960, 1965; Smith, 1978). The gametophytic differences, especially concerning vegetative leaf costa development, and the presence or absence of papillae/mammillae on the leaf lamina cells,

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and the presence or absence of paraphyllia, seem to be the reasons for such treatments. Character states that are typical for this clade are presented in Table 4.2. The most salient characteristics are found in the perichaetia and sporophytes, the inner perichaetial leaves being straight, erect and mostly plicate, the capsule cylindrical and curved, usually throughout, the long-pored stomata, the usually yellow or yellow-brown lower exostome in recently dehisced capsules, the mostly clearly widened exostome border in the zone where the outside ornamentation changes from cross-striolate to papillose, the narrowly split endostome processes, and the spore maturation time in the summer season (in species from temperate areas). Molecular and total evidence do not contradict a relationship between the above taxa (Gardiner et al., this volume; Vanderpoorten et al., 2002), even if Ignatov and Ignatova (2004) suggested a radically different interpretation of relationships for some of these taxa based on Gardiner et al. (this volume). However, further studies are still necessary before we can feel certain about the affiliations of many taxa in these families.

11.4.4 THE HOOKERIALES, SEMATOPHYLLACEAE

AND

PTYCHOMNIALES

Members of the Hookeriales, Sematophyllaceae and Garovagliaceae were found in the same clade in Hedenäs’ (1995) study. When Ptychomnion was included in the outgroup, most members of the just mentioned taxa were found in a basal grade, suggesting that the Ptychomniaceae could belong to the same grade or clade. A later morphology-based study of this group (Hedenäs, 1996) suggested (1) that a relationship exists between these taxa, including the Ptychomniaceae and Garovagliaceae, (2) that the Hypopterygiacaae may be close to the Hookeriales, and (3) that some taxa of the Hookeriales (Crosbya, Daltonia) may belong to the Sematophyllaceae, although several characters of the leaves and calyptras suggest that they belong to the Hookeriales. Obviously, the relationships suggested by morphology and anatomy are mainly due to similarities in sporophytic character states, such as the frequent lack of a separating annulus, the often furrowed or split lower outer peristomial layer of the exostome teeth, the often strongly developed trabeculae of the entire primary peristomial layer of the exostome, the frequently narrow processes and reduced cilia of the endostome, and the usually distinctly collenchymatous exothecial cells (Table 4.2). On the other hand, the vegetative gametophyte differs strongly between several of these taxa, as exemplified by the appearance of the leaf lamina cells and alar cells in different groups. Phylogenetic analyses based on molecular data have shown that the Hookeriales and Sematophyllaceae undoubtedly belong to two different major pleurocarpous moss lineages (Buck et al., 2000a; De Luna et al., 2000). The many striking sporophytic similarities, which place them together in cladistic analyses based on morphological characters (Hedenäs, 1995), are therefore not homologous and must be due to convergent evolution. It seems likely that some environmental factors that are decisive for the function of the capsule and peristome explain the sporophytic similarities, because members of these two taxa are frequently found in similar environments (Hedenäs, 2002). On the other hand, the relationship between the Hookeriales, the Garovagliaceae and the Ptychomniaceae that was suggested as a possibility by the morphological data has later been confirmed by analyses based on molecular information (Buck et al., 2005).

11.4.5 SOME GENUS-LEVEL RELATIONSHIPS Besides the earlier discussion of Calliergon, Campylium, Drepanocladus and Scorpidium, the circumscriptions of several other genera have been improved by both detailed morphological and molecular investigations. Other cases where both kinds of studies agree include Calliergonella (cf. Hedenäs, 1992b; Tsubota et al., 2002; Vanderpoorten et al., 2002) and Herzogiella (cf. Pedersen and Hedenäs, 2001, 2002).

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11.5 PROBLEMS WITH THE INTERPRETATION OF SOME SPOROPHYTE CHARACTERS The previous two sections suggest that morphological and anatomical evidence is highly informative and provides valuable evidence regarding relationships, which are often corroborated by molecular studies. Naturally, there are cases where morphological similarities are clearly analogous, such as between sporophytes in the Hookeriales and Sematophyllaceae, and in these cases morphological data may lead to erroneous conclusions regarding the relationships. Certain kinds of sporophytic evidence in particular have often been misleading in phylogenetic reconstructions, and some of the most salient problems with sporophytic characters in cladistic studies will therefore be discussed in more detail in the following section. Traditionally, most pleurocarpous moss capsules were characterized either as “horizontal,” with a perfect or “hypnoid” peristome, or “erect,” with a “neckeroid” or “leskeoid” peristome. In addition, many species have intermediate, so called “inclined” capsules, sometimes with peristomes that are intermediate between those in “horizontal” and “erect” capsules. Especially in tropical and subtropical areas “cernuous” or “pendulous” capsules are also relatively frequent, and these have usually more or less “hypnoid” peristomes. This division of capsules and peristome types is far too simplistic to reflect reality. The terminology is unfortunately very unclear and has added significantly to the incorrect ideas of pleurocarpous moss relationships that were predominant until recently, and gives false implications regarding the relationship between the sporophytes and the habitats in which they are found. So-called “horizontal” capsules found in different clades or grades are characterized by specific complexes of states in perichaetia and sporophytes. It therefore seems that bryologists who classified pleurocarpous mosses as being related to each other due to their “horizontal” capsules at the same time overlooked the significance of a large number of other characters of such sporophytes and their perichaetia. As shown in several studies of pleurocarpous mosses, the phylogenetic component is important in explaining the patterns of variation in such characters, and in addition numerous complexes of correlated sporophytic and perichaetial states associated with “horizontal” capsules are found in specific taxonomic entities (Hedenäs, 1999, 2001a, 2001b, 2002). To describe all more or less unspecialized peristomes as “hypnoid” overlooks the fact that there are “brachythecioid,” “plagiothecioid,” “isobryoid,” “sematophylloid” and other perfect peristomes as well. Since orthotropous (“erect”; cf. below and Figure 11.4) capsules can potentially cause serious misinterpretations in phylogenetic studies, such capsules and the reasons for their evolution need to be discussed. Orthotropous capsules are mostly found in epiphytes, and to some degree in species growing on dead wood or on rocks. In a study of the distribution of pleurocarpous moss character states among various habitats, and based on species from all over the world, orthotropous capsules were found in approximately 50% of the epiphytic species and in around 25% of those on dead wood and dry rocks (Hedenäs, 2001a). The corresponding figures for species growing on wet rocks, soil, in mires and in running water were between 0 and 9%. The relatively high figure for dead wood may at least partly be due to several facultative epiphytic species that persist on fallen trees. Because most species with orthotropous capsules are epiphytes or occur on rocks, their capsules are actually horizontal. Therefore, character states associated with orthotropous capsules are more likely explained by specific conditions in epiphytic and some epilithic habitats than by the capsule’s orientation in relation to the seta. Even if relaxed selective pressure rather than selection for specific states causes some of the changes seen in these capsules, the conditions under which this can occur are obviously met within the habitats just mentioned. Besides frequently having orthotropous capsules, epiphytic pleurocarps possess several other sporophytic character states more often than species of other habitats. These include short setae, ovoid to cylindrical and straight capsules, round stomatal pores, lack of or a poorly developed separating annulus, rostrate lids, papillose lower exostome outer surface, reduced exostome primary

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Average number of characters with correlated states 20 15 10 5 0 Average GAM character SPO GAM

Average SPO character

FIGURE 11.2 Patterns of correlations among characters of the “vegetative gametophyte” (GAM) and the “sexual branches plus sporophyte” (SPO), respectively. One correlation implies that one or several states of a specific character is or are correlated with one or several states of another character. The bars thus show the number of correlations between an average GAM or SPO character, and other GAM or SPO characters. (Adapted from Hedenäs, 2002.)

peristomial layers, low endostome basal membranes, short or lacking endostome cilia, and relatively large spores (Hedenäs, 2001a). In Hedenäs’ (2002) study of complexes of intercorrelated states among pleurocarpous mosses, it was shown that most such complexes occur among states of sporophytic characters (Figure 11.2). Sporophytic complexes may include more than 20 character states, which suggests that spore dispersal depends on an intricate set of many morphological structures. Although several such complexes typical for species with unspecialized capsules can be explained to a great extent by their phylogenetic history, the complex found in orthotropous capsules must have evolved numerous times as a more direct response to specific habitat factors. Besides orthotropous capsules, this complex includes specialized or absent exostomes, exostomes that are papillose on their lower outer surface, an entire or almost entire exostome margin, the absence of an exostome border, and a reduced exostome primary peristomial layer. Correlations exist also between some or several of the states just mentioned and capsules that are cylindrical to ovoid and straight or curved only near their base, a lack of a separating annulus, and short cilia, but the latter three states are correlated with states in other complexes of correlated states as well. Orthotropous capsules are thus part of a suite of correlated states that are associated with specific habitats rather than with a specific monophyletic group. Because morphology-based cladistic studies are often hampered by relatively small total numbers of characters, this presents a serious problem that needs to be considered in phylogenetic studies based solely on morphology. When all sporophytic characters are coded and included individually in such a study, there is a great risk that the results of an analysis will be skewed. Two studies of the Plagiotheciaceae, one based on morphology and anatomy and the other based on morphology, anatomy and molecular evidence illustrate this problem well (Pedersen and Hedenäs, 2001, 2002). In the morphology-based study all species with more or less reduced exostomes appeared in a single, terminal clade, whereas in the other study such taxa were found spread all over the resulting cladogram (Figure 11.3). The traditional terminology differentiating between so-called “horizontal” and “erect” capsules is illogical since in nature, in the normal habitats of the species having these two kinds of capsules, the capsules of both are mostly more or less horizontal. The terminology most likely has its origin in studies of material in herbarium packets, where specimens are frequently placed so that the sporophytes are directed upwards. This is obviously a good way of protecting the latter from

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? ? ?

A

? ? ? ?

B

239

Outgroup taxa Plagiothecium denticulatum Plagiothecium conostegium Plagiothecium nemorale Plagiothecium undulatum Plagiothecium curvifolium Pseudotaxiphyllum elegans Pseudotaxiphyllum laetevirens Pseudotaxiphyllum pohliaecarpum Catagonium politum Isopterygiopsis pulchella Isopterygiopsis muelleriana Bardunovia baicalensis Platydictya jungermannioides Myurella acuminata Myurella julacea Plagiothecium latebricola Struckia argentata Orthothecium intricatum Orthothecium rufescens Rhizofabronia perpilosa Herzogiella striatella Herzogiella seligeri Herzogiella cylindricarpa Outgroup taxa Acrocladium auriculatum Catagonium nitens Catagonium nitens subsp. maritimum Herzogiella seligeri Herzogiella cylindricarpa Herzogiella striatella Isopterygiopsis muelleriana Isopterygiopsis pulchella Rhizofabronia perpilosa Rhizofabronia sphaerocarpa Orthothecium chryseum Orthothecium intricatum Orthothecium rufescens Myurella julacea Myurella tenerrima Myurella acuminata Bardunovia baicalensis Platydictya jungermannioides Pseudotaxiphyllum elegans Pseudotaxiphyllum pohliaecarpum Pseudotaxiphyllum laetevirens Plagiothecium piliferum Struckia zerovii Plagiothecium curvifolium Plagiothecium latebricola Plagiothecium neckeroideum Plagiothecium undulatum Plagiothecium nemorale Plagiothecium conostegium Plagiothecium denticulatum

FIGURE 11.3 Hypotheses regarding relationships among the Plagiotheciaceae based on (A) morphology and anatomy alone (adapted from Pedersen and Hedenäs, 2001), and (B) morphology, anatomy and the chloroplast molecular markers rps4 and trnL-trnF (adapted from Pedersen and Hedenäs, 2002). Grey and black vertical bars indicate species with slightly reduced and strongly reduced to lacking exostomes, respectively. Question marks indicate that the state of the exostome is unknown.

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breaking in a herbarium, but has nothing to do with how the species grow and function in their habitats. Hedenäs (2002) suggested that the term “seta-oriented” should replace the common use of “erect” in order to explain what is structurally characteristic for this kind of sporophyte when compared with what has traditionally been called “horizontal,” “inclined,” “cernuous” or “pendulous” capsules. Considering how the spore capsules are oriented in nature, it seems desirable to use a terminology that differentiates between capsule orientation (1) in relation to the seta, and (2) in relation to the horizon in the habitat of the respective species. The first set of terminology should be used primarily to describe the sporophyte structure, whereas the second set refers to the capsule orientation in the habitat of the plant and is thus likely to be more directly important for understanding the biology of the plant. Capsule orientation in relation to the seta should not include reference to the horizon, and a novel terminology is therefore necessary for this. This new terminology, with explanations of the terms, is proposed in Figure 11.4A. “Orthotropous,” “homotropous” and “antitropous” are analogous to terms applied to the embryo of the seed (cf., Stearn, 1983), “orthogonal” refers to the right angle between the axes of the seta and capsule, and “reclinate” refers to the capsule that is turned downwards in relation to the seta. It should be noted that none of the categories are necessarily homogeneous morphologically or anatomically. For example, orthogonal capsules can be of many different kinds, such as those found in the Brachytheciaceae, Plagiotheciaceae and Sematophyllaceae. The terminology for capsule orientation in relation to the horizon in the habitat is the same as that which has been used for either kind of capsule orientation without clear discrimination (Figure 11.4B). Even if inclining (inclinatus) actually means “bent down, diverging downwards from the horizon” (Stearn, 1983), it is here suggested that “inclined” and the other terms in Figure 11.4B are retained as they are usually understood among bryologists (e.g., Malcolm and Malcolm, 2000) to indicate capsule orientation in relation to the horizon. When the suggested terminology is applied to a few example species, the orthotropous capsules of Sanionia georgicouncinata (Müll. Hal.) Ochyra and Hedenäs are erect in their habitat, whereas those of Homalothecium sericeum (Hedw.) Schimp. are horizontal. The orthogonal capsules of Hylocomium splendens (Hedw.) Schimp. are horizontal.

11.6 CONCLUDING REMARKS The history of how we attempt to reconstruct phylogenetic relationships among the pleurocarpous mosses parallels that of many other groups of organisms. Starting from the relatively simple “key character” stage, we have now reached a stage where all kinds of evidence can and should be included in the phylogeny reconstructions, including the vast source of data provided by DNA. In this context it is important to remember that morphological and/or ecological data are necessary to judge both the reliability and biological contexts of relationships. Phylogenies devoid of such information are of little interest or practical use to other life sciences. Finally, it is worth noting that although currently available morphological information is often insufficient to reveal the correct relationships among pleurocarpous mosses, such data rarely contradict well-supported relationships suggested by molecular evidence.

ACKNOWLEDGMENTS Input from A. E. Newton, especially concerning capsule orientation terminology, and from an unknown reviewer significantly improved this paper.

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Axis of seta

A

Orthotropous

Homotropous

Orthogonal

Reclinate

Antitropous

B

Horizon

Erect

Inclined

Horizontal

Cernuous

Pendulous

FIGURE 11.4 Suggested new sets of terminology describing the capsule orientation in pleurocarpous mosses. The axis of the capsule is indicated by short dotted lines through the capsule mouth. (A) In relation to the seta: orthotropous capsules have their longitudinal axis parallel with that of the seta, with the mouth pointing in the same direction as the apex of the seta; homotropous capsules have a longitudinal axis that deviates from that of the seta, intermediate between orthotropous and orthogonal; orthogonal capsules have their longitudinal axis perpendicular to that of the seta; reclinate capsules have a longitudinal axis that deviates from that of the seta, intermediate between antitropous and orthogonal; antitropous capsules have their longitudinal axis parallel with that of the seta, with the mouth pointing in the same direction as the base of the seta. (B) In relation to the horizon in nature: erect capsules have their longitudinal axis perpendicular to the horizon, with the mouth directed upwards, towards the sky; inclined capsules have their longitudinal axis intermediate between horizontal and erect; horizontal capsules have their longitudinal axis parallel with the horizon; cernuous capsules have their longitudinal axis intermediate between horizontal and pendulous; pendulous capsules have their longitudinal axis perpendicular to the horizon, with the mouth directed downward, towards the ground.

REFERENCES Akiyama, H. (1990a) A morphological study of branch development in mosses with special reference to pseudoparaphyllia. Botanical Magazine, Tokyo, 103: 269–282. Akiyama, H. (1990b) Morphology and taxonomic significance of dormant branch primordia, dormant buds, and vegetative reproductive organs in the suborders Leucodontineae and Neckerineae (Musci, Isobryales). Bryologist, 93: 395–408. Akiyama, H. and Nishimura, N. (1993) Further studies of branch buds in mosses; “Pseudoparaphyllia” and “Scaly leaves.” Journal of Plant Research, 106: 101–108. Arikawa, T. and Higuchi, M. (1999) Phylogenetic analysis of the Plagiotheciaceae (Musci) and its relatives based on rbcL gene sequences. Cryptogamie, Bryologie, 20: 231–245. Arikawa, T. and Higuchi, M. (2003) Preliminary application of psaB sequence data to phylogenetic analysis of pleurocarpous mosses. Hikobia, 14: 33–44.

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Arnell, H. W. (1875) De Skandinaviska löfmossornas kalendarium (PhD thesis). Esaias Edquists boktryckeri, Upsala. Brotherus, V. F. (1924) Musci. In Die natürlichen Pflanzenfamilien, Vol. 11(1), Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig. Brotherus, V. F. (1925) Musci. In Die natürlichen Pflanzenfamilien, Vol. 11(2), Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig. Buck, W. R. (1980) A generic revision of the Entodontaceae. Journal of the Hattori Botanical Laboratory, 48: 71–159. Buck, W. R. (1988) Another view of familial delimitation in the Hookeriales. Journal of the Hattori Botanical Laboratory, 64: 29–36. Buck, W. R. (1994) A new attempt at understanding the Meteoriaceae. Journal of the Hattori Botanical Laboratory, 75: 51–72. Buck, W. R. and Ireland, R. R. (1985) A reclassification of the Plagiotheciaceae. Nova Hedwigia, 41: 89–125. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000a) Novel relationships in pleurocarpous mosses as revealed by cpDNA sequences. Bryologist, 103: 774–789. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000b) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL-trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Buck, W. R., Cox, C. J., Shaw, A. J. and Goffinet, B. (2005). Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematics and Diversity 2: 121–145. Crum, H. and Anderson, L. E. (1981) Mosses of Eastern North America. Columbia University Press, New York. Crundwell, A. C. (1979) Rhizoids and moss taxonomy. In Bryophyte Systematics. The Systematics Association Special Volume 14 (ed. G. C. S. Clarke and J. G. Duckett). Academic Press, London, pp. 347–363. De Luna, E., Buck, W. R., Akiyama, H., Arikawa, T., Tsubota, H., González, D., Newton, A. E. and Shaw, A. J. (2000) Ordinal phylogeny within the Hypnobryalean pleurocarpous mosses inferred from cladistic analyses of three chloroplast DNA sequence data sets: trnL-F, rps4, and rbcL. Bryologist, 103: 242–256. Fleischer, M. (1902–1904) Die Musci der Flora von Buitenzorg. Band 2. E. J. Brill, Leiden. Fleischer, M. (1906–1908) Die Musci der Flora von Buitenzorg. Band 3. E. J. Brill, Leiden. Fleischer, M. (1915–1922) Die Musci der Flora von Buitenzorg. Band 4. E. J. Brill, Leiden. Fleischer, M. (1920) Natürliches System der Laubmoose. Hedwigia, 61: 390–400. Frey, W. (1970) Blattentwicklung bei Laubmoosen. Hedwigia, 20: 463–556. Frey, W. (1972) Entwicklungsgeschichte des Blattnetzes bei Leskeaceen und Thuidiaceen (Musci). Hedwigia, 23: 161–168. Frey, W. (1974a) Entwicklungsgeschichtliche Untersuchungen an Hypnodendron dendroides (Brid.) Touw (Hypnodendraceae, Musci). Hedwigia, 25: 229–249. Frey, W. (1974b) Vergleichende entwicklungsgeschichtliche Untersuchungen an Laubmoosblättern als Beitrag zur Systematik der Laubmoose. Bulletin de la Société Botanique de France, 121: 29–34. Grandcolas, P., Deleporte, P., Desutter-Grandcolas, L. and Daugeron, C. (2001) Phylogenetics and ecology: As many characters as possible should be included in the cladistic analysis. Cladistics, 17: 104–110. Granzow-de la Cerda, I. (1992) Análisis cladístico de la familia Anomodontaceae. Tropical Bryology, 6: 95–104. Hedenäs, L. (1987a) North European mosses with axillary rhizoids, a taxonomic study. Journal of Bryology, 14: 429–439. Hedenäs, L. (1987b) On the ontogeny of alar cells in Drepanocladus aduncus, D. exannulatus and some other species. Journal of Bryology, 14: 753–759. Hedenäs, L. (1989a) The genera Scorpidium and Hamatocaulis, gen. nov., in Northern Europe. Lindbergia, 15: 8–36. Hedenäs, L. (1989b) The genus Sanionia (Musci) in Northwestern Europe, a taxonomic revision. Annales Botanici Fennici, 26: 399–419. Hedenäs, L. (1989c) Some neglected character distribution patterns among the pleurocarpous mosses. Bryologist, 92: 157–163. Hedenäs, L. (1990) Axillary hairs in pleurocarpous mosses: A comparative study. Lindbergia, 15: 166–180. Hedenäs, L. (1992a) The genus Pseudocalliergon in northern Europe. Lindbergia, 16: 80–99.

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Hedenäs, L. (1992b) Taxonomic and nomenclatural notes on the genera Calliergonella and Breidleria. Lindbergia, 16: 161–168. Hedenäs, L. (1993) A generic revision of the Warnstorfia-Calliergon group. Journal of Bryology, 17: 447–479. Hedenäs, L. (1994) The basal pleurocarpous diplolepidous mosses: A cladistic approach. Bryologist, 97: 225–243. Hedenäs, L. (1995) Higher taxonomic level relationships among diplolepidous pleurocarpous mosses: A cladistic overview. Journal of Bryology, 18: 723–781. Hedenäs, L. (1996) A cladistic study of relationships between the Hookeriales, the Sematophyllaceae and some other taxa. Lindbergia, 21: 49–82. Hedenäs, L. (1997a) A cladistic overview of the “Hookeriales”. Lindbergia, 21: 107–143. Hedenäs, L. (1997b) The Drepanocladus s. str. species with excurrent costae (Musci: Amblystegiaceae). Nova Hedwigia, 64: 535–547. Hedenäs, L. (1997c) A partial generic revision of Campylium (Musci). Bryologist, 100: 65–88. Hedenäs, L. (1998a) Cladistic studies on pleurocarpous mosses: Research needs, and use of results. In Bryology for the Twenty-First Century (ed. J. W. Bates, N. W. Ashton and J. G. Duckett). Maney Publishing, Leeds, pp. 125–141. Hedenäs, L. (1998b) An evaluation of phylogenetic relationships among the Thuidiaceae, the Amblystegiaceae, and the temperate members of the Hypnaceae. Lindbergia, 22: 101–133. Hedenäs, L. (1998c) An overview of the Drepanocladus sendtneri complex. Journal of Bryology, 20: 83–102. Hedenäs, L. (1999) How important is phylogenetic history in explaining character states in pleurocarpous mosses? Canadian Journal of Botany, 77: 1723–1743. Hedenäs, L. (2001a) Environmental factors potentially affecting character states in pleurocarpous mosses. Bryologist, 104: 72–91. Hedenäs, L. (2001b) The importance of phylogeny and habitat factors in explaining gametophytic character states in European Amblystegiaceae. Journal of Bryology, 23: 205–219. Hedenäs, L. (2002) Important complexes of intercorrelated character states in pleurocarpous mosses. Lindbergia, 27: 104–121. Hedenäs, L. (2003) Amblystegiaceae (Musci). Flora Neotropica Monograph, 89: i–iv, 1–107. Hedenäs, L. (2004) Morphological and anatomical evidence suggest that “Hylocomiaceae” taxa belong to at least two clades. Journal of Bryology, 26: 125–135. Hedenäs, L. and Buck, W. R. (1999) A phylogenetic analysis of the Sematophyllaceae. Lindbergia, 24: 103–132. Hedenäs, L. and Kooijman, A. (1996) Phylogeny and habitat adaptations within a monophyletic group of wetland moss genera (Amblystegiaceae). Plant Systematics and Evolution, 199: 33–52. Hedenäs, L., Oliván, G. and Eldenäs, P. 2005. Phylogeny of the Calliergonaceae (Bryophyta) based on molecular and morphological data. Plant Systematics and Evolution, 252: 49–61. Hedwig, J. (1782) Fundamentum historiae naturalis muscorum frondosorum. Lipsiae. Hedwig, J. (1785–1787) Descriptio et adumbratio microscopico-analytica muscorum frondosorum … Vol. 1. Lipsiae. Hedwig, J. (1789) Descriptio et adumbratio microscopico-analytica muscorum frondosorum … Vol. 2. Lipsiae. Hedwig, J. (1791–1792) Descriptio et adumbratio microscopico-analytica muscorum frondosorum … Vol. 3. Lipsiae. Hedwig, J. (1797) Descriptio et adumbratio microscopico-analytica muscorum frondosorum… Vol. 4. Lipsiae. Hedwig, J. (1801) Species muscorum frondosorum. Lipsiae. Higuchi, M. (1985) A taxonomic revision of the genus Gollania Broth. (Musci). Journal of the Hattori Botanical Laboratory, 59: 1–77. Huttunen, S., Ignatov, M. S., Müller, K. and Quandt, D. (2004) Phylogeny and evolution of epiphytism in the three moss families Meteoriaceae, Brachytheciaceae and Lembophyllaceae. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 328–361. Hyvönen, J. and Enroth, J. (1994) Cladistic analysis of the genus Pinnatella (Neckeraceae, Musci). Bryologist, 97: 305–312. Ignatov, M. S. and Ignatova, E. A. (2004) Flora mchov srednej tjacti evropejskoj Rossii. Tom 2. FontinalaceaeAmblystegiaceae. Arctoa, 11, Suppl. 2: 609–944. Ireland, R. R. (1968) Pleuroziopsidaceae, a new family of mosses. Journal of the Hattori Botanical Laboratory, 31: 59–64.

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Ireland, R. R. (1971) Moss pseudoparaphyllia. Bryologist, 74: 312–330. Karczmarz, K. (1971) A monograph of the genus Calliergon (Sull.) Kindb. Monographiae Botanicae, 34: 1–209, Pl. I–XX. Kawai, I. (1968) Taxonomic studies on the midrib in Musci. I. Significance of the midrib in systematic botany. Science Reports of the Kanazawa University, 13: 127–157. Kawai, I. (1971) Systematic studies on the conducting tissue of the gametophyte in Musci. III. On the affinity regarding the inner structure of the stem in some species of Thuidiaceae. Science Reports of the Kanazawa University, 16: 21–60. Kawai, I. (1976) Systematic studies on the conducting tissue of the gametophyte in Musci. VI. On the essential coordination among the anatomical characteristics of the stem in some species of Hypnaceae. Science Reports of the Kanazawa University, 21: 47–124. Kawai, I. (1977a) Die systematische Forschung auf Grund der Zellteilungsweise für die Bryophyten. II. Die Zellteilungsweisen der Gametophyten in der Lebensgeschichte (1) Climacium. Science Reports of the Kanazawa University, 22: 45–90. Kawai, I. (1977b) Systematic studies on the conducting tissue of the gametophyte in Musci. VII. On the essential coordination among the anatomical characteristics of the stems in some species of Isobryales. Science Reports of the Kanazawa University, 22: 197–305. Kawai, I. (1978) Systematic studies on the conducting tissue of the gametophyte in Musci. VIII. On the essential coordination among the anatomical characteristics of the stems in some species of Amblystegiaceae. Science Reports of the Kanazawa University, 23: 93–117. Koponen, T. (1968) Generic revisions of Mniaceae Mitt. (Bryophyta). Annales Botanici Fennici, 5: 117–151. Lin, S.-H. (1983a) A taxonomic revision of Phyllogoniaceae (Bryopsida). I. Journal of the Taiwan Museum, 36: 37–86. Lin, S.-H. (1983b) A taxonomic revision of Phyllogoniaceae (Bryopsida). II. Journal of the Taiwan Museum, 37: 1–54. Loeske, L. (1907) Drepanocladus, eine biologische Mischgattung. Hedwigia, 46: 300–321. Malcolm, B. and Malcolm, N. (2000) Mosses and Other Bryophytes, an Illustrated Glossary. Micro-Optics Press, Nelson. Mishler, B. D. (1986) A Hennigian approach to bryophyte phylogeny. Journal of Bryology, 14: 71–81. Newton, A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Nishimura, N. (1985) A revision of the genus Ctenidium (Musci). Journal of the Hattori Botanical Laboratory, 58: 1–82. Nishimura, N. and Matsui, S. (1990a) SEM observations of moss pseudoparaphyllia. I. Isobryales. Hikobia, 10: 429–434. Nishimura, N. and Matsui, S. (1990b) SEM observations of moss pseudoparaphyllia. II. Hypnobryales. Bulletin of the Hiruzen Research Institute, Okayama University of Science, 16: 117–138. Noguchi, A. (1989) Illustrated Moss Flora of Japan, Part 3. The Hattori Botanical Laboratory, Nichinan. Noguchi, A. (1991) Illustrated Moss Flora of Japan, Part 4. The Hattori Botanical Laboratory, Nichinan. Noguchi, A. (1994) Illustrated Moss Flora of Japan, Part 5. The Hattori Botanical Laboratory, Nichinan. Nyholm, E. (1960) Illustrated Moss Flora of Fennoscandia, II, Musci. Fasc. 4. C. W. K. Gleerup, Lund. Nyholm, E. (1965) Illustrated Moss Flora of Fennoscandia, II, Musci. Fasc. 5. C. W. K. Gleerup, Lund. Ochyra, R. (1985) Hypnobartlettia fontana gen. et sp. nov. (Musci: Hypnobartlettiaceae fam. nov.), a unique moss from New Zealand. Lindbergia, 11: 2–8. Ochyra, R. (1989) Animadversions on the moss genus Cratoneuron (Sull.) Spruce. Journal of the Hattori Botanical Laboratory, 67: 203–242. Paton, J. A. and Pearce, J. V. (1957) The occurrence, structure and functions of the stomata in British bryophytes. Transactions of the British Bryological Society, 3: 228–259. Pedersen, N. and Hedenäs, L. (2001) Phylogenetic relationships within the Plagiotheciaceae. Lindbergia, 26: 62–76. Pedersen, N. and Hedenäs, L. (2002) Phylogeny of the Plagiotheciaceae based on molecular and morphological evidence. Bryologist, 105: 310–324. Ramsay, H. (1987) Cytological and other studies on the Hypnodendraceae. Memoirs of the New York Botanical Garden, 45: 135–153. Rohrer, J. R. (1985) A phenetic and phylogenetic analysis of the Hylocomiaceae and Rhytidiaceae. Journal of the Hattori Botanical Laboratory, 59: 185–240.

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Smith, A. J. E. (1978) The Moss Flora of Britain and Ireland. Cambridge University Press, Cambridge. Stearn, W. T. (1983) Botanical Latin, Ed. 3. David and Charles, Newton Abbot. Tsubota, H., Akiyama, H., Yamaguchi, T. and Deguchi, H. (2001) Molecular phylogeny of the Sematophyllaceae (Hypnales, Musci) based on chloroplast rbcL sequences. Journal of the Hattori Botanical Laboratory, 90: 221–240. Tsubota, H., Arikawa, T., Akiyama, H., De Luna, E., González, D., Higuchi, M. and Deguchi, H. (2002) Molecular phylogeny of hypnobryalean mosses as inferred from a large-scale dataset of chloroplast rbcL, with special reference to the Hypnaceae and possibly related families. Hikobia, 13: 645–665. Tuomikoski, R. and Koponen, T. (1979) On the generic taxonomy of Calliergon and Drepanocladus (Musci, Amblystegiaceae). Annales Botanici Fennici, 16: 213–227. Vanderpoorten, A., Hedenäs, L., Cox, C. and Shaw, A. J. (2002) Phylogeny and morphological evolution of the Amblystegiaceae (Bryopsida). Molecular Phylogenetics and Evolution, 23: 1–21. Vanderpoorten, A., Goffinet, B., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2003) A taxonomic reassessment of the Vittiaceae (Hypnales, Bryopsida): Evidence from phylogenetic analyses of combined chloroplast and nuclear sequence data. Plant Systematics and Evolution, 241: 1–12. Watanabe, R. and Kawai, I. (1975) Systematic studies on the conducting tissue of the gametophyte in Musci. V What is expected of systematics regarding the inner structure of the stem in some species of Thuidiaceae. Science Reports of the Kanazawa University, 20: 21–76. Wynne, F. E. (1944) Studies in Drepanocladus. I. History, morphology, phylogeny, and variation. Bulletin of the Torrey Botanical Club, 71: 207–225. Zomlefer, W. B. (1993) A revision of Rigodium (Musci: Rigodiaceae). Bryologist, 96: 1–72.

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Reduction and 12 Character Peristome Morphology in Entodontaceae: Constraints on an Information Source E. M. Kungu, Royce Longton, and L. Bonner (deceased) CONTENTS Abstract ..........................................................................................................................................247 12.1 Introduction...........................................................................................................................248 12.2 Sporophyte Morphology and the Delimitation of Taxonomic Boundaries.........................248 12.2.1 Exostome External Structure and Ornamentation ...................................................249 12.2.2 Endostome and Basal Membrane.............................................................................252 12.2.3 Peristome Internal Structure and Function ..............................................................254 12.2.4 Intraspecific Variation in Peristome Ornamentation and Structure .........................254 12.2.5 Spores .......................................................................................................................256 12.3 Gametophyte Morphology and Delimitation of Species Boundaries..................................256 12.3.1 Gross and Leaf Morphology ....................................................................................256 12.3.2 Axillary Hairs ...........................................................................................................259 12.3.3 Pseudoparaphyllia.....................................................................................................260 12.4 A Morphometric Case Study ...............................................................................................262 12.5 Evaluation of Characters ......................................................................................................263 12.6 Evolution of Reduction ........................................................................................................264 12.7 Discussion.............................................................................................................................265 Acknowledgments ..........................................................................................................................266 References ......................................................................................................................................266

ABSTRACT Evaluation of the morphological characters used to delimit taxa within the African Entodontaceae is problematic because of reduction of many of the morphologies. The characters available in both the sporophyte and gametophyte are described and assessed in the light of the restrictions incurred due to this reduction. Peristome ornamentation patterns provide key characters for delimiting both genera and species within the Entodontaceae. Gametophyte structures are examined for corresponding characters to reinforce these taxonomic boundaries. However, the use of peristome ornamentation patterns is confounded by the high level of variation associated with peristome reduction. Examination of internal peristome structure demonstrates a relationship with function and proves that the major differences in surface ornamentation between papillose and striate reflects a difference

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in internal deposition. Morphology indicates that the family as currently recognized is probably not monophyletic and the status of Pylaisiobryum is unresolved.

12.1 INTRODUCTION Traditional bryological studies have delimited taxa using morphological characters, and the historical perspective through the last two centuries has oscillated between the predominance of gametophytic and sporophytic characters in constructing these taxonomies. In recent decades the development of molecular techniques has focused a critical revision on many aspects of these traditional taxonomies and fostered ongoing reassessment at all levels. This account arose from a conventional morphological revision of the species boundaries within African Entodontaceae (Kungu, 2003), as currently recognized, and is unusual in looking solely at the minutiae of morphological variation in both generations as the basis for delimitation of taxa. Within this framework there is an attempt to evaluate the validity and the limitations of these predominantly reduced character states as the basis for species recognition and to discuss the ongoing evolutionary processes that generated the current range of morphological variation. The Entodontaceae, as currently recognized (Buck, 1980), comprises four genera, Entodon Müll. Hal., Erythrodontium Hampe, Mesonodon Hampe and Pylaisiobryum Broth., and the family is distinctive in that it is predominantly defined by suites of reduced characters and in that the peristome characters are significant in the delimitation of both genera and species. This study is based on a revision of the Entodontaceae within Africa which has been postulated as the location of the evolutionary origin of the family (Buck, 1980) and is the only region where all four genera occur. However, material from all continents has been examined to retain a global perspective. The Entodontaceae is characterized in the gametophyte by a leaf with a short double costa, elongated leaf cells and rectangular alar cells, and in the sporophyte by the co-occurring characters of erect capsules with reduced peristomes. These reduced peristomes combine extensive structural reduction with massive ornamentation of the outer face of the exostome and retain a residual function. Transmission electron microscope (TEM) studies have proved that the exostome ornamentation is not superficial; there is an internal structure that correlates with the residual peristome function. In evaluating the significance of peristome morphology in species delimitation consideration must be given to the evolution of reduction and the mechanics of retention of function within this reduced structure. There is a taxonomic conundrum to be unravelled as peristome ornamentation patterns, although highly informative at both generic and specific levels, also require much care in interpretation in order to determine which elements of these reduced structures are taxonomically informative, and which could be considered background noise. The largest of the four genera in the family is Entodon, with approximately 145 species globally, of which 11 occur in Africa. Erythrodontium has 16 species that are currently being revised, and four of these occur in Africa. There are two species in Mesonodon, one of which has an African and Asian distribution, and Pylaisiobryum is a monotypic African genus.

12.2 SPOROPHYTE MORPHOLOGY AND THE DELIMITATION OF TAXONOMIC BOUNDARIES Conventionally the sporophyte, and specifically the peristome, has been regarded as evolutionarily conservative and almost uniform at specific, generic, and for some pleurocarps, even family level. Buck (1991), considering the classification of pleurocarps, writes of the “sporophytic uniformity” of families in the Hypnales. However, the Entodontaceae is an exception to this generality, as variation in sporophyte morphology, and more particularly in peristome ornamentation patterns, provides key characters defining both species and genera within the family. A literature survey (Kungu, 2003) of all previous work on the largest genus, Entodon, demonstrated the importance

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of peristome characters, with over 33% of all identification characters referring to peristome features, and predominantly to variation in ornamentation patterns of exostome and endostome. The sporophyte in the Entodontaceae has an erect capsule, with an inset and reduced peristome. The correlation between an erect capsule and peristome reduction was first observed by Mitten (1859) and this combination of characters has long been regarded as a derived condition, which has evolved independently in a wide range of pleurocarpous families. Peristome reduction is often associated with a short seta, erect capsule and epiphytic or xerophytic habitat (Vitt, 1981; Hedenäs, 1999, 2001). There is relatively little published information about the range of variation in the peristomes of pleurocarpous mosses, especially reduced peristomes, at intraspecific, intrageneric or even family level. As the peristome is a relatively short-lived structure, the presumption has previously been that it was little subject to environmental modification (Buck, 1980). However, there was a lack of supporting evidence for the presumed absence of phenotypic variation in peristome morphology and ornamentation patterns or the effects, if any, of differing environmental conditions on sporophyte development. Recent work by Hedenäs (1999, 2001) has demonstrated that the sporophyte is not as evolutionarily conservative as previously maintained, and is subject to environmental pressures that correlate with morphology. Previous studies on variation in peristome morphology include an intergeneric survey of endostome variation in 70 species of diplolepidous mosses (Shaw and Rohrer, 1984), and studies of Bryaceae (Shaw, 1985) and Brachytheciaceae (Ignatov et al., 1998). The infraspecific variation in the exostome ornamentation in the reduced peristome of Pterigynandrum filiforme had resulted in a number of varieties being described (Buck, 1980).

12.2.1 EXOSTOME EXTERNAL STRUCTURE

AND

ORNAMENTATION

The diplolepidous peristome is formed from cells in the three innermost layers of the amphithecium of the developing capsule (Figure 12.1). The three layers forming the peristome were named by Blomquist and Robertson (1941) as: 1. The outer peristome layer (OPL) characteristically of 32 cells 2. The primary peristome layer (PPL) characteristically of 16 cells 3. The inner peristome layer (IPL), initially of eight cells, which undergoes a variable number of divisions depending on the taxon under consideration. Am

phi

the

ciu

m

OP LP PL IPL

Endostome

Exostome Operculum

FIGURE 12.1 Diagram of a transverse section through the developing capsule of Entodon in the region of the peristome showing the relationship of the OPL, PPL and IPL to the exostome and endostome.

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The exostome is formed from the common periclinal cell wall pair between the inner wall of the OPL and the outer wall of the PPL. The endostome is formed from the common periclinal cell wall pair between the inner wall of the PPL and the outer wall of the IPL (Figure 12.1). Autolysis of the anticlinal walls of the cells between the exostome and the endostome separates the two rings of the diplolepidous peristome, while autolysis of the periclinal walls between adjacent teeth separates the structures within each ring of the peristome. In reduced peristomes this autolysis may be incomplete, leaving adjacent structures partially attached. Peristomes in the Entodontaceae are inset 50 to 80 μm below the mouth of the capsule, are orange to reddish-brown, and show a number of features of reduction compared with a perfect peristome (Figure 12.2A). The exostome in the Entodontaceae (Figure 12.2B) has fewer OPL cells along the long axis and upper cells are relatively long in relation to their width. The dorsal median ridge is almost straight, only retaining a slight zigzag at the very base in those species that have horizontal striations and short plates at the base of the exostome. The exostome is reduced in length, with some species having a broad, blunt apex. The hypnoid shoulder is usually absent or much reduced, and when present is close to the base of the exostome, at the transition between horizontal and oblique striations. The exostome is irregularly bordered, usually with the cells of the OPL exceeding the cells of the PPL, though in some species the converse may occur. According to Buck (1980), Pylaisiobryum is the only genus in Entodontaceae retaining a border. However, most species in Entodontaceae have an intermittent border of 3 to 8 μm and in Erythrodontium lacoutourei Ren. & Card. the border, formed by the OPL exceeding the PPL, is up to 12 μm wide. Trabeculae of the OPL and PPL are usually reduced, and not proud of the surface. Peristome ornamentation is usually constant within genera (Ando, 1972), but in Entodontaceae precise variations in ornamentation patterns are critical in the delimitation of both species and genera. Massive ornamentation is retained on the OPL, and to a lesser extent on the PPL and IPL, contrasting with the reduced peristomes in the majority of pleurocarpous mosses which are hyaline and either totally lack, or have only faint, residual ornamentation. Species in Entodon subgenus Entodon, Erythrodontium and Mesonodon have a striate or partly striate exostome (Figure 12.2B, Figure 12.2C and Figure 12.2D), whereas in Entodon subgenus Erythropus the exostome is either uniformly papillose (Figure 12.2E) or occasionally striate at the base with papillae tightly packed or even partially occluded. Pylaisiobryum has a papillose exostome and the papillae are clearly separated from each other, and vary in shape from round, oval or rhomboid to C-shaped (Figure 12.2F). A detailed account of the peristome ornamentation patterns found in the African Entodontaceae is given in Kungu et al. (2003). Taxonomic recognition does not just depend on broad character states of exostome papillose or exostome striate. Within these categories, there are often subtle differences in ornamentation

FIGURE 12.2 (See figure, facing page.) External surface of the exostome. (A) Outer face of a perfect peristome of Pseudoscleropodium purum with numerous narrow cells separated by a zigzag median line on the exostome OPL and a well-developed shoulder where the exostome abruptly narrows. The endostome is well developed, with a high, pleated, basal membrane composed of numerous cells and several cilia between each split endostome process (UK, sin. leg. 146/1 RNG). (B) Outer face of the reduced peristome of Entodon dregeanus with few broad cells and a straight median line on the exostome OPL, and a narrow endostome with no basal membrane visible (Malawi, Longton M8438a RNG). (C) The outer face of the reduced exostome of Erythrodontium barteri (Sudan, Rojkowski 436 BM). (D) The reduced peristome of Mesonodon flavescens showing the outer face of the exostome with a truncated exostome tooth, and a small fragment of endostome (arrowed) adherent to the exostome PPL (Papua New Guinea, Koponen 29691 H). (E) The outer face of the reduced peristome of Entodon piovani showing the ornamentation on the exostome OPL with the endostome visible behind (Ethiopia, s. leg. 1844 BM). (F) The outer face of the reduced peristome of Pylaisiobryum abyssinicum, exostome OPL. Adjacent teeth are still fused, and the OPL is abnormal with only one tier of cells on at least part of each tooth (Cameroon, Mann s.n. BM).

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that are of critical taxonomic significance. Thus, for example, Entodon dregeanus (Hornsch.) Müll. Hal. is characterized by lower cells with many tightly packed striations (Figure 12.2B). In contrast, in other species of subgenus Entodon, such as E. stereophylloides Broth. or E. lacunosus Broth., striations are fewer, broader and more loosely packed. This difference is even more conspicuous in the American species E. macropodus (Hedw.) Müll. Hal., for which Townsend (1991) proposed synonymy with E. dregeanus. Entodon macropodus can be consistently distinguished from E. dregeanus by, among other characters, the loosely packed striations of the exostome that give it a distinctive appearance even under the light microscope. Preperistome plates adhere to the outer face of the exostome and are formed by deposition in the cell layer external to the OPL. These plates were previously used to delimit Mesonodon (Buck, 1980; Gradstein et al., 2001). However, these structures have been found to occur sporadically in a range of species in both Entodon and Erythrodontium and to be lacking in many specimens of Mesonodon (Figure 12.2D). They appear to be an occasional by-product of peristome reduction and of no taxonomic significance in this family.

12.2.2 ENDOSTOME

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BASAL MEMBRANE

Entodon is the only genus in the family in which an endostome, though considerably reduced compared to a typical hypnoid endostome, is consistently present and occasionally taxonomically informative (Figure 12.3A) though this is confounded to some extent by the high level of intraspecific variation (Kungu et al., 2003). Species in Entodon subgenus Entodon are characterized by a coloured, ornamented endostome, whereas species in Entodon subgenus Erythropus usually have a pale or hyaline endostome. In Erythrodontium (Figure 12.3B), Mesonodon (Figure 12.2D) and Pylaisiobryum (Figure 12.2F) the endostome is absent or fragmentary and, if present, retains only hyaline fragments adherent to the PPL of the exostome. Occasionally these fragments preserve a residue of ornamentation indicative of the ancestral condition. In Mesonodon flavescens (Hook.) W. R. Buck these fragments may be papillose, but in all other species they are smooth. A much-reduced basal membrane is consistently present only in Entodon (Figure 12.3A). In the remaining genera with much-reduced endostomes the basal membrane is usually fragmentary or absent (Figure 12.3B). When present the basal membrane is usually two or three cells deep, inset below the mouth of the capsule, and the ornamentation varies widely within a species, or sometimes within a population, from smooth or faintly textured, through striate to papillose or a combination of both. This ornamentation may be similar to that on the inner face of the exostome. The basal membrane of E. stereophylloides is highly distinctive, being consistently strongly perforate. Reduction or absence of endostomial cilia is commonly associated with peristome reduction. Residual cilia in Entodontaceae are only consistently found in E. stereophylloides where they have the same range of ornamentation as the endostome segments. Cilia remnants are only rarely found in the other species in Entodon subgenus Entodon.

FIGURE 12.3 (See figure, facing page.) The inner surface of the peristome and TEM internal structure. (A) Inner face of Entodon dregeanus peristome showing reduced basal membrane three to four cells deep and striate ornamentation on the endostome (Malawi, Longton M8230a RNG). (B) Inner face of Erythrodontium barteri peristome showing basal membrane and PPL of the exostome. The endostome (A) is reduced to a few remnant cells and the basal membrane (B) is only two cells deep. The upper cell of the exostome PPL (arrowed) shows the characteristic ornamentation of this species (Sierra Leone, Thomas 510 BM). (C) TEM cross section of the exostome of Entodon lacunosus in the region of the vertical striations (Guinea, Lisowski 62 BR). (D) The outer face of the reduced peristome of Mesonodon flavescens, exostome OPL, with the endostome (arrowed) adherent to the exostome (Malaysia, Tixier 1707 PC). (E) Mesonodon flavescens, inner face (PPL) of the exostome showing the strong ornamentation associated with this species and the endostome (arrowed) adherent to the exostome (Papua New Guinea, Koponen 29691 H). (F) Entodon lacunosus endostome with the characteristic papillose ornamentation (Guinea, Lisowski 75 BR).

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Previous work has demonstrated a relationship between internal structure and the function of the peristome. Studies on Splachnum (Koponen, 1982), Fissidens limbatus (Mueller, 1973) and Racopilum momentous (Schnepf et al., 1978) all related the internal structure and chemical composition of the teeth to the nature of the hygroscopic movements. Exostome teeth are hygroscopic, responding to changes in humidity, whereas the endostome is comparatively unresponsive. In xerocastique species the exostome teeth close over the mouth of the capsule during conditions of high humidity, thus preventing spore release and water entry. Upon moisture loss the teeth open, allowing spore release in dryer conditions. All African species of Entodontaceae are either xerocastique or modified xerocastique. Pylaisiobryum abyssinicum (Müll. Hal.) Cufod. and Entodon piovani Bizot both have papillose exostomes with a modified xerocastique peristome where the exostome closes or almost closes in wet and dry conditions and opens briefly on drying. Vitt (1981) commented on the correlation between loss of function, and fusion or reduction in the peristome, concluding that loss of function precedes peristome reduction or fusion in xerophytic environments. However, observation of all species of African Entodontaceae proved that these peristomes retain some residual function. Even in those genera with extreme peristome reduction the remaining exostome remnants respond to changing levels of humidity, and when closed prevent spore release. Exostome function is related to both the internal anatomy and chemistry of the exostome and the form of the external ornamentation. The retention of massive ornamentation of the OPL enables the residual peristome in Entodontaceae to function. The OPL is much thicker than the PPL in taxa in Entodon subgenus Entodon, where the PPL:OPL thickness ratio grades from 1:10 at the base to 1:2.5 in the region of the transition from horizontal to vertical striations and only in the upper exostome does the PPL equal or exceed the thickness of the OPL. This differential thickness allows much more rapid swelling of the OPL during hydration and inward flexion of the exostome. Additionally the OPL striations provide an increased surface area for water uptake, and capillary action allows water to move to the interior of the exostome which can consequently respond rapidly to changes in humidity. Furthermore the internal structure of the tooth, with materials of differing density, reflects the external ornamentation and causes differential responses to water uptake, allowing curvature of the tooth (Figure 12.3C). Mechanically, the horizontal striations in the lower regions of the exostome allow maximum flexion of the tooth in this region, and the tooth displays almost no curvature in the region of vertical striations where the PPL is thicker than the OPL (Figure 12.3C). The apical zone, which has interrupted striations or papillae, or lacks any ornamentation, is either erect or incurved and here the PPL is massive and the much thinner OPL eventually losses its internal structure. Entodon is the only genus in the Entodontaceae with an endostome which, though residual, is consistently present and when the exostome is open, partially covers the mouth of the capsule. In Entodon and Pylaisiobryum the closed peristome forms a cone over the capsule mouth, but in the other genera the teeth, being shorter, close flat over the mouth, and the fragmented endostome adheres to the inner face of the exostome when the peristome is open. Perfect peristomes actively eject spores during opening and closing (Ingold, 1959; Ignatov et al., 1998), and this mechanism is absent in these reduced peristomes. Once the exostome is open spore release is a passive process, probably aided by twisting movement of the seta. There is no experimental evidence on the way in which the fine details of structure and ornamentation of the peristome may affect its function. Shaw and Robinson (1984) suggest that variation in the detail of the peristome ornamentation and structure may alter the air vortexes at the mouth of the capsule and thus modify spore release.

12.2.4 INTRASPECIFIC VARIATION IN PERISTOME ORNAMENTATION AND STRUCTURE Magill and Horton (1982), when considering the role of scanning electron microscope (SEM) photography in moss taxonomy, commented on the need to consider the possibility of interpopu-

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lation variation in spore morphology. Similar comments could be made with regard to the use of peristome morphology in taxonomy. Intraspecific variation in peristome structure and ornamentation was examined at population and individual levels in order to determine the validity of peristome character states as taxonomic characters. Full details of intraspecific variation are given in Kungu et al. (2003) and a summary is presented here. The four genera are divergent in the levels of intraspecific variation. Pylaisiobryum abyssinicum has the lowest level of intraspecific variation, with an almost uniform ornamentation pattern across its range from Cameroon to Ethiopia: the only variation is structural, in the extent of fusion of adjacent teeth and reduction of the number of cells of the OPL (Figure 12.2F). As currently recognized, taxa in the three remaining genera all display a higher level of intraspecific variation. This is highest in Mesonodon which throughout its range from Africa to Asia shows differing extent of exostome truncation and fusion of adjacent teeth and a wide range in disruption of ornamentation patterns (compare Figure 12.2D and Figure 12.3D). The exostome PPL, however, has a constant and distinctive ornamentation pattern (Figure 12.3E). This range of variation was contrary to previous accounts (Buck, 1980) and was based largely on examination of Asian material as most of the available African specimens lacked sporophytes. The peristomes of Erythrodontium often have an exostome truncated at or just above the horizontal striations. This was particularly common in E. julaceum (Schwaegr.) Par. Erythrodontium barteri (Mitt.) Broth. has a consistent pattern of ornamentation, with the horizontal and vertical ornamentation overlain with papillae, fusions and occlusions and forming a distinctive pattern on the OPL combined with a consistent reticulate ornamentation on the upper exostome PPL (Figure 12.2C and Figure 12.3B). Peristomes in species of Entodon have the least structural reduction, with the exostome usually tapering towards the apex rather than being abruptly truncated, and up to 700 μm long in E. lacunosus Broth. At the intraspecific level the African species in subgenus Erythropus appear uniform in peristome structure and ornamentation patterns, but only limited material was available for examination. However, within subgenus Entodon three species, E. dregeanus, E. lacunosus and E. stereophylloides, were available in sufficient numbers for comparison. Entodon dregeanus incorporates the widest variety within the current species boundary. These variations in ornamentation patterns affect both the exostome OPL and PPL and the endostome IPL. Common trends include the development of papillae along striations, disruption of striations, the transition to a striatepapillose pattern or the reduction of ornamentation to give an almost smooth surface along part of the tooth. As these variations showed no correlation with gametophyte morphology and no discontinuation in the range of peristome patterns could be discerned, they were not accorded taxonomic status within Africa. The question of the relationship of E. dregeanus with the Asian E. plicatus Müll. Hal. is still unresolved; these two species have a similar morphology, and are separated at present on differences in the papillosity of the endostome. Peristome variation in E. lacunosus was limited, with no overlap with E. dregeanus even though the gametophytes appear almost identical. The African E. stereophylloides exhibits a similar range of variation in endostome morphology to the group of American species that includes E. jamesonii (Taylor) Mitt. In America these species are separated mainly by endostome ornamentation, specifically by the presence or absence of papillae on the endostome (Buck, 1994, 1998). The question then arises whether this variation should be accorded any taxonomic status within Africa, and if so, at what level. The relationship with the American group of species also needs to be resolved. Variation patterns in the endostome of E. stereophylloides did not correlate with variation in the development of papillae on the OPL or PPL of the exostome. In addition, individual capsules exhibited a range from smooth, diffusely striate or sparsely to densely papillose endostomes. Low papillae were visible under SEM on specimens that appeared smooth or textured with the light microscope. In consequence, sporophyte morphology was considered consistent with the recognition of a single species in Africa and this was reinforced by a morphometric study of gametophyte morphology which failed to discern any difference between specimens with differing endostome ornamentation.

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12.2.5 SPORES According to Clarke (1979), spore morphology in mosses is most useful in taxonomy at and above genus level. Traditionally spore morphology has been used most frequently in the taxonomy of acrocarpous species. Smith (1974) proposed a generic rearrangement of Polytrichaceae, which was reinforced by spore morphology. Hirohama (1977), working on Orthotrichaceae, found spore morphology characteristic of genera, but Lewinsky (1974, 1977) found that groups within Tortula and Orthotricum based on spore morphology did not correspond with groups based on other characters. Ireland (1987) studied spore morphology in Plagiothecium and discovered two different types of ornamentation in the genus, as well as intraspecific variation in distribution of deposition over the spore and interpopulation variation in the size and shape of the papillae. He concluded that spore morphology was more significant in the taxonomy of acrocarpous than of pleurocarpous mosses. The main taxonomic characters are variation in spore size and in the extent and pattern of perine deposition. In Entodontaceae these differences reinforce generic boundaries, and are informative at species level (Figure 12.4). Entodontaceae spores are thin walled, single celled, spherical, atreme (without an aperture), and apolar. They appear slightly to coarsely papillose under the light microscope, and SEM reveals differences in surface ornamentation. Spore diameter varies from 10–14 μm in Entodon dregeanus and E. lacunosus to 25–32 μm in Erythrodontium julaceum. Surface sculpturing of Entodon spores is fine, ranging from textured in E. piovani to papillose in Entodon dregeanus and E. lacunosus, with individual papillae less than 0.5 μm diameter. The species pair Entodon dregeanus and E. lacunosus have identical spores ranging from 10 to 14 μm, and E. stereophylloides is distinguished by larger (18 to 22 μm), more regularly verrucose spores. Spores from the remaining genera have coarse ornamentation, with individual papillae 0.8 to 2 μm diameter and range from papillose to gemmate in Erythrodontium, verrucose in Pylaisiobryum, and gemmate in Mesonodon. Deposition is irregular over the spore surface, as Ireland (1987) found in Plagiothecium, with textured or granulose areas between papillae.

12.3 GAMETOPHYTE MORPHOLOGY AND DELIMITATION OF SPECIES BOUNDARIES 12.3.1 GROSS

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Gametophyte morphology is of major taxonomic significance at generic and specific levels. For bryophytes in general, and tropical pleurocarpous mosses in particular, there is only limited information on the influence of environmental parameters on these gametophyte character states. Work on widespread genera of acrocarpous mosses has demonstrated relationships between morphological variation within a species and geographical location, in relation to both genotypic and phenotypic variation. Longton (1981) examined Bryum argenteum over its global range and Montagnes and Vitt (1991) studied Meesia triquetra over the arctic-boreal gradient. Both species exhibit morphological variation in relation to geographical location and this has also been observed in pleurocarpous mosses such as Hylocomium splendens (Montagnes and Vitt, 1991). There is no information about the environmental effects of microclimate on the morphology of tropical bryophytes, most work until now having looked at temperate or higher latitude species, but the possibility of phenotypic plasticity cannot be excluded. One of the main limitations of working with only herbarium specimens is the absence of information about ecology or microenvironmental conditions. There is much anecdotal and some experimental evidence of phenotypic plasticity of the gametophyte, which often generates problems in identification. Early experimental work on a range of genera such as Drepanocladus (Lodge, 1959, 1960) and Dicranum (Briggs, 1965) confirmed this plasticity, and found that the phenotypic variation in some characters was so great that it masked any genotypic variation present and that different characters exhibited different

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FIGURE 12.4 Range of spore ornamentation displayed by the taxa currently included in Entodontaceae. (A) Entodon lacunosus (Guinea, Lisowski 75 BR); (B) Entodon dregeanus (Democratic Republic of Congo, Lisowski 5237 BR); (C) Entodon stereophylloides (Malawi, Longton M8411a RNG); (D) Entodon piovani (Ethiopia, s. leg.1844 BM); (E) Erythrodontium julaceum (Uganda, Chandler 2704 BM); (F) Erythrodontium barteri (Nigeria, Bup s.n. Oyesiku personal herbarium); (G) Pylaisiobryum abyssinicum (Ethiopia, Bassecco PC); (H) Mesonodon flavescens (Tanzania, Pócs and Lung’wecha 6880/V MO).

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ranges of variation in different taxa. Investigation of Brachythecium (Wigh, 1975, 1976) demonstrated that morphology was influenced by changes in humidity. Similarly Schofield (1981) reported an unpublished study by Williams, which demonstrated that the morphology of Isothecium stoloniferum depended on habitat, with specimens from exposed rock habitats having strongly julaceous shoots, while those from all other environments have more or less divergent leaves. However, under uniform conditions all these forms developed an identical morphology. In the Entodontaceae, Buck (1990) commented on a comparable variation in form displayed by Entodon mackaviensis Müll. Hal. in Australia and New Caledonia. It has a slender form when growing as an epiphyte in sheltered conditions and a robust and turgid form in exposed habitats, often on rocks. As numerous intermediates occur these forms were not given any nomenclatural status. Similarly, Ignatov et al. (1996), discussing the growth forms of Entodon schleicheri (Schimp.) Demet., commented that plants from very shaded or dry habitats were much thinner than those from other habitats. It is apparent, therefore, that although bryophyte taxonomy at the level of genus and species is founded primarily upon gametophyte morphology, there are inherent problems if species boundaries are based solely on a restricted number of gametophyte characters. Bryophytes are relatively simple plants with a limited range of morphologies available for taxonomy. The range of gametophyte characters available can be further constricted by evolutionary reduction, which may follow parallel or convergent paths in unrelated taxa. Phenotypic plasticity has been demonstrated in a variety of pleurocarpous mosses, and affects a different range of characters in different taxa, thus reducing the value of these plastic characters for species delimitation. Consequently, although much valuable taxonomic information can be obtained from the gametophyte, the possibility of phenotypic plasticity and ecotypic variation must be considered when species boundaries are based on a limited number of potentially correlated characters. Many aspects of gametophyte morphology are invariant within the family and unite the Entodontaceae as currently recognized. Characters in African taxa include leaves with numerous alar cells forming a triangular to rectangular alar region, laminal cells elongate, prosenchymatous and smooth, costa short and double, rhizoids smooth and reddish brown, and the morphology of the perichaetia and perigonia. However, the four genera can be defined by their gametophyte morphology (Figure 12.5). Entodon, the largest genus, lacks leaf decurrencies and has rectangular to trapezoidal alar regions. Erythrodontium is characterized by julaceous shoots with imbricate, decurrent leaves and a large triangular alar region of sub-quadrate cells extending up to half way up the leaf margin. Mesonodon has elongate triangular, plicate and decurrent leaves, whereas Pylaisiobryum has triangular leaves with distinctive margins; the marginal cells are slightly larger and with minutely thicker cell walls than adjacent laminal cells. This results in a subtle difference in the leaf margin, which is recurved in the dry leaf and plane or recurved above when hydrated. It is also the only genus lacking a central strand in the stem, and the axillary hairs and the development sequence of the branch primordia in Pylaisiobryum differs from all other genera in the family. Mizushima (1960) recognized two subgenera in Entodon and both are present in Africa. They are primarily distinguished by sporophyte characters, which are reinforced by differences in gametophyte morphology. Subgenus Entodon is predominantly complanate, while subgenus Erythropus is predominately julaceous. Species recognition in the gametophyte in Entodontaceae is frequently dependent on subtle variations in morphology. The only characters consistently useful at this level are overall leaf shape, especially the leaf apex, the shape and size of the alar region as expressed by the relative extent of the alar region along the leaf insertion and margin, and the shape of the alar cells. Understanding the sources of morphological variation within the gametophyte is a necessary precursor to trying to determine distinguishing characters for species with very similar gametophytes. One such source of morphological variation is the position of the leaf on the stem, especially in complanate species. To examine this relationship, leaves were recorded separately from the dorsal/ventral and lateral positions on both stems and branches in all complanate taxa. Dorsal/ventral

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FIGURE 12.5 Gross morphology of the four genera in Entodontaceae. (A) E. piovani (Ethiopia, Piovano 156 BM); (B) Erythrodontium julaceum (Tanzania, Pócs 6214/B PC); (C) Pylaisiobryum abyssinicum (Ethiopia, Bassecco s.n. PC); (D) Mesonodon flavescens (Malawi, Townsend 80/141 personal herbarium at K).

leaves have a transverse leaf insertion. Lateral leaves are at the side of the stem with an oblique insertion and only one alar region visible when viewed from above. The gametophytes of E. dregeanus and E. lacunosus are both strongly complanate and show significant differences in the means of all variables, except leaf length of E. dregeanus, between dorsal/ventral and lateral leaves on both stems and branches. The direction of the differences is the same on stems and branches of both species, but the magnitude of the differences is marginally greater on the stem leaves. The lateral leaves are broader, more elliptical in shape, and have the widest point higher up the leaf. Furthermore, the apex of lateral leaves is more obtuse, and the alar region is markedly larger, with more numerous and larger alar cells along both the margin and the insertion. The costa is longer in lateral leaves and the alar region more often extends to the costa. In contrast, the gametophytes of both E. stereophylloides and E. madagassus Müll. Hal. are terete to complanate. In these species there is little or no difference for many variables between dorsal/ventral and lateral leaves on either stems or branches. In E. stereophylloides the main difference between the lateral and dorsal/ventral leaves is in the larger alar region and longer alar cells of lateral leaves as compared with dorsal/ventral leaves.

12.3.2 AXILLARY HAIRS Although axillary hairs are not reduced structures per se, recent work has highlighted the taxonomic value of axillary hairs, particularly at the generic level. However, Hedenäs (1989) concluded that axillary hairs are uniform only within a genus if that genus is clearly delimited by other characters. Buck (1980) found axillary hairs of no value in the taxonomy of “higher pleurocarps”, but they

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have been useful in family level studies of Hookeriales (Buck, 1987) and Bartramiaceae (Griffin and Buck, 1989). Axillary hairs consist of one or two coloured basal cells and a number of hyaline ovate-cylindrical terminal cells with the apical cell the longest and often swollen. These hairs are believed to secrete mucilage and to have a protective function for the developing leaves. Taxonomic characters of the hairs include number per axil, number and colour of basal cells and number, shape and size of terminal cells. Buck (1980) found hairs only in the axils of young leaves, but in Entodontaceae some hairs usually persist after the leaves mature. The hairs closest to the costa tend to be longer and with more component cells than marginal hairs, as was observed by Newton and De Luna (1999) in a range of pleurocarpous genera. Axillary hairs in Entodontaceae are similar in shape but differ among the four genera in the size and number of terminal cells and number of hairs per axil. In Entodon these hairs are 90 to 165 μm long by 7 to 10 μm wide, and there are usually two to four hairs per axil. The basal cell is short, only 5 to 12 μm long, and slightly coloured. There are two to four terminal cells, all hyaline, 20 to 45 μm long, with the apical cell the longest. Pylaisiobryum abyssinicum has the longest hairs in the family at 145 to 240 μm with one to two coloured basal cells, four to seven terminal cells and only one or two hairs per leaf axil. Mesonodon and Erythrodontium both have shorter hairs, 50 to 110 μm long, with two to three terminal cells. The number of hairs per leaf axil is of very limited taxonomic value because hairs are caducous and the relative importance of environmental and genetic factors is unknown. However, the structural differences between the hairs in different genera appear to be consistent.

12.3.3 PSEUDOPARAPHYLLIA Pseudoparaphyllia also, although not reduced characters, are included here as they have been used as taxonomic characters in a range of pleurocarpous families and genera such as Plagiothecium (Iwatsuki, 1970), Hypnum (Ando, 1972) and Amblystegiaceae (Kanda, 1975). Problems of definition have constrained their use in the past as there was no consensus on the naming of the peripheral structures around the leaf primordial or the distinction between foliose pseudoparaphyllia and the outermost scale leaves surrounding the developing primordial (Hedenäs, 1995). Ireland (1971) surveyed the presence of pseudoparaphyllia in North American pleurocarps but found them only in one out of seven species of Entodon examined. Foliose pseudoparaphyllia were found in E. macropodus. Buck (1980) also reported the presence of foliose pseudoparaphyllia in Entodontaceae. The Entodontaceae has Climacium-type branch development (Akiyama, 1990), with branch primordia surrounded by inner scale leaves, which are broadly triangular and arch over the central primordium, covering it completely. External to these inner scale leaves there are erect peripheral structures, previously identified as foliose pseudoparaphyllia (Figure 12.6A). These peripheral structures are located at the junction of the stem epidermis and branch primordial cells. Stem transverse sections clearly show that the outer peripheral structures originate from the same tissue as branch primordial cells, which are distinguished from cortical stem cells by their larger size with thinner walls lacking pigmentation. In Entodon, Erythrodontium and Mesonodon these peripheral structures are present prior to enlargement of the primordium, and appear to develop from the initial divisions of the meristem. The peripheral structures form cell walls, whereas the cells of the inner scale leaves are still undifferentiated. Pylaisiobryum appears to have a different development sequence in that the first scale leaves in Pylaisiobryum are uniseriate and differ from those in the other genera (Figure 12.6B). Subsequent scale leaves are broader and occasionally divided at the apex. The preliminary scale leaves are presumed to have a protective function for the developing primordium. They are pushed apart and become more erect as the central primordium enlarges. The peripheral structures associated with the primordia are often arranged in whorls of three but the number of erect peripheral scale leaves per primordium can vary on a single stem, and they may be partially caducous once

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25 µm

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FIGURE 12.6 Vegetative branch primordial. (A) Entodon dregeanus branch primordium (Democratic Republic of the Congo, Lisowski 5237 BR). (B) Pylaisiobryum abyssinicum branch primordium (Ethiopia, Bassecco s.n. PC). (C) Mesonodon flavescens branch primordium with axillary hair in the axis of the outer pseudoparaphyllia (Tanzania, Pócs and Lung’wecha 6880/V MO).

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the inner scale leaves supplant their protective function. Axillary hairs can occasionally be found in the axils of both the outer erect and inner scale leaves (Figure 12.6C). Newton and De Luna (1999), looking at the transition to pleurocarpy, also found axillary hairs in the axils of erect peripheral scale leaves of the American Entodon hampeanus. In Entodontaceae these observations confirm the homology of outer peripheral structures with embryonic leaves. Within Entodontaceae there are several different shapes of outer scale leaves from usually broadly triangular in E. piovani to narrowly lanceolate in E. dregeanus (Figure 12.6A). The shape may vary among primordia along a single stem, as in E. stereophylloides. Nishimura (1985), working on Ctenidium, reported that interspecific variation in the shape of scale leaves paralleled that found in leaf shape. However, this does not consistently apply to Entodontaceae. Some specimens of Erythrodontium with concave julaceous leaves have lanceolate peripheral scale leaves around the primordia, whereas on the same stem peripheral scale leaves may be divided at the apex, have lateral teeth or even bifurcate. This range of shape could be a consequence of the caducous nature of the peripheral structures. The youngest primordia are usually protected by elongate lanceolate to filamentous structures, which are shed as the primordium enlarges and would be replaced at the periphery by the inner, broader scale leaves. The branch primordia along the stem do not necessarily mature in sequence. Consequently, it is possible to find immature primordia some distance from the apex, and below already developed branches. The definition of dormant in relation to branch primordia is problematic as a series of primordia at different stages of development occur on a single stem. It is possible that dormancy may not occur in these taxa which, growing in humid tropical habitats, do not experience seasonality and could potentially grow throughout the year.

12.4 A MORPHOMETRIC CASE STUDY There are two species of Entodon with overlapping ranges and almost identical gametophytes. E. dregeanus, mainly a southern, eastern and central African species, and E. lacunosus, which is found in central and West Africa. Both species occur on a similar range of substrates and Buck (1993) suggested that they may be synonymous, but they are clearly delimited by a suite of peristome characters. E. dregeanus has tightly packed, horizontal striations on the exostome OPL, extending up to or, rarely, two to three plates above, the capsule mouth, with oblique and vertical striations above (Figure 12.2B). These striations often bear papillae or become interrupted towards the apex. In contrast E. lacunosus has fewer, more loosely packed, horizontal striations extending three to eight plates above the capsule mouth, with oblique and vertical striations limited to 2–4 plates, and fine, dense, striate-papillose or interrupted papillose-striate ornamentation above. The endostome of E. lacunosus is fine to coarsely papillose and conspicuously perforate (Figure 12.3F), whereas that of E. dregeanus is striate to papillose-striate or fragmented-striate above, and strongly keeled but not perforate (Figure 12.3A). Both species may occasionally have endostomes grading to smooth, especially at the apex. Although easily distinguished when fruiting, the gametophytes of E. dregeanus and E. lacunosus are very similar and no qualitative differences could be found on examination of stem anatomy, axillary hairs, rhizoids, the peripheral structures around branch primordia, and perichaetia or perigonia. Canonical discriminate analysis (CDA) was used to explore the differences in leaf shape between these two species and assess whether any corresponding differences in the gametophytes reinforced those of the sporophyte generation. CDA requires a priori recognition of two distinct classes based on characters not included in the analysis and derives linear combinations of quantitative variables that summarize the between-class variation. Here CDA was used to analyse 11 measurements of leaf shape from dorsal/ventral and lateral stem and branch leaves of the two species of Entodon previously defined by peristome ornamentation. Discriminate analysis also computes a discriminate function (DF) which can be used to classify observations. The success of the DF in classifying observations was measured by two data-based

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error estimators, resubstitution and cross validation. Resubstitution involves classifying each observation in the dataset using the DF generated by the dataset and calculating the number of misclassifications. Cross validation is more rigorous, as each observation in turn is omitted from the dataset and the DF recalculated on n–1 observations, and this new DF is used to classify the single observation omitted from the dataset. This is repeated for all observations to give a direct estimator of error rate. The final analysis using a reduced character set of the ten most informative characters, each variable being the mean of five replicate observations, achieved 100% discrimination between the two species as assessed by both methods of error estimators. It was therefore concluded that there was a real difference in the gametophyte morphology, reinforcing discernable differences in peristome morphology (Kungu, 2003). A comparable analysis was undertaken with the two groups of specimens within E. stereophylloides with differing endostome ornamentation to test for any corresponding differences in gametophyte morphology. No significant difference was found; rather these endostome groups were associated with a gradation in gametophyte morphology. This conclusion reinforced evidence from the sporophyte that, although the two extremes of the range ornamentation pattern were very distinct (and initial response may be to accord them taxonomic status), there are numerous specimens which appear to be intermediate, and cannot easily be assigned to either group. Consequently, no taxonomic recognition was accorded to groups with different endostome ornamentation, and the single species E. stereophylloides was recognized in Africa.

12.5 EVALUATION OF CHARACTERS The extent of phenotypic plasticity in morphological characters is difficult to access in this type of study, but some impression can be formed by consideration of the range of character states exhibited by individual plants and populations. Some characters, such as leaf margin serration and costa length, are clearly highly variable within a single population, and carry little taxonomic information at the species level. Others, such as colour, are distinctive for some species, but are subject to modification by environmental conditions, and are therefore of limited value. The suite of characters associated with the alar region is highly informative in Entodontaceae, but care is required in interpretation of these character states. Experimental work on temperate genera, such as Drepanocladus, has shown that the morphology of the alar region can be highly plastic in some taxa. In addition, as number of alar cells and size of those cells vary according to the position of the leaf on the stem, the overall size of the alar region and extent along the insertion axis will depend on the position of the leaf on the stem. Consequently, these characters, which are modified by environmental conditions or exhibit systematic variation within a specimen, can contribute valuable taxonomic information, but only once the different ranges of variation are known. There is a need for critical examination of character states used to delimit taxa in genera where gametophyte morphology is very similar. Buck (1990) differentiated between the gametophyte of the African Entodon dregeanus and the Asian E. plicatus because the alar region of E. dregeanus extended to the costa in most leaves. However, this character state is very variable and most specimens of E. dregeanus have some basal cells between the alar region and costa. Recent attention given to axillary hairs and pseudoparaphyllia has proved of limited value in Entodontaceae. Pylaisiobryum is separated from the remaining genera in the family by axillary hairs and branch primordia as well as leaf shape and growth form. The three remaining genera had some size differences in axillary hairs and branch primordia, but there is no clear separation in these characters between the genera. Peristome morphology is fundamental to taxonomy of the Entodontaceae. It defines the family in the combination of reduced and strongly ornamented peristomes that are not found in other pleurocarpous taxa. Genera, and subgenera within Entodon, are also delimited by sporophyte morphology. However, species delimitation based on peristome morphology is complex, owing to the range of variation in ornamentation patterns associated with reduced peristomes. There are

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some clear species boundaries in sporophyte morphology, when a suite of consistently correlated characters provides species definition. The separation of E. dregeanus and E. lacunosus is one such example, where species delimitation based on sporophyte characters is also reinforced by subtle but statistically significant differences in gametophyte morphology. There are ranges of intraspecific variation in sporophyte morphology, and specifically peristome ornamentation patterns, and common trends are found in the three species of Entodon examined in detail. These common trends include fragmentation of striations, papillae borne along the length of the striations or reduction of the underlying striae and replacement by papillae. The striate basis of ornamentation is usually apparent in the SEM photographs. Additional trends include ornamentation absent or sparse towards the apex, exostome PPL, endostome and/or basal membrane smooth, and wide variation in the presence and width of the exostome border. These variation patterns occur in all three widespread African species of Entodon. Taxonomic recognition of species or varieties based on these features would result in the description of an unnecessarily large number of taxa, with no clearly defined boundaries and based on features that may not be stable from generation to generation.

12.6 EVOLUTION OF REDUCTION The Entodontaceae is distinguished by the coincidence of a number of reduced features in both generations. This predominance of reduced features creates a problem for determining the relationship of the Entodontaceae to the other families within the Hypnales. Few molecular studies include taxa from the Entodontaceae and some of those only include a single exemplar (Buck et al., 2000; Tsubota et al., 2000). Tsubota (2001a, 2001b) sequenced five species of Entodon and demonstrated the family as sister to the Sematophyllaceae. Unfortunately his exemplars included only Asiatic members of Entodon subgenus Erythropus and consequently fail to resolve the family, as currently recognized, as monophyletic. The evolution of reduction is acknowledged as an advanced state recurrent across a wide range of acrocarpous and pleurocarpous taxa. In particular peristome reduction is consistently associated with the adoption of the epiphytic habit. This convergent evolution across such a broad taxonomic spectrum indicates a strong adaptive advantage. The value of this suite of reduced and co-occurring character states in the peristome as synapomorphies defining the family is therefore called into question. Interpretation of the range of ornamental patterns found within the family as currently recognized is also problematic. Are these ancestral states that predate the evolution of reduction? Given the complexity of the internal anatomy of the striate and papillose exostomes, it is tempting to consider these as ancestral. The alternative hypothesis that the peristome evolved the reduced state and concurrently or subsequently evolved these different ornamental patterns together with the marked internal differentiation seems contradictory. A further complication is the degree of variation in ornamentation occurring within species as currently recognized. This would seem to be indicative of recently acquired variation, presumed superficial, and not associated with internal differentiation or function. Unfortunately the peristomes of only a limited number of species have been examined in transverse section, so this remains to be confirmed. Variation in the ornamentation of the endostome is almost certainly superficial as none of the endostomes sectioned so far displays any internal differentiation, as would be expected given the absence of hygroscopic response by the endostome. The taxonomic implication of this range of variation is more difficult to discern in genera such as Mesonodon where the global distribution includes a distinctive range of variation based on a striate foundation. The Neotropical/African disjunction also requires further examination. Currently the African E. stereophylloides is considered sister to the American complex of species which includes E. jamesonii. Further work may resolve this complex as one or a number of species with a Neotropical/African disjunction or a number of distinct African and American taxa. The possibility of recent radiation and cryptic speciation has to be considered in both these cases.

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Given that the degree of structural reduction and the detailed pattern of peristome ornamentation can vary within a single capsule, factors other than genotype must also exert an influence on the developing sporophyte, which appears to retain a certain level of plasticity although the determining factors are at present unknown. Evidence from Pterigynandrum filiforme also indicates that peristome reduction may be associated with increased variation in peristome ornamentation patterns (Buck, 1980). Tolerance of a greater range of variation in ornamentation would be possible when reduction in structure co-occurs with reduction or loss of function and a range of peristome variations, which were compatible with the reduced level of function, could persist in the population. It is suggested that the high level of variation in both structure and ornamentation of the peristome is a corollary of reduction as aberrant forms can survive in the population if the abnormality is not detrimental to the residual function of the peristome. Differences between capsules on the same plant or within a population could be the consequence of the breeding system. African Entodontaceae are autoicous, and work on other autoicous mosses has demonstrated very short fertilization distances (Anderson and Lemmon, 1974). Stark (1983), working on the reproductive biology of Entodon cladorrhizans (Hedw.) Müll. Hal., also an autoicous species, did not consider fertilization distance. He did, however, examine phenology and concluded that self-fertilization predominates. The possibility for occasional cross-fertilization remains if the population contains a range of genotypes and this out-crossing would produce new combinations, the successful variants among which would be perpetuated in the population by the predominant self-fertilization (Longton, 1994). Given that African Entodontaceae are autoicous and self-fertilization may predominate, the expectation is that there will be limited variation within a colony but higher levels of variation among populations, depending on the range of genotypes present and the extent of out-crossing in the breeding system. Isolated populations may often be single clones and the sporophytes resulting from persistent self-fertilization would be homozygous and little or no morphological variation, unless due to phenotypic plasticity, would be expected within that colony. However, even occasional out-crossing would increase variation within a genetically diverse population and interpopulation variation could result from founder effect and genetic drift in genetically heterogeneous colonies. Hedenäs (2001), from a survey of 439 pleurocarpous mosses, identified a suite of sporophytic traits correlated with the epiphytic condition. These included erect, straight, ovoid to cylindrical capsules, hydrocastique peristomes (peristomes that open in conditions of high humidity and close when dry), absence of annulus, rostrate opercula, short seta, reduced exostomes, papillose or smooth lower exostomes, absence of exostome border, reduced PPL, low basal membrane, short cilia and large spores. The African species of Entodontaceae are predominantly epiphytic, and the different genera demonstrate a gradation in the adaptation to epiphytism. Entodon has the least modified peristome, with a reduced but intact exostome and an endostome. However, the African species are xerocastique rather than hydrocastique and some species of Entodon which are not strictly epiphytic also have small spores and longer seta. Mesonodon and Pylaisiobryum, in contrast, are strictly epiphytic and both have larger spores and a strongly reduced peristome lacking an endostome.

12.7 DISCUSSION The range of variation in both structure and ornamentation patterns associated with the reduced peristomes in Entodontaceae calls into question the reliability of distinguishing species, especially in Entodon, using only single peristome characters without additional support from the morphology of the gametophyte. As a consequence of this, much of the variation in peristome ornamentation in Africa is not accorded taxonomic status at present. However, in spite of the fact that these are highly reduced structures with very variable ornamentation patterns, peristome structure and ornamentation can be highly informative taxonomically at both generic and species levels. There must be some reservations about the monophyly of a family united on the basis of cooccurring characters of erect capsule and reduced peristome, since this combination occurs repeat-

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edly throughout the pleurocarps in a wide variety of families. It is true that the retention of massive ornamentation on the OPL is an unusual characteristic among reduced peristomes, which are more commonly smooth and hyaline, but the range of ornamentation patterns exhibited by the taxa within the Entodontaceae questions the value of this characteristic as a defining trait for the family. Morphological studies have raised a number of questions which could be addressed by the available range of molecular techniques. 1. Are the Entodontaceae and Entodon monophyletic? 2. What is the relationship between the taxa with papillose and striate peristomes, and is this a recent or ancient divergence? 3. What is the relationship between the African and American taxa? 4. Is the observed intraspecific variation in peristome ornamentation patterns a result of cryptic speciation, clonal variation or phenotypic variation? 5. What is the age of the evolutionary divergence of these taxa? Certainly the morphological studies question the position of Pylaisiobryum which differs from the other genera in a number of key characters. Recent work on microsatellites in the liverwort genus Anastrophyllum has resolved the identification of two disjunct and previously confused species (Squirrell and Long, personal communication). Such population studies may resolve some of the issues of species delimitation presently unresolved by morphological studies, such as the true relationship between the African Entodon stereophylloides and the group of American species that includes E. jamesonii or between the African Entodon dregeanus and the Asian E. plicatus.

ACKNOWLEDGMENTS Thanks are due to the curators from the following herbaria who loaned material for this study: B, BM, BOL, BR, C, E, EGR, F, FH, FI, G, H, HBG, JE, L, LIVU, M, MANCH, MICH, MO, NAI, NMW, NY, OXF, PC, PRE, RNG, RO, S, TOM and ZT. This work has been partly assisted by a grant by the International Association of Bryologists (IAB) from the Stanley Greene Award to E. M. Kungu. Thanks to Mr. A. E. and Mrs. J. W. Field and the late Miss M. Pavier who provided financial support towards research costs.

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Magill, R. E. and Horton, D. G. (1982) The scanning electron microscope and moss taxonomy. In Bryophyte Taxonomy: Methods, Practices and Floristic Exploration (ed. P. Geissler and S. W. Greene). Nova Hedwigia, 71: 137–147. Mitten, W. (1859) Musci Indiae Orientalis; an enumeration of the mosses of the East Indies. Journal of the Linnaean Society, Botany, 1: 1–171. Mizushima, U. (1960) Japanese Entodontaceae. Journal of the Hattori Botanical Laboratory, 22: 91–158. Montagnes, R. J. S. and Vitt, D. H. (1991) Patterns of morphological variation in Meesia triquetra (Bryopsida: Meesiaceae) over an Arctic-Boreal gradient. Systematic Botany, 16: 726–735. Mueller, D. M. J. (1973) The peristome of Fissidens limbatus. University of California Publications in Botany, 63: 1–34. Newton A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Nishimura, N. (1985) A revision of the genus Ctenidium (Musci). Journal of the Hattori Botanical Laboratory, 58: 1–82. Schnepf, E., Stein, U. and Deichgräber, G. (1978) Structure, function and development of the peristome of the moss, Racopilum tomentosum, with special reference to the problem of microfibril orientation by microtubules. Protoplasma, 97: 221–240. Schofield, W. B. (1981) Introduction to Bryology. Macmillan, New York. Shaw, J. (1985) The correlation between taxonomy and peristome structure in the Bryaceae. Journal of the Hattori Botanical Laboratory, 59: 79–100. Shaw, J. and Robinson, H. (1984) On the development, evolution, and function of peristomes in mosses. Journal of the Hattori Botanical Laboratory, 57: 319–335. Shaw, J. and Rohrer, J. R. (1984) Endostomial architecture in diplolepideous mosses. Journal of the Hattori Botanical Laboratory, 57: 41–61. Smith, G. L. (1974) New developments in the taxonomy of Polytrichaceae: Epiphragm structure and spore morphology as generic characters. Journal of the Hattori Botanical Laboratory, 38: 143–150. Stark, L. R. (1983) Reproductive biology of Entodon cladorrhizans (Bryopsida, Entodontaceae). I. Reproductive cycle and frequency of fertilisation. Systematic Botany, 8: 381–388. Townsend, C. (1991) Notes on mosses from Ceylon and India. VIII. Another moss with three names in three continents. Journal of Bryology, 16: 601–605. Tsubota, H., Nakao, N., Yamaguchi, T., Seki, T. and Deguchi, H. (2000) Preliminary phylogenetic relationships of the genus Brotherella and its allied genera (Hypnales, Musci) based on chloroplast rbcL sequence data. Journal of the Hattori Botanical Laboratory, 88: 79–99. Tsubota, H., Akiyama H., Yamaguchi, T. and Deguchi, H. (2001a) Molecular phylogeny of the Sematophyllaceae (Hypnales, Musci) based on chloroplast rbcL sequences. Journal of the Hattori Botanical Laboratory, 90: 221–240. Tsubota, H., Akiyama H., Yamaguchi, T. and Deguchi, H. (2001b) Molecular phylogeny of the genus Trismegistia and related genera (Sematophyllaceae, Musci) based on chloroplast rbcL sequences. Hikobia, 13: 529–549. Vitt, D. H. (1981) Adaptive modes of the moss sporophyte. Bryologist, 84: 164–186. Wigh, K. (1975) Scandinavian species of the genus Brachythecium (Bryophyta). I. Modification and biometric studies in the B. rutabulum–B. rivulare complex. Botaniska Notiser, 128: 463–475. Wigh, K. (1976) Scandinavian species of the genus Brachythecium (Bryophyta). II. Morphology, taxonomy and cytology in the B. rivulare complex. Botaniska Notiser 128: 476–493.

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of Stem 13 Homologies Structures in Pleurocarpous Mosses, Especially of Pseudoparaphyllia and Similar Structures Michael S. Ignatov and Lars Hedenäs CONTENTS Abstract ..........................................................................................................................................269 13.1 Introduction...........................................................................................................................270 13.2 The Ontogeny of Stem Parts................................................................................................270 13.3 Stem Structures: Review of Current Knowledge and Ideas................................................270 13.3.1 Rhizoids ....................................................................................................................271 13.3.2 Axillary Hairs ...........................................................................................................271 13.3.3 Branches ...................................................................................................................272 13.3.3.1 Ordinary Branches ....................................................................................273 13.3.3.2 Sympodial Branches .................................................................................273 13.3.3.3 Subterminal Branches ...............................................................................274 13.3.3.4 Brood Branches.........................................................................................274 13.3.3.5 Sexual Branches ........................................................................................274 13.3.4 Leaves .......................................................................................................................274 13.3.5 Pseudoparaphyllia and Paraphyllia ..........................................................................275 13.3.5.1 Pseudoparaphyllia .....................................................................................275 13.3.5.2 Paraphyllia.................................................................................................276 13.3.5.3 An Alternative Classification of Paraphyllia and Pseudoparaphyllia ......277 13.3.5.4 The Differentiation between Pseudoparaphyllia and Proximal Branch Leaves ...........................................................................................283 13.4 Summary and Conclusions...................................................................................................284 Acknowledgments ..........................................................................................................................284 References ......................................................................................................................................285

ABSTRACT An overview of current definitions of different stem structures in pleurocarpous mosses is given, covering rhizoids, axillary hairs, branches, leaves, pseudoparaphyllia, and paraphyllia. Paraphyllia are usually considered as structures not concentrated around branch primordia, but our observations revealed that in Alsia, Cratoneuron, Leptodon, Leskea and Palustriella, as well as in the 269

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secondary branches of Thuidium, “paraphyllia” are more abundant near branch primordia or situated, often in pairs, at sites of undeveloped branch primordia. Therefore, we suggest that in these taxa “paraphyllia” are probably homologous to pseudoparaphyllia. This fact was previously neglected due to the diffuse distribution of pseudoparaphyllia along the stem far from branch primordia, and in the extreme cases, such as Thuidium, these pseudoparaphyllia covered the stem densely. These structures are different from “true paraphyllia,” which are evenly distributed throughout the stem. The latter are found in Climacium, Hylocomiastrum, Hylocomium, Lescuraea and Loeskeobryum and are characterized by their arrangement on low longitudinal ridges. The distinction between pseudoparaphyllia and proximal branch leaves remains unclear; a set of characters for the description of the diversity of foliose structures found at the base of branches, or around branch primordia is suggested. This replaces the commonly generalized character of pseudoparaphyllia absence versus presence.

13.1 INTRODUCTION Definitions of many stem structures in pleurocarpous mosses are currently inconsistent, unclear or both, which has led to many differing morphological interpretations. Few bryologists would dispute what a stem or branch leaf is, even if some botanists insist on a terminology that reflects the nonhomology between bryophyte and vascular plant leaves (e.g., Sitte et al., 1998), whereas there exists a serious gap in our understanding of most other stem and branch structures. In this chapter we therefore explore how to improve our understanding and definitions of a number of stem structures. We will focus especially on the controversies concerning what proximal branch leaves (also called scaly or juvenile leaves), pseudoparaphyllia and paraphyllia are, and on how they relate to each other. Ideally, we believe that such definitions should be consistent with our knowledge of the morphology, anatomy and position of the structures, as well as with our knowledge regarding their origin or ontogeny. Here we present an overview of stem structures that takes into account the knowledge accumulated so far, at the same time acknowledging that future morphological and ontogenetic studies of such structures may challenge our current view.

13.2 THE ONTOGENY OF STEM PARTS The early ontogeny of the successively homologous stem portions in pleurocarpous mosses, the metamers, has been the subject of several studies (Berthier, 1971; Crandall-Stotler, 1984; Frey, 1970; Goebel, 1898, 1915; Kawai, 1977; Müller, 1909). The stem grows from a meristematic tetrahedral apical cell that splits off cells, the apical cell derivatives, which later form one metamer each (Figure 13.1). Each apical cell derivative divides into two cells, the inner of which (II) gives rise to the main portion of the stem tissue. When the outer cell (I) divides, its daughter cells give rise to the branch primordia and associated outermost stem layer(s) (I1) and to the leaf and leaf base, including some outer stem tissue near the leaf base (I2), respectively (Figure 13.1). The origin of stem structures in one of these three early derivatives of the apical cell could be important for the circumscriptions of different stem structures and assessments of their homology. This origin of structures will be discussed in the next section.

13.3 STEM STRUCTURES: REVIEW OF CURRENT KNOWLEDGE AND IDEAS In this overview we include structures that are inserted directly on the stem, and structures that are mostly found on the stem, but which may in some cases be found also on the leaves. The main topic of this chapter is not perichaetia and perigonia, but these highly specialized organs are nevertheless discussed briefly under “Branches.”

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I2 Leaf and lead base (including some outer stem tissue). I Apical cell derivative

I3 Branch primordia and outer stem layer(s).

II

Main portion of stem tissue.

Apical cell

FIGURE 13.1 Early divisions of a single metamer. Shoot apex photo of Floribundaria floribunda (Dozy & Molk.) M. Fleisch. Diagrammatic portion of the figure after Frey (1970), based on Neckera crispa Hedw. and Calliergonella lindbergii (Mitt.) Hedenäs.

13.3.1 RHIZOIDS Rhizoids are uniseriate filamentous structures with oblique walls between adjacent cells. Most pleurocarpous mosses have red-brown rhizoids, but in the Plagiotheciaceae numerous taxa have purplish rhizoids. In many Hookeriales taxa, Anacamptodon, Plagiothecium and Thuidium delicatulum (Hedw.) Mitt. rhizoids may be entirely or in large portions hyaline. Most pleurocarp rhizoids are smooth, but sometimes they are granular-papillose (Plagiotheciaceae), or warty-papillose (e.g., Amblystegiaceae). In many groups of mosses creeping growth on hard substrates, such as rocks and bark, induces abundant rhizoid production all along the stem on the substrate-facing side. However, when pleurocarpous moss rhizoids develop “spontaneously,” that is, not as a response to the shoot touching a substrate, they are usually found at the dorsal transition zone between the leaf costa and stem. In some pleurocarps, for example in some species of the Antitrichiaceae, Calliergonaceae, Cryphaeaceae, Fabroniaceae and Plagiotheciaceae, rhizoids are frequently found high up on the dorsal side of the leaf costa. Many species, for example in the Hookeriaceae, Calliergonaceae and Plagiotheciaceae, have rhizoids that arise from various parts of the leaf lamina, especially from rhizoid initials close to the leaf apex. These positions suggest an origin of most rhizoids from cell I2 (Figure 13.1). However, rhizoids may also develop from scattered positions on the stem (e.g., in many Calliergonaceae), from around branch primordia, or from the stem just above the leaf axils, “axillary rhizoids” (e.g., in many Plagiotheciaceae). This means that they have their origin in cell I1 (Figure 13.1). In the Hylocomiaceae axillary rhizoids are found in the most distal portions of the branches in species that otherwise have rhizoids arising from the more common position of the costa-stem transitions. In the Calliergonaceae rhizoids developing from scattered points of the stem are found in many species, for example in Calliergon and Warnstorfia, where rhizoids can also develop from the leaves. The diverse positions of rhizoids of various ontogenetic origins in different taxa refute their positional homology. However, the fundamentally similar structure of all rhizoids implies that they nevertheless have a similar genetic background and are therefore considered to be homologous.

13.3.2 AXILLARY HAIRS Axillary hairs are supposedly mucilage-secreting structures (Schofield and Hebant, 1984), although other functions may be as important (Hedenäs, 1990). Berthier (1971: Plate 12, Figure 6, etc.) showed that in the earliest stages of development, axillary hairs cover the cell that later differentiates into a branch. The hairs consist of a basal portion with mostly small and often pigmented cells, and a distal portion of larger, usually elongate and mostly hyaline cells. The latter may become brown in old shoot portions. The hairs are usually unbranched and uniseriate but in a few cases, such as in the Meteoriaceae, the hairs may be biseriate or branched (Quandt et al., in 2004). They

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TABLE 13.1 Species in Which Axillary Hairs Were Observed at Various Stem Positions Outside the Leaf Axils Occasional or Single Hairs from Scattered Points along the Stem Brachythecium plumosum (Hedw.) Bruch et al. Eurhynchium asperipes (Mitt.) Dix. Neckera douglasii Hook. Rauiella scita (P. Beauv.) Reimers Regmatodon polycarpus (Griff.) Mitt. (just outside branch primordia) Vesiculariopsis spirifolium (Dusén) Broth. Hairs from Scattered Points on the Stem and in Paraphyllia Axils Abietinella abietina (Hedw.) M. Fleisch. Actinothuidium hookeri (Mitt.) Broth. Boulaya mittenii (Broth.) Cardot Helodium blandowii (F. Weber & D. Mohr) Warnst. Hairs Scattered among Paraphyllia Hylocomium splendens (Hedw.) Bruch et al. Haplocladium microphyllum (Hedw.) Broth. Occasional Hairs in Axils of Paraphyllia Thuidium tamariscinum (Hedw.) Bruch et al.

are usually inserted in the leaf axils or on the stem 1 cell above the axil. This suggests that their origin is from cell I2 (Figure 13.1; cf. Kawai, 1977). However, in numerous pleurocarpous mosses, especially in those with paraphyllia, “axillary hairs” are regularly or occasionally found at other stem positions, clearly outside the leaf axils (Table 13.1). In these cases the axillary hairs must have originated from cell I1 (Figure 13.1). Although their traditional definition and even their name imply that axillary hairs are in an axillary position we believe that, by analogy with the case for rhizoids, the striking morphological and anatomical similarities imply a similar genetic background and that they are therefore homologous. More or less gradual transitions between axillary hairs and paraphyses are found within perichaetia. These transitions clearly suggest the homology of these structures, and it is especially obvious in mosses that have special colours of their axillary hairs or some of its cells (cf. Zolotov and Ignatov, 2001).

13.3.3 BRANCHES Like the stems, the branches consist of metamers that show successive homology. Branches are initiated as branch primordia from the outermost cell layers of the stem (Frey, 1970), or possibly from a cell of the layer below the epidermis, covered or semicovered by a cell that further develops into an axillary hair (Berthier, 1971). In both cases branches originate from cell I1 (Figure 13.1) of a young stem module. Most branches can produce all structures produced by the stems, including branch primordia and sometimes also secondary branches, but sometimes character states of stems and branches differ (e.g., the rhizoid positions in the Hylocomiaceae). In contrast to most stems in pleurocarpous mosses a typical branch has a limited growth, terminated after a number of modules have been produced from the branch apical cell. For descriptive purposes several types of branches can be recognized in mosses.

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13.3.3.1 Ordinary Branches Usually referred to simply as “branches,” these are a result of monopodial branching (La FargeEngland, 1996) of the stem, producing secondary modules borne on primary modules. These branches are determinate, i.e., have a limited ability to elongate (in many genera, like Abietinella, Hypnum, Ptilium and Sanionia, the branches are about 10 times shorter than the stems), resulting in a pinnate appearance of the plants. Plants with numerous well-defined ordinary branches often show differences between stem and branch leaves. In many taxa the branch leaves are smaller than the stem leaves, and relatively narrower, with more strongly serrate margins, and have shorter laminal cells and less well-differentiated alar cells. Sometimes there is a clear difference in leaf shape between stem and branch leaves. 13.3.3.2 Sympodial Branches These are the result of sympodial branching, forming a chain of modules at the same level of hierarchy. Sympodial branches may exhibit the same heteroblastic series of leaves as the main stem. The difference between monopodial and sympodial branching has been discussed by La Farge-England (1996), who explained their differences in a series of illustrations and in terms of module hierarchy. Ordinary branches are modules of level N+1 borne from modules of level N (example: branches of Ptilium), whereas sympodial branches are modules of level N borne from modules of level N (example: shoot innovation of Hylocomium). This definition is helpful in mosses with dendroid or otherwise complex architecture, where the level of module hierarchy can usually be determined without difficulty. However, in some families the level of hierarchy is not always apparent, and may not always be expressed in an integer. Both ordinary branches and sympodial branches possess branch primordia in leaf axils, and therefore potentially ordinary branches do not differ from sympodial branches; thus their difference is functional rather than structural. In branches, the lateral primordia are usually dormant (except species with regular bior three-pinnate branching). Release from dormancy is a cytokinin-dependent process (Bopp, 1981); thus the developmental program of a module can be changed during its growth due to internal and external factors. In Brachythecium or Amblystegium, for example, there are many branches that are difficult to attribute to definite levels of module hierarchy. For example, branches can be longer than ordinary branches and slightly branched, but not branched as much as in sympodial branches. Leaves in these intermediate branches are also intermediate between stem and branch leaves. However, the presence of a few ordinary branches (those that are much shorter than the stem) implies monopodial branching. This branching is usually called sparsely pinnate or irregularly pinnate versus regularly pinnate. It seems important to separate the cases with poor differentiation between ordinary and sympodial branches from the cases where only sympodial branching occurs, as in Plagiothecium and Hookeria. In these genera, the “branches” are structurally almost indistinguishable from “stems” and usually develop at a distance from the apex of the “stem” (often where gametangia develop). The shoots never exhibit pinnate branching although the position of the branch primordia would suggest a pinnate branching pattern. It seems incorrect to us to consider any branches in Hookeria and Plagiothecium as “ordinary” in the sense described above, and likewise to call any of the leaves in these groups “branch leaves.” In a way, the branching pattern in these taxa resembles that found in some acrocarpous mosses, such as Polytrichum or Schistostega, where the “stems” could just as well be called sympodial branches unless they were derived from protonemal buds (probably a minority in most populations). Thus, what we describe as ordinary branches, and the pinnate branching pattern, have most likely evolved in the pleurocarps (fasciculately arranged ordinary branches evolved independently in Racomitrium and Sphagnum). Special cases of sympodial branches are those that form stolons, i.e., specialized shoots with small and often quite distant leaves. At a certain stage stolons either gradually transform into normal

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stems (Leucodon, Anomodon), or lateral branch primordia develop into what are usually called secondary stems (Neckeraceae). In Neckera, for example, stolons may be borne on ordinary branches, representing a decrease in the level of hierarchy. 13.3.3.3 Subterminal Branches Subterminal branches are sympodial branches that develop just below a terminal gynoecium or androecium. Subterminal branching is especially common in acrocarpous mosses, and in many groups most of the shoots are just a series of subterminal branches (e.g., Pottiaceae, Grimmiaceae). Subterminal branches, or secondary axes from the basal part of perichaetia in cladocarpous mosses, are present in many members of the Hypnales (La Farge-England, 1996), but their role in the plant architecture is almost never comparable with that of ordinary branches. 13.3.3.4 Brood Branches Brood branches are much smaller than ordinary branches and are easily broken off. They are usually clustered in leaf axils just below the stem apex. They are always a result of monopodial branching. 13.3.3.5 Sexual Branches Sexual branches are terminated by sexual organs, and fertilized female organs on such branches produce one or occasionally several sporophytes. Sexual branches in the Hypnales can grow both from stems and branches, though rarely from other sexual branches. Exceptions occur mainly in some cladocarpous species, for example within the Cryphaeaceae. Male branches produce perigonial leaves, axillary hairs, rhizoids, antheridia and paraphyses. Female branches produce perichaetial leaves, axillary hairs, rhizoids, sometimes paraphyllia, rarely branch primordia, archegonia and paraphyses. In synoicous species, antheridia may be found mixed with archegonia on such branches. In autoicous species, perigonia and perichaetia are frequently produced in a specific order, at least under seasonal climates. For example, in the Calliergonaceae, perigonia are normally found below the perichaetia on the stem. Although sexual branches are not the subject of this chapter, it is worth noting that in perichaetia and perigonia there is a striking serial homology in the transition series from basal to upper leaves, and also there are structures for which morphology, but not position, suggest that they are homologous (e.g., axillary hairs and paraphyses). There are also varying degrees of suppression of some structures such as branch primordia and paraphyllia.

13.3.4 LEAVES The leaves are probably the most important structures in terms of photosynthetic activity, contact with the surrounding atmosphere, and often the uptake of water, minerals and nutrients. Leaves are always produced from cell I2 (Figure 13.1), but are otherwise variable in both shape and structure. As noted above some structures that are mostly associated with the stem, such as rhizoids and paraphyllia (see below), may grow from various parts of the leaves. Stem and branch leaves may be more or less similar in irregularly branched species, as in Amblystegium serpens (Hedw.) Bruch et al., or strikingly different, as in Kindbergia praelonga (Hedw.) Ochyra. In addition, the proximal branch leaves are mostly very different from the leaves further up on the branches, with a series of transitional leaves in between. The distinction between proximal branch leaves, or scaly leaves, and pseudoparaphyllia is not always clear, and this will be discussed in more detail below.

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13.3.5 PSEUDOPARAPHYLLIA

AND

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PARAPHYLLIA

13.3.5.1 Pseudoparaphyllia The existence of structures called pseudoparaphyllia was noted about a century ago (Limpricht, 1895–1904; Warnstorf, 1904–1906) and many bryologists have included them for certain species in various treatments. The term “pseudoparaphyllia” was introduced by Warnstorf (1904–1906) for foliose structures around the branch primordia in Rhynchostegium confertum (Dicks.) Bruch et al., and the term was later used for similar structures in Rhytidiadelphus and Chrysohypnum by Mönkemeyer (1927). Iwatsuki (1963) suggested that pseudoparaphyllia should be classified into the two types: filamentose (uniseriate at insertion) and foliose. However, the first more comprehensive overview of the diversity of pseudoparaphyllia among pleurocarpous mosses was that of Ireland (1971). He also reviewed different interpretations of these structures up to the 1970s. Interestingly, Ireland (1971) considered both Rhynchostegium and Rhytidiadelphus to lack pseudoparaphyllia, although the term was originally coined for structures in these taxa. Ireland (1971) thought that all studied members of the Brachytheciaceae and Meteoriaceae lacked pseudoparaphyllia, while most members of the Amblystegiaceae had these organs. It is unclear exactly what Ireland meant by the absence of pseudoparaphyllia, but probably he restricted this term to structures that deviated significantly from “normal” leaves. At first pseudoparaphyllia seem easily defined as filamentose or foliose structures that are present around branch primordia and, later, on or around branch bases (Figure 13.2). However, their interpretation has proved to be more difficult, and several attempts have been made to clarify what pseudoparaphyllia really are and how they relate to proximal branch leaves and paraphyllia (e.g., Akiyama, 1990a, 1990b; Akiyama and Nishimura, 1993; Nishimura and Matsui, 1990a, 1990b; Rohrer, 1985). The latter authors named most of what had earlier been called pseudoparaphyllia “scaly leaves” based on the development of these from branch buds, and they restricted the term “pseudoparaphyllia” to adventitiously derived structures. However, from the figures of the sectioned

A (I1) B (I1 or I2)

C (I2)

FIGURE 13.2 Schematic illustration of a pleurocarpous moss stem with one branch and one branch primordium, illustrating the positions of proximal branch leaves (A), pseudoparaphyllia (B) and paraphyllia (C). Numbers in parentheses indicate the origin of the different structures (see Figure 13.1).

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branch buds in their paper (Akiyama and Nishimura, 1993), no differentiation can be seen between the tissue from which the “pseudoparaphyllia” are derived and that of the rest of the branch bud, whereas there is a distinct demarcation between the tissue of the branch bud and the tissue surrounding the branch bud. The same applies to “scaly leaves,” suggesting that pseudoparaphyllia and “scaly leaves” are homologous and that the main difference between them may be in the timing of their growth rather than a difference in position (Hedenäs, 1995). Ignatov (1999), in his studies of pseudoparaphyllia in the Brachytheciaceae and Meteoriaceae, treated “scaly leaves” (sensu Akiyama and Nishimura, 1993) together with pseudoparaphyllia in the sense of only adventitiously derived structures. Ignatov et al. (1996) and Budyakova et al. (2003) suggested that structures that, although they develop around a branch bud, are found only on the branch well above the stem when the branch is mature should not be called pseudoparaphyllia, because their transition to the branch leaves is gradual. This can be seen in Orthothecium, for example, and has been called Bryum-type branching (Akiyama, 1990a). Although the distinction of the Bryum- and Climaciumtype, where structures remain on the stem around mature branches, has not been widespread in studies of pleurocarpous mosses, a few studies suggest that the Bryum-type, or “absence of pseudoparaphyllia,” may be plesiomorphic among pleurocarpous mosses (Budyakova et al., 2003). Pseudoparaphyllia are unambiguously lacking in taxa such as Isopterygiopsis, where the branch primordia are quite naked on the stem. This situation has also been called concave or convex branch primordium without appendages (Akiyama and Nishimura, 1993). In most pleurocarpous mosses, however, the branch primordia are surrounded by variously shaped chlorophyllose structures, called pseudoparaphyllia or proximal branch leaves. These structures may be filiform, as in Isopterygium, narrowly triangular, as in Ectropothecium, triangular as in Taxiphyllum, or broad and more or less rounded, as in Bryocrumia. The interpretation of pseudoparaphyllia has implications for determining their potential homologies. Whereas “scaly leaves,” if homologous with proximal branch leaves, are derived from cell I2 (Figure 13.1), pseudoparaphyllia, when this term is restricted to structures that are derived from surface stem tissue outside the branch primordium, are derived from cell I1. The origin from I1 is also true for most paraphyllia, except those occurring on leaf margins and costae (see below), and could suggest homologies between pseudoparaphyllia and paraphyllia in at least some cases. Problems with separating pseudoparaphyllia and paraphyllia will be discussed further below. Contrary to the situation for rhizoids and axillary hairs, there is no overall structural similarity between proximal branch leaves, “scaly leaves,” pseudoparaphyllia, and paraphyllia that suggests that all these structures with different positions have a similar genetic background. It therefore seems like they cannot all be homologous (cf. below). 13.3.5.2 Paraphyllia Paraphyllia are variously shaped chlorophyllose structures found on the stem (thus originating from cell I1; Figure 13.1) and in some species sometimes on basal leaf portions (originating from cell I2; e.g., Abietinella abietina (Hedw.) M. Fleisch., Bryonoguchia molkenboeri (Sande Lac.) Z. Iwats. & Inoue, Helodium blandowii (F. Weber & D. Mohr) Warnst., Neckeradelphus menziesii (Drumm.) Steere, Thuidium glaucinum (Mitt.) Bosch & Sande Lac.). Paraphyllia may be sparse (e.g., Hygroamblystegium, Campylium protensum (Brid.) Kindb.) or abundant (Hylocomium, Thuidium). Contrary to pseudoparaphyllia, paraphyllia are not restricted to branch primordia (Ireland, 1971). A useful review of opinions regarding the origin of paraphyllia and their relation to pseudoparaphyllia is found in Rohrer (1985), who also discussed the different kinds of paraphyllia. Vanderpoorten et al. (2002) recognized two kinds of paraphyllia: (1) linear-lanceolate or ovate paraphyllia that are frequently inserted in transverse or oblique rows and usually consist of linear, smooth cells that are more or less tapering in their ends, and uniseriate, or in basal part sometimes 2-, 3-, or 4seriate (found in Cratoneuron, some Hygrohypnum species, Leskea, Neckera, and Palustriella); and (2) frequently branched paraphyllia that are inserted on spread points all over the stem and usually

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FIGURE 13.3 Position of a branch primordium in a moss at a very early (A) and at subsequent developmental stages (B, C). The figure is a schematic summary based on Berthier and Hebant (1970) and Berthier (1971), and on our own observations in the Amblystegiaceae; only four neighbouring leaves are shown, numbered in order of increasing age from N to N+3; the hatched area in A shows a branch primordium at a very early stage; α and β indicate the first and second pseudoparaphyllia, respectively.

consist of transversely rectangular, quadrate or rectangular, frequently papillose or prorate cells with square walls (found in Haplocladium, Helodium and Thuidium). Despite the above-mentioned studies, paraphyllia are still one of the structures in the mosses that have received little attention. Schofield and Hebant’s (1984) section on paraphyllia and pseudoparaphyllia in their chapter on moss gametophyte morphology and anatomy in the New Manual of Bryology is only ten lines long, explaining that unlike pseudoparaphyllia, paraphyllia are not concentrated around branch primordia. However, careful observations reveal that paraphyllia in Palustriella, Leskea (Figure 13.3G), and some other pleurocarps are more abundant in the proximity of branches, thus obscuring such a differentiation. In the Thuidiaceae the paraphyllia closest to the branch bases are larger, broader, and less branched than paraphyllia on the general stem surface, and their shape is transitional between paraphyllia on the general stem surface and pseudoparaphyllia. As a conclusion to this part, it can be seen that almost all the stem structures discussed could potentially be derived from both cells I1 and I2 (Figure 13.1). Similar structures could therefore possibly be the result of the same genes expressing in different tissues. If so, positional homology may not, or not always, explain how these structures should be interpreted in relation to each other. Thus, other approaches are needed to understand certain stem surface organs and one such approach is discussed in the next section. 13.3.5.3 An Alternative Classification of Paraphyllia and Pseudoparaphyllia Branch development in mosses is still not known as well as in, for example, hepatics (Crandall, 1969; Thiers, 1984, 1985). One of the most comprehensive studies on this subject was made by Berthier and Hebant (1970) and Berthier (1971). In Figure 13.3 we schematically summarize their results, simplifying and reformulating some details (thus taking responsibility for any possible misinterpretations). At approximately the stage when the tenth leaf develops (i.e., at a distance of three or four cells from the apical cell), a branch primordium zone is segregated from the lower part of leaf N (Figure 13.3A), usually about halfway between the leaf middle and leaf margin at the leaf insertion. This zone is covered from below by the corners of leaves N+1 and N+2, and even further down, almost straight below is the axil of N+3 leaf (Figure 13.3A). Following this stage, the activated branch apical cell cuts off its first leaves, and as the stem continues to grow this branch primordium is displaced downwards to the N+3 leaf axil, at the same time displacing the corners of leaves N+1 and N+2 (Figure 13.3B and C); these leaf corners were called “cathodic” and “anodic,” respectively by Berthier (1971). Leaf decurrencies start to develop at this stage, as at the earliest stages of the leaf development decurrencies do not exist because the leaves are then tightly appressed to each

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FIGURE 13.4 The three most common types of arrangement of the first pseudoparaphyllium around branch primordia in the Hypnales. In all three cases the stem apex is directed upwards. (A) The four-eleven-o’clock type, which is the most common one, found in the Amblystegiaceae, Hylocomiaceae, Leskeaceae, etc. (B) The Brachytheciaceae and Meteoriaceae type, with the first pseudoparaphyllium pointing downwards, and the second and third at 120° to the first one. (C) The low spiral type; known from taxa such as Thamnobryum and Trachyloma.

other, with very little space between. In many, if not most, species of pleurocarps the first two pseudoparaphyllia (cf. Figures 13.4, 13.5A to D) around a branch primordium are found in a “four o’clock position” (if the stem surface is studied with the stem apex directed upwards) and the second appears in a position close to 180° from the first, at about the “eleven o’clock position” (Figure 13.4A). This pattern we will call below the “first pseudoparaphyllium in four o’clock position.” Note, however, that within a single species, the leaves can be arranged on the branch in left and right spiral, resulting in two symmetrically mirroring cases (Figure 13.4A). We consider these to be variations of the same “four o’clock position.” We have not been able to find an explanation for this arrangement in the literature. Our explanation is that in the early stages the branch initial is found between the “cathodic” (N+1) and “anodic” (N+2) leaf corners, which are at that time in “four o’clock position” and “eleven o’clock position” in relation to the branch primordium (Figure 13.3B). It thus appears that the positions of the first two pseudoparaphyllia are related to the positions of leaves N+1 and N+2 in most pleurocarps. Other positions of the first pseudoparaphyllium, such as those found in the Brachytheciaceae or in Thamnobryum (Figure 13.4B and C, respectively), are apparently not related to the positions of the laterally adjacent leaves and need further studies. The positional relationships of branch primordia with respect to leaves N+1 and N+2 allows us to interpret the paired arrangement of paraphyllia usually present in some species. In Leptodon smithii the structures commonly called paraphyllia are usually situated in an oblique line between the “cathodic” and “anodic” leaf corners (Figure 13.6). This is seen most clearly when relatively few “paraphyllia” are developed, like the small ones in Figure 13.6A and B. Somewhat below the “cathodic” and “anodic” leaf corners (Figure 13.6D) or sometimes between the leaf corners (Figure 13.6C) one usually finds groups of more numerous “paraphyllia,” two of which are larger than the other ones and are inserted obliquely in relation to the axis of the stem. When such groups are found closer to the leaf axil, they typically have two much larger “paraphyllia,” which surround a branch primordium (Figure 13.6E to F, H). These patterns can be interpreted as a series of expressions of the same fundamental development, where the actual level of expression depends

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FIGURE 13.5 Pseudoparaphyllia around branch primordia in (A) Iwatsukiella leucotricha (Mitt.) W. R. Buck & H. A. Crum; (B) Sanionia uncinata (Hedw.) Loeske; (C) Straminergon stramineus (Kindb.) Hedenäs; (D) Hygroamblystegium varium (Hedw.) Mönk., (E)–(H) Neckera complanata (Hedw.) Huebener. In A–D the pattern “four-eleven-o’clock position” is apparent (α and β = first and second pseudoparaphyllia); in (E)–(H) the pseudoparaphyllia either evenly surround the branch primordium (G)–(H), or in some, possibly less developed, initials they are present mostly in “four-eleven-o’clock position” (note, that in the latter case they are close to cathodic leaf corners, CLC (anodic leaf corner not visible), while in the former they are close to the leaf axils, beside the ends of the leaf decurrencies, LD).

on where the development stops. If the development stops early, the tetrahedral apical cell never arises (or remains inactive), and two obliquely positioned pseudoparaphyllia are the only indication of the potential of this stem surface zone to produce a branch. If, on the other hand, the development reaches its end, a well-developed branch primordium, including pseudoparaphyllia, will be found. Such a mechanism could be analogous to hormone-dependent cases, such as that recently found for mammal teeth, where different levels of a single signalling protein cause differences in both the number of teeth and in tooth size and ornamentation (Kangas et al., 2004).

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FIGURE 13.6 Pseudoparaphyllia between cathodic and anodic leaf corners (A)–(D), (G), and around branch primordia (E), (F), (H) in Leptodon smithii (Hedw.) F. Weber & D. Mohr (CLC and ALC = cathodic and anodic leaf corners, respectively; LD = leaf decurrency).

According to traditional definitions paraphyllia differ from pseudoparaphyllia in their positions in relation to the branch primordia. However, if the above interpretation is correct many paraphyllialike structures in pleurocarpous mosses are most likely pseudoparaphyllia. Besides in Leptodon, similar arrangements of so-called paraphyllia can be found in several taxa, such as Alsia, Cratoneuron, Leskea, Neckera and Palustriella. When the “paraphyllia” are sparse, they are clearly concentrated either around branch primordia, or between the “cathodic” and “anodic” leaf corners (Figure 13.7). Since groups of “paraphyllia” in the latter position can be assumed to represent very undeveloped branch primordia we need to reconsider what the “paraphyllia” in these groups actually represent. One possibility is to widen the definition of paraphyllia to include all similar structures, meaning that the difference between pseudoparaphyllia and paraphyllia would be reduced to a positional one. Alternatively, the structures in taxa, such as those just discussed, have to be interpreted as pseudoparaphyllia that have partly “escaped” from their original position and are now found diffusely spread

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FIGURE 13.7 (A)–(C) Alsia californica (Hook. & Arnott) Sull.: pseudoparaphyllia in the region between (A) cathodic (CLC) and (B) anodic (ALC) leaf corners and around a branch base (C). (D)–(G) Leskea polycarpa Hedw.: pseudoparaphyllia around branch primordia, shown in (D), (G) and between CLC and ACL, shown in (E), (F); (H)–(J) Cratoneuron filicinum (Hedw.) Spruce: paired pseudoparaphyllia between CLC and ALC; juvenile branch structures are discernable between the leaves in H.

on the stem surface. In the above review we mentioned that rhizoids and axillary hairs may appear in different positions, and pseudoparaphyllia may be one more example of this phenomenon. The second interpretation makes sense if other kinds of “paraphyllia” exist that are not concentrated around branch primordia. According to our observations such paraphyllia exist, for example in Climacium, Hylocomiastrum, Hylocomium, Lescuraea and Loeskeobryum. The most obvious case is Lescuraea where paraphyllia are not so dense and their bases are clearly seen. In this genus some cortical cells are shorter than the neighbouring ones and form low longitudinal ridges. In the distal parts of these ridges lanceolate projections develop (Figure 13.8G and H). Frequently two or three projections arise from the same ridge. Similar ridges were noticed in Climacium and Pleuroziopsis by Norris and Ignatov (2000), who compared them with the devel-

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FIGURE 13.8 (A), (B) Hypnum cupressiforme Hedw.: pseudoparaphyllia around branch primordium. In the better developed initial in (B), the two lateral (outermost?) pseudoparaphyllia are larger than the others). (C)–(F) Pireella angustifolia (Müll. Hal.) Arzeni: subsequent stages of branch development, showing pseudoparaphyllia that shift in position from the stem to the branch base. (G)–(H) Lescuraea saxicola (Bruch & al.) Mol.: paraphyllia in longitudinal rows on stem.

opment of micronemata in the Mniaceae, described by Koponen (1968). In both cases some cortical cells are shorter and they have the potential to form outgrowths, which are little branched, brown and rhizoid-like in the Mniaceae, whereas they are much branched, green and paraphyllia-like in Climacium. One more similarity between Climacium-like paraphyllia and micronemata is that the apical cell is separated from the cells below by an oblique wall. This is different from the paraphyllia-like structures in taxa such as Leptodon, the Neckeraceae and Palustriella. However, also in Lescuraea the upper cell is separated from those below by a transverse cell wall. Although members of the Brachytheciaceae are usually considered as lacking paraphyllia, Ignatov and Huttunen (2003) described ridges of the kind just described. These are probably homologous with the paraphyllia-bearing ridges of Lescuraea and Climacium.

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Members of the Hylocomiaceae and Thuidiaceae are probably the most well-known examples of species with “paraphyllia,” and in these taxa the structures are inserted on almost all the stem surface cells. In Thuidium observations were made in T. tamariscinum (Hedw.) Bruch et al., a species with relatively sparse “paraphyllia” on its secondary branches. In these secondary branches, paraphyllia mostly occur in three positions: (1) associated with leaf decurrencies; (2) in the region between the “cathodic” and “anodic” leaf corners; and (3) at the base of tertiary branches, in a lateral four o’clock position, and usually there is a single pseudoparaphyllium, identical in structure to the “paraphyllia” that are inserted in other positions on the same branches. If these observations are extrapolated to be valid for the so-called paraphyllia in other positions in the plants, the latter structures should be interpreted as extremely densely arranged but diffusely distributed pseudoparaphyllia all over the stems. Contrary to the case in Thuidium, in Hylocomium we failed to find concentrations of “paraphyllia” around branch initials. Instead, in the apical stem region and in the thin secondary branches the paraphyllia are arranged more or less in rows on series of short longitudinal cells, thus apparently representing structures homologous to those found in Climacium. However, more observations are needed to confirm the nature of the structures in this case. After the elongation of stem surface cells, paraphyllia in Hylocomium and Hylocomiastrum appear attached to the corners (or ends) of two neighbouring stem surface cells, the upper corner of a proximal cell and the lower corner of a distal cell. Therefore the paraphyllia are biseriate at their base. In Loeskeobryum, however, paraphyllia are attached to the central part of a stem surface cell and are therefore mostly unicellular to their base. Interestingly, in mature stem parts of Thuidium and Helodium the attachment of “paraphyllia” to the stem is structurally very similar to that found in Hylocomium and Hylocomiastrum. Summarizing, we suggest that “paraphyllia,” as traditionally understood, should be differentiated into two types: (1) true paraphyllia, which are arranged in ± longitudinal rows and inserted on rows of short stem surface cells throughout the stem surface (e.g., Climaciaceae, Hylocomiaceae, Lescuraea), and (2) pseudoparaphyllia, which are associated with leaf decurrencies, found between the “cathodic” and “anodic” leaf corners with no branch primordium visible, or around branch primordia, but which may appear to be diffusely spread on the stem (e.g., Alsia, Thuidiaceae, Cratoneuron, Leptodon, some Neckeraceae, Palustriella). 13.3.5.4 The Differentiation between Pseudoparaphyllia and Proximal Branch Leaves Several attempts, stressing different criteria, have been made to differentiate between pseudoparaphyllia and proximal branch leaves. As mentioned above, the suggestion of Akiyama and Nishimura (1993) to confine the term pseudoparaphyllia to adventitious structures around branch buds is problematic because these adventitious structures are not sharply delimited from foliose structures that clearly belong to the bud. Enroth (in a lecture in Helsinki in 1999) suggested the main criterion for pseudoparaphyllia to be their lack of phyllotaxis. Since the latter is obvious in, for example the Meteoriaceae and Brachytheciaceae, these families must then be considered as having no pseudoparaphyllia, in agreement with Ireland (1971) and Allen (1987). However, Ireland (1971) believed that pseudoparaphyllia were present in the Amblystegiaceae s. lat. and many other families where the first pseudoparaphyllium is situated in a “four o’clock” position, and the second in an “eleven o’clock” position, i.e., a quite clear phyllotaxis. Even when only two foliose appendages are present around what we interpret as a potential branch primordium (cf. Leskea, Figure 13.7), these pseudoparaphyllia have a quite fixed arrangement (“four-eleven o’clock”). Thus, the presence or absence of phyllotaxis is obviously not a good criterion to distinguish between pseudoparaphyllia and proximal branch leaves. Budyakova et al. (2003) suggested that the term pseudoparaphyllia should be restricted to structures that remain on the stem after branch development, and extended the term proximal branch leaves to cover structures that appear on the stem before the branch starts to elongate but which are later displaced to a position on the base of the elongating branch. This made it possible to

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define a wider concept of “absence of pseudoparaphyllia,” to include not only the most obvious cases of Plagiothecium and Isopterygiopsis, but also other members of the Plagiotheciaceae (sensu Pedersen and Hedenäs, 2002), Habrodon, Hookeria, the Fontinalaceae, i.e., groups which in some phylogenetic analyses appear basal to the rest of the pleurocarps (Tsubota et al., 2004; Gardiner et al., 2005). However, the definition by Budyakova et al. (2003) can probably not be applied universally as a common case in the Pterobryaceae was not covered in the discussion of these authors. As illustrated here for Pireella (Figure 13.8), in this family trichome-like structures are commonly displaced from the stem to the branch base during the branch growth, but at the same time there is a rather clear limit between such trichomes and triangular proximal branch leaves at the basal part of the branch. Akiyama (1990a: Figure 3A-C) illustrated a similar case for Symphysodon. Similarly, a delimitation is more or less obvious in the Neckeraceae, where narrowly lanceolate “outer pseudoparaphyllia” contrast with broadly triangular “inner pseudoparaphyllia” or “proximal branch leaves” (Figure 13.5E to H). Note, however, that in Campylophyllum, and Hypnum recurvatum (Lindb. & Arnell) Kindb. the transition from subfiliform outer pseudoparaphyllia to lanceolate and subsequently ovate-lanceolate inner ones is fairly gradual, so the criterion of a sudden transition in shape of the structures is not a plausible one for the differentiation of two different kinds of structures.

13.4 SUMMARY AND CONCLUSIONS Our current understanding of the nature of pseudoparaphyllia and proximal branch leaves does not allow a universal distinction between these. Possibly, these structures are actually homologous, but show a great variation in appearance and position among taxa. We therefore suggest that the term pseudoparaphyllia is used for any structures developed near or at the branch base. For the sake of phylogenetic analyses it is best not to treat them as a single inexact character with the states “pseudoparaphyllia absent” versus “pseudoparaphyllia present.” Instead, the following aspects need to be considered when this character and its states are described. 1. Pseudoparaphyllia that are diffusely spread upon stem absent, or present (i.e., more or less lanceolate appendages occur regularly along the internodes). 2. Pseudoparaphyllia that remain on the stem after branch elongation, or their positions are all displaced to the branch base during the branch growth. 3. Outer pseudoparaphyllia that are very different in shape from the inner ones (“proximal branch leaves”) are present, or the outer ones are similar or only slightly different in shape, usually shorter and broader compared with mature leaves. 4. When the outer pseudoparaphyllia are clearly different from the inner ones, the transition is sudden, or the transition between them is gradual. 5. Pseudoparaphyllia are arranged in (cf. Figure 13.4) the following patterns: (a) first pseudoparaphyllium is in “four o’clock position”; (b) first pseudoparaphyllium is pointed downward and the second and third ones are found at angles of 120° and 240° in relation to the first one (cf. Ignatov, 1999); or (c) pseudoparaphyllia are arranged in a low spiral (e.g., Pireella, Figure 13.8E).

ACKNOWLEDGMENTS During the preparation of this manuscript, we have profited much from discussions with Angela Newton. The studies of MI were partly supported by RFBR grant 04-04-48774 and the Programme “Biodiversity” of the Russian Academy of Sciences; the studies of LH were supported by the Swedish Research Council (Vetenskapsrådet, project no. 621-2003-3338).

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REFERENCES Akiyama, H. (1990a) A morphological study of branch development in mosses with special reference to pseudoparaphyllia. Botanical Magazine, Tokyo, 103: 269–282. Akiyama, H. (1990b) Morphology and taxonomic significance of dormant branch primordia, dormant buds, and vegetative reproductive organs in the suborders Leucodontineae and Neckerineae (Musci, Isobryales). Bryologist, 93: 395–408. Akiyama, H. and Nishimura, N. (1993) Further studies of branch buds in mosses; “Pseudoparaphyllia” and “Scaly leaves.” Journal of Plant Research, 106: 101–108. Allen, B. (1987) On distinguishing Pterobryaceae and Meteoriaceae by means of pseudoparaphyllia. Bryological Times, 42: 1–3. Berthier, J. (1971 [1972]) Recherches sur la structure et le développement de l’apex du gamétophyte feuillé des mousses. Revue Bryologique et Lichénologique, 38: 421–551. Berthier, J. and Hebant, C. (1970 [1971]) Phyllogenèse, nématogenèse et caulogenèse au niveau des initiales superficiales des mousses. Revue Bryologique et Lichénologique, 37: 877–929. Bopp, M. (1981) Entwicklungsphysiologie der Moose. In Advances of Bryology, Vol. 1 (ed. W. SchultzeMotel). J. Cramer, Vaduz, pp. 11–77. Budyakova, A. A., Ignatov, M. S., Yatsentyuk, S. P. and Troitsky, A. V. (2003) Systematic position of Habrodon (Habrodontaceae, Musci) as inferred from nuclear ITS1 and ITS2 and chloroplast trnL intron and trnL-trnF spacer sequence data. Arctoa, 12: 137–150. Crandall, B. J. (1969) Morphology and development of branches in the leafy Hepaticae. Beihefte zur Nova Hedwigia, 30: 1–261. Crandall-Stotler, B. (1984) Musci, Hepatics and Anthocerotes — an essay on analogues. In New Manual of Bryology (ed. R. M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 1093–1129. Frey, W. (1970) Blattentwicklung bei Laubmoosen. Hedwigia, 20: 463–556. Gardiner, A., Ignatov, M., Huttunen, S. and Troitsky, A. (2005) On resurrection of the families Pseudoleskeaceae Schimp. and Pylaisiaceae Schimp. (Musci, Hypnales). Taxon 54(3): 651–663. Goebel, K. (1898) Organographie der Pflanzen, 2(1) Bryophyten. Verlag von Gustav Fischer, Jena. Goebel, K. (1915) Organographie der Pflanzen, 2(1) Bryophyten, Ed. 2. Verlag von Gustav Fischer, Jena. Hedenäs, L. (1990) Axillary hairs in pleurocarpous mosses: A comparative study. Lindbergia, 15: 166–180. Hedenäs, L. (1995) Higher taxonomic level relationships among diplolepidous pleurocarpous mosses: A cladistic overview. Journal of Bryology, 18: 723–781. Ignatov, M. S. (1999) Bryophyte flora of the Huon Peninsula, Papua New Guinea. LXIII. On the pseudoparaphyllia in Brachytheciaceae and Meteoriaceae (Musci). Acta Botanica Fennica, 165: 73–83. Ignatov, M. S. and Huttunen, S. (2003) Brachytheciaceae (Bryophyta) — a family of sibling genera. Arctoa, 11: 245–296. Ignatov, M. S., Ando, H. and Ignatova, E. A. (1996) Bryophyte flora of Altain mountains. VII. Hypnaceae and related pleurocarps with bi- or ecostate leaves. Arctoa, 6: 21–112. Ireland, R. R. (1971) Moss pseudoparaphyllia. Bryologist, 74: 312–330. Iwatsuki, Z. (1963) Bryological miscellanies. XII–XIII. Journal of the Hattori Botanical Laboratory, 26: 63–74. Kangas, A. T., Evans, A. R., Thesleff, I. and Jernvall, J. (2004) Nonindependence of mammalian dental characters. Nature, 432: 211–214. Kawai, I. (1977) Die systematische Forschung auf Grund der Zellteilungsweise für die Bryophyten. II. Die Zellteilungsweisen der Gametophyten in der Lebensgeschichte (1) Climacium. Science Reports of the Kanazawa University, 22: 45–90. Koponen, T. (1968) Generic revisions of Mniaceae Mitt. (Bryophyta). Annales Botanici Fennici, 5: 117–151. La Farge-England, C. (1996) Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99: 170–186. Limpricht, K. G. (1895–1904) Die Laubmoose Deutschlands, Oesterreichs un der Schweiz. III. Abtheilung. Verlag von Eduard Kummer, Leipzig. Müller, C. (1909) Musci (Laubmoose). In Die natürlichen Pflanzenfamilien, Vol. 1(3) (ed. A. Engler and K. Prantl). Verlag von Wilhelm Engelmann, Leipzig, pp. 142–202. Mönkemeyer, W. (1927) Die Laubmoose Europas. IV. Band, Ergänzungsband. Andreaeales-Bryales. Leipzig.

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Nishimura, N. and Matsui, S. (1990a) SEM observations of moss pseudoparaphyllia. I. Isobryales. Hikobia, 10: 429–434. Nishimura, N. and Matsui, S. (1990b) SEM observations of moss pseudoparaphyllia. II. Hypnobryales. Bulletin of the Hiruzen Research Institute, Okayama University of Science, 16: 117–138. Norris, D. H. and Ignatov, M. S. (2000) Observations on stem surface anatomy in Climacium and Pleuroziopsis (Climaciaceae, Musci). Arctoa, 9: 151–154. Pedersen, N. and Hedenäs, L. (2002) Phylogeny of the Plagiotheciaceae based on molecular and morphological evidence. Bryologist, 105: 310–324. Quandt, D., Huttunen, S., Streimann, H., Frahm, J.-P. and Frey, W. (2004) Molecular phylogenetics of the Meteoriaceae s. str.: Focusing on the genera Meteorium and Papillaria. Molecular Phylogenetics and Evolution, 32: 435–461. Rohrer, J. R. (1985) A phenetic and phylogenetic analysis of the Hylocomiaceae and Rhytidiaceae. Journal of the Hattori Botanical Laboratory, 59: 185–240. Schofield, W. B. and Hebant, C. (1984) The morphology and anatomy of the moss gametophyte. In New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 627–657. Sitte, P., Ziegler, H., Ehrendorfer, F. and Bresinsky, A. (1998) Lehrbuch der Botanik für Hochschulen (Strasburger). Gustav Fischer, Stuttgart. Thiers, B. M. (1984) Branch characters significant to subfamilial classification of Lejeuneaceae (Hepaticae). Systematic Botany, 9: 33–41. Thiers, B. M. (1985) Branching in Lejeuneaceae. III. Ptychantoideae. Beihefte zur Nova Hedwigia, 80: 31–61. Tsubota, H., De Luna, E., Gonzalez, D., Ignatov, M. S. and Deguchi, H. (2004) Molecular phylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcL sequences of mosses. Hikobia, 14: 149–170. Vanderpoorten, A., Hedenäs, L., Cox, C. and Shaw, A. J. (2002) Phylogeny and morphological evolution of the Amblystegiaceae (Bryopsida). Molecular Phylogenetics and Evolution, 23: 1–21. Warnstorf, C. (1904–1906) Kryptogamenflora der Mark Brandenburg und angrenzender Gebiete. Laubmoose, Zweiter Band. Verlag von Gebrüder Borntraeger, Leipzig. Zolotov, V. I. and Ignatov, M. S. (2001) On the axillary hairs of Leptobryum (Meesiaceae, Musci) and some other acrocarpous mosses. Arctoa, 10: 189–200.

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Architecture in 14 Branching Pleurocarpous Mosses Angela E. Newton CONTENTS Abstract ..........................................................................................................................................287 14.1 Introduction...........................................................................................................................288 14.2 Architectural Features in Pleurocarpous Mosses.................................................................292 14.2.1 Primary Module Termination ...................................................................................293 14.2.2 Primary Module Orientation ....................................................................................294 14.2.3 Primary Module Point of Origin..............................................................................294 14.2.4 Hierarchical versus Alternating Arrangement of Modules ......................................295 14.2.5 Secondary Module Orientation ................................................................................297 14.2.6 Secondary Module Point of Origin..........................................................................298 14.2.7 Branching Order and Density of Secondary Modules ............................................299 14.2.8 Length and Determinancy of Secondary Modules ..................................................300 14.2.9 Reiteration.................................................................................................................301 14.2.10 Formation of Plagiotropous Modules .....................................................................301 14.2.11 Perichaetial Module Point of Origin.......................................................................302 14.2.12 Presence of Subperichaetial Innovations ................................................................302 14.3 Architectural Groundplans ...................................................................................................303 14.3.1 How Many Ways Are There to Make a Dendroid Moss? .......................................303 14.3.2 Dendroid and Shelf Mosses .....................................................................................305 14.4 Conclusions...........................................................................................................................305 Acknowledgments ..........................................................................................................................306 References ......................................................................................................................................306

ABSTRACT The concepts of acrocarpy and pleurocarpy in mosses have profound implications for the understanding and utilization of morphological characters related to branching architecture in the systematic study of pleurocarpous mosses. The need for precision in observation and character analysis is made very apparent when such information is included in cladistic analysis, and traditional terms such as “dendroid” can be shown to include a variety of combinations of independent characters. Deconstruction of growth form into individual characters or character systems that can be coded for cladistic analysis allows systematically informative characters to be identified and evolutionary patterns investigated. Here the components of branching architecture are analysed, described, and figured, including case studies of individual species.

287

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14.1 INTRODUCTION The concepts of acrocarpy and pleurocarpy in mosses reflect the position of the gametangia, terminating either the main stem (resulting in terminal production of the fruiting body, Figure 14.1A, B) or lateral branches (resulting in the production of many fruiting bodies Figure 14.1C, D). These concepts have been used extensively in classifications since the nature of the gametangia was first recognized by Hedwig (1778) and since Bridel (1819) first used the terms Acrocarpi and Pleurocarpi. However, the value of these concepts has frequently been questioned (e.g., Cavers, 1911; Watson, 1968; Vitt, 1984) due to the appearance of lateral archegonia in various groups among the acrocarpous mosses (e.g., in Fissidens, Mielichoferia and Pleurochaete) suggesting that the pleurocarpous mosses are not a natural group. The additional concept of cladocarpy, which includes a variety of situations where gametangia terminate lateral branches longer than those typically found in pleurocarpous mosses (see La-Farge England, 1996), complicates the picture. Definitions of terms relating to growth form and branching pattern were supplied by La-Farge England (1996: Table 1). Cladocarpous mosses occur in small groups throughout the acrocarpous and pleurocarpous taxa, and have sometimes been interpreted as representing a transition between acrocarpy and pleurocarpy (La Farge-England, 1996; Vitt, 1984). Recent research using molecular data (Beckert et al., 1999, 2001; Bell and Newton, 2004, 2005, Chapter 3; Cox and Hedderson, 1999; Cox et al., 2000, 2004; De Luna et al., 1999; Newton et al., 2000) indicates that acrocarpous

B

A

D C FIGURE 14.1 Acrocarpy and pleurocarpy: (A) acrocarpous plant with primary modules terminated by formation of archegonia and further growth by the development of a subperichaetial innovation. Mature adult vegetative leaves (sensu Mishler and De Luna, 1991) are present on the module when archegonia are initiated. (B) Sporophytes terminate primary modules, with one perichaetium per module. (C) Pleurocarpous plant with archegonia formed terminating lateral (reproductive) modules, so that the primary modules are able to continue vegetative growth — when archegonia are initiated, only mature juvenile leaves are present on the module. (D) Sporophytes terminate lateral (reproductive) modules, with many sporophytes possible per primary module.

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mosses form a grade of distinct groups basal to a monophyletic group containing the majority of pleurocarpous mosses, and that the formation of gametangia terminal on lateral branches is a synapomorphy for the Hypnanae (sensu Buck and Goffinet, 2000), Hookeriales, and the “Rhizogoniales” (Newton et al., 2000; Bell and Newton, 2004, 2005, Chapter 3). The remaining “pleurocarpous” taxa embedded in the acrocarpous mosses represent examples of parallel evolution, as do the various groups of cladocarpous mosses, while acrocarpous mosses embedded in the principal pleurocarpous lineages are interpreted as reversals. Where sporophytes or gametangia are absent or scarce, the determination of acrocarpy or pleurocarpy can be problematic. Consequently these concepts have become associated with a large number of secondary characters, many of which are not restricted to one group or the other, but are used in combination (Meusel, 1935; Watson, 1968). The most notable features, in addition to the position of the gametangia (and therefore the sporophytes), include the length, shape and surface features of lamina cells, length and differentiation of the costa, and “general habit and mode of branching” (Watson, 1968), in particular whether the plants are orthotropous or plagiotropous (Meusel, 1935). These features have become associated with “pleurocarpy” and “acrocarpy,” making these complicated, difficult to apply, and systematically uninformative. For example, Koponen (1988) considered a monopodial habit as diagnostic of “true pleurocarpy,” and the determinate habit of the vegetative primary module in the Rhizogoniaceae as indicative of acrocarpous growth. This concept possibly lingers in the retention of the Rhizogoniaceae in the acrocarpous Bryales by many authors. In his comprehensive and detailed studies of growth form, Meusel (1935) described and illustrated the branching patterns of many taxa, including juvenile stages. This included a classification into growth types, based on orientation of “primary stems” and branch origin (Meusel 1935, pp. 259–268.) These growth-form concepts have been widely used subsequently, in particular in ecological studies, and have had a role in systematic treatments. However, these categories are largely artificial, and although they were useful in synthetical, knowledge-based descriptive methodology, in the analytical, data-based methodology epitomized by cladistic analysis there is a need for explicit morphological characters that can be coded for inclusion in matrices. In this chapter, the growth form of pleurocarpous mosses is “deconstructed” into individual characters or character systems that can be coded for cladistic analysis, allowing the systematically informative characters to be identified and studied. Branching pattern is strongly related to the position of the gametangia, and is a consequence of the interaction of a number of different characters that result in a range of morphologies. It may also be the consequence of environmental modification, necessitating the examination of material from a range of habitats. An individual growth form may be the result of the combination of several different characters, which can be discerned through “deconstruction” of the growth form, whereas very different patterns may be the consequence of modification of only single characters. For example, a “dendroid” growth form usually consists of an upright “stipe” and a distal highly branched or leafy frond region. This may consist of an erect primary module with pinnate or umbellate distal secondary modules as in many taxa such as Thamnobryum and Hypnodendron; an erect primary or secondary module as a branch from a creeping primary module as in the Leucodontaceae and Leptodontaceae; an erect primary module with pinnately arranged distal secondary modules and distal reiteration of the stipe-branch modular series as in Pireella. The term “dendroid” has even been applied to plants with erect primary modules that lack distal branches but instead have distal tufts of large leaves forming a coma (“palm tree”), as in some members of the Mniaceae and Bryaceae. A pattern of branching identical to that seen in some forms of dendroid mosses produces a completely different appearance with the modification of the single character of primary module orientation. Plants with orthotropous primary modules form dendroid plants, whereas those with plagiotropous primary modules form layers or shelves, for example as in Neckera. “Branching architecture” is used here to refer to the pattern of interaction of such characters. The discussions here mostly refer to character systems, rather than individual characters, each of

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which is conceived as an independent, hereditable character that can be coded for cladistic analysis and optimized on a phylogenetic topology that may be derived from molecular, morphological or combined data. These are of course subject to modification as additional taxa are studied, and additional characters may be found to be necessary, but this group of characters has formed the basis for studies of the morphology associated with the evolution of pleurocarpy (Bell and Newton, 2004, 2005, Chapter 3; Newton and De Luna, 1999). A key element of the analysis of the branching architecture of mosses is the concept of a hierarchy of modules (Mishler and De Luna, 1991). In mosses, the morphology of the mature plant results from the development of a series of apical cells, each of which is responsible for the formation of an individual module. Following the concept of White (1984), as summarized in Mishler and De Luna (1991), each apical cell continually cuts off a series of merophytes, which in turn divide to form a small number of cells. These further divide, expand and differentiate to form the tissues of the module — usually cortex, epidermal cells, leaves, other stem structures, and lateral apical cells that permit branching. As the apical cell matures, the structures formed may change in size, shape or density, resulting in a heteroblastic series along the module (Figure 14.7C). The orientation of each module may also be variable. Primary modules may be terminated by gametangia (acrocarps), cease growth without formation of gametangia (both acrocarps and pleurocarps), or be indeterminate (“cladocarps” and pleurocarps). The apical cells of the branch primordia repeat the process of dividing and differentiating merophytes; however, the modules formed may be identical to the primary module (stem or stipe), or may differ, forming vegetative secondary modules (branches) or reproductive secondary modules (perichaetia and perigonia). In some cases additional levels of differentiated vegetative secondary modules may form, with each successive module differentiated from the previous. The arrangement of modules into monopodial and sympodial growth forms is a component of branching architecture that is discussed in depth by Tangney in Chapter 15, and is not included in detail here. In contrast to the study of branching architecture in vascular plants (Hallé et al., 1978), it must be remembered that each module in a moss is the product of a single apical cell, rather than a meristem composed of multiple cells. The branching structure in mosses is comparatively simple and the individual modules are distinct at plant maturity, allowing the components to be more readily recognized than in vascular plants. Terms such as stolon, primary and secondary stem, and branch, have often been used without careful attention to the role of the apical cell in formation of each of these features. Consequently, a “primary stem” in one taxon may equate to a “stolon” in a second, and a “branch” in a third, while a “secondary stem” may be the continuation of the primary stem but with a different orientation, a new primary module, or a secondary module (a “branch”). This lack of clarity reduces the information content of these terms and makes structural comparisons between taxa difficult or meaningless, especially for determination of homology in cladistic analysis. Acrocarpous mosses form relatively few architectures (Figure 14.2), possibly a reflection of the limitation imposed on branching patterns by termination of stem growth by production of gametangia. In the majority of taxa, branching occurs as the result of the formation of one or more new primary modules from innovations, often immediately below the terminal gametangium (Figure 14.2A), resulting in the growth form of small or large cushions (Figure 14.2G) or dense or loose turfs (Figure 14.2H). Consequently, variation reflects the frequency of branching and speed of growth, resulting in dense or open aggregates of plants that vary in size (e.g., cushions and turfs; Proctor and Smith, 1995, and papers cited therein) rather than differences in branching architecture. Examples include Andreaea (dense cushions and swards), Tetraphis (open low turfs), Tortula (small or large cushions and open tall turfs), Grimmia (small dense cushions and dense velvety swards), Dicranum (dense or open, low or tall turfs), Bryum (open cushions and open turfs), Philonotis (open turfs) and Funaria (ephemeral open turfs). Variations do occur, however, and were discussed by Meusel (1935).

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D

A E

F

B

C

G

H

FIGURE 14.2 Architecture of acrocarpous mosses: (A) typical branching pattern of an acrocarpous moss, with orthotropous modules formed subterminally immediately below perichaetia; (B) plagiotropous orientation of primary modules formed at mid-point; (C) plagiotropous orientation of primary modules formed subterminally; (D) plagiotropous (pendulous) orientation of primary modules formed subterminally; (E) orthotropous primary modules formed at the module base and distally ( perigonium); (F) plagiotropous secondary (vegetative) modules formed subterminally on orthotropous primary modules; (G) acrocarpous cushion habit; (H) acrocarpous turf habit.

Principal architectural elements that are found in acrocarps include orientation of the primary module (orthotropous or plagiotropous), point of origin of the primary module (subterminal, distal, nonspecific or basal), and presence or absence of secondary modules. Vegetative branches that may or may not be differentiated from the primary module, and that may remain sterile or eventually be terminated by gametangia, are found in a variety of taxa and result in a deeper or more extensive growth form, e.g., Sphagnum, with differentiated tufted vegetative branches forming deep cushions and turfs, and Racomitrium and Bartramia, with determinate vegetative branches forming large cushions. Certain acrocarpous mosses have developed a pendulous or creeping growth form, e.g., species of the tropical genus Leucoloma (La Farge-England, 1996, 1998) and Bryowijkia, or a dendroid growth form with a distal coma of determinate vegetative branches (Philonotis, Leucolepis). In contrast, the pleurocarpous mosses have rather more architectural components, especially those related to formation and distribution of secondary modules, which in different combinations form a much wider range of growth forms (Figure 14.3 and Figure 14.4). Some structural combinations are not possible. For example, there are no indeterminate erect mosses, since they lack the necessary structural tissues to support growth to any height, and lack features (twining, tendrils) that would allow them to use other vegetation for support. The largest erect determinate mosses can reach 45 cm or more (e.g., Polytrichum, Dawsonia superba; various specimens in BM) but

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B

A

C

D

E F

G

H

FIGURE 14.3 Architecture of pleurocarpous mosses: A–F, characters 1 to 3 (primary module termination, orientation and origin); G–H, character 4 (module hierarchy). (A) Primary module with plagiotropous stolon and orthotropous distally, new module formed at transition point; (B) orthotropous primary module with new module formed subterminally; (C) orthotropous primary modules with new modules formed basally; (D) all modules terminated by perichaetia (“acrocarpous”) as a reversal from the pleurocarpous condition; (E) primary module initially orthotropous becoming plagiotropous, new module formed in mid region; (F) primary module plagiotropous, new module location nonspecific; (G) primary and secondary vegetative modules hierarchical; (H) primary module with alternating phases, secondary modules differentiated or not.

may be supported in a tuft of close-packed stems. Erect indeterminate mosses would become sprawling mosses beyond this height.

14.2 ARCHITECTURAL FEATURES IN PLEUROCARPOUS MOSSES The following architectural characters were originally derived from examination of a wide range of pleurocarpous and acrocarpous mosses for cladistic study of the evolution of the pleurocarpous mosses (De Luna et al., 1999; Newton and De Luna, 1999), and have subsequently been further modified in connection with studies of the early diverging lineages of pleurocarpous mosses (see Bell and Newton, 2004, 2005, and Chapter 3). 1. 2. 3. 4. 5. 6.

Primary module termination Primary module orientation Primary module point of origin Hierarchical and alternating modularity Secondary module orientation Secondary module point of origin

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3° 4°

293

2°

1°

2°

1°

B

A

C 1°

2°

D FIGURE 14.4 Architecture of pleurocarpous mosses: A–C, characters 5 to 8 (secondary module orientation, origin, branching order and determinancy); D characters 8 to 9 (reiteration and formation of stolons and flagelliforme shoots). (A) Secondary modules complanate, in a distal frond, with tertiary branching (p.p.), determinate; (B) secondary modules orthotropous, randomly distributed, unbranched, long, and determinate; (C) secondary modules plagiotropous, initiated regularly just behind primary module apex and therefore throughout length of primary module, complanate, unbranched, short and determinate; (D) reiteration by formation of new primary modules out of the normal hierarchical sequence. (Note: in Figure 4A only part of the higher-order branches are illustrated.)

7. 8. 9. 10. 11. 12.

Branching order and density Determinancy and length of secondary modules Reiteration Formation of plagiotropous modules Perichaetial module point of origin Presence of subperichaetial innovations

14.2.1 PRIMARY MODULE TERMINATION In the majority of taxa in the pleurocarpous clade, the primary module is not terminated by the formation of gametangia, and is therefore potentially free to continue vegetative growth indefinitely. In some taxa this appears to be the case, where the primary module seems to grow indefinitely (monopodial growth, Figure 14.3F) often with short, determinate secondary modules forming a creeping plume (Figure 14.4C), e.g., in Hypnum and Thelia (Appendix 14.1b; Appendix 14.1 on the companion CD shows examples of branching architecture of specific taxa [from collections as noted]). Only if the original apical cell is damaged or destroyed does a new primary module replace the previous one. Growth may halt seasonally or during adverse conditions, but then resume from the same apical cell. Careful examination of the shoot may be necessary to determine that growth is truly indeterminate, since changes in the appearance of the shoot may occur without a changeover of the primary module, or replacement of the original apical cell may be masked by surrounding leaves. In some cases seasonal changes or contact with the substrate may result in changes in

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branching pattern or leaf formation without replacement of the apical cell, as is seen, for example, in some members of the Meteoriaceae (Appendix 14.1e). In many taxa the primary module appears to be vegetatively determinate, with growth ceasing without clear evidence of damage. This results in a sympodial growth form, with a succession of primary modules of similar length and branching pattern, with the oldest clearly moribund (Figures 14.3A and C). Where a reversal to apparent acrocarpy has occurred, as in some members of the Cryphaeaceae (Figure 14.3D), primary modules are terminated by perichaetia.

14.2.2 PRIMARY MODULE ORIENTATION The orientation of the plant can be considered in absolute terms (erect/vertical or creeping/horizontal) or relative to the substrate (orthotropous or plagiotropous) or to incident light (Bell and Newton, 2005). However, the orientation of the substrate can influence the application of these terms (see also the discussion in Chapter 12 with regard to sporophyte orientation and morphology). Where the substrate is horizontal (flat earth or rock surface, or the upper surface of horizontal trunks or branches) the terms erect, vertical and orthotropous are synonymous (for understanding orientation), as are creeping, horizontal and plagiotropous. Where the substrate is vertical or sloping, as on cliff or rock faces, earth banks and the sides of trunks and branches, the terms become more difficult to apply. A plant that grows perpendicular to a vertical substrate is actually horizontal and can easily become drooping or pendulous distally, especially in older plants (e.g., Calyptothecium). Some taxa may grow at an acute angle to such a substrate, so effectively growing in an approximation of vertical orientation (e.g., Spiridens). Others may start out growing perpendicular to the substrate, but then proceed to grow over the backs of fronds beneath them, which provide a substitute horizontal substrate (e.g., Neckera). Plants appressed to a vertical substrate are plagiotropous, and may be growing horizontally or in a vertical direction that may be upwards or downwards — and may also change the angle of their orientation (e.g., Thelia). The terms orthotropous (orthotropic) and plagiotropous (plagiotropic) have been used in bryology for some time (e.g., Meusel, 1935) but are absent from the glossaries in all the standard bryological floras. These terms are preferred, however, since they express orientation relative to the effective substrate rather than reflecting an absolute concept based on the direction of gravity. In many taxa, this character complex is further complicated by changes in orientation reflecting heteroblastic changes, as where a creeping (plagiotropous) stolon turns perpendicular to the substrate to form an erect (orthotropous) frond (Figures 14.3A, 14.4D, e.g., Pseudocryphaea, Appendix 14.1i, Thamnobryum, Appendix 14.1j), or where an erect stipe becomes horizontal at the point of branch initiation to form a flattened frond (Figure 14.3e, 14.3g, e.g., Thuidium, Appendix 14.1h, Hylocomium). More than one change in orientation may occur. In Hypopterygium (see Figure 14.8D) the plagiotropous stolon forms an orthotropous stipe that then bends at the point of branch initiation to form an oblique frond. Thuidium switches frequently between orthotropous and plagiotropous modes (Appendix 14.1h), whereas Anomodon switches not only orientation but leaf form as well (Appendix 14.1f). Plants may also alter growth form in response to external factors: a plagiotropous flagelliform branch may become orthotropous when it contacts a substrate, initiating rhizoids and changing leaf morphology, or at the point where two plagiotropous stolons meet both may initiate orthotropous growth (both examples observed in Pireella). Plants growing horizontally on a flat substrate such as branches or twigs may become vertical (pendulous) when they grow beyond the support of such a substrate (e.g., Isothecium) and may also change leaf morphology in these circumstances.

14.2.3 PRIMARY MODULE POINT

OF

ORIGIN

The differentiation of merocytes results in the formation of the apical cell of a branch primordium below every leaf. In many acrocarps the apical cell does not differentiate as an obvious branch primordium, or may be represented by a tuft of rhizoids or a small flat or concave area of

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differentiated cells. Only when the apical cell of the primary module is terminated does one or more of these apical cells develop into a branch primordium, often immediately below the module apex. In contrast, pleurocarpous mosses may have dormant branch primordia visible along the length of the primary module, in extreme cases (e.g., Thuidium) with a primordium associated with virtually every leaf. Factors controlling the development of these primordia are virtually unstudied, especially those related to different types of module. During normal growth primordia develop into primary, secondary or reproductive modules in a pattern characteristic of the taxon, but the factors determining the fate of a given primordium are unknown. Primordia that develop to form new primary modules may initially not be detectably different from branch primordia that form secondary or reproductive modules, although La FargeEngland (1996) considers that the latter two may be developmentally differentiated. Sometimes, however, primary modules may be in a different plane than the secondary modules, which is easily noted in plants with plumose branching (e.g., Thuidium, Appendix 14.1h) but not in plants where branches radiate in all directions (e.g., Climacium). In the absence of damage to the apical cell, new primary modules initiate at a distance from the apex; however, where damage occurs, a succession of primary modules may form, each immediately behind the damaged apex of the previous module (Figure 14.3C; Pleurozium, Appendix 14.1a). Normal initiation of primary modules may be nonspecific, appearing anywhere along the existing primary module (Figure 14.3F; e.g., Meteorium, Appendix 14.1e; Thelia, Appendix 14.1b), but in many taxa new primary modules form in specific areas. For example in many dendroid mosses, a new primary module grows plagiotropically as a stolon from the point where the previous primary module changes from plagiotropous growth (stolon) to orthotropous (stipe or frond) (Figures 14.3A, 14.3H, 14.4B, 14.4D, e.g., Hypopterygium, Figure 14.8D, Pseudocryphaea, Appendix 14.1i, Thamnobryum, Appendix 14.1j). This is also seen in shelf-forming mosses (e.g., Neckera, Appendix 14.1k) where the whole system is plagiotropous, but the same pattern of changes of orientation is seen. In layered mosses new primary modules are initiated among the basal branches of the frond (Figures 14.3E, 14.3G, e.g., Hylocomium, Thuidium, Appendix 14.1h). New primary modules may also initiate in the older regions of indeterminate fronds (Figure 14.3F, e.g., Plagiothecium, Appendix 14.1c: Hookeria, Appendix 14.1D), or at the very base of existing determinate primary modules, as in many of the tufted pleurocarps (Figures 14.3C, 14.5B; e.g., Pyrrhobryum, Figure 14.8B). In the tufted pleurocarps, the branching points are very close together, usually densely matted with rhizoids, and often very fragile, so that dissection and clear analysis has been difficult. Meusel (1935), for example, shows Hypnodendron as having a long creeping stolon as in Thamnobryum. However, in the tufted pleurocarps, both at the basal branching point and where distal branching of primary modules occurs, numerous branch primordia form and develop into primary modules that are either orthotropous or have extremely short initial plagiotropous sections (Figure 14.6).

14.2.4 HIERARCHICAL

VERSUS

ALTERNATING ARRANGEMENT

OF

MODULES

A hierarchical arrangement of modules is present in the majority of taxa, comprising (at least) primary modules, secondary modules and reproductive modules (Figure 14.3G). Recognition of this is dependent on the identification of secondary modules differentiated from the primary modules. Variation in leaf form (anisophylly, Figure 14.7A) between the levels of the heirarchy is the most obvious indicator, but should be distinguished from heterophylly and heteroblasty. Anisophylly and heterophylly have often been treated as synonymous in bryological glossaries (e.g., Magill, 1990; Malcolm and Malcolm, 2000). Heterophylly (Figure 14.7B) is the regular alternation of leaf form within a module, as in Racopilum and Hypopterygium, whereas heteroblasty (Figure 14.7C) is the change in form seen along every module as it develops. In anisophylly the primary module leaves are clearly differentiated in size or shape from secondary module leaves. For example, in Thuidium and Eurhyncium praelongum, primary module leaves are both larger and different in

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A B

D C

FIGURE 14.5 Architecture of pleurocarpous mosses: characters 11 to 12 (perichaetial module origin and subperichaetial innovations). (A) Perichaetial modules formed distally on primary modules and on secondary modules, subperichaetial innovations absent (Pireella); (B) perichaetial modules basal on primary modules, subperichaetial innovations present, fertile only (Pyrrhobryum); (C) perichaetial modules formed distally on primary module, subperichaetial innovations present, fertile only (Cryphaea); (D) perichaetial modules formed nonspecifically on primary module, subperichaetial innovations present, both fertile and vegetative (Amblystegium).

shape from secondary module leaves. In other taxa, for example in Pireella, leaves on the primary module undergo extreme heteroblastic transformations in both size and shape, but at all stages differ in both size and shape from the leaves of the secondary modules. Other taxa may have primary module leaves smaller and different in shape than those of the secondary module, especially where the primary module is stoloniform, or the leaves may differ in shape but not size, or size but not shape. Other features that can be used to distinguish between primary and secondary modules are the relative diameter of the axis, the point on the subtending module at which the module originates, and whether or not it appears to be determinate or indeterminate. However, in some cases there may be no obvious difference between modules, and no objective criterion that can be used, in which case all vegetative modules have to be regarded as primary. In some taxa even though there is a clear differentiation between modules it may not be possible to determine which is “primary.” For example, in Leucodon julaceus, no obvious “secondary” modules are formed, but stolons and stems give rise to the alternate morphology by branching, and may also transform into the other through heteroblasty. (Confirmation of this requires careful dissection to ascertain that the transformation is not due to a terminal innovation following death of the original apical cell.) In such cases of alternating morphology, the convention is used here that the module that supports gametangial modules is considered primary, and the morphology of this phase is used for comparison with other taxa, while the alternate form (usually stoloniferous) is regarded as a mode of vegetative reproduction. However, other interpretations are possible. Although La Farge-England (1996) states that the juvenile leaves surrounding secondary modules and reproductive modules can differ in size and shape, this seems to refer to their morphology after the module has developed sufficiently to be classified, i.e., by swelling and initiating gamet-

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†* †

FIGURE 14.6 Origin of primary modules in “tufted” pleurocarps (Hypnodendron subspininervium ssp. arborescens, Ellis 380). Note that only one frond has been drawn (of the other three, two were moribund † and the third robust ) and the majority of secondary modules have been omitted. The branching points are expanded for clarity, and would normally be obscured by dense growth of rhizoids.

angia (La Farge-England, personal communication). In small branch primordia, perichaetia, perigonia and vegetative branches can be differentiated by these characters, as well as by the differences in shape of the associated leaves. However, at initiation, prior to gametangia differentiation, there is a phase where it does not seem possible to predict the hierarchical level of the module from the shape of the juvenile leaves of the branch primordium.

14.2.5 SECONDARY MODULE ORIENTATION As with primary module orientation, the angle of branching includes absolute or relative orientation, but also the orientation of the branches to the primary module and to other secondary modules. This assemblage of characters can be usefully considered as (a) orientation relative to the substrate (orthotropous or plagiotropous), (b) orientation relative to the other secondary modules (complanate or radial) and (c) orientation relative to the long axis of the primary module (angle of branching). However, these are not necessarily completely independent. In a plant with an orthotropous primary module and secondary modules at an acute angle, the branches will also be effectively orthotropous. Where secondary modules are at a broad angle to an orthotropous primary module the branches will be closer to plagiotropous. The majority of pleurocarpous taxa with orthotropous primary modules have secondary modules at approximately 45° to the primary module. These may have an arrangement that is radial (e.g., Climacium, Figure 14.9.2B), or complanate (e.g., Pireella, Figures 14.9.2A; 14.9.2C). In plants with plagiotropous primary mod-

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A

Anisophyllic differentiation of adult leaves between modules

B

Heterophyllic differentiation (alternation) of adult leaves

C Heteroblastic leaf sequence juvenile

adult leaf form

FIGURE 14.7 Variation in leaf form. (A) Anisophylly, leaves on the secondary module differ from the leaves on the primary module in size, shape, development of the costa, or other features (e.g., Thuidium, Eurhynchium praelongum); (B) heterophylly, leaves alternate along a module, with successive leaves differing in size, shape, costa development, lamina cell size and shape, leaf margins (e.g., Racopilum, Hypopterygium); (C) heteroblasty, leaves differ in a regular progression along the module, with juvenile leaves at the base (left) and adult leaves in the distal regions (right). Each leaf develops from its initiation to its final mature form within this sequence (see Mishler and De Luna, 1991). Every module (including those in A and B) shows heteroblasty, but in some taxa it is more pronounced and easier to recognize (e.g., in Thamnobryum.) In addition, in some taxa heteroblastic alternation of leaf forms can occur (e.g., in Anomodon). This differs from heterophylly in that all leaves will have one form in a given section of the module, changing into a different form further along.

ules the orientation of the secondary modules may also not be clearly independent from the orientation of the primary modules. In Myurium hochstetteri the primary module is plagiotropous with secondary modules orthotropous, and thus necessarily at 90° to the long axis of the primary module. Many taxa, whether adpressed to the substrate (e.g., Hypnum) or elevated above it by an orthotropous stipe (e.g., Hylocomium), have the secondary modules plagiotropous with respect to the substrate, in a single plane relative to each other (or in two planes at a slight angle to each other), and at an angle of between 30° and 90° to the axis of the primary module, possibly reflecting convergence on an ecological optimum.

14.2.6 SECONDARY MODULE POINT

OF

ORIGIN

In many determinate frondose or dendroid mosses the secondary modules develop almost exclusively in the distal region of the primary module, leaving the lower portion differentiated as a stipe free of branches (e.g., Hylocomium) or as a stolon and stipe (e.g., Pireella). In other frondose and plumose taxa, branches develop along the length of the orthotropous region of the primary module, leaving only the plagiotropous stolon region free of branches (e.g., Calyptothecium). This is also the case with plants with plagiotropous primary modules but frondose growth, such as Neckera (Appendix

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1° 1°

A B 2° 1°

C

1°

2°

D

E 1° 2°

FIGURE 14.8 Examples of branching architecture of specific taxa (generalized). (A) Hypnodendron, (B) Pyrrhobryum spiniforme, (C) Spiridens, (D) Hypopterygium tamariscinum, (E) Racopilum tomentosum.

14.1k), where only the stolon is free of branches. Secondary modules usually occur along the length of plants with indeterminate primary modules (Figure 14.4C; e.g., Pleurozium, Appendix 14.1a). Formation of secondary modules exclusively at the base of the primary module is rare in extant taxa. Plants with exclusively basal branching in the early-diverging pleurocarps (“Rhizogoniales”, hypnodendroid pleurocarps and some members of Ptychomniales, see Chapter 3) form only primary modules or reproductive modules in this position (Figure 14.5B and Figure14.8B). However, in taxa with plagiotropous and indeterminate primary modules, the secondary modules may initiate at a distance from the module apex, so the branches near the base of the active portion of the primary module are larger and more likely to show secondary branching than those close to the apex (e.g., Pseudoscleropodium). Branches may also initiate and grow to variable lengths in an apparently random manner, with no obvious pattern of development relative to the primary module apex or to other branches, producing a very irregular and weft-like growth form (e.g., Amblystegium, Appendix 14.1g; Brachythecium; Pleurozium, Appendix 14.1a; Rhytidium).

14.2.7 BRANCHING ORDER

AND

DENSITY

OF

SECONDARY MODULES

In most cases branches higher in the modular hierarchy (secondary and above) are very similar to those subtending them, differing primarily in a gradual diminution of size with each successive module, but without differentiation of shape or abrupt discontinuities. It therefore might be more accurate to regard such levels of the hierarchy as further levels of secondary modules, rather than tertiary or quaternary modules. Most taxa develop only one or two levels of additional modules, but some can form three or more levels (Figure 14.4A), e.g., in Thuidium tamariscinum. The formation of the secondary modules reflects the action of several processes controlling the development of the lateral primordia. Each merophyte has the potential to form an apical cell that

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can develop into a branch primordium and then into a new module, so that if all apical cells developed fully there would be a branch associated with each leaf, and numerous orders of modules, resulting in a very densely branched structure. Branching of this density rarely occurs in nature — Thuidium tamariscinum is an example, but even here, branch primordia are not formed on all merophytes, nor do they all develop into branches. Many branch primordia initiate just a few juvenile leaves and then remain dormant, while others develop as secondary modules, reproductive modules or new primary modules. Most work on control of development and growth in mosses has been carried out on protonema and gametophore initiation (Christianson, 2000), and although the mechanisms of release from dormancy have been studied, it is not known whether individual branch primordia are preprogrammed to develop into a given modular type, or the extent to which external factors exert control. The distribution of secondary modules reflects interaction between the number and distribution of branch primordia, and control of dormancy. Although a branch primordium can potentially be formed at each leaf, there are usually fewer — for example, in some taxa there may be one at approximately every fifth leaf, whereas in others there may be only one for every twenty leaves. There may be differences in the numbers of primordia formed between levels of the modular hierarchy, with more primordia formed on secondary modules than on primary, or vice versa. There may also be differences in the pattern along a module. In taxa in the basal pleurocarp grade, very large numbers of branch primordia are seen at the bases of primary and secondary modules, but very few are formed along the rest of the module, with the exception of dendroid species where branch primordia are found in the mid-region of the primary module (e.g., Hypnodendron). This is in contrast to other dendroid taxa, (e.g., the Pterobryaceae) which have branch primordia that are evenly distributed along the primary module, but development of branch primordia into secondary modules is localized in the frond region. Although merophytes (and leaves) usually develop in a spiral pattern, and branch primordia can be formed at any of these positions, secondary modules often develop in a complanate pattern. Branch primordia on the “sides” of the primary modules develop into secondary modules or reproductive modules, whereas those on the dorsal and ventral surfaces do not develop, or form primary modules. Where branch primordia are found evenly distributed along the module, but development of primordia into secondary modules is localized or complanate, it can be supposed that the branching pattern seen reflects mechanisms involving control or release of dormancy. The role of auxins, specifically indolyle-3-acetic acid (IAA), in apical dominance has been shown to be similar to that in vascular plants (see Cooke et al., 2002, for summary), and can be expected to have an important role in the suppression or release from dormancy of branch primordia. For example, if the apical cell of the primary module is producing auxins that suppress development, branch primordia will develop only when they are sufficiently far from the apical cell for the levels of auxin to have dropped to a certain level. Similarly, the density of secondary modules may also reflect auxin control of module development, with branch primordia remaining dormant where the density of secondary modules has reached a local optimum. There is also evidence that IAA can control development of body-plan (i.e., selective development of branch primordia) (Cooke et al., 2002).

14.2.8 LENGTH

AND

DETERMINANCY

OF

SECONDARY MODULES

Although there is some variation, the pattern of growth of secondary modules is often characteristic of given taxa, with, for example, classic plume-shaped mosses such as Ptilium cristra-castrensis and Hypnum imponens contrasting strongly with straggling plants such as Brachythecium rutabulum. Although determinancy of growth can only be inferred from observation of specimens, the presence of many secondary modules all the same length, or that do not grow beyond a general maximum, suggests that the final length of the module is determined. It seems probable that growth of secondary modules in the vast majority of pleurocarpous mosses is determinate, with primary modules providing extension growth and secondary modules filling out the photosynthetic surface area.

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14.2.9 REITERATION Although primary and secondary modules have a hierarchical relationship to each other, the branch system (Mishler and De Luna, 1991), composed of one or more primary modules or a primary module and its associated secondary modules, repeats in a manner (Figure 14.3G; 14.5A; 14.8D; Pseudocryphaea, Appendix 14.1i; Neckera, Appendix 14.1k) that is not hierarchical. A given primary module may go through a heteroblastic transformation, for example as in Hypopterygium (Figure 14.8D), forming first a plagiotropous stolon with scale-like leaves, then turning perpendicular to the substrate and forming enlarged stipe leaves but no branches, and then forming determinate secondary modules in the distal portion of the determinate primary module. Each secondary module also produces leaves and may produce additional modules (vegetative or reproductive). Continued plant growth is from a branch primordium in the area where the original primary module switches from plagiotropous to orthotropous, and the pattern is repeated. In taxa with a less complex growth form (including plants with indeterminate primary modules, or alternating morphology) a similar pattern is seen — the primary module undergoes heteroblastic transformation, producing a succession of leaves and secondary modules, that is then repeated. A new branch system may also develop in a position other than that predicted by normal growth patterns. This occurs in the majority of taxa following death of the apex of the primary module. A new module develops directly behind the old module apex, even if it would not normally do so, probably reflecting the loss of apical dominance (see 14.2.7). In some taxa additional branch systems develop readily, apparently without loss of the existing apical cell, and sometimes omitting part of the heteroblastic series. Thus, a branch primordium on the stipe or frond section of a primary module may develop into a stolon, initiating a new branch system, or it may form another stipe, without going through the usual preceding stolon phase (Figure 14.4D; 14.9.2D–E). Interpolation of a new branch system is referred to as reiteration (Hallé, 1999). This provides a means of regeneration following death or damage of the primary modules, but can also provide a means of “bulking up” of the plant as part of the normal growth pattern.

14.2.10 FORMATION

OF

PLAGIOTROPOUS MODULES

Plagiotropous modules, often with highly reduced leaves (“scale leaves”) are found in many taxa. There are two principal forms (stolons and shoots), that are probably not homologous to each other and that may have arisen numerous times within the pleurocarps. In taxa where plagiotropous modules occur they are often involved in reiteration (see Section 14.2.9). Stolons are normally formed from the base of the orthotropous region of a module (primary or secondary, Figures 14.3H and 14.8D; e.g., Pseudocryphaea and Thamnobryum, Appendix 14.1i, 14.1j; Neckera and Forsstroemia, Appendix 14.1k, 14.1l) or from other stolons. They may also develop in distal regions of orthotropous or plagiotropous modules. Typically stolons grow downwards for a short distance, then become plagiotropous. They are closely attached to the substrate by rhizoids, and may often grow through the upper surface of soil or bark, or among other vegetation. Orientation may reflect responses to gravity, light or contact with the substrate. In contrast, flagelliform shoots are primarily aerial, developing in the distal regions of primary modules, and usually represent a modified secondary module (Figure 14.4D). Flagelliform branches may develop directly from a branch primordium, or an existing secondary module may become flagelliform. In taxa where the secondary module is usually determinate, this represents a transformation of the apical cell to an indeterminate mode of growth. As with stolons, the leaves are usually greatly reduced in size and are often distantly spaced, but the branch usually lacks rhizoids except in occasional tufts. The flagelliforme branch is also plagiotropic, supported by other vegetation or becoming pendulous when unsupported. On contact with a hard substrate, it becomes more stolonlike, developing rhizoids and adhering to the substrate, and will frequently then become orthotropous, reestablishing the heteroblastic sequence of the primary module.

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14.2.11 PERICHAETIAL MODULE POINT

OF

ORIGIN

In nearly all taxa of the pleurocarpous mosses gametangia are produced terminating specialized reproductive modules that lack normal vegetative leaves. Although many cladocarpous mosses were included within the pleurocarpous mosses (Vitt, 1984) most have now been transferred to other lineages. However, some cladocarps are retained within the pleurocarp clade, and appear to represent reversals rather than plesiomorphic states. For example, Schoenobryum in the Cryphaeaceae has perichaetia terminating long branches (Figure 14.3D) that have numerous undifferentiated vegetative leaves by the time the perichaetia are formed. The morphology closely resembles that of acrocarpous mosses, with all mature modules terminated by gametangia, and no apparent differentiation of secondary modules. There is considerable variation in the location on the primary module at which the perichaetial modules are formed. (Perigonial modules have not yet been studied in sufficient detail to discuss here, but their distribution is usually similar to that of perichaetia, differing primarily in number rather than position.) In the majority of taxa, perichaetial modules are formed on the primary module among the secondary modules, and often also on the bases of secondary modules. They may be sparse or very abundant, equalling or exceeding the secondary modules in number (Figures 14.1D and 14.5). In dendroid mosses, where secondary modules form primarily in the frondose region of the primary module (i.e., acrotonous, see La Farge-England, 1996) perichaetial modules are also restricted to this position (Figures 14.5A, and 14.8A, C–D). In weft-forming mosses, where such restriction of distribution of secondary modules does not occur, perichaetial modules may be evenly distributed, with no apparent pattern (Figure 14.8E; e.g., Hookeria, Appendix 14.1d; Amblystegium, Appendix 14.1g) or they may be restricted to certain regions of the primary module (e.g., Plagiothecium, Appendix 14.1c). Seasonal or environmental cues may be responsible for such distributions. The perichaetial modules may be formed at the base of orthotropous primary modules (i.e., basitonous distribution, La Farge-England, 1996) in some mosses in the basal grade of the pleurocarpous clade (Rhizogonium and Pyrrhobryum Section Pyrrhobryum, Figure 14.5B and Figure 14.8B; Bell and Newton 2005; Chapter 3).

14.2.12 PRESENCE

OF

SUBPERICHAETIAL INNOVATIONS

In the acrocarpous mosses further growth of the plant (following termination of the existing primary module by the formation of gametangia) usually takes place by the formation of a subperichaetial innovation, that is, on the reproductive module. This may be directly behind the module apex, or some distance further down the module, leaving a short stub that makes the branching pattern more apparent (Figures 14.1A and B). In the vast majority of pleurocarpous mosses branch primordia do not seem to be formed on the reproductive modules, and this character was used (in combination with differentiated juvenile leaves and swollen module base) by La Farge-England (1996) to define pleurocarpy. However, in certain pleurocarpous taxa, especially species of Cryphaea (Figure 14.5cC) and Amblystegium (Figures 14.5D and 14.1), branch primordia (vegetative or reproductive) do develop on the reproductive modules. The ability of specialized reproductive branches to form branch primordia is not restricted to the perichaetial modules, but also occurs on the (often much smaller) perigonial modules. These male branches are sometimes clustered, that is, growing as innovations on other male branches, as for example, in Fabronia. The presence of subperichaetial innovations has been noted in several pleurocarpous taxa (e.g., members of the Cryphaeaceae, Amblystegium) that are unquestionably pleurocarpous, and have been shown to be nested within the clade of pleurocarpous mosses by several large-scale studies (e.g., Buck et al., 2000; Newton et al., Chapter 17; Tsubota et al., 2002). In the Crypheaceae a range of conditions has been observed (Leon, unpublished data), from plants that are essentially acrocarpous, with primary modules terminated by perichaetia (and perigonia terminating short lateral branches; Schoenobryum), through those that are cladocarpous, with gametangia terminating short vegetative

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PLATE 14.1 Subperichaetial branching in Amblystegium serpens. The stump of a vegetative branch subtends the remains of an old perichaetial branch in the centre, with a vegetative branch to the left, a developing sporophyte behind, and a young branch to the right. Careful dissection reveals that the young branch (probably vegetative) and perichaetial branch originate from the old perichaetial branch.

branches (Dendropogonella), to pleurocarpous species with perichaetial modules single or, rarely, clustered (Cryphaea). In Amblystegium, innovations on the perichaetial modules may produce both additional perichaetial modules and vegetative branches (see Figure 14.5D, Plate 14.1). In Rhizogonium and Pyrrhobryum Section Pyrrhobryum, innovations on the perichaetial modules form new perichaetial modules (Figure 14.5B), but not vegetative primary modules (discussed further in Chapter 3). The placement of these taxa in the pleurocarpous mosses, in a basal grade containing several acrocarpous taxa (Bell and Newton, 2005, see also Chapter 3), could indicate that the presence of subperichaetial innovations in these taxa is a retained plesiomorphic condition, whereas in taxa such as Amblystegium this condition is an independently derived reversal.

14.3 ARCHITECTURAL GROUNDPLANS There are probably almost as many different combinations of these characters as there are species, with even closely related species showing variations from each other. However, in many cases an “architectural groundplan” can be found for closely related groups of taxa sharing some unique combination of these characters. Examination of these different features allows variation within individual species, and comparison between taxa, to be made with more objectivity. It also allows features that represent convergence due to environmental constraints to be studied. In the following section several examples of the application of these characters are given.

14.3.1 HOW MANY WAYS ARE THERE

TO

MAKE

A

DENDROID MOSS?

A “dendroid” moss consists of an erect, unbranched stipe with leafy branches, or in some cases, large spreading leaves. Different architectural elements can be combined to produce very similar morphologies. A range of different combinations is illustrated in Figure 14.9 (see figure captions for details). These demonstrate the effect of different architectural elements on the structure of the “dendroid” moss, and can appear in combinations of varying complexity. Some combinations are mutually exclusive, such as complanate and radial secondary branching. Rather more combinations

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1a

1c

1b

2a

2b 2c

2d

2f

2e

3

FIGURE 14.9 How many ways are there to make a dendroid moss? (1) Tufted orthotropic primary modules with (a) pinnate secondary modules, (b) umbellate secondary modules, (c) reiteration. (2) Primary modules with differentiation of stolon and stipe with (a) complanate secondary modules, (b) radial secondary modules, (c) second- and third-order branching of secondary modules, (d) reiteration through distal development of primary modules, (e) reiteration by conversion of determinate secondary module to plagiotropous primary module (“flagelliforme branch”), (f) reiteration by development of primary module as an orthotropous branch. (3) Alternating orthotropous and plagiotropous primary modules, with erect stems formed on creeping stolons.

are possible than are shown here. A simple dendroid moss might have tufted orthotropic primary modules, complanate secondary branching and no reiteration. A complex structure might include several changes in orientation of the primary module with alternating morphology, radial branching of the secondary modules with several orders of branching, and reiteration of both primary and secondary modules. Two such morphologies are described, with the number of each character from above given in brackets. In Hypnodendron (Figure 14.9.1A–C) the primary modules are determinate (1), orthotropous (2) and tufted (3), branching from the base of the preceding module with virtually no plagiotropic component. The growth is hierarchical (4), with primary and secondary modules differentiated by anisophylly and module orientation. The secondary module orientation (5) is plagiotropous, complanate, and at approximately 90° to the long axis of the primary module. The secondary module origin (6) is either pinnate (regularly spaced) or umbellate (concentrated at one point) in different taxa. Branching order (7) is single or double in different taxa, and the secondary modules are determinate (8) and moderately long. Reiteration (9) is present in some taxa, with a new primary module formed in the mid region rather than basally. Stolons and flagelliforme shoots (10) are absent. Perichaetial modules (11) are formed distally and no subperichaetial innovations (12) have been observed. A “typical” example of a dendroid plant in the hypnanaean pleurocarps is provided by Thamnobryum alopecurum (Appendix 14.1j). Here the primary modules are determinate (1), pla-

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giotropous becoming orthotropous (2), and new primary modules (3) develop at the point where the plagiotropous stolon becomes orthotropous, although new modules do initiate by reiteration omitting the stolon phase. The growth is hierarchical (4), with primary and secondary modules differentiated by anisophylly. The secondary module orientation (5) is plagiotropous, radial, and at approximately 45° to the long axis of the primary module. The secondary module origin (6) is pinnate but irregularly spaced. Branching order (7) is double, and the secondary modules are determinate (8) and moderately long. Reiteration (9) occurs, with new primary modules (both stolons and stipes) formed in the mid to distal region of the primary module. Stolons (10) are present but flagelliforme shoots are absent. Perichaetial modules (11) are formed distally and no subperichaetial innovations (12) have been observed. In some taxa the orthotropous stipe develops as a branch on a plagiotropous stolon, which may remain plagiotropous or itself become orthotropous. Interpretation of these modules as primary or secondary is problematic, especially where the two forms of module alternate. The traditional use of the term “primary stem” for the plagiotropous module and “secondary stem” for the orthotropous module may be more accurate in these taxa than in those where a single module is both plagiotropous and orthotropous. An example is Forsstroemia trichomitria (Appendix 14.1l). These plants are very similar to the hypnanean dendroid moss as exemplified by Thamnobryum, but differ in that the determinate orthotropous modules mostly develop as branches from an indeterminate plagiotropous stolon.

14.3.2 DENDROID

AND

SHELF MOSSES

The morphology of dendroid mosses and shelf-forming mosses can be very similar when examined in detail, the principal difference being the orientation of the primary module. Examples shown here include dendroid Thamnobryum (Appendix 14.1j) and Pseudocryphaea (Appendix 14.1i) with distal primary modules orthotropic, and shelf-forming Neckera (Appendix 14.1k), with modules plagiotropic throughout. In all these taxa there are stoloniform primary modules that change direction to grow at right angles to their previous orientation, and that form new primary modules at the point of change in orientation, but in Neckera these remain in the same plane, forming a series of flat shelves growing over each other.

14.4 CONCLUSIONS In the centuries since Hedwig (1778) first described archegonia and antheridia, and Bridel (1819) used gametangial position to classify mosses under the categories of cladocarp, acrocarp or pleurocarp, the use of these concepts in classification and the study of growth form in mosses has been variously accepted and rejected. The distribution of taxa with lateral perichaetia thoughout the acrocarps, although in small numbers, and the “intermediate” form of cladocarps complicated the picture so the homology, or otherwise, of these features was obscured. The advent of molecular data and cladistic analysis has allowed the development of a robust phylogenetic hypothesis for the relationships of the mosses, which has confirmed that the majority of pleurocarps form a monophyletic group, but other apparent “pleurocarps,” with gametangia formed on short branches, are scattered throughout the acrocarps. Similarly, the taxa considered to be cladocarps have long been recognized as being scattered throughout the range of mosses (see Vitt, 1984; La FargeEngland, 1996), placements that have been confirmed and supported subsequently by a variety of molecular studies. The non-monophyly of the groups in which “cladocarpy” occurs, and of the taxa in which “pleurocarpy” seems to occur outside the Hypnidae + Rhizogonianae (sensu Goffinet and Buck, 2004) confirms the homoplasious nature of these morphologies. Although Meusel (1935) described the growth form of mosses in detail, the confusion of the strict technical terms “acrocarpy” and “pleurocarpy” with various associated characters such as shoot orientation and features of the cells, costa and leaf, has reduced the systematic value of

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morphology. By focusing on modular structure, the elements of branching architecture can be revealed. Careful examination and precise recording of features as discrete characters are necessary to allow morphology to be appropriately studied in the context of modern methods of phylogenetic analysis, and to allow the study of the evolution of morphological features.

ACKNOWLEDGMENTS Thanks to Catherine La-Farge for valuable comments on the manuscript.

REFERENCES Beckert, S., Steinhauser, S., Muhle, H. and Knoop, V. (1999) A molecular phylogeny of bryophytes based on nucleotide sequences of the mitochondrial nad5 gene. Plant Systematics and Evolution, 218: 179–192. Beckert, S., Muhle, H., Pruchner, D. and Knoop, V. (2001) The mitochondrial nad2 gene as a novel marker locus for phylogenetic analysis of early land plants: A comparative analysis in mosses. Molecular Phylogenetics and Evolution, 18: 117–126. Bell, N. and Newton, A. E. (2004) Systematic studies of non-hypnalean pleurocarps: Establishing a phylogenetic framework for investigating the origins of pleurocarpy. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 290–319. Bell, N. and Newton, A. E. (2005) The paraphyly of Hypnodendron and the phylogeny of related nonhypnaneaen pleurocarpous mosses inferred from chloroplast and mitochondrial sequence data. Systematic Botany, 30: 34–51. Bridel, S. E. (1819) Muscologiae Recentiorum Supplementum Pars IV. A. Ukertum, Gothae. Buck, W. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL-trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Cavers, F. (1911) Interrelationships of the Bryophyta. New Phytologist, London. Christianson, M. L. (2000) Control of morphogenesis in bryophytes. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 199–224. Cooke, T. J., Poli, D.-B., Sztein, A. E. and Cohen, J. D. (2002) Evolutionary patterns in auxin action. Plant Molecular Biology, 49: 319–338. Cox, C. and Hedderson, T. A. J. (1999) Phylogenetic relationships among the ciliate arthrodontous mosses: Evidence from chloroplast and nuclear DNA sequences. Plant Systematics and Evolution, 215: 119–139. Cox, C., Goffinet, B., Newton, A. E., Shaw, A. J. and Hedderson, T. A. J. (2000) Phylogenetic relationships among the diplolepidous-alternate mosses (Bryidae) inferred from nuclear and chloroplast DNA sequences. Bryologist, 103: 224–241. Cox, C., Goffinet, B., Shaw, A. J. and Boles, S. (2004) Phylogenetic relationships among the mosses based on heterogenous Bayesian analysis of multiple genes from multiple genomic compartments. Systematic Botany, 29: 234–250. De Luna, E., Newton, A. E., Withey, A., Gonzalez, D. and Mishler, B. D. (1999) The transition to pleurocarpy: A phylogenetic analysis of the main diplolepidous lineages based on rbcL sequences and morphology. Bryologist, 102: 634–650. Goffinet, B. and Buck, W. R. (2004) Systematics of Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Brytophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Hallé, F. (1999) Ecology of reiteration in tropical trees. In The Evolution of Plant Architecture (ed. M. H. Kurmann and A. R. Hemsley). Royal Botanic Gardens, Kew, pp. 93–107. Hallé, F., Oldeman, R. A. A. and Tomlinson, P. B. (1978) Tropical Trees and Forests. An Architectural Analysis. Springer-Verlag, Berlin.

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Hedwig, J. (1778) Vorläufige Anzeige seiner Beobachten von den wahren Geschlechtstheilen der Moose und ihre Fortpflanzung durch Saamen. Leipziger Sammlungen Physik Naturgeschichte, 1(3). Koponen, T. (1988) The phylogeny and classification of Mniaceae and Rhizogoniaceae. Journal of the Hattori Botanical Laboratory, 64: 37–46. La Farge-England, C. (1996) Growth form, branching pattern and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99: 170–186. La Farge-England, C. (1998) The infrageneric phylogeny, classification and phytogeography of Leucoloma Brid. (Dicranaceae, Bryopsida). Bryologist, 101: 181–220. Magill, R. E. (1990) Glossarium Polyglottum Bryologiae. Missouri Botanical Garden Press, St. Louis. Malcolm, B. and Malcolm, N. (2000) Mosses and Other Bryophytes. An Illustrated Glossary. Micro-optics Press, Nelson. Meusel, H. (1935) Wuchsformen und Wuchstypen der europäischen Labmoose. Nova Acta Leopoldina (Neue Folge), 3(12): 123–277. Mishler, B. D. and De Luna, E. (1991) The use of ontogenetic data in phylogenetic analysis of mosses. Advances in Bryology, 4: 121–167. Newton, A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Newton, A. E., Cox, C., Duckett, J. G., Wheeler, J., Goffinet, B., Hedderson, T. A. J. and Mishler, B. D. (2000) Evolution of the major moss lineages. Bryologist, 103: 187–211. Proctor, M. C. and Smith, A. J. E. (1995) Ecological and systematic implications of branching patterns in bryophytes. In Experimental and Molecular Approaches to Plant Biosystematics (ed. P. C. Hoch and A. G. Stephenson). Missouri Botanical Garden Press, St Louis. Tsubota, H., Arikawa, T., Akiyama, H., De Luna, E., Gonzalez, D., Higuchi, M. and Deguchi, H. (2002) Molecular phylogeny of hypnobryalean mossees as inferred from a large-scale dataset of chloroplast rbcL, with special reference to the Hypnaceae and possibly related families. Hikobia, 13: 645–665. Vitt, D. (1984) Classification of the Bryopsida. In New Manual of Bryology (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 676–759. Watson, E. V. (1968) British Mosses and Liverworts. Cambridge University Press, Cambridge. White, J. (1984) Plant metamerism. In Perspectives on Plant Population Ecology (ed. R. Dirzo and J. Sarukhán). Sinauer Associates, Sunderland, Massachusetts.

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and Monopodial 15 Sympodial Growth in Mosses: Examples from the Lembophyllaceae (Bryopsida) Ray Tangney CONTENTS Abstract ..........................................................................................................................................309 15.1 Introduction...........................................................................................................................309 15.2 Architectural Concepts .........................................................................................................310 15.2.1 Growth: Shoot Construction.....................................................................................310 15.2.2 Repeated Units..........................................................................................................311 15.2.3 Branching..................................................................................................................312 15.3 Mosses ..................................................................................................................................313 15.3.1 The Lembophyllaceae ..............................................................................................314 15.3.2 Further Examples......................................................................................................316 15.4 Summary and Conclusions...................................................................................................317 References ......................................................................................................................................318

ABSTRACT By emphasizing architectural concepts, this chapter examines the way in which structural terms, as used in the analysis of Tracheophytes, have increased our understanding of branching patterns in mosses. Architectural concepts and their application to mosses are reviewed. With reference to the Lembophyllaceae, monopodial and sympodial growth are differentiated and growth units are discussed. The chapter introduces the concept of the architectural unit, not previously applied to mosses, and shows how this concept facilitates the recognition of branching type and the hierarchical level at which branching occurs. The emphasis is on the differences in the nature of sequential growth (i.e., branching that builds architectural units) and reiterative growth (i.e., growth that repeats the architectural units).

15.1 INTRODUCTION The value of branching analysis in mosses has long been recognized, from the ground-breaking analysis of Meusel (1935) to the more ecologically focused growth form and life form analyses of Gimingham and Robertson (1950), Magdefrau (1982), During (1979), and Richards (1984). Branching in these analyses were perceived as influenced by the environment, blurring the distinction

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between growth form and life form, and the stability of the morphological characters of branching and their taxonomic utility became unclear (La Farge-England, 1996; Tangney, 1998). More recently, as part of a reevaluation of morphological characters in moss systematics, there has been an increased interest in a strictly morphological analysis of branching. The application of branching analysis has recently extended to a range of studies in moss systematics: (1) taxonomy (Rohrer, 1985; De Luna, 1990; Tangney, 1997, 1998; Buck, 1998; Buck and Goffinet, 2000); (2) phylogenetic analysis (Mishler, 1986, 1988; La Farge-England, 1998; Newton and De Luna, 1999); (3) understanding the origins of pleurocarpy (Newton and De Luna, 1999); and (4) the nature of growth forms (Tangney, 1998). Mishler and De Luna (1991) outlined a hierarchical system for the description of development in mosses. They emphasized a structural approach and placed their system in the tradition of architectural analysis of Tracheophytes (e.g., Hallé et al., 1978). This approach is focused on development and the genetic basis of growth that is independent of environmental factors, yielding an analysis that is primarily morphological rather than adaptive. With the increase in phylogenetic analyses of morphological data, architectural analysis of mosses provides an increasing accuracy for determining homologous characters (Newton and De Luna, 1999; De Luna et al., 1999). This approach has been broadly embraced by muscologists. The term architecture has been used in reference to analysis of both the gametophyte and the sporophyte. There has also been a corresponding increase in the usage of architectural terms associated with branching analysis. La Farge-England (1996) reviewed and provided definitions for terminology associated with branching and growth form. Importantly, she explicitly recognized that monopodial and sympodial branching occur at different hierarchical levels. Despite this recognition, there has been a lack of emphasis on these processes occurring at different hierarchical levels. The use of the dichotomous opposition of monopodial versus sympodial branching has proved to be problematic, with Buck et al. (2000) noting the possibility that this division of branch types may not be best represented as a single character. If branching type is to be utilized in phylogenetic analyses of morphological characters, it is important to determine developmental homologues, which requires that the concepts and terminology are clear. By emphasizing architectural concepts traditionally applied to tracheophytes, this chapter examines the way in which terminology has increased our understanding of branching patterns in mosses. It outlines architectural concepts and then looks at their application to mosses. The concept of the architectural unit (not previously applied to mosses) is introduced. This concept facilitates the recognition of both the type of branching and the hierarchical level at which branching occurs, aspects of branching analysis that have had insufficient emphasis. It differentiates the nature of branching within and between architectural units.

15.2 ARCHITECTURAL CONCEPTS Architectural study of plants is the analysis of their construction, identifying the types of axes (shoots, branches, etc.) present and their construction and relative position. Central to this approach is the recognition that plants grow through the development of a limited and well-defined set of growth units. Descriptive plant architecture focuses on a search for repeated units of growth, axes or groups of axes. The following outline is based on recognizing growth and branching as two separate processes, after Hallé et al. (1978) and Bell (1991).

15.2.1 GROWTH: SHOOT CONSTRUCTION There are two ways in which a plant shoot can be produced, monopodially or sympodially (Figure 15.1). Monopodial growth is the product of a single apical meristem, and produces a single shoot unit called a monopodium. The monopodium may have limited growth (i.e., determinate), or grow

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A

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FIGURE 15.1 Growth and repeated units. (A) Growth: (i) monopodial growth produces a monopodium, a single unit of growth; (ii) sympodial growth produces a sympodium, a series of connected growth units (modules). (B) Repeated units: (i) modules (m) are the products of individual apical cells. They occur hierarchically: primary modules (10m), secondary modules (20m), tertiary modules (30m). Individual growth units forming a sympodium are called modules (Figure 15.1A (ii)). (ii) The architectural unit (a.u) comprises the branch categories potentially produced by a species. In mosses, the architectural unit is the primary module and the growth units (secondary modules, tertiary modules, reproductive structures, etc.) produced on it.

indefinitely (i.e., indeterminate). In either case, no lateral or axillary bud takes over further extension growth of the monopodium. The monopodium may or may not have determinate lateral branches. Sympodial growth produces an axis called a sympodium, comprising a series of connected shoot units, each derived from a different apical meristem. The shoot units that make up the sympodium are called sympodial units, or modules, and each sympodial unit provides further shoot extension growth from a lateral meristem. The sympodium may or may not have determinate lateral branches, and the sympodial units themselves may be determinate or indeterminate.

15.2.2 REPEATED UNITS The module is a sympodial unit that is repeated to make up a shoot unit, the sympodium (Figure 15.2). It may be determinate or indeterminate. In a broader definition it commonly refers to any part of the plant that is reiterated. Because of these two distinctly different meanings, the term module has given “modularity” a broad definition, and to ensure precision care must be taken in using the term module. Growth and branching in plants occur in an orderly sequence. Within that sequence shoots appear in their “correct” positions, producing the basic format to which the species conforms. The

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2om 2om o 1 m

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FIGURE 15.2 Branching and reiteration. (A) Branching: (i) monopodial branching (sensu La Farge-England, 1996) produces branches of a lower hierarchical order; (ii) sympodial branching produces branches of the same hierarchical order; (iii) monopodial and sympodial branching together. Note that monopodial branching (lateral branching) can also produce new primary modules (see Figure 15.3, C3). (B) Reiteration (R) is branching that repeats the developmental sequence. In mosses, this repeats the primary module producing new architectural units. Sympodial reiteration (SR), monopodial reiteration (MR).

observation of a number of distinct plant formats, determined by branching pattern, growth rhythm, axis orientation and distribution of sex organs (Hallé, 1999), has led to the recognition of architectural models (Hallé et al., 1978). Many different species can exhibit the same architectural model, but they may differ in how the model is produced. The specific expression of the architectural model, the group of axes that are reproduced to make up the particular model, is called the architectural unit (Hallé, 1999). Recognition of the architectural unit for any particular species involves description of the various branch types produced. Through accumulation of multiple architectural units, plants are often not individuals, but colonies of repeated units. The architectural unit is interpreted as a synopsis, from juvenile to adult, and comprises the branch categories that are produced during that development. It is thus a summary of the branch potential of the plant. It can vary from a simple structure (e.g., a single monopodium without lateral branches) to more complex structures consisting of numerous axis types at different hierarchical levels.

15.2.3 BRANCHING During development branches occur that have the potential to subsequently produce all the subsidiary axes that make up the architectural unit for that species. This process is reiteration. Bell

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and Tomlinson (1980) and Hallé (1999) distinguish between reiteration and sequential branching, which is branching that produces the subsidiary axes. The concept of architectural unit allows recognition of where and when reiteration occurs and allows a distinction to be made between growth and branching within (and producing) the architectural unit, i.e., sequential branching, and branching that repeats the architectural unit, i.e., reiteration. Specifically, reiteration involves redevelopment of the principal axis, axis-type 1 (Bell, 1994). The term reiteration is used in two senses: as a part of normal development, and as part of the response of the plant to damage or injury. The latter, partial or traumatic reiteration, is a response to damage to a component of the architectural unit (e.g., a secondary or tertiary branch). It is repaired by regrowth of only a single component. Reiteration can be monopodial or sympodial. Both types reproduce the developmental sequence from juvenile to mature. Monopodial reiteration involves the dedifferentiation of the apical meristem, which reverts to the production of “juvenile” tissue (e.g., repeating the heteroblastic series of axis development). The result in this case is a continuous axis with the heteroblastic series repeated in tandem. In contrast, sympodial reiteration develops from dormant lateral buds to reproduce the architectural unit as a lateral branch.

15.3 MOSSES Mosses are amenable to architectural analysis. They are built up through a series of repeated, connected growth units. In the same way that a “branch” of a tracheophyte can be monopodial or sympodial, so too a moss “shoot” can have different developmental constructions and be either a monopodium or a sympodium. Mosses also exhibit leaf and shoot heteroblasty, facilitating the recognition of both branch type and hierarchical level. As there is no secondary growth to obscure the pattern of growth, in many cases the developmental history is fixed in the morphology and is readily analysed. Mosses produce a range of recognizable growth patterns or formats (“models,” Bell and Newton, Chapter 3). While they lack a trunk, part of the (tree-based) architectural model, it is likely that they produce variations of the known models as do lianes (Bell, 1991) and herbaceous plants (Jeannoda-Robinson, 1977; Bell, 1991). The concepts of monopodial versus sympodial growth and branching, and reiteration have been used in the description of moss growth and branching pattern. Following Meusel’s (1935) pioneering analyses, descriptions of moss growth and branching took place mainly in an adaptive context — growth forms were considered to be plastic with respect to the environment — rather than in a strictly morphological one (Tangney, 1998), and a more explicit architectural approach has developed only in the past two decades. De Luna (1990) discussed branching pattern in terms of modularity and Mishler and De Luna (1991) outlined a framework for ontogenetic description of mosses, providing a basis for analysis of branching architecture. Their framework based on that used for vascular plants identified architectural scale for mosses. They equated moss merophytes with vascular metamers, and bryophyte modules with vascular shoot units. The bryophyte primary module therefore is the bryophyte principal axis, axis-type 1 (Bell, 1994), the basis of the architectural unit. Reiteration in mosses is here defined as branching that reproduces the primary module and with it the potential to produce all subsidiary axes at other hierarchical levels. La Farge-England (1996) provided a detailed overview of growth form, branching pattern and perichaetial position in mosses. She also provided definitions of sympodial and monopodial branching patterns, indicating that these processes occurred at different hierarchical levels. Despite these advances problems continue with the application of these concepts, specifically that monopodial and sympodial branching as defined occur at different hierarchical levels (meaning that they are different processes), and that two aspects of these processes are being combined: extension growth and branching. The following discussion seeks to provide clarification of the differences between monopodial and sympodial branching.

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De Luna (1990) utilized the concept of module in describing the architecture of Hedwigia ciliata with respect to monopodial and sympodial branching and pleurocarpy and acrocarpy, respectively. He described the branching pattern of H. ciliata as sympodial; the primary modules are terminated by perichaetia and continued by a subapical lateral innovation. The shoot of H. ciliata is therefore a sympodium, a series of connected modules. The capsules are displaced to a lateral position by extension growth of the lateral innovation, producing a “pseudo-pleurocarpous” growth form in an acrocarpous moss. La Farge–England (1996) described two types of branching. She defined the terms sympodial and monopodial in terms of branching pattern; sympodial branching as “a chain of connected modules of the same level of hierarchy” (La Farge-England, 1996: 172), and monopodial branching as “a module with … subsidiary modules (lateral branches) of a different level of the branch hierarchy” (La Farge-England, 1996: 172). Here there is a clear difference in definitions between sympodial and monopodial branching. Monopodial branching produces determinate lateral branches, branches of a lower hierarchy, and sympodial branching produces branches of the same hierarchy. The type of branching is defined by the potential of the branch but the type of growth is also included, so that two separate aspects of the process are being combined. One relates to branching, in particular the position and potential of branches, and the other relates to growth, the nature of the extension growth of the shoot, whether the shoot produced is a monopodium or a sympodium. However, monopodial and sympodial growth can be defined without reference to lateral branching, as both a monopodium and a sympodium may or may not have lateral branches. In this sense monopodial branching is lateral branching on a monopodium and sympodial branching is branching that produces a sympodium. By producing determinate or indeterminate branches at the level of primary module sympodial branching is reiterative. It is full reiteration rather than partial reiteration. The new primary module produced in this way has the potential to produce all the subsidiary branches and structures of lower hierarchical levels characteristic of the species (i.e., the components of the architectural unit). Sympodial branching then produces new architectural units. Less commonly sympodial branching may also produce shoots at other hierarchical levels, but the most important level for moss structure is that of the primary module. In contrast, monopodial branching (as defined by La Farge-England, 1996) occurs within the architectural unit. By producing branches of a different hierarchy, monopodial branching assembles the components of the architectural unit, the secondary and tertiary modules and reproductive structures that are produced by that species. Recognition of the architectural unit is therefore helpful in drawing a distinction between sympodial and monopodial branching. Recognition of module types (or growth units) and their hierarchical position within the architectural unit defines the taxonspecific architectural unit. However, lateral branching on a monopodium (monopodial branching in a broader sense) can also produce branches at the same level of hierarchy as the parent axis. For example new innovation shoots can be produced as lateral branches on a monopodium. These new primary modules develop new architectural units. This view extends the definition of monopodial branching to cover the production of lateral branches of the same level of hierarchy as the parent axis, i.e., new primary modules borne on a primary module that is, or is part of (see monopodial reiteration), a monopodium.

15.3.1 THE LEMBOPHYLLACEAE Camptochaete arbuscula (Figure 15.3A) has an architectural unit made up of: a primary module, consisting of a stolon, stipe and frond axis; secondary modules, determinate lateral branches of the frond axis, the frond axis and the lateral branches together making up the frond; tertiary modules, determinate lateral branches of the secondary modules; perigonia and perichaetia (lateral on secondary fertile axes on the frond axis); and flagelliferous frond axis tips which become

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FIGURE 15.3 Architecture of the Lembophyllaceae: architectural unit and reiteration. (A) Camptochaete arbuscula; (B) Weymouthia (i) W. cochlearifolia, (ii) W. mollis; (C) Isothecium alopecuroides, showing linear development of the architectural unit, and change from monopodial growth to sympodial growth and reiteration, including laterally produced reiteration shoots, after Meusel (1935). Architectural unit (a.u.), sympodial reiteration (SR), monopodial reiteration (MR), reiteration complex (RC). Phases of increasing developmental level numbered.

geotropic and rhizoidal. There are four distinct phases of growth in the primary module: stolon, stipe, frond axis and flagelliferous tips. Lateral branches that will produce new primary modules initially exhibit stoloniferous morphology, contrasting with the secondary modules which are determinate lateral branches. Stoloniferous morphology has erect imbricate leaves which closely clothe the stem, whereas secondary modules have largely spreading leaves, which give them a typically leafy appearance. These morphological differences make recognition of primary and secondary modules straightforward. Reiteration of the architectural unit occurs by new primary modules being produced as branches of the stolon, as basal branches of the stipe, or as lateral branches of the frond axis. Reiteration in these ways is sympodial, producing a series of connected determinate primary modules. Reiteration may also be monopodial, through new stolons being produced as direct extensions or continued growth of the frond axis. The frond axis tips become flagelliferous, the production

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of lateral branches ceases, and a stoloniferous morphology develops. The flagelliferous shoot becomes geotropic and rhizoidal where it contacts the substrate, producing a new stolon. This stolon may then become erect to produce a new stipe and frond axis. An arching and rooting form is then produced (Tangney, 1997, 1998). This is reiteration by dedifferentiation of the terminal apical cell of the frond axis, reproducing an earlier phase in the development of the primary module. The result is a series of connected primary modules, each comprising a stolon, stipe, frond and flagelliferous shoot, producing a succession of architectural units along a continuous axis by monopodial reiteration. An important variation of this pattern of sympodial dendroid-stipitate growth is the production of elongate creeping or pendant forms. In these forms the distinction between stolon, stipe and frond is not clear and the orderly production of new primary modules breaks down. The result is an unsettled morphology with a mix of stolon, stipe and frond characteristics. These are called reiteration complexes, emphasizing that it is occurring at the point of reiteration, the point of production of a new architectural unit (Tangney, 1998). In the genus Weymouthia, two variations of this basic architectural pattern occur (Tangney, 1998). In Weymouthia cochlearifolia (Figure 15.3B) the architectural unit consists of a primary module that exhibits stolon, stipe and frond characters as in Camptochaete. The frond is rather weakly developed, with lateral branches only occasionally produced. Reiteration occurs as basal innovations of the stipe and as flagelliferous geotropic frond axis tips. Usually, however, W. cochlearifolia produces extensive elongate monopodial forms of creeping stems with erect lateral branches. These forms also become pendant. Determinate lateral branches predominate but new primary modules are also produced in this way. The morphology of this creeping stem alternates between stoloniferous characters and characters typical of the frond axis with prominent leaves. Through dedifferentiation of the terminal apical cell, typical frond axis growth is replaced by stoloniferous morphology, an earlier phase of development. This axis, exhibiting monopodial growth, is constructed of a series of connected primary modules which is an example of monopodial reiteration. In the truly pendant Weymouthia mollis (Figure 15.3B), the architectural unit consists of a primary module with somewhat distant determinate lateral branches. Reiteration is by distal lateral innovation. There is no stipe development, but there is leaf differentiation between the main axis (primary module) and the lateral branches (secondary modules). Primary module leaves are erect-imbricate and longer and narrower than the erect spreading leaves of the secondary modules. There is no variation in leaf morphology and orientation along the primary module to suggest a series of primary modules connected by monopodial reiteration.

15.3.2 FURTHER EXAMPLES Argent (1973) described four axis types for the Pterobryaceae: (1) stolons, (2) stems, (3) branches, and (4) flagellae, and distinguished them morphologically. The description of these axis types and the reproductive structures that occur on them constitutes the architectural unit when specifically applied. Argent used these architectural components to distinguish between the Pterobryaceae (axis types 1 to 3 and sometimes type 4), and the Meteoriaceae (axis types 2 and 3, but not 1). According to Argent, the Meteoriaceae have flagelliferous shoots, type 4, but in the Meteoriaceae they are similar to stems type 3. This reduction in components of the architectural unit associated with the largely pendant Meteoriaceae parallels differences between the pendant Weymouthia mollis and related stipitate forms in the Lembophyllaceae. Meusel (1935) has drawn attention to developmental variation in the nature of growth and reiteration. His figures distinctly show predominately monopodial growth in the initial stages of growth and sympodial growth in the later stages of growth in species such as Eurhynchium striatum, Isothecium alopecuroides and Thamnobryum alopecurum. By illustrating long continuous shoots

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he shows that early developmental stages are characterized by monopodial growth of a creeping axis with determinate lateral branches (Figure 15.3C). Intermediate stages have a mixture of (increasingly larger) determinate lateral branches and lateral substipitate innovation shoots. Later stages of development have sympodial growth, with the creeping shoot becoming erect and stipitatefrondose and basal innovations producing new creeping stem and erect axes, the pattern of reiteration typical of the species. This suggests that monopodial and sympodial growth and branching are considered by Meusel to be different development phases in these species. Meusel also indicates distinct periodicity along the horizontal axes, suggesting that during development the periodicity produces a series of connected primary modules expressing increasing levels of developmental potential along a continuous axis.

15.4 SUMMARY AND CONCLUSIONS In considering branching patterns in mosses it is important to distinguish between two components: growth and branching. Growth is the way in which extension or directional growth occurs (i.e., how the axis is constructed). Branching relates to the potential of the branch and its position with respect to the main axis. Reiteration is the mode of repetition and focuses on the hierarchical relations of the repeated units. Growth can be monopodial or sympodial. Monopodial growth produces a single axis, a monopodium, the product of a single terminal apical cell. Sympodial growth produces a sympodium, a series of connected units, in which each is the product of a different terminal apical cell. In a sympodium extension growth is continued by the activity of the terminal apical cells of subsequent units. There are two types of branching in mosses: sequential branching, which refers to branching within the architectural unit (i.e., that which makes up the architectural unit), and reiteration, which refers to branching that repeats the architectural unit. The architectural unit is the structural unit that includes all the axis types from juvenile to mature stages of development, that are characteristic of a particular taxon. The architectural unit is therefore an important concept in analysing growth and determining the nature of branching and the hierarchical level at which it is taking place. The utility of the architectural unit is that it requires an explicit recognition of axis types, necessitating a distinction to be made between branching within the architectural unit and reiteration. Branching may be monopodial or sympodial. Monopodial branching (sensu La Farge-England, 1996) produces determinate lateral branches of a lower hierarchical order. Lateral branching from a monopodium may also produce innovation shoots, axes of the same hierarchical order as the parent axis. This can also be referred to as monopodial branching. Sympodial branching produces determinate or indeterminate lateral branches of the same hierarchical order, producing a series of connected modules of the same hierarchical order. Reiteration is typically sympodial, and also may be monopodial. Reiteration may be full or partial. Full reiteration reproduces the basic repeated units of construction of mosses, including all the axis types produced by any particular species, as well as any other structures (perigonia, perichaetia, etc.). In mosses this means reproduction of the primary module. The plants are made up of a series of connected primary modules and all the structures that are borne on them. Reiteration may be sympodial or monopodial. Sympodial reiteration produces a series of connected primary modules due to the activity of a series of different terminal apical cells. It is the combination of complementary activities of sympodial growth and sympodial branching. Monopodial reiteration produces a series of connected primary modules along a continuous axis that is the product of a single apical cell. Such activity is recognized by the presence of repeated heteroblastic leaf series along a continuous axis, or by the presence of repeated phases of growth (e.g., stolen–stipe–frond–flagelliferous tip) along a continuous axis. Monopodial reiteration occurs

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by the dedifferentiation of the terminal apical cell, which “reverts” to an earlier phase of development within the primary module and then repeats the pattern. Partial reiteration occurs within the same hierarchical level, for example, a secondary or tertiary module, and repair of that component only. Sympodial growth of other structures within the architectural unit is not strictly reiterative.

REFERENCES Argent, G. C. G. (1973) A taxonomic study of African Pterobryaceae and Meteoriaceae. I. Pterobryaceae. Journal of Bryology, 7: 353–378. Bell, A. D. (1991) Plant Form: An Illustrated Guide to Flowering Plant Morphology. Oxford University Press, Oxford. Bell, A. D. and Tomlinson, P. B. (1980) Adaptive architecture in rhizomatous plants. Botanical Journal of the Linnean Society, 80: 125–160. Bell, A. D. (1994) A summary of the branching process in plants. In Shape and Form in Plants and Fungi (eds. D. S. Ingram and A. Hudson). Linnean Society of London, Academic press, London, pp. 119–142. Buck, W. R. (1998) Pleurocarpous Mosses of the West Indies. New York Botanical Garden, New York. Buck, W. R., and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on TRNL-TRNF and RPS4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. De Luna, E. (1990) Developmental evidence of acrocarpy in Hedwigia ciliata (Musci: Hedwigiaceae). Tropical Bryology, 2: 53–60. De Luna, E., Newton, A. E., Withey, A., Gonzales, D. and Mishler, B. D. (1999) The transition to pleurocarpy: A phylogenetic analysis of the main diplolepidous lineages based on rbcL sequences and morphology. Bryologist, 102: 634–650. During, H. J. (1979) Life strategies of bryophytes: a preliminary review. Lindbergia, 5: 2–18. Gimingham, C. H. and Robertson, E. T. (1950) Preliminary investigations on the structure of bryophyte communities. Journal of Bryology, 1(3): 330–344. Hallé, F., Oldeman, R. A. A. and Tomlinson P. B. (1978) Tropical Trees and Forests: An Architectural Analysis. Springer Verlag, New York. Hallé, F. (1999) Ecology of reiteration in tropical trees. In The Evolution of Plant Architecture (eds. M. H. Kurmann and A. R. Hemsley). Royal Botanic Gardens, Kew, pp. 93–107. Jeannoda-Robinson, V. (1977) Contribution a l’étude de l’architecture des herbes. Thèse Docteur de Specialité de Sciences Biologique. Université des Sciences et Techniques du Languedoc, Montpellier, France. La Farge-England, C. (1996) Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99 (2): 170–186. La Farge-England, C. (1998) The infrageneric phylogeny, classification, and phytogeography of Leucoloma (Dicranaceae, Bryopsida). The Bryologist, 101(2): 181–220. Magdefrau, K. (1982) Life forms of bryophytes. In Bryophyte Ecology (ed. A. J. E. Smith). Chapman & Hall, London. Meusel, H. (1935) Wuchsformen und Wuchstypen der europaischen Laubmoose. Nova Acta Leopoldina (Neue Folge), 3(12): 219–277. Mishler, B. D. (1986) Ontogeny and phylogeny in Tortula (Musci: Pottiaceae). Systematic Botany, 11: 121–167. Mishler, B. D. (1988) Relationships between ontogeny and phylogeny, with reference to bryophytes. In Ontogeny and Systematics (ed. C. J. Humphries). Columbia University Press, New York. Mishler B. D. and De Luna, E. (1991) The use of ontogenetic data in phylogenetic analyses of mosses. Advances in Bryology, 4: 121–167. Newton, A. E. and De Luna E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Richards, P. (1984) The ecology of tropical forest bryophytes. In The New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 1233–1270.

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Rohrer, J. R. (1985) A phenetic and phylogenetic analysis of the Hylocomiaceae and Rhytidiaceae. Journal of the Hattori Botanical Laboratory, 59: 185–240. Tangney, R. S. (1997) A taxonomic revision of the genus Camptochaete Reichdt., Lembophyllaceae (Musci). Journal of the Hattori Botanical Laboratory, 81: 53–121. Tangney, R. S. (1998) The architecture of the Lembophyllaceae (Musci). Journal of the Hattori Botanical Laboratory, 84: 37–47.

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Pleurocarpous 16 Did Mosses Originate before the Cretaceous? Michael S. Ignatov and Dmitry E. Shcherbakov CONTENTS Abstract ..........................................................................................................................................321 16.1 Introduction...........................................................................................................................321 16.2 Palaeozoic Fossils.................................................................................................................322 16.2.1 Uskatia conferta Neub..............................................................................................322 16.2.2 Polyssaievia Neub. and Bajdaievia Neub. ...............................................................323 16.2.3 Rhizinigerites neuburgiae S. V. Meyen....................................................................324 16.2.4 Merceria augustica Smoot & T.N. Taylor ...............................................................324 16.3 Mesozoic Fossils ..................................................................................................................324 16.3.1 Muscites guesceliniae Townrow...............................................................................325 16.3.2 Tricostium papillosum Krassilov..............................................................................325 16.3.3 Muscites fontinaloides Krassilov .............................................................................326 16.3.4 Bryokhutuliinia jurassica Ignatov ............................................................................326 16.3.5 Palaeodichelyma sinitzae Ignatov & Shcherbakov..................................................327 16.3.5.1 Characteristics of Locality ........................................................................327 16.3.5.2 Characteristics of the Collection...............................................................327 16.3.5.3 Holotype ....................................................................................................330 16.3.5.4 Etymology .................................................................................................330 16.3.5.5 Differentiation ...........................................................................................334 Acknowledgments ..........................................................................................................................334 References ......................................................................................................................................334

ABSTRACT Selected Palaeozoic and Mesozoic mosses are discussed, focusing on their possible relationships to pleurocarpous groups. Among them, Palaeozoic, Triassic and some Jurassic fossils are similar to pleurocarps in some respects, but some other peculiarities of these mosses make their immediate placement into extant groups difficult. One new genus and species, Palaeodichelyma sinitzae, is described from the Upper Jurassic of Transbaikalia. This fossil moss is probably the most similar to pleurocarps among the pre-Cenozoic fossils.

16.1 INTRODUCTION Pleurocarpous mosses were recognized by Bridel (1819) as one of two major groups of Bryopsida, characterized by mostly creeping growth and lateral position of sporophytes (more precisely, 321

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sporophytes are terminal on short lateral branches, thus looking lateral), which can be quite numerous on one plant. In contrast to pleurocarps, acrocarpous mosses are characterized mostly by upright growth, a clearly terminal sporophyte, which is usually solitary, or more rarely several, two to three (up to seven). Pleurocarpous mosses are a young, rapidly diversified monophyletic group, classified now into three orders: Ptychomniales, Hookeriales and Hypnales (Shaw et al., 2003; Goffinet and Buck, 2004). Though structurally and taxonomically less diverse than acrocarps (which include approximately 20 orders), pleurocarps include about a half of extant species, and by biomass in the planet they obviously much exceed the rest of the mosses (excluding Sphagnum). The earliest occurrence where a quite diverse pleurocarpous moss flora is known is in the Baltic amber of Eocene age, overviewed recently by Frahm (2000). Frahm listed, among others, Barbella sp., Brotherella sp., Ephemeropsis sp., Fabronia cf. ciliaris, Fabronia sp., Haplocladium angustifolium, Hypnum sp., Mastopoma sp., Merillobryum cf. fabronioides, Rhytidiadelphus squarrosus and Symphyodon sp. Besides these taxa, he listed 20 other species from acrocarpous groups. The proportion of pleurocarps to acrocarps is therefore about 1:2, i.e., fairly similar to that in many recent floras. This similarity and also the fact that many specimens from amber can be referred to contemporary genera and even to some contemporary species, suggest that pleurocarpous mosses evolved no later than the Cretaceous. The undoubted pleurocarps, however, are almost absent or at least extremely rare in earlier deposits. This fact, along with the other evidence, leads to the tentative conclusion (e.g., Buck, 1991), that the evolution of pleurocarps followed the habitat diversification of the angiosperms, i.e., occurred in the Cretaceous. At the same time, an analysis of fossil data lead Krassilov and Schuster (1984) to the conclusion that the pleurocarpous mosses appeared no earlier than the Jurassic. In this chapter we present an overview of those Palaeozoic and Mesozoic mosses that can be linked to pleurocarps, and also discuss in detail one species found in Upper Jurassic deposits of Transbaikalia, South Siberia by the second author and his colleagues. It is important to note that the main diagnostic characters of pleurocarps (gametangia position, sporophyte structure, presence of leaf-like structures around branch primordia and dormant buds, etc.) are usually not available in fossil collections. Thus, we have no other way than to be satisfied with the less taxonomically important characters, such as pattern of laminal cell areolation, density of foliage, presence/absence of costa and branching pattern.

16.2 PALAEOZOIC FOSSILS Pre-Permian plants referred to mosses (Renauld and Zeiller, 1885, 1888; Lignier, 1914; Thomas, 1972; Busche, 1968) are not discussed here as their structure is too poorly known. Some Permian mosses have clear acrocarp-like morphology; for example most of those described by Neuburg (1960), Fefilova (1978), and Ignatov (1990), and are not commented upon here. Other Permian mosses that exhibit some similarity to pleurocarps or were once compared with this group are as follow: (1) Uskatia conferta Neub. (Neuburg, 1960); (2) Polyssaievia spinulifolia (Zal.) Neub., P. deflexa Neub. and Bajdaievia linearis Neub. (Neuburg, 1960); (3) Rhizinigerites neuburgiae S. V. Meyen (Gomankov and Meyen, 1987; Ignatov, 1990); (4) Merceria augustica Smoot & T. N. Taylor (Smoot and Taylor, 1986). We provide here a brief summary of species morphology, taking selected characters from descriptions and illustrations. However, in doing this, we are not necessarily agreeing with all the interpretations and terminology of authors in their descriptions, and do not discuss characters not clearly seen in the available illustrations.

16.2.1 USKATIA

CONFERTA

NEUB.

Uskatia conferta Neub., Upper Permian, Kuznetsk Coal Basin (Il’inskoe and Erunakovo Groups), South Siberia (Neuburg, 1960). This species is found as numerous foliated and branching shoots. Cell structure is well represented in different leaf parts, with less clear structure of the leaf base.

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Shoots are no less than 3 cm long, densely foliated, more or less regularly branched (with the distance between branch bases approximately 0.5 cm); branches spreading at about 90°, 1 to 2 cm long, foliage similar to stems, but leaves somewhat smaller. Leaves spreading at about 30 to 45° at base, straight, or sometimes in the middle gently reflexed, up to 70°, 2.6 to 3.8 × 0.7 to 1.3 mm, lanceolate from an ovate base; gradually tapered to the apex, more or less keeled above; margin entire, bordered throughout by one or two rows of elongate thick-walled cells, unistratose; costa ending in or close to apex, 150 μm at base, gradually narrowing above; laminal cells elongatehexagonal or shortly rectangular or rhombic, 35 to 60 (up to 73) × (10 to) 16 to 20 μm; cells arranged at places in longitudinal rows, at other places in oblique rows. The pinnate branching in Uskatia is the main feature of comparison with the pleurocarps — similar patterns in other groups of mosses are known to be rather rare exceptions (Racomitrium and Sphagnum). However, Uskatia probably belongs to a different lineage of mosses, which have leaves attached to the stem only by the costa — a character never found in any contemporary groups. This character itself is not seen in Uskatia conferta due to its dense foliage, but can be observed in Intia sp. (Neuburg, 1960) and Uskatia dentata Fefilova, both from Pechora Coal Basin. The probable close relationship between Uskatia and Intia (and also with Protosphagnum) was discussed by Ignatov (1990). The laminal cells in Uskatia are longer than in Intia, only at some places exhibiting the clear arrangement of cells in oblique rows similar to many Mniaceae taxa and very clearly seen in Intia. Abramov and Savicz-Ljubitskaya (1963) suggested that Intia should be referred to Mniaceae, but Ignatov (1990) considered these numerous similarities to be superficial.

16.2.2 POLYSSAIEVIA NEUB.

AND

BAJDAIEVIA NEUB.

These two genera differ from the rest of the collection described in detail by Neuburg (1960) in having more elongate cells and relatively long, ovate lanceolate leaves. She classified the material, all from the Upper Permian, into two genera and three species: Bajdaievia linearis Neub., Polyssaievia spinulifolia (Zal.) Neub., P. deflexa Neub. (two former from Erunakovo Group, Kuznetsk Coal Basin, South Siberia and P. spinulifolia also from Pelyatka Formation, Tunguska Coal Basin, Central Siberia; P. deflexa from Pechora Group, Pechora Coal Basin, north-east Europe). Polyssaievia spinulifolia is known from numerous foliated shoots, whereas the two other species are described from a few shoots each. We consider these genera and species to be related closely enough to be discussed here together. Shoots are no less than 2 cm long, densely to moderately densely foliate; branches few, 1.0 to 1.3 cm long, branch foliage similar to that of stem. Leaves from wide clasping base rather suddenly reflexed in mid-leaf, thus distally forming (70° to) 80 to 90° (up to 120°) angle with the stem, 3 to 5 mm long and 1.5 to 3 mm wide, lanceolate from a broadly ovate base, gradually tapered to the apex, more or less keeled above; margin entire, bordered throughout by one or two rows of elongate, thick-walled cells, unistratose; costa ending in or close to the apex, approximately 100 μm wide at base, gradually narrowing above; laminal cells elongate or rectangular, 20 to 93 × 10 to 20 μm, forming longitudinal and oblique rows in places with shorter cells; this pattern of oblique rows is not apparent in places with longer cells, which usually compose the distal half of the leaf. Numerous strips, one to three cells wide, of darker, more thick-walled and more elongate cells form a net in the basal part of the leaf, a peculiar pattern called by Neuburg “net venation.” Veins are dichotomously branching and anastomosing, forming irregular loops 4 to 8 cells wide, (6 to) 10 to 15 cells long; upwards the veins become paler, gradually becoming not discernible. It is worth comparing these two genera with pleurocarps, due to their elongate cells in the upper leaf, leaf shape, and presence of branches with limited growth. However, the variation pattern allows both Polyssaievia and Bajdaievia to be linked to Uskatia, as they are similar in many leaf characteristics, including a border throughout the margin and at places the cells are in oblique rows. If their relationship is true, then one may conclude that these two genera also have leaves attached

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to the stem by the costa only. Also, the peculiar “net venation” is unique among mosses, making further comparison with other groups unnecessary.

16.2.3 RHIZINIGERITES

NEUBURGIAE

S. V. MEYEN

Rhizinigerites neuburgiae S. V. Meyen, Upper Permian of North of Russian Platform (Severodvinian and Vyatkian Horizons), north-east European Russia (Gomankov and Meyen, 1987; Ignatov, 1990). About ten foliated shoots and also dispersed leaves were obtained from bulk maceration, and mounted on slides to observe their microstructure. Shoots are no less than 4 cm long, with rhizoids clustered on small protrusions shortly below leaf insertions; loosely foliated, sparsely branched; foliated branches with smaller and more delicate leaves, with lower leaves on branches longer than further above; some secondary axes are totally naked, others with sparse rhizoid clusters similar to those below leaves on stem. Leaves deviating from stem at 30 to 100° (seem quite slender and easily damaged), up to 6 mm long and 2 mm wide, lanceolate, gradually tapered to a shortly acute apex, plane, unbordered, margin irregularly dentate; costa approximately 100 μm at base, reaching 0.9 to 0.95 of leaf length; laminal cells 30 to 40 × 12 to 15 μm, elongate, rhombic, in more or less distinct oblique and longitudinal rows, with some cells missing in many places in the basal parts of the leaves, thus forming a moderately regular net; basal cells not much different from mid-leaf ones; leaf insertion line of at least six times broader than the width of the costa at the base. The general appearance, areolation, lack of leaf border, attachment of leaf not only by the costa, and rhizoids just below the leaf are the features similar to pleurocarps. However, the presence of leafless axes bearing rhizoids, the strange order of leaves on branches, where the lowest leaf is the largest, as well as a reticulate pattern in lower leaf (due to some cells fallen off) are not known in any other group of mosses. This makes further comparison unnecessary.

16.2.4 MERCERIA

AUGUSTICA

SMOOT & T.N. TAYLOR

Merceria augustica Smoot & T.N. Taylor (Smoot and Taylor, 1986), Upper Permian of Antarctica (Buckley Formation). The species was found in numerous transverse sections showing excellently preserved cell structure and a few fragments showing laminal areolation. Stems have rhizoids with characteristic oblique walls. Leaf laminal cells are elongate, on average 87 × 11 μm. Leaves are up to 2.3 mm wide, thus having about 90 rows of cells from each side of the costa. The costa is up to 20 cells wide and 4 to 6 (up to 7) cells thick, in cross section exhibiting certain differentiation in cell size, but without obvious stereids. Some cross sections exhibit strongly incurved margins, similar to the cross section of Polytrichum juniperinum in the upper leaf (incurved portions of the lamina almost totally cover the median part of the lamina from above). The elongate cells and the very numerous cell rows between the costa and leaf margin could be evidence for the pleurocarpous nature of the moss. Though a differentiated costa anatomy is not a characteristic of pleurocarps, certain heterogeneity of cells is known in mosses with robust costae, such as Cratoneuron, Thuidium, Donrichardsia and Platyhypnidium. The strongly incurved margin, however, is too odd for a pleurocarpous moss, and may rather suggest an affinity to the Polytrichaceae. In the latter case elongate cells can be interpreted as basal ones; however, further comparison would be probably too speculative, as we still have no evidence as to which part of the leaf these elongate cells are. Concluding, despite a certain similarity to extant pleurocarpous mosses, all Palaeozoic species possess some features that make their immediate linkage to pleurocarps difficult.

16.3 MESOZOIC FOSSILS Mesozoic records of mosses are surprisingly few. As with the Palaeozoic ones, most of them are either acrocarp-like, or not very well understood due to poor material preservation. One Triassic

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moss from South Africa and four Upper Jurassic mosses from Transbaikalia and/or Mongolia are relevant for the current discussion: (1) Muscites guesceliniae Townrow (Townrow, 1959); (2) Tricostium papillosum Krassilov (Krassilov, 1973); (3) Muscites fontinaloides Krassilov (Krassilov, 1973); (4) Bryokhutuliinia jurassica Ignatov (Ignatov, 1992); and (5) Palaeodichelyma sinitzae, and are described below in more detail.

16.3.1 MUSCITES

GUESCELINIAE

TOWNROW

Muscites guesceliniae Townrow, Triassic of South Africa, Molteno Group (Townrow, 1959). The moss is represented by 15 short fragments of foliated shoots whose preservation allows the cell structure to be seen in some places. Leaves are densely spirally arranged, erect to spreading, approximately 2 mm long, 0.5 mm wide, ovate-lanceolate, costa absent, cells quadrate to shortly rectangular, mostly 35 × 25 μm, thick-walled, rather clearly arranged in longitudinal rows; cells along the leaf median are in few (roughly three) rows, somewhat elongate, up to 50 × 20 μm, but still unistratose; laminal cells have papillose thickenings (observed as darker and thicker structures) in cell corners (usually at the junction of four cells). Townrow (1959) compared this moss with Leucodontaceae and some other groups, such as Fontinaliaceae, Hookeriaceae, Cryphaeaceae and Erpodiaceae, and suggested that the first family is probably the closest, because of the lack of a costa and the presence of papillose projections in the cell corners of some species. However, these latter projections are situated in Leucodontaceae above the upper end of the cell, not in the corners, and short and broad cells throughout the lamina are totally odd for Leucodontaceae. More similarity with the Erpodiaceae can be found, though in this family the costa is either strong or totally lacking, thus never like the rows of little elongated cells along the leaf median line, as in M. guesceliniae. Townrow included in his discussion the Erpodiaceae because this family was traditionally considered as pleurocarpous (Brotherus, 1925), but according to recent studies it belongs to the haplolepidous acrocarps (Goffinet and Buck, 2004; Tsubota et al., 2004). Summarizing, the absence of a costa is probably the only character suggesting a pleurocarpous relationship for M. guesceliniae, but some acrocarpous mosses as well as Andreaea also have ecostate leaves and are in other respects more similar to M. guesceliniae. There is probably no possibility of finding a definite relative among known moss groups.

16.3.2 TRICOSTIUM

PAPILLOSUM

KRASSILOV

Tricostium papillosum Krassilov (Krassilov, 1973). Late Jurassic, Bureya River (Russian Far East), Talynjan Formation. This moss is represented by a few short shoot fragments (up to 3 mm) and a number of isolated leaves obtained from bulk maceration that have excellent microstructure preservation. Leaves are erect, 1.2 mm long, 0.5 mm wide, ovate to narrowly ovate, gradually and rather broadly tapered to the somewhat blunt apex, cordate at the base, more or less serrate distally. The median costa ends quite sharply four to five cells below the apex, thus reaching approximately 0.95 of leaf length, and about 50 μm wide along most of the leaf length; lateral costae are parallel to leaf margins at 5 to 20 cells from them, about twice as narrow as the median costa, reaching 0.5 to 0.9 of the leaf length, end as sharply as the median costa; cells hexagonal to hexagonalrectangular, in longitudinal rows, 15 to 18 μm wide, isodiametric to slightly elongate with length to width ratio 1–2:1, with 8 to 10 papillae above the lumina (seen as fine granulose roughness); basal cells not differentiated from those in the mid-leaf. A triple costa is a unique structure among mosses. Though many extant mosses have a bior oligostratose border, it is usually marginal or at least submarginal, separated by just one or two cells from the margin. The pluripapillose isodiametric cells suggest an affinity with the Pottiaceae, where a serrate margin, though rare, is sometimes present; for example, in Leptodontium, which however usually has larger leaves. Note that the bulk maceration method favors the recovery of smaller specimens. Larger fragments, even if they existed and were present in treated

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rocks, could be easily broken during maceration when carbonated material is solving in nitric and chloric acids. The submarginal costae and size of the leaves are also reminiscent of Thamnobryum negrosense (E. B. Bartr.) Z. Iwats. B. C. Tan (Ochyra, 1990), whose leaves have bistratose marginal to submarginal borders. The leaves are also similar in shape, size, marginal serration and areolation in most of the lamina to those of Tricostium. Their differences include smooth laminal cells and, more importantly, elongate cells at the base. The latter is the common case in most extant groups with short cells in their mid-leaf. If this character is of primary importance, then Tricostium has to be compared with Trachycystis-like Mniaceae and also the other representatives of Rhizogoniales as defined by Goffinet and Buck (2004). Note that, according to Frahm (2000), three species from Baltic amber belong to Trachycystis. However, in the extant Mniaceae cells are invariably smooth and the costa is single.

16.3.3 MUSCITES

FONTINALOIDES

KRASSILOV

Muscites fontinaloides Krassilov (Krassilov, 1973), Late Jurassic, Bureya River (Russian Far East), Talynjan Formation. This moss is represented by eight short shoot fragments, up to 2.5 mm long. Leaves on the shoots are mostly broken in the upper part, but in shape and size more or less agree with the single illustrated complete leaf, which is 0.7 mm long and 0.4 mm wide (according to Krassilov’s description the leaves are 0.6 to 0.8 mm long), carinate, ovate, acuminate, slightly constricted at the base; margin entire, unbordered; costa absent; cells approximately 30 × 11 μm. One specimen is a dark elliptic structure 1.15 × 0.6 mm, tapered distally at 60° (i.e., similar to the conic operculum of many mosses), surrounded at the base by leaves (one is approximately 1 mm long); among leaves a slightly curved “seta” approximately 0.4 mm long and 0.2 mm wide is seen. This elliptic structure was interpreted by Krassilov as a capsule, and there is no disagreement with this in its overall appearance, though the size of such an operculate capsule is almost at the lower possible size limit in mosses. Similarly, the leaves of this species are among the smallest in mosses. Thus, the affinity with Fontinalis (one of the largest living mosses) seems to us unlikely. There is not enough evidence, however, to present a well-based alternative: similarly small capsules are known in ephemeral acrocarps (Pseudephemerum, Microbryum, Ephemerum), as well as among the pleurocarps in families such as Daltoniaceae, Fabroniaceae and others. Further comparisons seem unnecessary because although the outline of capsule suggest its rather mature state, this cannot be substantiated.

16.3.4 BRYOKHUTULIINIA

JURASSICA IGNATOV

Bryokhutuliinia jurassica Ignatov (Ignatov, 1992), Upper Jurassic (or Lowermost Cretaceous; Ponomarenko, 2003), Southern Gobi, Mongolia, Ulugey Formation. This moss is represented by several imprints, with few of them permitting us to see the areolation pattern. The stem is more than 5 mm long, loosely foliated, and very sparsely branched. Leaves are up to 4.0 × 0.8 mm, lanceolate, bordered (structure of the border unknown), ecostate; laminal cells are 100 to 150 ×20 to 30 μm, arranged in longitudinal rows with transverse cell walls approximately perpendicular to the leaf length. The combination of characters does not allow an interpretation of the systematic position, but the areolation pattern might suggest a hookerialean affinity. However while Bryokhutuliinia is quite evidently aquatic (Ignatov, 1992), this group has no living aquatic representatives. This genus was rather widespread; collections of Srebrodolskaya (1980) from Transbaikalia of about the same age have moss remains (though without preserved cell structure) referred to another species of Bryokhutuliinia (Ignatov, 1992).

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16.3.5 PALAEODICHELYMA

SINITZAE IGNATOV

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& SHCHERBAKOV

Palaeodichelyma sinitzae Ignatov & Shcherbakov, genus et species nov.; Plates 16.1 to 16.5. Late Jurassic, Transbaikalia in South Siberia. Type species: Palaeodichelyma sinitzae Ignatov & Shcherbakov. 16.3.5.1 Characteristics of Locality This moss was found in two localities: (1) Daya, Chita Province, Shelopugino District, left bank of Daya River upstream of Shiviya River mouth (51° 50N and 117° 28E); Upper Jurassic (?Lower Cretaceous), Glushkovo Formation; collected in 2002 by Shcherbakov et al.; PIN no. 5092/1-19; (2) Unda, Chita Province, Baley District, right bank of Unda River upstream of the village of Zhidka (51° 46N and 117° 17E); Upper Jurassic (?Lower Cretaceous), Glushkovo Formation; collected in 2002 by Shcherbakov et al.; PIN no. 5093/1. The Unda and Daya localities belong to the Glushkovo Formation. Fossil remains are rich in insects and other freshwater invertebrates: various crustaceans, namely abundant Prolepidurus (Notostraca), Chirocephalus (Anostraca; Daya only), Palaeolynceus and other genera (Conchostraca), and ostracodes, along with bivalves. The rich insect assemblage (13 orders) is dominated by lower Diptera (midges and craneflies). Plant megafossils are rare (e.g., conifer seeds and needles), except for horsetail shoots and the mosses described here. The palynocomplex rich in Classopollis (Bashurova, 2001), the ostracodes and several insect groups all indicate a Late Jurassic age. The Glushkovo Formation in South Siberia was dated Late Jurassic by Sinitza and Starukhina (1986), Kovalev (1990: 127–131) and some others, but late Early Cretaceous by Zherikhin (1978), and now seems most probable to be terminal Jurassic, or, maybe, basal Cretaceous (Rasnitsyn and Quicke, 2002). These finely laminated tuffaceous mudstones (exposed in a number of outcrops in Baley and Shelopugino Districts, Chita Region, Transbaikalia) probably accumulated in rather large cold mountain lakes situated in a volcanic region. Similar and possibly roughly synchronous faunal assemblages occur in other areas within East Transbaikalia. The Ulugey Formation in Mongolia, from where Bryokhutuliinia jurassica was described (Ignatov, 1992), probably represents the same type of environment (A.G. Ponomarenko, personal communication). 16.3.5.2 Characteristics of the Collection The collection consists of 20 imprints (8 have counterparts) of leafy shoots (numbered), and on the surface of the rock there are also six less-preserved shoots (unnumbered) and dispersed leaf fragments. Plant material is attached to the rock surface and well preserved, allowing us to see the areolation and to measure cell width at least in a few places per specimen; fewer specimens are preserved well enough to show clear cell outlines and allow us to measure cell length. The density of leaf arrangement along the stem and leaf shape varies much, but the range of variations is quite similar to that observed in many extant subaquatic mosses, for example, Drepanocladus aduncus (Hedw.) Warnst. or Warnstorfia fluitans (Hedw.) Loeske. More densely foliated shoots (Plate 16.1A, F; Plate 16.2A, D) usually have narrower leaves, deviating from the stem at a narrower angle, whereas shoots with remotely arranged leaves (Plate 16.3A and Plate 16.1B “7”) are characterized by broader erecto-patent to patent leaves with a more lax areolation. Because there are specimens in which transitional characteristics can be seen, all the available material from these localities is interpreted as a single species. The longest shoot is 30 mm long (Plate 16.1E), and five others are longer than 20 mm. Branching is very poor: # 5093/1 has two branches, close to each other at about 15 mm from the stem apex (Plate 16.2A to C); another shoot (Plate 16.2E) has two branches arranged suboppositely on an otherwise simple axis, at no less than 10 mm from the stem end. The specimen in Plate 16.2D has the zone with more dense leaf arrangement, and above it two shoots are visible. Details of the branch base are not seen among the leaves, but the general appearance of these parts in

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PLATE 16.1 Palaeodichelyma sinitzae Ignatov & Shcherbakov, from Daya. (A), (B), 5092/7, 8 and 9; (C), (D) 5092/8; (E), (F) 5092/5; (G) 5092/6; (H) 5092/7). Habit, showing variation.

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PLATE 16.2 Palaeodichelyma sinitzae Ignatov & Shcherbakov, from Unda: (A) to (C) 5093/1); and Daya: (D) 5092/17, (E) and (F) 5092/14). Fragments of branched shoots.

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three specimens shows no difference from what is usually seen in extant pleurocarps. Leaf outlines are visible, although the extreme apex is rarely seen clearly enough to identify the exact end of the costa; also, the margins are rather obscure and it is difficult to observe if they are always entire or sometimes serrulate. The mode of attachment of the leaves is clearly visible in relatively few places, and there is no one clear view showing attachment other than only by the costa. However, at the same time there are some places in different specimens where attachment involving parts of the base other than the costa is suggested (Plate 16.1G; Plate 16.4B to E; and Plate 16.5G). One quite remotely foliated shoot (Plates 16.3A to D) has in its middle part two structures which we interpret as perichaetia, by their characteristic position, shape, size, and to a less extent the microstructure, which is poorly preserved in overlapping leaves. Stem surface cells can be traced by the outlines of strongly coalified material (Plates 16.3F and 16.4D). Some stem fragments have strongly ribbed stem surfaces, but we are uncertain if this is an artifact, because this pattern is seen only at places, or whether it is evidence for the presence of a hyalodermis. After the decomposition of thin outer cell walls in species with a hyalodermis, the periclinal cell walls, which are usually much thicker than outer cell walls and do not decompose as easily, may form a similar ribbed pattern. The stem is up to 30 mm long, 0.13 to 0.35 mm wide; surface cells 40 to 90 × 12 to 20 μm; paraphyllia absent. Branching is very remote, branches solitary or subopposite, up to 20 mm long, deviating from the stem at 5 to 30° angle, simple, differing from the stem in smaller leaves. Shoots are densely to loosely foliate along the stem, being variable in leaf density among separate individuals; within the individual shoot leaf arrangement rather even, though at places leaves are larger and thus the leaf arrangement looks somewhat denser. Leaves are polystichous (or tristichous?), erect to patent (deviating from the stem at 20 to 45° (up to 110°), if erect then often gently reflexing in the middle to the wider angle; (1.7 to) 2.5 to 3.5 (up to 4.2) mm long, (0.7to) 0.8 to 1.5 mm wide, ovate-lanceolate to lanceolate, gradually acuminate, in the upper part distinctly keeled to almost plane, rounded to narrow insertion; margin entire; costa reaching almost to the apex, 50 μm in widest part of the leaf base; mid-leaf cells 35 to 80 (up to 110) μm long, 8 to 10 (up to 12) μm wide, elongate to narrowly rectangular, thus mostly with cell walls perpendicular to leaf length, more rarely oblique, usually in clear longitudinal rows; marginal cells undifferentiated; cells wider towards base and across the whole base or only close to leaf corners, or in narrower leaves little differentiated; basal cells up to 40–55 × 17–22 (up to 30) μm. Perichaetia on stems, sitting at 60 to 70° with stem, 0.7 mm long, formed by three to four leaves up to approximately 0.7 mm long, 0.2 to 0.3 mm wide, lanceolate, shortly acuminate, at least some of them with indistinct costa; laminal areolation rather lax, cells approximately 30 × 10 μm. 16.3.5.3 Holotype Russia, Transbaikalia, Chita Province, Shelopugino District, left bank of Daya River upstream of Shiviya River mouth (51° 50N and 117° 28E); Upper Jurassic (?Lower Cretaceous), Glushkovo Formation; collected in 2002 by Shcherbakov et al.; PIN no. 5092/1a and 1b. Paratypes: same locality, PIN no. 5092/2-19; also Russia, Transbaikalia, Chita Province, Baley District, right bank of Unda River upstream of the village of Zhidka (51° 46N and 117° 17E); Upper Jurassic (?Lower Cretaceous), Glushkovo Formation; collected in 2002 by Shcherbakov et al.; PIN no. 5093/1 (kept in the Paleontological Institute (PIN) of the Russian Academy of Sciences). 16.3.5.4 Etymology The generic name reflects the superficial similarity to Dichelyma (Fontinalaceae, Hypnales). The specific epithet is in honour of Sofia Sinitza, a paleontologist who did much for the exploration of the fossil flora and fauna of Transbaikalia.

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PLATE 16.3 Palaeodichelyma sinitzae Ignatov & Shcherbakov, from Daya (all from 5092/1a, holotype, except (B), which is counterpart, 5092/1b). (A) Leafy shoot with putative perichaetia; (B) stem fragment with leaf base and putative perichaetium; (C) perichaetia; (D) part of leafy shoot; (E) leaf base; (F) stem surface; (G) cells of leaf base.

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PLATE 16.4 Palaeodichelyma sinitzae Ignatov & Shcherbakov, from Daya: (A) to (C) 5092/17; (D) 5092/6; (E) 5092/7; (F) to (J) 5092/2). Leaves, showing variations.

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PLATE 16.5 Palaeodichelyma sinitzae Ignatov & Shcherbakov, from Daya: (A) 5092/5; (B) to (F) 5092/17; (G) 5092/15; (H) and (I) 5092/17; (J) to (L) 5092/7). Cells of upper to median (A to F) and basal (G to L) portions of leaves. All scale bars are 100 μm.

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16.3.5.5 Differentiation By its general appearance, branching, elongate laminal cells, and lateral perichaetia, Palaeodichelyma is very similar to extant representatives of some aquatic pleurocarps, especially Amblystegiaceae and Dichelyma (Fontinalaceae). Branching pattern, costa up to about the apex, and keeled leaves, sometimes showing a tristichous aspect (Plates 16.1A and B) resemble those of extant species of Dichelyma. The important difference from most extant pleurocarps is in the shape of the laminal cells, which when elongate usually have oblique cell walls at their upper and lower ends, whereas in Palaeodichelyma these walls are mostly perpendicular to the leaf length, thus allowing longitudinal rows of cells to be traced. The latter pattern is never so obvious in extant Hypnales, though at places it can be found, for example in Hylocomiaceae, Pseudoleskeaceae and Fontinalaceae (especially Fontinalis itself). More frequently clear longitudinal rows and transverse cell walls can be seen in plants in the orders Hookeriales and Ptychomniales (Hookeriopsis, Daltonia), but both orders are represented in modern flora only by 200 species (compared with approximately 4000 in the Hypnales), represented by highly specialized, mostly tropical groups, which are never aquatic or subaquatic. Interestingly, a very similar areolation pattern was found in Bryokhutuliinia jurassica, almost sympatric and synchronous to Palaeodichelyma. Palaeodichelyma differs from Jurassic Muscites fontinaloides and Bryokhutuliinia jurassica by the presence of costa, and from Tricostium by the elongate laminal cells and single costa (in fact, differences are very numerous, but there is no reason to list them for such different plants). The Palaeozoic Bajdaievia is similar to Palaeodichelyma in many details (leaf size and shape, pattern of foliage), but lacks the loose areolation in the basal part of the leaf, where “net venation” (briefly explained in Section 16.2.2 Polyssaievia and Bajdaievia) is developed. Uskatia conferta is similar to Palaeodichelyma in general appearance and leaf dimensions, but differs in the presence of a distinct leaf border and at places the apparent oblique rows of laminal cells. We consider them also to be fundamentally different in their patterns of leaf attachments, although this character is not always observed in both species. In conclusion, the question, “Did pleurocarpous mosses originate before the Cretaceous?” has to be answered, “Yes, they did.” Overall similarity and, especially lateral perichaetia of Palaeodichelyma provide enough evidence for this. Even if the dating of the deposits with Palaeodichelyma shifts to the basal Cretaceous, the fact of its distribution in several localities means its origin must be at least in the Late Jurassic. Bryokhutuliinia and Muscites fontinaloides can also be pleurocarps, though additional evidence is necessary to say this for sure.

ACKNOWLEDGMENTS We are grateful to S. M. Sinitza and D. M. Vasilenko for the information about localities and help in fieldwork and to A. G. Ponomarenko for valuable discussion of paleoenvironments. This work of was supported partly by RFBR grant 04-04-48774 and by the program “Biosphere Origin and Evolution” of the Russian Academy of Sciences.

REFERENCES Abramov, I. I. and Savicz-Lyubitskaya, L. I. (1963) Division Bryopsida. In Osnovy paleontologii, Volume “Vodorosli, mkhi, psilofity, plaunovye, chlenistostebelnye, paporotniki” (Ed. Yu. A. Orlov). Gosgeoltekhizdat, Moscow, pp. 344–414 (in Russian). Bashurova, N. F. (2001) Palinologicheskoe obosnovanie stratigrafii sredne-verhneyurskih otlozheniy Vostochnogo Zabaykal’ya [Palinological substantiation of the Middle-Upper Jurassic deposit stratigraphy of eastern Transbaikalia]. In Proceedings of 2d International Symposium “Evolution of life on the Earth,” November 12–15, 2001 (ed. V. M, Podobina). NTL, Tomsk, pp. 317–319 (in Russian).

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Bridel, S. E. (1819) Muscologiae Recentiorum Supplementum Pars IV. A. Ukertum, Gothae. Bridel, S. E. (1826) Bryologia universa seu systematica ad novan methodium dispositio, historia et descriptio omnium muscorum frondosorum hucusque cognitorum cum synonymia ex auctoribus probatissimis. Vol. 1. Joh. Ambros, Barth, Lipsiae. Brotherus, V. F. (1925) Musci, in Die natürlichen Pflanzenfamilien, Vol. 11., Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–542. Buck, W. R. (1991) The basis for familial classification of pleurocarpous mosses. Advances in Bryology, 4: 169–185. Busche, R. von (1968) Als Laubmossreste gedeutete Pflanzenfossilien aus den Lebacher Schichten (Autunien) von St. Wendel, Saar. Argumenta Palaeobotanica, 2: 1–14. Fefilova, L. A. (1978) Permian Mosses of European North of USSR [Listostebelnye mkhi permi Evropeiskogo Severa SSSR]. Nauka, Leningrad (in Russian). Frahm, J.-P. (2000) Neue Laubmoosfunde aus Baltischem Bernstein. Cryptogamie Bryologie, 21: 121–132. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanic Garden Press, St. Louis, pp. 205–239. Gomankov, A. V. and Meyen, S. V. (1987) Tatarina flora (composition and distribution in the Late Permian of Eurasia) [Tatarinovaya flora (sostav i rasprostranenie v pozdnej permi Evrasii)]. Trudy Geologicheskogo Instituta Akademii Nauk SSSR 401: 1–174 (in Russian). Ignatov, M. S. (1990) Upper Permian mosses from the Russia Platform. Palaeontographica Abt. B, 217: 147–189 + Pl. 1–9. Ignatov, M. S. (1992) Bryokhutuliinia jurassica, gen. et spec. nova, a remarkable fossil moss from Mongolia. Journal of the Hattori Botanical Laboratory, 71: 377–388. Kovalev, V. G. (1990) Flies. Muscida. In Pozdnemezozoiskie nasekomye Vostochnogo Zabaikal’ya [Late Mesozoic insects of Eastern Transbaikalia] (ed. Rasnitsyn, A. P.). Trudy Paleontologicheskogo Instituta Akademii Nauk SSSR, 239: 123–177 (in Russian). Krassilov, V. A. (1973) Mesozoic bryophytes from the Bureja Basin, Far East of the USSR. Palaeontographica Abt. B, 143: 95–105 + Pl. 41–51. Krassilov, V. A. and Schuster, R. M. (1984) Paleozoic and Mesozoic fossils. In New Manual of Bryology (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 1172–1193. Lignier, O. (1914) Sur une mousse houillère a structure conservee. Bulletin de la Société Linnéenne de Normandie, Ser. 6, 7: 128. Neuburg, M. F. (1960) Mosses from the Permian of Angaraland [Listostebelnye mkhi iz permskikh otlozhenij Angaridy]. Trudy Geologicheskogo Instituta Akademii Nauk SSSR, 19: 1–104 + 78 pl. Ochyra, R. (1990) On the relationships of Thamnobryum negrosense (Bartr.) Iwats. and Tan (Musci: Thamnobryaceae). Journal of the Hattori Botanical Laboratory, 68: 293–302. Ponomarenko, A. G. (2003) Hutuliin. http://www.palaeoentomolog.ru/Collections/hutuliin.html (in Russian). Rasnitsyn, A. P. and Quicke, D. L. J. (eds.) (2002) History of Insects. Kluwer Academic Publishers, Dordrecht. Renauld, B. and Zeiller, R. (1885) Sur des Mousses de l’époque houillère. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences, 100: 660–662. Renauld, B. and Zeiller, R. (1888) Études sur les terrain houiller de Commentry. Livre deuxième. Flore fossile. Imprimateur Théolier and Cie, St. Étienne, pp. 3–366. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution 57: 2226ñ2241. Sinitza, S. M. and Starukhina, L. P. (1986) Novye dannye i problemy stratigrafii i paleontologii verkhnego mesozoya Vostochnogo Zabaikal’ya [New data and problems in stratigraphy and palaeontology of the Upper Mesozoic in East Transbaikalia]. In Novye dannye po geologii Zabaikal’ya [New data on geology of Transbaikalia]. Ministerstvo Geologii RSFSR, Moscow, pp. 46–51 (in Russian). Smoot, E. L. and Taylor, T. N. (1986) Structurally preserved fossil plants from Antarctica. II. A Permian moss from the Transantarctic Mountains. American Journal of Botany 73: 1683–1691. Srebrodolskaya, I. N. (1980) Novye pozdemesozoiskie listostebelnye mkhi iz Zabaikaliya [New Late Mesozoic mosses from Transbaikalia] Trudy Vsesoyuznogo Nauchno-Issledovatelskogo Geologicheskogo Instituta, 204: 27–28 (in Russian). Thomas, B. A. (1972) A probable moss from the Lower Carboniferous of the Forest of Dean, Gloucestershire. Annals of Botany, 36: 155–161. Townrow, A. (1959) Two Triassic bryophytes from South Africa. Journal of South African Botany. 25: 1–22.

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Tsubota, H., Arikawa, T., Akiyama, H., De Luna, E., Gonzalez, D., Higuchi, M. and Deguchi, H. (2002) Molecular phylogeny of hypnobryalean mosses as inferred from a large-scale dataset of chloroplast rbcL, with special reference to the Hypnaceae and possibly related families. Hikobia 13: 645–665. Zherikhin, V. V. (1978) Razvitie i smena melovykh i kainozoiskikh faunisticheskikh kompleksov (trakheinye i khelitserovye) [Development and changes of the Cretaceous and Cenozoic faunal assemblages (Tracheata and Chelicerata)]. Trudy Paleontologicheskogo Instituta Akademii Nauk SSSR, 165: 1–198 (in Russian).

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the Diversification of 17 Dating the Pleurocarpous Mosses Angela E. Newton, Niklas Wikström, Neil Bell, Laura Lowe Forrest, and Michael S. Ignatov CONTENTS Abstract ..........................................................................................................................................337 17.1 Introduction...........................................................................................................................338 17.2 Materials and Methods .........................................................................................................340 17.2.1 Taxonomic Sampling................................................................................................340 17.2.2 DNA Extraction, Amplification, Sequence Editing and Alignment........................340 17.2.3 Phylogenetic Analyses..............................................................................................345 17.2.4 Divergence Time Analyses .......................................................................................345 17.2.5 Calibration Point and Minimum Age Constraints ...................................................346 17.2.6 Lineage Diversification Data....................................................................................349 17.3 Results...................................................................................................................................351 17.3.1 Phylogenetic Analyses..............................................................................................351 17.3.2 Divergence Times .....................................................................................................351 17.3.3 Lineage Diversification Data....................................................................................352 17.4 Discussion.............................................................................................................................352 17.4.1 Moss Relationships...................................................................................................352 17.4.2 Acrocarpy and the Transition to Pleurocarpy ..........................................................355 17.4.3 Patterns of Species-, Genus-, and Family-Level Diversity......................................356 17.4.4 Diversification in Pleurocarpous Lineages...............................................................357 17.4.5 The Origin of Pleurocarpy s. str., and the Implications for the Evolution of the Pleurocarpous Mosses ..............................................................................................357 17.4.6 Pleurocarpous Mosses and the Angiosperms...........................................................359 17.4.7 Implications for the Interpretation of Fossils of Pleurocarpous Mosses.................360 17.5 Conclusions...........................................................................................................................361 17.5.1 Perichaetia Terminating Lateral Branches ...............................................................361 17.5.2 Diversification of the Angiosperms..........................................................................362 Acknowledgments ..........................................................................................................................362 References ......................................................................................................................................363

ABSTRACT The pleurocarpous mosses are a highly diverse monophyletic lineage, comprising about 42% of the approximately13,000 extant species of mosses. Phylogenetic analysis of molecular data suggests that the pleurocarps diversified over a (geologically) short period of time. The absence of a good fossil record has hindered attempts to determine when this group evolved and the processes

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implicated. In particular, the idea that evolution of pleurocarpous mosses was associated with the appearance of angiosperm forests has been untestable, and needs further study. We explored the patterns of diversification of the pleurocarps and estimated possible dates for their origins. Phylogenetic analyses, using Bayesian inference procedures, were conducted using molecular gene sequence data from the plastid rps4 and rbcL genes sampled for 12 vascular plants, 2 hornworts, 34 hepatics and 103 mosses. Ages for well-supported nodes were estimated using penalized likelihood and calibrated on the fossil date of 450 myr for the origin of land plants. The appearance of pleurocarpy was dated at 194–161 mya, significantly earlier than the radiation of the majority of pleurocarp lineages about 165–131 mya. This radiation coincides with the diversification of the angiosperms in the Early Cretaceous, but predates appearance of complex angiosperm forests in the early Cenozoic. The hypothesis that pleurocarpous mosses evolved to exploit the angiosperm forests is modified — pleurocarpous mosses diversified in the same time frame as the early angiosperms and the recovered pattern suggests a putative correlation of these diversification events.

17.1 INTRODUCTION The use of a combination of phylogenetic analysis and molecular data over the last ten years has resulted in a rapidly increasing improvement in our understanding of, and confidence in, moss relationships. Many recognized relationships based on strong morphological synapomorphies have been confirmed (e.g., monophyly of the Polytrichales and the Sphagnales), others have either been established or are undergoing refinement (e.g., circumscription of the haplolepidae; La FargeEngland et al., 2000, 2002), and more satisfactory placements have been proposed for anomalous taxa (e.g., Wardia [Hedderson et al., 1999] and Oedipodium [Newton et al., 2000]). It is clear from a number of studies (Beckert et al., 1999; 2001; Cox and Hedderson, 1999; Cox et al., 2000, 2004; De Luna et al., 1999, 2000; Goffinet and Cox, 2000; Hedenäs, 1994; Newton et al., 2000; Newton et al., 2000) that the acrocarpous taxa form a grade of distinct and (mostly) well-resolved lineages, whereas the pleurocarpous taxa, although monophyletic (Bell and Newton, 2005; O’Brien, Chapter 2 in this volume), form a “bush” of lineages with relationships that remain poorly resolved and not well supported. Exceptions are the hypnodendroid pleurocarps, a well-resolved and strongly supported clade that is sister to the hypnidean pleurocarps (Bell and Newton, 2005), the Ptychomniales (Buck et al., 2005) and the Hookeriales. The majority of orders of mosses in the acrocarpous grade are very small, with 8 of the 27 orders currently recognized (Goffinet and Buck, 2004) containing 5 or fewer species, and a further 6 orders containing between 12 and 95 species, with a total of 310 species in these 14 orders. Most diversity in the mosses is found in just 2 subclasses, the acrocarpous Dicranidae (with 30% of extant species, 24 families and 6 orders) and the pleurocarpous mosses, consisting of the subclass Hypnidae and the paraphyletic superorder “Rhizogoniales” (42% of extant moss species, 58 families and 4 orders). This pattern, with a grade of well-defined, relatively species-poor monophyletic groups terminating in a speciose “bush” of taxa that are less well resolved, is also repeated at lower taxonomic levels in the mosses. For example, in the Polytrichaceae, there is a grade of about a dozen clades of individual genera or small groups of genera, and a distal group of four poorly defined genera (Hyvönen et al., 2004) that include about 60% of the species in the family (from Crosby et al., 1999). Similar patterns are suggested elsewhere, but have not yet been supported by published phylogenetic analyses involving dense taxon sampling. The “bush” of poorly resolved pleurocarpous lineages usually includes two major clades, corresponding to the Hypnales and Hookeriales, and these are subtended by a number of smaller clades such as the Ptychomniales and members of the paraphyletic Rhizogoniales. Both in the Hookeriales and in the smaller clades, internal branches are generally long and relationships well supported, whereas in the Hypnales internal branch lengths are extremely short and relationships among hypnalean taxa are currently not well understood. In a molecular study of the diversification

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of the pleurocarpous mosses, Shaw et al. (2003) concluded that the Hypnales showed evidence of a rapid diversification but that the Hookeriales did not. However, they used the Ptychomniales as the outgroup, ignoring the grade of pleurocarpous taxa in the Rhizogoniales and patterns of diversification in the pleurocarps as a whole. Patterns of relationships and diversity of extant taxa raise questions relating to the processes by which such patterns came about, and the influence of major events in Earth history. However, our understanding of the processes underlying the diversification of mosses is poor, and most attempts to explain such patterns consist of narrative based on observation of modern distribution and ecology. In the absence of significant fossil material from much of the history of moss evolution, no direct contemporary evidence of ecology or distribution can be taken into account, further weakening such arguments. The observed pattern of species distribution in the pleurocarpous mosses could be the result of widely different processes (Givnish, 1997; Sanderson, 1998; Bateman, 1999). For example, it might be the result of fundamental features of lineage diversification, maintenance and extinction, independent of evolutionary events. Alternatively, species diversification (character or morphological diversification; Sanderson, 1998) might have been prompted by an intrinsic factor, such as the appearance of a morphological, physiological or reproductive innovation that might have provided a stimulus for greatly increased rates of speciation. An adaptive radiation (ecological diversification; Sanderson, 1998) might have occurred in response to extrinsic features of the environment that provided a range of new habitats. Each of these processes, or others, or a combination, might be responsible for the observed pattern in the pleurocarpous mosses. Rates of origin and extinction of lineages could result in the appearance of high levels of diversity in the distal lineages of an extant clade at any given time, with over time the majority becoming extinct, leaving progressively more depauperate remnants in a paraphyletic, species-poor grade. With such a process, at any given time in the past a similar pattern of diversity might have been observed in the extant lineages, with the implication that the current observed pattern is no different from what might have been seen at any other time, i.e., that the appearance of radiations might be an artifact. Patterns of speciation rates versus extinction rates have been explored in depth by a number of workers (e.g., Benton, 2003; Nee, 2001), with considerable implications for interpretation of observed diversity. A possible morphological innovation which might have enabled or promoted increased species diversification is the feature of pleurocarpy, which relates to the formation of gametangia on the tips of modified branches, as lateral perichaetia. This allows the primary stem to grow in an indeterminate manner, facilitating the extensive horizontal growth seen in many lineages. This is in contrast to acrocarpy, in which the main stem is terminated by the formation of gametangia so that further extension growth can occur only through the formation of new segments of main stem by the development of lateral buds. These differences in habit have significant implications for the ecological relationships, reproductive biology, physiology and further morphological evolution of the pleurocarpous mosses. Creeping habit and prolonged vegetative growth might be expected to influence the persistence and dominance of pleurocarpous mosses in any given habitat. These morphological features may also significantly increase reproductive viability by allowing members of dioicous taxa to persist and extend their “territory” until a member of the opposite sex becomes established or grows close enough to allow transfer of antherozoids to occur. Ability to form more than one sporophyte per unit of stem growth may also significantly increase reproductive success. Dendroid, weft-forming and pendulous growth forms have been shown (Rice et al., 2001; Rice and Schneider, 2004) to differ significantly from the tight cushion and turf growth forms of acrocarpous mosses in their modes of water, nutrient and gas exchange, with potential implications for variation of physiology. A morphological innovation with such a large potential impact on the adaptive success and competitiveness of the pleurocarpous mosses might also be expected to stimulate further diversification of lineages. Alternatively, the “bush-like” pattern of high diversity may reflect the influence of extrinsic environmental features, with a burst of speciation (or increased lineage survival) in response to the

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appearance of favourable conditions occurring after a period in which conditions were less conducive to diversification. The greatly increased ecological possibilities presented by the appearance of the angiosperms in the mid to Late Cretaceous (Crane, 1987; Crane et al., 1995) might have been such an influence. The possibility that the pleurocarp diversification represents a response to earlier forests such as those formed by coniferous trees (Behrensmeyer, 1992) or even “tree ferns” (O’Brien, Chapter 2 in this volume) also needs to be considered, and can be rejected only if dates for the diversification of the different groups can be obtained. Pleurocarpous mosses are abundant in temperate and tropical forests, forming extensive carpets and bolsters that may provide a very large proportion of the biomass on the forest floor, on tree trunks, branches, twigs and rotting logs. Although the other, acrocarpous, members of the moss clade are also found in forest habitats they rarely occupy as much territory or develop as much biomass as pleurocarpous mosses. The frequency with which pleurocarpous mosses are found in forest habitats has led to the idea that these mosses may have differentiated in response to the appearance of angiosperm forests (Shaw et al., 2003; Vitt, 1984). However, without data from fossil material of pleurocarps and their predecessors, this hypothesis has been difficult to test. Did the massive diversification of the pleurocarpous mosses result from the appearance of the lateral perichaetium, the stabilization of this morphology into the form now dominant, or to some feature of the environment such as the development of a landscape dominated by angiosperms? One way to address these questions is to estimate ages for the nodes representing the intrinsic evolutionary events, and relate them to the timing of extrinsic evolutionary events. This may in turn allow us to reject or modify some of these hypotheses. Although fossil-based age estimates may not be achievable, age estimates for the nodes of interest can be obtained by analysing the divergence in molecular gene sequence data (e.g., Magallón, 2004; Sanderson, 2004). We followed the approach of Schneider et al. (2004), in estimating times of divergence for critical nodes, and also in looking at the lineages-through-time (LTT) plots to compare the rates and patterns of diversification of the lineages of angiosperms and bryophytes. By estimating ages for well-supported nodes in a topology derived from phylogenetic analysis of the mosses, liverworts, hornworts and vascular plants, we have aimed to explore possible relationships between these nodes and the processes involved in the evolution of the pleurocarpous mosses. This also allows us to explore the implications of the known fossils for understanding of the evolution of different morphological features, and, reciprocally, to explore the impact of dating different nodes on the placement of these fossils in the topology.

17.2 MATERIALS AND METHODS 17.2.1 TAXONOMIC SAMPLING Previous phylogenetic analyses (Bell and Newton, 2004, 2005; Cox et al., 2000, 2004; Cox and Hedderson, 1999; Forrest and Crandall-Stotler, 2004; Schneider et al., 2004) were used to develop a strategy for sampling across land plant lineages. This information was used to determine the taxa and genes to be included in the analyses, with one or more exemplars chosen from each major group (see Table 17.1). A small number of exemplars were sampled for vascular plants (12 genera), while other groups were sampled at low (hepatics 34 spp., hornworts 2 spp.) or moderate density (mosses 103 spp.). Target genes for critical taxa not otherwise available were extracted, amplified and sequenced in the laboratories at NHM (shown in bold in Table 17.1).

17.2.2 DNA EXTRACTION, AMPLIFICATION, SEQUENCE EDITING AND ALIGNMENT Plastid rbcL and rps4 genes were amplified and sequenced for all taxa in our data availability matrix for which these genes were missing. Procedures used to extract and amplify DNA are as given in Bell and Newton (2005). Forward and reverse sequences were edited and assembled using

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TABLE 17.1 GenBank Accession Numbers for Gene Sequences Used Taxon

Chara vulgaris L. Chaetosphaeridium globosum (Nordst.) Kleb.

rps4 Outgroup DQ229107 AF494278

rbcL

Voucher

AF097167 AF408250

Vascular Plants Lycophytina Isoetes engelmannii A. Braun Isoetes lacustris L. Selaginella apoda (L.) Spring Huperzia selago (L.) Bernh. ex Schrank & Mart. Lycopodium clavatum L. Moniliformopses Equisetum fluviatale L. Osmunda banksiifolia Pr. Osmunda cinnamomea L. Spermatophyta Cycas revoluta Thunb. Ginkgo biloba L. Pinus thunbergii Parl. Pinus sylvestris L. Magnolia stellata (Siebold & Zucc.) Maxim. Oryza sativa L. Zea mays L. Hornworts Anthoceros punctatus L. Notothylas orbicularis (Schwein.) Sull. Hepatics Treubiales Treubia lacunosa (Colenso) Prosk. Phyllothallia nivicola E. A. Hodgs. Haplomitrales Haplomitrium hookerii (SM.) Nees Blasiales Blasia pusilla L. Marchantiopsida Conocephalum conicum (L.) Underw. Marchantia polymorpha L. Monoclea gottschei Lindb. Sphaerocarpos texanus Austin Metzgeriales I Metzgeria furcata (L.) Corda Verdoornia succulenta R. M. Schust. Metzgeriales II Hymenophyton flabellatum (Labill.) Dumort. Moerckia flotoviana (Nees) Schiffn. Pallavicinia lyellii (Hook.) Carruth. Podomitrium phyllanthus (Hook.) Mitt. Symphyogyna brongniartii Mont. Symphyogyna undulata Colenso

AF313592 AF313586 AF313605 DQ463115 DQ463116 AF313602

AJ010855 AJ010854 Y07934 Y07936

N148; Bell 1286 BM

DQ463101

N177; Bell 1302 BM

AB024949 AF313609 AF313611 AF313612

AF462411 AJ235804

AY188233 NM_197450 X86563

AB019809 AF238057 AY522330 X86563

AJ250117 DQ463117

U87063 AF231888

AY507468 AY507459

AY507428 AY507418

AF231890

U87072

AY507436

AF536232

DQ463118 X04465 AJ251063 AY507466

U87067 U87079 U87083 AY507425

N152; Newton 6375 BM

DQ463119 AY507470

U87081 AY507430

N172; Newton 6373 BM

AY507448 AY688796 AY688798 AY507460 AY688803 AY688804

AY507406 AY507413 AY507416 AY507419 AY688789 AY688790

N217; Newton 6679 BM

Continued.

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TABLE 17.1 (Continued) GenBank Accession Numbers for Gene Sequences Used Taxon Fossombroniales Calycularia crispula Mitt. Fossombronia angulosa (Dicks.) Raddi Pellia epiphylla (L.) Corda Jungermannidae Aphanolejeunea gracilis Ast Austrolejeunea nudipes (Hook. f. & Taylor) Grolle Diplophyllum obtusifolium (Hook.) Dumort. Frullania dilatata (L.) Dumort. Jungermannia leiantha Grolle Lejeunea catanduana (Steph.) H. A. Mill., H. Whittier & B. Whittier Lepidolaena taylorii (Gottsche) Trevis. Lophocolea heterophylla (Schrad.) Dumort. Mastigolejeunea auriculata (Wilson & Hook.) Schiffn. Nipponolejeunea pilifera (Steph.) S. Hatt Plagiochila asplenioides (L.) Dumort. Plagiochila adianthoides (Sw.) Lindenb. Porella pinnata L. Ptilidium pulcherrimum (F. Weber) Hampe Scapania nemorea (L.) Grolle Trocholejeunea sandvicensis Mizut. Mosses Takakiopsida Takakia lepidozioides Hatt. & Inoue Sphagnopsida Sphagnum palustre L. Andreaeopsida Andreaea rothii Web. & Mohr. Andreaobryopsida Andreaobryum macrosporum Steere & B. Murr. Oedipodiopsida Oedipodium griffithianum (Dicks.) Schwaegr. Polytrichopsida Alophosia azorica (Renauld & Cardot) Cardot Atrichum undulatum (Hedw.) P. Beauv. Dawsonia papuana Schlieph. & Geheeb Polytrichum commune Hedw. Tetraphidopsida Tetraphis pellucida Hedw. Bryopsida Buxbaumiidae Buxbaumia aphylla Hedw. Diphysciidae Diphyscium foliosum (Hedw.) Mohr Funariidae Bryobrittona longipes (Mitt.) D.G. Horton Encalypta rhaptocarpa Schwaegr. Funaria hygrometrica Hedw. Timmia sibirica Lind. & Arnell

rps4

rbcL

Voucher

AY507437 AY507440 DQ463120

AY507395 AY507398 AY688787

N158; Newton 6376 BM

AY462338 AY462339 AY507439 AJ250454 AY507451 AY462363

AY302443 AY302445 AY507397 AY125929 AY507409 AY125943

AY462368 AF231889 AY462371 AY462376

AY462310 U87076 AY125933 AY125937 AY149839

AY438204 AY330481 AY462388 AY507464 AY462401

U87088 AY302460 AY507423 AY125934

AF231894

AF231058

AF231892

AF231887

AY312866

AF231060

AF306953

AF231059

AF306968

AF478202

AY312924 DQ463121 AF208419 AF208428

AY330476 DQ463102 AF208410 LJ87087

AF231896

U87091

AF231897

AF231062

AF223034

AY312928

AF023778 AF023777 AF023776 AF023775

AJ275168 AJ275167 AF231067 AJ275166

N143; Bell 904 BM

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TABLE 17.1 (Continued) GenBank Accession Numbers for Gene Sequences Used Taxon Dicranidae Ceratodon purpureus (Hedw.) Brid. Dicranoweissia cirrata (Hedw.) Lindb. Dicranum scoparium Hedw. Fissidens taxifolius Hedw. Grimmia pulvinata (Hedw.) Sm. Pottia truncata (Hedw.) Bruch & Schimp. Ptychomitrium gardneri Lesq. Schistostega pennata (Hedw.) F. Weber & D. Mohr Scouleria aquatica Hook. Tortula ruralis (Hedw.) G.M.S. Bryidae Splachnales Leptobryum pyriforme (Hedw.) Wilson Splachnum ampullaceum Hedw. Orthotrichales Orthotrichum lyellii Hook. & Taylor Ulota crispa (Hedw.) Brid. Hedwigiales Hedwigia ciliata (Hedw.) P. Beauv. Bryales Aulacomnium androgynum (Hedw.) Schwaegr. Aulacomnium turgidum (Wahlenb.) Schwaegr. Bryum alpinum Huds. ex. With. Mnium hornum Hedw. Orthodontium lineare Schwaegr. Philonotis fontana (Hedw.) Brid. Plagiomnium affine (Blandow ex Funck) T. J. Kop. Plagiomnium japonicum (Lindb.) T. J. Kop. Plagiopus oederi (Brid.) Limpr. Pohlia cruda (Hedw.) Lindb. Rhodobryum giganteum (Schwaegr.) Paris Rhizogoniales Bescherellia cryphaeoides (Müll. Hall.) M. Fleisch. Bescherellia brevifolia Hampe Braithwaitea sulcata (Hook.) A. Jaeger & Sauerb. Calomnion brownseyi Vitt & H. A. Mill. Cryptopodium bartramioides (Hook.) Brid. Cyrtopus setosus (Hedw.) Hook. f. Goniobryum subbasilare (Hook.) Lindb. Hymenodon pilifer Hook. f. & Wilson Hypnodendron dendroides (Brid.) Touw Leptotheca boliviana Herzog Leptotheca guadichaudii Schwaegr. Mesochaete taxiforme (Hampe) Watts & Whitel. Powellia involutifolia Mitt. Pterobryella praenitens Müll. Hal. Pyrrhobryum bifarium (Hook.) Manuel

rps4

rbcL

AF435271 DQ463122 AF231277 DQ463123 AF222900 DQ463124 AF023779 AY631171 AF023780 AF023831

DQ463103 AF478227 AF231067 DQ463104 AF231305 DQ463105 AF005549 AY631206 AF226822 AJ275169

AF023802 AJ251308

AF231072 AF231071

AF023814 AF306972

AF005536 AY631208

AJ251309

AF005517

AF023811 AF023809 AF023783 AF023776 AF023800 AF023801 AF023797

AY631174 AJ275180 AY163023 AF226820 AJ275174 AY631192

AF023833

AB050992 DQ481540

AF023795 AF023789

AJ275175 AJ275176

AY524473 AY524472 AY524469 AY631140 AY631142 AY524479 AY631148 AY631149 AY524482 AF023816 AY631151 AY524462 AY524465 AY524483 AY631159

AY524445 AY524444 AY524441 AY631177 AF231084 AY524451 AY631184 AY631186 AY524454 AY631188 AY631189 AY524434 AY524437 AY524455 AY631195

Voucher

N161; Bell 903 BM N179; Bell 1304 BM N157; Bell 912 BM N159; Bell 911.5 BM

A85; Hedderson 11784 RNG

Continued.

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TABLE 17.1 (Continued) GenBank Accession Numbers for Gene Sequences Used Taxon Pyrrhobryum dozyanum (Sande Lac.) Manuel Pyrrhobryum medium(Besch.) Manuel Pyrrhobryum spiniforme (Hedw.) Mitt. Pyrrhobryum vallis-gratii (Hampe in Mull. Hal.) Manuel Racopilum cuspidigerum (Schwägr.) Ångstr. Racopilum spectabile Reinw. & Hornsch. Rhizogonium distichum (Sw.) Brid. Rhizogonium graeffeanum (Müll. Hal.) A. Jaeger Rhizogonium novahollandiae (Brid.) Brid. Spiridens vieillardii Schimp. Hypnidae Ptychomnianae/Ptychomniales Euptychium cuspidatum (Mitt.) Mitt. Garovaglia elegans (Dozy & Molk.) Hampe ex Bosch & Sande Lac. Glyphothecium scuirioides (Hook.) Broth. Hampeella alaris (Dixon & Sainsbury) Sainsbury Ptychomnion cygnisetum (Müll. Hall.) Kindb. Hypnanae Hookeriales Ancistrodes genuflexa (Müll. Hal) Crosby Crossomitrium patrisiae (Brid.) Müll. Hall. Cyathophorum bulbosum (Hedw.) Müll. Hal Hypopterygium tamarisci (Sw.) Brid. ex Müll. Hal Leucomium strumosum (Hornsch.) Mitt. Lopidium concinnum (Hook.) Wilson Hypnales Brachythecium rutabulum (Hedw.) Schimp. Catagonium brevicaudatum Müll. Hall. ex Broth.

rps4

rbcL

AY631160 AY631162 AY524485 AY631167 AY524477 AY524478 AY524461 AY631168 AY631169 AY524474

AY631196 AY631198 AY524457 AY631202 AY524449 AY524450 AY524433 AY631203 AY631204 AY524446

AY631144 AY631145

AY631180 AY631181

AY631147 AY524463 DQ463125

AY631183 AY524435 DQ463106

AY631138 DQ467881 AY631143 AF143077 AF143068 AY631153

AY631173 DQ467872 AY631179 AF232695 AF161161 AY631190

AF023818 DQ467884

DQ463107 DQ467879

Catagonium nitens (Brid.) Cardot Cryphaea heteromalla (Hedw.) D. Mohr Cryphaea patens ((Hornsch.) ex Müll. Hall. Entodon hampeanus Müll. Hall. Eurhynchium praelongum (Hedw.) Schimp. Fabronia pusilla Raddi

AF307003 DQ463126

DQ463108

DQ467882 DQ463127 AY908199

DQ481541 DQ467877 DQ463109 DQ467874

Fontinalis antipyretica Hedw. Hypnum cupressiforme Hedw. Hypnum lindbergii Mitt. Jaegerina scariosa (Lorentz.) Arzeni Lepyrodon tomentosus (Hook.) Mitt.

AF023817 DQ467883 AF143035 DQ463128 AY908585

AJ275183 DQ467878 AF232696 DQ463110 DQ467875

Leucodon sciuroides (Hedw.) Schwaegr.

AY908186

DQ467876

Neckera crispa Hedw. Orthostichopsis tetragona (Sw. ex Hedw.) Broth. Pilosium chlorophaea (Hornsch.) Müll. Hall. Plagiothecium undulatum (Hedw.) Schimp. Pseudocryphaea domingensis (Spreng.) W. R. Buck

AJ269692 AY908192 AF143059 AJ251315 AY908188

DQ463111 DQ481542 DQ463112 AB024634 DQ467873

Voucher

N167; Bell 965 BM

B24; Newton 4548 BM

N142; Bell 911 BM B19; Churchill et al. 16297 DUKE N150: Bell 1030 BM N174, Newton 6374 BM A42; De Luna 2243 XAL De Luna 2261 XAL N141; Bell 907 BM A17; Hedderson 9230 RNG A91; Cox 599 BM N186; Newton 6155 BM A54; De Luna and Keller 2246, XAL A75; Hedderson 8852 RNG N145; Bell 1296 BM A49; Newton 4616, BM N215; Newton 6253 BM A57; Newton 4542, BM

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TABLE 17.1 (Continued) GenBank Accession Numbers for Gene Sequences Used Taxon Pterobryon densum Hornsch. Pterogonium gracile (Hedw.) Sm. Rhytidiadelphus triquetrus (Hedw.) Warnst. Rutenbergia madagassa Geh. & Hampe Stereophyllum radiculosum (Müll. Hal.) A Jaeger Thuidium delicatulum (Hedw.) Schimp. Thuidium tamariscinum (Hedw.) Schimp. Trachyloma diversinerve Hampe

rps4 AF143013 AY631157 AY524464 AY524486 DQ467885 AF143039 AF143021

rbcL

Voucher

AF158175 AY631194 AY524436 AY524458 DQ467880

B16; Zardini 7102 DUKE

DQ463113 DQ463114

N156; Bell 1300 BM N181; Newton 6589 BM

Note: Vouchers are given for those taxa for which sequences were newly obtained for this project or not previously published (shown in bold). Isolate number precedes collector information (Cox isolates A and B; Bell isolates N). Nomenclature follows that used in TROPICOS-MOST http://mobot.mobot.org/W3T/Search/most.html

SeqMan II and SeqEdit (LaserGene System Software, DNAStar Inc.), and consensus sequences for each gene were input and manually aligned in SeAl (Rambaut, 1996). The complete data matrix is available in the acompanying CD (Appendix 17.1).

17.2.3 PHYLOGENETIC ANALYSES Phylogenetic analyses were conducted using Markov Chain Monte Carlo methods (Larget and Simon, 1999) within a Bayesian framework. The data was partitioned into two sets corresponding to the rbcL and rps4 genes. In total, 2006 aligned characters were included (1367 rbcL and 639 rps4), and both regions were present in all taxa sampled. Lengths of included unaligned characters varied for rbcL between 1367 and 1041 (absolute majority of taxa with more than 1300) characters and for rps4 between 621 and 464 (majority of taxa with 570 to 600) characters. In the Bayesian analyses, a GTR + I + G model was chosen for both partitions following the results of hierarchical likelihood ratio tests conducted using MrModelTest 2.0 (Nylander, 2004), a modified version of Modeltest 3.5 (Posada and Crandall, 1998). The analyses were done using MrBayes v3.0B4 (Huelsenbeck and Ronquist, 2001). Three separate runs, each including 1,000,000 generations and sampling one tree every hundredth generation, were conducted. After removing the first 5000 sampled trees from each run, trees sampled during the burn-in phase of the MCMC chain, the results from the three independent runs were checked to verify convergence. The resulting trees and parameter estimates, sampled after the burn-in phase of the MCMC chain, were pooled and the final posterior distribution included 15,000 trees and parameter estimates. To further evaluate if the three independent runs had reached stationarity, their posterior distribution was compared to a fourth run that was kept running for an additional 9,000,000 generations.

17.2.4 DIVERGENCE TIME ANALYSES Divergence times were estimated for all nodes with 95% or higher posterior probability using penalized likelihood (PL) as implemented in r8s 1.60 (Sanderson, 2003). A point estimate for each node was obtained by using the all-compatible majority rule tree resulting from our Bayesian posterior distribution. To account for phylogenetic and branch length uncertainty in our estimates, 100 trees and parameter estimates were randomly drawn, using the RANDOM Bourne-Again Shell (bash) variable, from the posterior distribution and used as input in the age estimation analyses. For each node the posterior distribution of divergence time, conditional to the phylogenetic model (tree and GTR + I + G), and the calibration point, were obtained by local density estimation using

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the program LOCFIT (Loader, 1999), implemented in the “R” statistical package (Ihaka and Gentlemen, 1996). To summarize the fitted distributions, we report their modes and 90% highest posterior density (HPD) limits (Table 17.2). The mode represents the most likely divergence time value under the specified model, and the HPD limits the confidence interval for the estimates. The log10 smoothing factor was set to 2.0 in all r8s age estimation analyses. In principle the smoothing factor should be calculated by cross validation analyses, as outlined by Sanderson (2002), and set individually on each tree. This would, however, become too computer intensive. The 2.0 value used was obtained by averaging the optimal values from cross validation analyses over 10 trees randomly drawn from our posterior distribution. The optimal values across the 10 randomly selected trees ranged between 1.75 and 2.25 indicating that our 2.0 value is close to optimal for most trees. To prevent the r8s age estimation algorithm from converging on a local optimum, the searches were started at three different initial time estimates (num_time_estimates = 3) for each search. Local stability of the solutions was checked by perturbation and restarting the search three times (num_restarts = 3).

17.2.5 CALIBRATION POINT

AND

MINIMUM AGE CONSTRAINTS

To convert the relative ages obtained through the penalized likelihood analyses into estimates of absolute ages, a calibration point has to be selected, and most often this is done with reference to some fossil-based information. The Palaeozoic and Mesozoic moss fossils currently known, whether acrocarpous or supposedly pleurocarpous, lack sufficient character information to relate them to any but the broadest of extant higher-level taxa (see discussion by Ignatov and Shcherbakov, Chapter 16 in this volume). These fossils consequently make little direct contribution to our understanding of early relationships or evolutionary events in the pleurocarpous mosses, nor can they be used to calibrate or constrain nodes for the dating analysis. We therefore used the root node (crown group embryophytes) as our calibration point and the age of this node was fixed at 450 myr in all divergence time analyses. The fossil-based age estimate for this node is based on the presence of spore tetrad fossils from the Middle Ordovician (Gray, 1993). Two features of these fossils are considered diagnostic of land plants (Kenrick and Crane, 1997a, 1997b): the retention of the spores in tetrads (indicating that meiosis has occurred) and the resistance of the spores to decay (implying the presence of sporopollenin). Although not unequivocally associated with the crown group of extant embryophytes, a liverwort affinity for some of these early fossils is suggested by spore wall morphology (Wellman et al., 2003). Macrofossils that are stem group members of extant tracheophytes unequivocally occur in the Middle Silurian (Wenlockian: 428–423 myr ago). These fossils are almost as old as our 450 myr embryophyte calibration point and it is unlikely that we are overestimating the true age for crown group embryophytes (Kenrick and Crane, 1997a, 1997b; Sanderson, 2003). Seven minimum age constraints were enforced during all divergence time analyses. A minimum age constraint establishes a minimum permitted age for the constrained node during the analyses, forcing our analyses to consider only solutions compatible with the enforced constraint. Six of the seven constraints enforced concern tracheophyte relationships: 1. The split between Magnolia and the two monocot taxa (node 32) was constrained at 123 myr. Magnoliales (stem group Winteraceae) and monocots are both documented from the Late Barremian or Early Aptian (Doyle, 2000, Friis, 2004). 2. Seed plant crown group (node 31) was constrained at 310 myr based on the occurrence of conifers in the Late Carboniferous (Miller, 1999). 3. Monilophyte crown group (node 30) was constrained at 354 myr based on the appearance of the lineage leading to extant horsetails in the Early Carboniferous (Bateman, 1991; Schneider et al., 2004). 4. Euphyllophyte crown group (node 29) was constrained at 380 myr based on stem group monilophytes from the Middle Devonian (Kenrick and Crane, 1997b; Schneider et al., 2004).

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TABLE 17.2 Divergence Time Estimates Showing Estimated Ages of Nodes Supported by 95% or Higher Posterior Probability in the Phylogenetic Analyses Node

Lineage

% Posterior Probability

Point Estimate

Mode

LHPD

2 3‡ 4* 5 6‡ 7> 8 9> 10 11 12 13‡ 14 15‡ 16‡ 17‡ 18 19 20 21‡ 22‡ 23 24‡ 25 26 27 28 29* 30* 31 32*‡ 33 34* 35‡ 36 37 38 39 40‡ 41 42‡ 43 44 45 46

Hepatics Marchantiopsida Sphaerocarpos Marchantia Conocephalum/Monoclea Leafy and simple thalloid hepatics Leafys and Metzgeriales Leafy hepatics Jungermanniales Lophocoleineae Jungermannineae Scapaniaceae Porellales/Lejeuneaceae Jubulineae Lejeuneaceae s. lat Lejeuneaceae s. s. Lejeuneaceae s. s. Lejeuneaceae s. s. Lejeuneaceae s. s. Metzgeriales I “Fossombroniales” Phyllothallia/Metzgeriales Metzgeriales II Metzgeriales II Metzgeriales II Metzgeriales II Haplomitrales/Treubiales Euphyllophytes Monilophytes Seed plants Angiosperms Monocotyledons Gymnosperms Ginkgo/Pinus Lycopodiaceae Mosses/hornworts Hornworts Mosses Andreaeobryum Andreaea Oedipodium Polytrichales Polytrichaceae Polytrichaceae Diphyscium

100 100 100 100 100 100 99 100 100 100 99 100 100 100 100 100 100 100 100 100 100 100 100 100 100 97 96 100 100 100 100 100 99 96 100 100 100 99 100 96 100 100 100 99 100

367.41 248.23 203 154.26 125.44 291.54 272.16 238 157.39 134.43 131.29 49.07 190.14 166.2 109.28 50.11 30.85 19.82 22.36 213.76 212.49 187.15 155.72 85.78 40.33 75.38 353.03 410.97 354 329.55 188.35 37.42 310 266.82 142.35 403.24 235.08 380.44 320.98 310.61 291 226.12 131.22 101.08 240.68

369.21 245.66 203 157.47 129.14 287.32 272.55 232.15 157.21 133.91 127.87 44.48 188.47 162.69 106.37 49.15 30.21 19.97 22.74 201.02 226.61 194.48 162.99 87.84 39.61 76.86 360.05 411.79 354 328.52 178.41 39.54 310 258.79 145.53 401.15 229.64 378.59 329.54 317.44 292.26 230.53 140.44 102.65 245.7

338 231.41 203 136.2 106.12 261.69 242.92 206.63 130.25 114.04 106.94 38.22 168.19 146.53 93.77 41.34 24.59 14.88 14.6 186.44 189.47 167.4 141.57 75.51 32.47 66.39 315.78 403.26 354 321.04 168.53 32.23 310 237.71 116.88 388.89 210.23 362.49 304.33 295.07 280.13 206.73 111.8 82.89 229.58

UHPD 403.23 267.51 203 175.07 149.86 331.25 310.06 274.77 185.17 165.5 155.45 58.53 221.21 196.94 134.11 61.68 37.82 25.24 34.37 245.47 244.14 216.71 178.11 104.09 50.13 91.07 395.96 422.28 354 339.94 214.23 44.52 310 291.41 184.6 420.53 263.39 399.49 341.61 334.11 316.02 253.04 159.4 129.13 272.29 Continued.

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TABLE 17.2 (Continued) Divergence Time Estimates Showing Estimated Ages of Nodes Supported by 95% or Higher Posterior Probability in the Phylogenetic Analyses Node 47 48 49‡ 50‡ 51 52 53 54 55‡ 56 57 58 59 60 61 62‡ 63 64 65 66‡ 67‡ 68 69 70 71> 72> 73‡ 74‡ 75 76‡ 77> 78 79 80‡ 81> 82 83 84 85 86 87 88‡ 89 90‡ 91 92‡

Lineage Arthrodontous mosses Funariidae Dicranidae Grimmiales/Dicranales/Pottiales Grimmiales Dicranales/Pottiales

Pottiales Scouleria / Timmia Diplolepidous mosses Bryidae p.p. Splachnales Bryaceae Orthotrichales Bartramiaceae Mniaceae Mniaceae Pleurocarps s. lat. Rhizogoniaceae I Pyrrhobryum p.p. Calomnion / Cryptopodium Rhizogoniaceae II Rhizogonium Rhizogonium Hymenodon / Leptotheca Hypnodendroid pleurocarps Hypnodendraceae/Cyrtopodaceae Cyrtopodaceae Bescherellia Racopilaceae Racopilum Braithwaitea/Pterobryella Aulacomnium Hypnidae Ptychomnianae Ptychomniales p. p. Garovagliaceae Hypnanae Hypopterygiaceae Hypopterygiaceae Hypnales/Hookeriales

Hookeriales

% Posterior Probability

Point Estimate

Mode

LHPD

UHPD

100 100 96 100 100 95 98 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 96 100 100 95 95 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 97 100 99 100

213.8 172.34 185.46 154.11 98.41 139.99 114.26 104.3 109.45 30.82 124.76 190.29 177.66 111.65 79.49 15.26 127.75 92.87 59.44 166.35 143.77 48.78 83.3 134.99 71.39 60.21 95.61 91.99 69.79 23.99 11.47 38.11 24.05 71.48 46.97 148.3 82.03 40.58 21.42 138.61 107.43 54.45 132.71 113.55 83.62 74.28

219.24 187.46 202.75 156.19 105.04 148.61 121.48 108.59 111.08 33.53 135.68 195.5 183.67 116.12 82.55 14.42 137.48 103.56 63.83 172.79 141.32 50.41 89.68 140.84 67.23 59.77 119.11 111.25 78.84 22.11 9.4 41.3 27.64 87.68 50.01 151.28 87.91 42.5 22.09 142.78 113.26 55.16 140.62 107.03 81.51 71.17

204.74 162.12 176.12 144.53 82.45 129.87 101.03 88.51 96.45 22.74 111.32 181.46 165.16 95.11 67.67 9.05 101.96 78.85 47.37 161.34 122.03 30.49 62.1 112.33 57.1 45.53 94.67 87.69 58.98 15.89 6.44 30.48 17.7 67.07 41.87 140.76 72.21 30.19 16.56 130.75 98.19 45.92 123.45 92.67 55.13 60.68

242.75 208.93 220.43 187.66 131.25 174.58 145.1 134.12 141.27 44.09 158.55 215.63 203.72 137.56 99.66 24.68 165.75 125.64 80.66 194.45 174.94 75.52 120.8 163.62 91.43 84.04 136.15 123.52 100.59 38.29 18.75 56.55 39.36 102.34 71.88 172.86 100.44 52.71 28.38 165.1 131.7 70.96 157.15 136.42 116.55 91.82

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TABLE 17.2 (Continued) Divergence Time Estimates Showing Estimated Ages of Nodes Supported by 95% or Higher Posterior Probability in the Phylogenetic Analyses Node 93 94 95‡ 96‡ 97 98

Lineage

Stereophyllaceae Brachytheciaceae Pterobryaceae p.p.

% Posterior Probability

Point Estimate

100 100 100 100 100 98

49.06 60.73 73.63 38.75 66.78 67.53

Mode

LHPD

UHPD

46.98 62.31 66.97 34.66 71.51 78.47

38.66 39.32 53.86 25.37 56.01 57.46

60.63 81.29 117.57 66.46 96.14 101.08

Note: Node numbers correspond to those on the chronogram (Figure 17.1). Point estimates are from analyses of the all-compatible majority rule consensus tree and posterior probability values are reported. The Mode value represents the most likely divergence time value under the specified model (obtained by local density estimation calculated over the 100 random trees drawn from the posterior distribution of trees and parameters), and the HPD values limits the confidence interval for the estimates. (* node constrained; ‡ age estimates show bimodal distribution across the 100 random trees; > age distribution with a pronounced right tail across the 100 random trees)

5. The split between Euphyllophytes and lycopsids was constrained at 408 myr based on stem group lycopsid fossils in the Early Devonian (Kenrick and Crane, 1997b). 6. Crown group lycopsids was constrained at 390 myr based on the occurrence of Protolepidodendrales (lineage leading to extant quillworts) in the Early Devonian (Kenrick and Crane, 1997b). Two of the nodes constrained, the split between Euphyllophytes and lycopsids (90% posterior probability) and lycopsid crown group (90% posterior probability), were not well supported in our phylogenetic analyses (Figure 17.1). Consequently, these nodes were constrained only on the sampled trees where they occurred. In addition to the six tracheophyte constraints, one minimum age constraint was enforced among liverworts. Two taxa indicate a minimum age of 203 myr for the split (node 04) between Sphaerocarpales and the complex thalloid liverworts (Marchantiales). These are Naiadita lanceolata J.P. Brodie., from the Late Triassic of England, putatively related to Sphaerocarpales (Schuster, in Krassilov and Schuster, 1984), and Marchantites cyathodoides (Townrow) H.M. Anderson, from the Late Triassic of S. Africa, a liverwort that has a two-layered thallus with air chambers and an epidermis with pores, considered closely related to the Marchantiales (Krassilov and Schuster, 1984). No age constraints were enforced among mosses. Fossil mosses either indicate minimum ages that are so young that they will have no effect on the analyses, or are not well enough characterized to be used as minimum age constraints. Although a number of works (e.g., Oostendorp, 1987; Krassilov and Schuster, 1984) have discussed the variety of fossil mosses currently known, in the majority of cases the plants cannot be confidently assigned to the extant taxa in such a way as to provide dates for specific nodes.

17.2.6 LINEAGE DIVERSIFICATION DATA The most recent classification of mosses (Goffinet and Buck, 2004) and data from the Checklist of Mosses (http://www.mobot.org/mobot/tropicos/most/checklist.shtml [Crosby et al., 1999, update February 2000]), were used to estimate species-, genus- and family-level diversity in different lineages. To evaluate temporal variation in rates of diversification, an LTT plot was calculated based on the 100 calibrated phylogenies resulting from our age estimation analyses.

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51 50

53 52

54

49

55

47

56

57 60 59

61 62

58 63 64

65

67

68 69 70

66

71

72

73 75 76 74 78

79

80

81 83

84 85

87

82

90

88 91 92

86

93

89

94

95

96 97 98

Silurian

Devonian

Palaezoic

Carboniferous

Permian

Trias

Jurassic

Mesozoic

E. Cretaceous

77

)

48

46

)

45

%

44

(1 8. 7%

43

42

.1

41

(4 0

40

e

39

an ae

36 38 37

na

33

35

ry

34

)

32 31

.2 %

30 29

(1

26 27

)

25 28

01

%

24

.3

23

(0

22

ae

19 20

21

na

18 17

H yp

16

07

*a *n Po pe em ly ris rid at tric to ae od ha m at (4 ont les e D . ( m 4 ic m % os 1.7 ra os ) se %) ni se da s s (0 e (3 .3 (3 .0 % 0. % ) 3% ) )

15

08

na

14

13

Fu

12

*B

11

10 09

02

Blasia Sphaerocarpos Marchantia Conocephalum Monoclea Lophocolea Plagiochila Jungermannia Diplophyllum Scapania Ptilidium Porella Lepidolaena Frullania Nipponolejeunea Lejeunea Aphanolejeunea Austrolejeunea Mastigolejeunea Trocholejeunea Metzgeria Verdoornia Pellia Calycularia Fossombronia Phyllothallia Moerckia Hymenophyton Symphyogyna undulata S. brongniartii Pallavicinia Podomitrium Haplomitrium Treubia Equisetum Osmunda Magnolia Oryza Zea Cycas Ginkgo Pinus Selaginella Isoetes Huperzia Lycopodium Anthoceros Notothylas Sphagnum Takakia Andreaeobryum Andreaea Oedipodium Alophosia Dawsonia Atrichum Polytrichum Tetraphis Buxbaumia Diphyscium Bryobrittonia Encalypta Funaria Grimmia Ptycomitrium Dicranum Fissidens Dicranoweisia Schistostega Ceratodon Pottia Tortula Scouleria Timmia Leptobryum Splachnum Bryum Rhodobryum Orthotrichum Ulota Hedwigia Philonotis Plagiopus Pohlia Mnium Plagiomnium Pyrrhobryum dozyanum P. medium P. spiniforme Calomnium Cryptopodium Goniobryum Rhizogonium distichum R. graeffeanum R. novae−hollandiae Leptotheca guadichaudii Orthodontium Hymenodon Leptotheca boliviana Hypnodendron Spiridens Cyrtopus Bescherellia brevifolia B. cryphaeoides Powellia Racopilum spectabile R. cuspidigerum Braithwaitea Pterobryella Pyrrhobryum bifarium P. vallis−gratiae Mesochaete Aulacomnium turgidum A. androgynum Hampeella Ptychomnion Glyptothecium Euptychium Garovaglia Cyathophorum Hypopterygium Lopidium Pseudocryphaea Rutenbergia Trachyloma Hookeria Crossomitrium Leucomium Catagonium nitens C. brevifolium Lepyrodon Fabronia Pilosium Stereophyllum Hypnum cupressiforme Neckera Pterogonium Rhytidiadelphus Brachythecium Eurhynchium Leucodon Hypnum lindbergii Entodon Thuidium Pterobryon Cryphaea Jaegerina Orthostichopsis Fontinalis Ancistrodes Plagiothecium

ia na e

06

on

05

og

04

hi z

03

100 Myr

*R

200 Myr

m ni an

300 Myr

Pt yc ho

400 Myr

L. Cretaceous

Cenozoic

FIGURE 17.1 Chronogram of the embryophyte lineages. Results from the phylogenetic analyses are presented as a calibrated all-compatible majority rule consensus tree. Numbered nodes are all supported by 95% or higher posterior probabilities. See Table 17.1 for molecular age estimates and age constraints. The root node (1: crown group embryophytes) was used as the calibration point, with the age fixed at 450 myr in all divergence time analyses. Seven minimum age constraints were enforced, mostly in the tracheophytes (nodes 4 and 29 to 32, see text for details). The tree is rooted on two exemplars of the streptophyte algae (Chara in the Charales and Chaetosphaeridium in the Coleochaetales, not shown). Species diversity (%) contributed by each named lineage is shown on the right (see Table 17.1 for lineage circumscription).

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17.3 RESULTS 17.3.1 PHYLOGENETIC ANALYSES Results from the phylogenetic analyses are presented as a calibrated all compatible majority rule consensus tree in Figure 17.1. Numbered nodes are all supported by 95% or higher posterior probability. The tree is rooted on two exemplars from the streptophyte algae (Chara in the Charales and Chaetosphaeridium in the Coleochaetales) that were pruned from the figure. These taxa were included in the phylogenetic analyses only for rooting purposes and in the r8s analyses for obtaining branch length estimates of the first land plant dichotomy. The four land plant clades (liverworts, hornworts, mosses and tracheophytes) are all resolved as monophyletic, although liverworts (87%) and tracheophytes (90%) are supported by less than 95% posterior probability. Hornworts (node 38), mosses (node 39) and tracheophytes together form a monophyletic group (90%) with liverworts as sister. Hornworts are the sister group to mosses and together they constitute a well-supported (100%) group resolved as sister group to the tracheophytes. In mosses (node 39), Sphagnum and Takakia are grouped together (88%) and as sister to a well-supported clade (node 40) including all remaining taxa. Aperistomate and nematodontous mosses constitute a paraphyletic grade of taxa including: 1. 2. 3. 4. 5.

The The The The The

two other taxa with linear capsule dehiscence (Andreaeobryum and Andreaea) operculate but aperistomate Oedipodium monophyletic nematodontous clade Polytrichales (node 43; 100%) nematodontous Tetraphis transitional taxa Buxbaumia and Diphyscium

Within the arthrodontous mosses (node 47; 100%) Funaridae, including Encalyptales and Funariales (node 48; 100%) and the haplolepidous mosses (Dicranidae, node 49; 96%), are grouped and resolved as sister to the mosses with diplolepidous-alternate peristomes (node 58; 100%). In the diplolepidous-alternate mosses (node 58), a clade containing the Splachnales (node 60; 100%), Orthotrichales (node 62; 100%) and Bryaceae (node 61; 100%) is sister to the remaining taxa. The remainder of the acrocarpous Bryanae form a paraphyletic grade. Pleurocarpous taxa (node 66; 100%) form a monophyletic group. However, a few acrocarpous and anomalous taxa are nested within this pleurocarpous clade. The backbone of the topology in the pleurocarpous clade is largely unsupported, particularly in Rhizogonianae which is here resolved as a paraphyletic grade. Within the hypnidaean pleurocarps (node 82; 100%), Ptychomnianae (node 83; 100%) is monophyletic and grouped sister to Hypnanae (node 86; 100%), which in turn includes a monophyletic Hypopterygiaceae (node 87; 100%), Hookeriales, and the Hypnales. Neither Hookeriales nor Hypnales are here resolved as monophyletic groups.

17.3.2 DIVERGENCE TIMES Divergence time estimates are reported for nodes that received 95% or higher posterior probability in the phylogenetic analyses. Estimates are reported in Table 17.2 and in the form of a chronogram in Figure 17.1. Node numbers in Table 17.2 correspond with those used in the chronogram, and specific ages in the chronogram correspond to the point estimates in Table 17.2, obtained for the all compatible majority rule consensus tree. Table 17.2 further reports the mode (the most likely divergence time value under the specified model) and lower and upper HPD values (limiting the 90% confidence interval for this estimate) as calculated over the 100 trees and parameters randomly drawn from the posterior distribution.

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17.3.3 LINEAGE DIVERSIFICATION DATA Estimates of species-, genus- and family-level diversity in different lineages are summarized in Table 17.3, with classification based in part on that of Goffinet and Buck (2004), and in part on Crosby et al. (1999). Temporal variation in rates of diversification was evaluated in a LTT plot and reported in Figure 17.2. The plot is calculated across all age estimates obtained for the 100 trees randomly drawn from the posterior distribution. For comparison, corresponding curves calculated for angiosperms and polypod ferns by Schneider et al. (2004) are included in Figure 17.2.

17.4 DISCUSSION 17.4.1 MOSS RELATIONSHIPS The emphasis of the present analyses is on mosses, in particular pleurocarpous mosses, and although our analyses include a taxon sample covering all major groups of land plants, relationships among non-moss taxa will not be discussed here. Within mosses, the results from our phylogenetic analyses are largely congruent with those found in previous analyses (Newton et al., 2000; Bell and Newton, 2004, 2005, Chapter 3 in this volume; Cox et al., 2000, 2004; Cox and Hedderson, 1999). Sphagnum and Takakia group together and are placed as sister to the remaining mosses; aperistomate and nematodontous groups are resolved as a paraphyletic grade; Oedipodium is sister to the peristomate mosses as a monophyletic group (not well supported); Buxbaumia is sister to the monophyletic group of arthrodontous mosses (node 46; including Diphyscium); haplolepideous mosses (node 49; including Timmia) are monophyletic; and taxa with diplolepideous-alternate peristomes (node 58) form a monophyletic group. These patterns have all been hypothesized and supported by some of the previous analyses. Within the diplolepidous-alternate mosses, several previously recognized groups are well supported in our analyses, with the monophyletic group of pleurocarpous mosses emerging from a paraphyletic and unsupported grade of acrocarpous Bryales. The sister group to the pleurocarpous mosses cannot yet be confidently identified using molecular data. However, various morphological features in the possible candidates suggest that structural innovations converging on pleurocarpy may have been occurring in the ancestors of these groups. Resolution of this group of taxa using molecular data, and exploration of morphological features related to branching architecture and control of branch differentiation, will be necessary to address this problem. The monophyletic group of pleurocarpous mosses (from node 66) consists of a grade of small clades basal to the highly diverse clade of hypnidean pleurocarps (node 82). Several nodes within the grade are not supported at 95% posterior probability in our current analyses, but agree with results of our other analyses, especially with regard to clade composition (Bell and Newton, 2004, 2005). Individual clades within the grade show a diversity of fruiting modes, including pleurocarpy, acrocarpy and anomalous arrangements. Taxa are pleurocarpous and distal-fruiting (Bell and Newton, Chapter 3) unless noted otherwise. One clade (node 67) contains Pyrrhobryum dozyanum, the basal-fruiting species of Pyrrhobryum (node 68), and two acrocarpous taxa (Calomnium and Cryptopodium, node 69). A second clade (node 70) includes Goniobryum and basal-fruiting Rhizogonium (nodes 71, 72). A third clade (with less than 95% posterior probability but recognized by Bell and Newton, 2004, 2005) includes Hymenodon (basal fruiting), Leptotheca (acrocarpous) and the anomalous Orthodontium, which has a unique branching mode (Bell and Newton, Chapter 3). The fourth clade contains the hypnodendroid pleurocarps (Bell and Newton, 2005, node 74) and a clade containing Mesochaete, the remaining (distal-fruiting) taxa of Pyrrhobryum, and the acrocarpous Aulacomniaceae (node 81). The hypnodendroid pleurocarps are almost fully resolved (nodes 74 to 80), and in our other analyses this clade is strongly supported as sister to the hypnidaean pleurocarps. The presence of a variety of reproductive modes in the supported groups of rhizogonian

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TABLE 17.3 Species Diversity of Extant Moss Lineages Node 92 89(–92) 89 87 86 83 81 — 74 — 70 67 66(–82) 66

58(–66) 58 48

49

43

39–42

Clade or Grade Hookeriales “Hypnales” Hypnales + Hookeriales (pp) Hypopterygiales Hypnanae Ptychomniales Aulacomnuium “Pyrrhobryum clade” Hypnodendrales Leptotheca clade Rhizogonium clade Pyrrhobryum medium clade “Rhizogonianae” Pleurocarps s. l. Mniaceae Bartramiaceae Hedwigiaceae Splachnaceae/Meesiaceae Orthotrichaceae Bryaceae “Bryanae” Diplolepidous-alternate Funariales/Encalyptales Scouleriaceae Bryoxiphiales Grimmiales Archidiaceae Dicranales Pottiales Dicranidae Diphysciales Buxbaumiales Tetraphidales “Nematodont” mosses Polytrichales Oedipodiales Andreaeales Andreaeobryales Sphagnales/Takakiales “Aperistomate” mosses Total

Genera

Species

49 419 468 4 472 9 1 2 11 4 2 3 20 501 17 11 10 12 23 18 91 592 32 3 1 23 1 123 97 248 3 1 2 6 18 1 1 1 2 5 900

730 4414 5144 74 5218 42 6 5 106 23 9 8 157 5417 369 384 44 91 841 705 2434 7851 573 11 3 429 34 2045 1419 3941 21 12 5 38 218 1 95 1 290 387 13008

Clade or Grade % Total Species 5.61 33.93 P3 39.54 0.56 P2 40.10 0.32 — — 0.81 0.17 — — 1.2 P1 41.64 2.84 2.95 0.33 0.70 6.46 5.42 18.7 60.34 4.40 — — 3.29 0.26 15.72 10.90 30.29 0.16 — — 0.29 1.67 — 0.73 — 2.23 2.9

Note: P1, P2, P3 refer to principal nodes in the pleurocarp clade; grades are in inverted commas, taxa for which the total number of species represents less than 0.1% of total species are indicated as – in column five. Classification based on Goffinet and Buck, 2004, number of taxa taken from Crosby et al., 1999.

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1 0.95 0.9 0.85 0.8 0.75 0.7 0.65

Pleurocarp mosses Angiosperms 1 Angiosperms 2 Polypod ferns

0.6 0.55 0.5 0.45 0.4 0.35 0.3 0.25 0.2 0.15 0.1 0.05 0 240 250

230

220 200 180 160 140 120 100 80 60 40 20 0 210 190 170 150 130 110 90 70 50 30 10

FIGURE 17.2 Lineages-through-time (LTT) plot for pleurocarpous mosses calculated across age estimates obtained for 100 random trees drawn from the posterior distribution. The plots show number of lineages present at intervals of 10 myr as a proportion of the terminal taxa. Angiosperm and polypod fern plots from Schneider et al., (2004) are included for comparison. Their two plots for angiosperms (Angiosperms 1 and Angiosperms 2) result from analyses that used two alternative age constraints on the angiosperm crown group. Angiosperms 1 is strict and comes from analyses that fixed the angiosperm crown group at 132 myr. Angiosperms 2 results from more relaxed analyses where the same age constraint was applied as a minimum age constraint only, allowing older dates for the angiosperms.

pleurocarps implies a real pattern of diversity in reproductive modes during the period of origin of these groups. Within the hypnidean pleurocarps three deep internal nodes (82, 86 and 89) provide support for three principal clades. The Ptychomnianae (nodes 83 to 85) are sister to the Hypnanae (node 86) containing the Hookeriales (node 92) and the Hypnales. This relationship has been recognized recently in several studies (Buck et al., 2005; Pedersen and Newton, Chapter 18 in this volume; Shaw et al., 2003). However, within the Hypnanae, our results show the Hypopterygiaceae (node 87), which are placed by Goffinet and Buck (2004), in the Hookeriales, sister to a clade consisting of a paraphyletic Hypnales including the remainder of the Hookeriales. This result has been found in previous work (Newton and Cox, unpublished) using a different selection of taxa and gene sequence data, where it was also well supported. Buck et al. (2005), and Shaw et al. (2003), resolved both the Hookeriales and Hypnales as monophyletic; however, taxon sampling in these studies was somewhat different to that used here. Buck et al. (2005), included very few Hypnales in their analysis, while Shaw et al. (2003), used a much larger taxon selection but did not include most of the taxa that our analyses placed adjacent to the Hookeriales. Only a small proportion of the sub-clades and few of the mid-level nodes within the Hypnales and Hookeriales are supported, reflecting the impossibility of adequate sampling, for this study, within this massive clade. Of the nodes supported here, most are recognized in other studies, but few conclusions can be drawn from this about higher-level relationships within the Hypnales.

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Exceptions are the placement of Rhytidiadelphus sister (node 95) to the family Brachytheciaceae, represented by the exemplars of Brachythecium and Eurhyncium (node 96); and the three pairs of genera, Pilosium and Stereophyllum (node 94); Entodon and Thuidium (node 97); and Jaegerina and Orthostichopsis (node 98). In each case, these groups or pairs of exemplars belong to taxa that are sufficiently well known for these dated nodes to be placed in context.

17.4.2 ACROCARPY

AND THE

TRANSITION

TO

PLEUROCARPY

The transition from acrocarpy to pleurocarpy has proved problematic to resolve, but recent studies (Bell and Newton, 2004, 2005, Chapter 3; De Luna et al., 1999; O’Brien, Chapter 2) using comprehensive sampling and detailed morphological studies in combination with molecular sequence data from a range of genes has clarified the picture. The vast majority of pleurocarpous mosses fall into a single group that has long been recognized both with respect to general growth form and habit, and with regard to the single well-defined character (pleurocarpy) of formation of gametangia terminating lateral branches instead of main stems. A small number of taxa (e.g., Sphagnum, some members of Fissidens, a few small genera such as Mielichhoferia and Pleurochaete) have gametangia located terminally on short lateral branches, but these species are not closely related to the pleurocarpous mosses and the feature is therefore not considered homologous at this level, and such taxa are excluded from consideration here. However, the picture has been somewhat confused by the variations in expression of both growth form and the location of the gametangia so that “pleurocarpy” has come to be almost synonymous with a sprawling habit and various associated characteristics (discussed further in Newton, Chapter 14). Prostrate or pendulous growth occurs most widely in pleurocarpous mosses, but also occurs in certain acrocarps. Where these are clearly acrocarpous (e.g., Dicranoloma in the Dicranaceae) this has not been problematic. In contrast, a number of groups with highly reduced peristomes and less obvious affinities have traditionally been classified together in the pleurocarps, usually at the beginning of the Leucodontales, and with implications of primitive origins. These have included Wardia, Erpodium, Hedwigia and Bryowijkia, taxa that have prostrate growth and perichaetia that appear to be lateral; the Orthotrichaceae, in which several genera have main stems that are prostrate with erect vegetative branches terminated by perichaetia; and the Cryphaeaceae, where perichaetia terminate elongate modules that could variously be interpreted as stems or branches, or occur in clusters, with subperichaetial innovations forming a succession of perichaetial modules. Taxa in the Rhizogoniales have traditionally been considered to be the most derived members of the acrocarpous Bryales, with affinities to the Mniaceae and Bartramiaceae (Koponen, 1988). In many members of this group the main stems are erect and determinate with coarse, strongly toothed leaves, sporophytes are often formed in a basal position on the stem and with subperichaetial innovations, and peristomes are complete, with little of the reduction seen in many of the derived pleurocarpous mosses. It has been asserted (Koponen, 1988) that the reduced lateral perichaetial modules in plants such as Pyrrhobryum spiniforme represent reduced stems rather than reduced branches, and that they are therefore acrocarps rather than pleurocarps. The stems determinate and erect rather than indeterminate and prostrate are also cited by this author as evidence against accepting these taxa as pleurocarps. A number of recent morphological and molecular studies have helped significantly to clarify this situation. Careful dissection of members of the Hedwigiaceae revealed that the apparent lateral perichaetia terminate the main stem, but are pushed sideways by the growth of a new primary module immediately below the capsule (De Luna, 1990). Molecular data has shown that Wardia, Erpodium and Bryowijkia and other problematic taxa have affinities with the haplolepidous mosses, and that the Orthotrichales are closely related to the Bryales. The Crypheaceae are embedded within the pleurocarpous mosses, and the cladocarpous or acrocarpous perichaetial position and appearance of subperichaetial innovations in these taxa are therefore interpreted as derived rather than plesiomorphic. The Rhizogoniales remain in a transitional position between the acrocarpous Bryinae and

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the pleurocarpous Hypninae, exhibiting considerable diversity and parallelism in the morphology of the perichaetial position and form. In some taxa there appear to be reversals to an acrocarpous condition (Bell and Newton, Chapter 3). Despite these variations it is apparent that the pleurocarpous mosses represent a monophyletic group, within which various morphologies appeared in the ancestors of the extant lineages basal in the group, with one morphology eventually becoming “fixed” and the dominant form in the majority of extant pleurocarp lineages.

17.4.3 PATTERNS

OF

SPECIES-, GENUS-,

AND

FAMILY-LEVEL DIVERSITY

Assessing diversity by counting taxa inevitably reflects the taxonomic concepts used, and can only be an approximation, especially given that many of the taxa in question may continually be undergoing taxonomic modification. We chose to count species, genera and families as convenient measures of diversity, and although species per higher-level taxon will be somewhat variable depending on the classification used, the general patterns are similar. For example, in Hookeriales, Crosby et al. (1999) recognize 54 genera and 804 species in the six families usually placed in the Hookeriales (including Hypopterygiaceae but excluding Symphyodontaceae), whereas Buck and Goffinet (2000) recognize 48 genera and 743 species, and Goffinet and Buck (2004) accept 53 genera. The numbers cited here (Table 17.3, 49 genera and 730 species) reflect the classification of Crosby et al. (1999), but excluding the Hypopterygiaceae. An alternative method was used by Shaw et al. (2003), who calculated the molecular diversity in two chloroplast regions to obtain estimates of phylogenetic diversity (PD; Faith, 1992) in Hookeriales and Hypnales. Phylogenetic diversity reflects the sum of the branch lengths in the selected clade, expressed as a percentage of all branch lengths in the group under study. A clade in which average branch lengths are short will have a much lower PD than one in which the average lengths are long. However, this measure is susceptible to differences in taxon sampling between clades. Estimates of molecular diversity in these groups were found by Shaw et al. (2003) to disagree with estimates of biodiversity based on species numbers. Phylogenetic diversity in the Hypnales was found to be approximately half that in the Hookeriales, with branch lengths in the Hypnales sampled, on average, half the length of those in the Hookeriales. This is also strikingly apparent in phylograms of these taxa, where branch lengths in the Hookeriales are mostly relatively long, whereas those in the Hypnales, especially the interior nodes, are extremely short. A possible inference from this conclusion is that species diversity in the Hypnales is in part a taxonomic artefact. Nevertheless, the difference in species diversity between the Hookeriales and Hypnales (representing 14% and 86%, respectively, of the species diversity of the Hypnidae) is so great that it must reflect a real difference in species diversity between these taxa. The majority of extant species in the mosses are found in just three taxa, the Dicranidae (node 49) with 30% of the total species diversity, the Bryanae (paraphyletic between nodes 58 and 66) with 18% and the Hypnanae (node 86) with 40% (Figure 17.1). Although it is not apparent from the necessarily limited and stratified taxon sampling used to generate the tree topology, this diversity is further concentrated in a small number of groups (Table 17.3) within these three taxa: in the Dicranidae these are the Dicranales (15.7%) and Pottiales (10.9%); in the paraphyletic Bryanae, the Orthotrichaceae (6.5%) and Bryaceae (5.4%); and in the Hypnanae, the Hookeriales (5.6%) and Hypnales (33.9%). Within the Hypnales, 61% of the species diversity in the order is found in just four families (Brachytheciaceae 13.2%; Hypnaceae 20.6%; Neckeraceae 7.3%; and Sematophyllaceae 20%). The nodes subtending the three major taxa (Dicranidae node 50, paraphyletic Bryanae nodes 58 to 66, Hypnanae node 86) are dated within the Jurassic. However, much of the species diversity in these clades has arisen much more recently, during the Cretaceous or Cenozoic (Figure 17.1). The Pottiaceae (here with a distal node dated within the Cenozoic) are well known as a highly diverse but taxonomically difficult lineage (Zander, 1993) and at least the three most diverse of the pleurocarp families (Brachytheciaceae, Hypnaceae and Sematophyllaceae) are also problematic,

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with poorly differentiated taxa and morphological characters that are highly plastic and labile, features suggesting recent origin and active speciation (Vitt, 1984, p. 729). A similar asymmetry is evident in the clade of liverworts. Although the taxa selected mostly represent deeper nodes, and differences in diversity are not apparent from the chronogram, the leafy liverworts (node 9) contain at least ten times the species diversity of either of the other two major lineages, the complex thalloids (node 5) and the simple thalloids (paraphyletic, node 7 p.p.). Again, even within the leafy liverworts most of the diversity is found in a relatively small number of very large genera such as Frullania, Jungermannia, Plagiochila and Radula, or in the highly diverse family Lejeuneaceae (Gradstein et al., 2001; Paton, 1999).

17.4.4 DIVERSIFICATION

IN

PLEUROCARPOUS LINEAGES

Fossils of organisms that are clearly mosses exist from the Palaeozoic, from the Carboniferous and Permian periods onwards (see Krassilov and Schuster, 1984 and Oostendorp, 1987 for comprehensive discussion of these), but it is evident from our results that the majority of lineages of extant mosses originated in the Mesozoic, with considerable diversification occurring in the Cretaceous and in the Cenozoic (Figure 17.1). The LTT plot (Figure 17.2) allows comparison of the pattern of diversification of extant taxa in the pleurocarpous mosses with the equivalent curves for the angiosperms and polypod ferns as calculated by Schneider et al. (2004). Note that the shape of these plots is susceptible to differences in the sampling strategy (Nee et al., 1994; Pybus and Harvey, 2000; Shaw et al., 2003). Issues of systematic sampling bias were not explored by Shaw et al. (2003), who concentrated instead on the effect of randomized incomplete sampling, allowing them to accept or reject different models of diversification rates. Shaw et al. (2003) concluded that diversification in the Hypnales was extremely rapid during the first 20% of the evolutionary history of the order, but that diversification in the Hookeriales probably occurred at a constant rate thoughout. These patterns are not borne out in our analyses, and the LTT plot (Figure 17.2) indicates no significant changes or shifts in rates of diversification through time among pleurocarpous mosses. One possible reason for this discrepancy is our considerably less dense sample of species from Hypnales and Hookeriales. It is possible that by including a denser sample of species from these taxa, we would be able to identify an increase in diversification rate shortly after the origin of the Hypnales. Most relationships among the small number of hypnalean pleurocarps sampled for this study are poorly supported, with a multitude of alternative solutions with respect to both topology and branch lengths, and this in turn results in many possibilities with respect to divergence times. In our LTT plot we are unable to identify any changes or shifts in diversification rates during the evolution of pleurocarpous mosses. It is evident that LTT plots have to be interpreted with some caution. In Figure 17.2 the angiosperm and polypod lineage plots, as calculated by Schneider et al. (2004), are included for comparison. Angiosperms 1 is based on the strict (fixed) age constraint on the angiosperm crown group whereas Angiosperms 2 is based on the relaxed (minimum) age constraint of this node (Schneider et al., 2004). Under the strict model of angiosperm diversification, the initial diversification of the pleurocarpous mosses preceded that of the angiosperms, with approximately 50% of sampled lineages of both groups appearing about 100 mya. Under the relaxed model, in contrast, diversification of the pleurocarpous mosses shadowed that of angiosperms, with a similar slope but approximately 50 million years later.

17.4.5 THE ORIGIN OF PLEUROCARPY S. STR., AND THE IMPLICATIONS EVOLUTION OF THE PLEUROCARPOUS MOSSES

FOR THE

The morphological character “pleurocarpy” is viewed here in the strict sense, as the formation of archegonia on a reduced lateral module that has juvenile perichaetial leaves but lacks differentiated

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vegetative leaves at the time of archegonium initiation (Newton and De Luna, 1999). This is similar to the definition presented by La Farge-England (1996), but is in contrast to the more general concept of pleurocarpy. This refers primarily to the pleurocarpous habit of growth (e.g., Koponen, 1988; Meusel, 1935; Watson, 1968) typically (but not necessarily) with stems that (at least in part) are creeping, indeterminate and monopodial, and lateral sporophytes (see Newton, Chapter 14, for a more extensive discussion about branching architecture in pleurocarpous mosses). The clade in which pleurocarpy s. str. is first present among extant taxa corresponds to node 66, dated at 194–161 mya. Sampling in this region of the phylogeny was denser than elsewhere, in order to obtain a more detailed picture of the relationships of these taxa. The topology closely reflects that found in our other analyses (Bell and Newton, 2004, 2005, Chapter 3) but several nodes supported in those analyses were found here at less than the 95% posterior probability. As in the other analyses, taxa with a variety of arrangements of archegonia are found in four different clades arranged in a paraphyletic grade immediately distal to node 66. The perichaetia terminate primary modules in the acrocarpous Aulacomnium, Calomnium, Cryptopodium and Leptotheca, and also in the anomalous Orthodontium, which produces gametangia on a variety of module-based and adventitious structures. Perichaetia terminating lateral modules are found in the pleurocarpous taxa, but in some (Rhizogonium, the Pyrrhobryum medium clade, and Hymenodon) the perichaetial modules are formed only in a basal position (“basal-pleurocarpous”), while in the remaining taxa, perichaetial modules are formed in a variety of positions (“distal-pleurocarpous”). In all four clades combinations of acrocarpous, basal-pleurocarpous and distal-pleurocarpous mosses are found supported at 95% or greater posterior probability, with the exception of the clade containing the acrocarpous Aulacomnium, sister to the distal-pleurocarpous Mesochaete. Although this node is not supported in the present analysis, in Bell and Newton (2004) the clade was supported with 98% bootstrap. In all clades more distal in the topology (with the exception of obvious reversals in the derived Cryphaeaceae), plants are pleurocarpous with distal perichaetial modules. It therefore seems that, during a relatively short period of time between node 66 (194–161 mya) and node 82 (173–141 mya), considerable variation in the placement and form of the perichaetial module was occurring in the ancestors of the pleurocarpous mosses. Which of the morphologies seen in the extant taxa represent parallelisms and which are reversals has not yet been fully resolved (Bell and Newton, Chapter 3). The extant form, present now in all members of the pleurocarpous clade (with the noted exceptions) is that of reduced perichaetial modules formed in a variety of positions distally. Although, by these estimates, pleurocarpy first appeared in the Early to Middle Jurassic, it was not until sometime later that the diversification of extant lineages occurred, resulting in the current speciose Hypnales, with the attendant problems of short internal nodes and severe lack of resolution within the order. Although Shaw et al. (2003) and Buck et al. (2005) find support for three distinct orders (Ptychomniales, Hypnales and Hookeriales) using rps4 and trnL–trnF, the same genes plus rbcL consistently place several additional taxa from the Hypnales basal to the Hookeriales (Newton and Cox, unpublished data). Branch lengths subtending these taxa in phylograms (not shown) are very short, indicating the possibility that extensive diversification within pleurocarpous mosses followed the origin of the Ptychomniales but preceded the differentiation into Hypnales and Hookeriales. Unfortunately Shaw et al. (2003) excluded these pleurocarps from their analyses, concentrating on the three distal orders, so that nothing can be said from their results about diversification rates in the early period of pleurocarp evolution. Although these authors did not calculate absolute dates for the diversification of these taxa, they did state that the rapid diversification in the Hypnales occurred in approximately the first 20% of their evolutionary history. If node 89 (157–123 mya), which subtends both the Hypnalean and Hookerialean clades in our analysis, is taken as the point of origin of the extant Hypnalean lineages, this implies that the greatest diversification of this order occurred between 157 and 98 mya (Late Jurassic to Early Cretaceous). Despite this conclusion, it is evident that additional diversification undoubtedly occurred during later periods. Of the three most diverse lineages of hypnalean mosses (Hypnaceae, Sematophyllaceae and Brachytheciaceae), our sampling did not allow us to date nodes within the first two

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families. However, in the Brachytheciaceae we included two closely related exemplars, Brachythecium rutabulum and Eurhyncium (Kindbergia) praelongum, together with Rhytidiadelphus, a close outgroup (Huttunen et al., Chapter 6). Our results indicate that the family originated no earlier than the Late Cretaceous (node 95, 117–53 mya) and that diversification occurred significantly later, in the mid Cenozoic (node 96, 66–25 mya). Similarly, the Hypopterygiaceae originated during the Early Cretaceous with the divergence of Cyathophorum and the remainder of the family (node 87, 131–98 mya), with further diversification occurring during the early Cenozoic. The topologies found by Buck et al. (2005) and Kruijer (Chapter 4 in this volume) show Lopidium as sister to Hypopterygium and the other members of the family. Our results date this node (node 88) at 71–45 mya, which is consistent with the idea that much of the diversification in Hypopterygiaceae has been relatively recent. Similar patterns are seen in other groups. The clade containing the Hypnodendraceae, Racopilaceae, etc. (Figure 17.1) dates from the early Late Cretaceous (node 74, 123–87 mya) but the highly diverse Racopilum is more recent (node 79, 39–17 mya). The Ptychomniales originated between node 82 (172–140 mya) and node 83 (100–72 mya) but much of the diversification in the family is much more recent (node 84, 52–30 mya). In particular, the highly diverse and morphologically plastic genus Garovaglia (discussed by Pedersen, Chapter 18) diverged from Euptychium (node 85) only 28–16 myr ago.

17.4.6 PLEUROCARPOUS MOSSES

AND THE

ANGIOSPERMS

The date of the first appearance of the pleurocarpous clade in our analysis is somewhat later than the appearance of the early angiosperms, represented here by the split between the magnoliids and the monocots (node 32) at the date of 214–169 mya, but the most extensive diversification of the pleurocarpous mosses did not occur until considerably later (node 89, 157–123 mya). The two LTT plots for the angiosperms presented by Schneider et al. (2004) differ quite significantly in their implications regarding the influence of angiosperms on pleurocarpous moss diversification. Unlike the polypod ferns, in which diversification was shown to follow diversification of the angiosperms regardless of the application of the angiosperm fossil age (Schneider et al., 2004), in the pleurocarpous mosses diversification either precedes (fixed fossil age) or follows (minimum fossil age) diversification of the angiosperms. The fixed fossil age is naturally closely congruent with the abundant fossil history of the angiosperms (Crane et al., 1995; Friis et al., 1999; Wing and Boucher, 1998) and is also more in line with other analyses using sequence divergence data (Magallón and Sanderson, 2005; Bell et al., 2005; Soltis et al., 2002; Wikström et al., 2001). The LTT plot for angiosperms based on fixed fossil age therefore might be preferred over that based on minimum fossil age. Application of a minimum age constraint on the angiosperm crown group shows the diversification of the angiosperms preceding that of the pleurocarpous mosses by about 50 myr, with the trajectory of the pleurocarp LTT plot mirroring that of the angiosperms (Figure 17.2). The scenario that this seems to present, of the pleurocarpous mosses diversifying in response to the evolution of angiosperm forests, is most closely in accordance with thinking among bryologists (Shaw et al., 2003; Vitt, 1984). In contrast, with a fixed crown group age of angiosperms, the LTT plot shows the pleurocarps appearing approximately 60 myr before the angiosperms. The plots cross in the mid Early Cretaceous, at a period when approximately 50% of the sampled taxa had appeared in both lineages, implying that a large proportion of the pleurocarpous moss lineages had appeared prior to the appearance of the majority of angiosperm lineages. Combined with the conclusion of Shaw et al. (2003), that the Hypnales in particular diversified early in their history, this implies that pleurocarp diversification significantly preceded the angiosperm diversification. It must also be noted that, if the fossil record accurately reflects the diversity of terrestrial ecosystems, the dense, complex angiosperm forests that we currently know, with their rich diversity of habitats, would have appeared relatively late in the process of diversification of angiosperm lineages (Behrensmeyer, 1992) further emphasizing the uncoupling of pleurocarpous moss diversification from

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the appearance of angiosperm forest habitats. Evidence for the appearance of complex angiosperm forests varies. Most detailed studies have been restricted to northern America or Europe, and the pattern of diversification in other areas is less well known. In North America, there is evidence that, even as late as the Maastrichian of the Late Cretaceous, although angiosperm species diversity (especially dicots) accounted for as much as 68% of the taxonomic diversity in some forest habitats (Wing et al., 1993), the actual abundance was much less, amounting to no more than 12% cover. For the most part these consisted of herbs and shrubs, especially as early successional colonizers of disturbed and riparian habitats (Behrensmeyer, 1992; Crane, 1987; Wing et al., 1993; Wing and Boucher, 1998). In contrast, pteridophytes, gymnosperms, and to some extent monocotyledons, though with much lower species diversity, were probably ecologically dominant through the Late Cretaceous in all but disturbed and floodplain environments (Wing et al., 1993; Wing and Boucher, 1998). In addition, very little dicot wood has been found in the fossil record prior to the late Cretaceous, suggesting that large dicot trees were uncommon before the Cenozoic (Wing and Boucher, 1998) and the absence of liana-type leaves also suggests that complex, multilayered forest was absent (Wolfe and Upchurch, 1987). In lower palaeolatitudes, however, species diversification appears to have progressed earlier (Lupia et al., 2000), and closed canopy rainforest appeared in the equatorial moist climate zone in the Campanian to Maastrichtian (Morley, 2000). By the end of the Cretaceous and into the early Palaeogene angiosperms reached as much as 80% relative diversity and abundance (Lupia et al., 2000) and flowering plant trees and lianas dominated the Palaeogene (Collinson, 2000). The complex forest habitat with a wide diversity of habits and ecological roles characteristic of extant angiosperm forests would not have been a major element of terrestrial vegetation until at least this time, while the epiphytic and epiphyllous habitats occupied by bryophytes, especially pleurocarpous mosses and leavy liverworts, may not have appeared until significantly later. At present the relationships of most groups within the pleurocarpous mosses are poorly resolved or unsupported, so that it is not possible to propose dates for the appearance of any of the epiphytic clades. However, it is now widely accepted that different members of the largely epiphytic Leucodontales have arisen independently from within the Hypnales (in the traditional sense), reflecting convergence in response to ecological pressures (Buck et al., 2000), and in a study of one clade of pleurocarps, Huttunen et al. (2004), showed that epiphytic clades arose independently a number of times.

17.4.7 IMPLICATIONS FOR THE INTERPRETATION PLEUROCARPOUS MOSSES

OF

FOSSILS

OF

The majority of the moss fossil record cannot provide us with useful information about the possible ages of nodes, for the most part being too recent or too poorly characterized to be used as constraints or to contribute much to our understanding of the timing and sequence of evolutionary events (Krassilov and Schuster, 1984; Miller, 1984). However, our age estimates can possibly suggest something about our interpretation of the fossils. Only fossils credibly considered to be pleurocarpous are discussed here (see also Ignatov and Shcherbakov, Chapter 16). Among the older fossils, those from the Permian deposits that were considered by their authors to be possibly pleurocarpous (Permian Angaraland Uskatia [Neuberg, 1960], Rhizinigerites and Aristovia [Ignatov, 1990]; Lower Permian of Germany, unistratose lamina [Busche, 1968]) are considerably older (299–251 mya; all dates cited are from the International Commission on Stratigraphy www.stratigraphy.org) than the date that our results indicate for the origin of the pleurocarpous mosses (node 66, 194–161 mya). During this period a diverse bryoflora existed, some species of which possessed features that we now associate with the pleurocarpous clade, but with other unique features that have been lost from the extant flora. Evidence for a catastrophic die-back of terrestrial vegetation associated with the Permian-Triassic transition (Ward, 2000) at about 250 mya suggests that much of the existing bryoflora may have been wiped out at this point, with the surviving remnants providing the basis for further diversification. It is notable that the time spans in this area of the chronogram (around node 46 at 240 mya) are extremely long, although taxon sampling here

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(at the generic level) is almost complete. This suggests either very low rates of lineage origination, or extremely high rates of extinction. A few lineages persisted, notably the Sphagnales, Polytrichales and several aperistomate and nematodont lineages, together with the ancestor of the arthrodontous mosses. Patterns of diversification in each of these groups, at least based on observations of the extant taxa, seem to have been very different. The extant Sphagnales seem to represent a closely related group that diversified rather recently (Shaw et al., 2004). In contrast, the extant lineages of the Polytrichales show evidence of having diversified gradually over a long period of time (from 253–207 mya, node 43, Alophosia) with subsequent diversification (Koskinen and Hyvonen, 2004; Hyvönen et al., 1998, 2004). The fossil Eopolytrichum, dated at 84–71 mya (Konopka et al., 1997) was included in combined molecular and morphological analyses by Hyvönen et al. (1998). These authors placed Eopolytrichum within the diverse distal clade of Polytrichaceae, which is consistent with diversification of this clade relatively early compared with other groups. The aperistomate and nematodont lineages have very few extant taxa, while the arthrodontous mosses account for about 95% of all extant mosses, with several highly diverse groups (including the pleurocarpous mosses). Specimens from the Callovian–Oxfordian stages of the Jurassic (Muscites fontinaloides (Krassilov, 1973), and a previously undescribed taxon (Ignatov and Shcherbakov, Chapter 16) are both of interest as putative pleurocarps. They have structural features that are associated with modern-day pleurocarps, and are placed at a time during which it is highly likely that early pleurocarps would have existed. The material of Muscites fontinaloides consists of several stems with mostly broken leaves that are ecostate and carinate with short broad cells (30 × 11 μm), and also a possible sporophyte, which appears to have a short weak seta and to be partly immersed in a perichaetium. It is tempting to view the short subtending section of stem as evidence that the sporophyte was formed on a reduced lateral branch, although it could equally well be the result of damage to the plant before deposition or to the fossil subsequently. Additional material from this period would be of great interest for increasing our knowledge of the early evolution of the pleurocarps. Of the more recent fossils, Aulacomnium heterostichoides (Janssens et al., 1979), dated at 48–37 mya, is closely related to the remainder of the genus, and the age of this fossil is more or less consistent with our divergence-based estimate for node 81 (A. androgynum and A. turgidum) at 72–42 mya. In contrast, the fossil of the supposed Hypnodendron (Dixon, 1922), dated at 90–65 mya (Zherikhin and Ross, 2000), can be placed on the topology only as belonging somewhere in the Bryales, originating somewhere between nodes 58 (216–181 mya) and 82 (173–141 mya). It cannot be assigned to any extant genus with confidence, and indicates only that at least one additional lineage of the Bryales existed but went extinct before the present day.

17.5 CONCLUSIONS 17.5.1 PERICHAETIA TERMINATING LATERAL BRANCHES Was the appearance or stabilization of the feature of the perichaetia terminating lateral branches a key innovation that promoted or allowed the diversification of the pleurocarpous mosses? The lateral perichaetium appeared in the history of the pleurocarpous mosses at a much earlier date than the diversification of the extant lineages. Although we have no clues from fossils as to the actual rate of speciation, the number of extant species in lineages originating after the appearance of pleurocarpy and before the main diversification is relatively small. Stabilization of the lateral perichaetium into the “distal” form also appeared at a relatively early date. Lateral perichaetia are found in a number of other lineages, not closely related to the pleurocarpous moss clade, and with much lower species diversity, reinforcing the idea that possession of a lateral perichaetium, per se, does not immediately promote diversification. However, the development of lateral perichaetia does allow a much wider range of branching architecture (Newton, Chapter 14). The development of lateral perichaetia can therefore be proposed to be a key innovation that allowed further morphological innovation, although in itself it did not promote lineage diversification.

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17.5.2 DIVERSIFICATION

Pleurocarpous Mosses: Systematics and Evolution

OF THE

ANGIOSPERMS

Did the diversification of the angiosperms or the development of a landscape dominated by angiosperms, including complex forests, promote an adaptive radiation in the pleurocarpous mosses? If the minimum age constraint on the date of the angiosperm crown group is adopted, our results show that diversification of the pleurocarpous mosses followed that of the angiosperms by about 50 myr. This scenario is compatible with the diversification of the mosses in angiosperm forest, if it is accepted that complex forests did not appear until some time after diversification of the angiosperms. However, the LTT plot based on the fixed age constraint for the angiosperm crown group is in closer agreement with the fossil history. This constraint is preferred here, leading to the conclusion that pleurocarpous mosses originated and started to diversify before the origin of angiosperms, and significantly before the development of complex forests dominated by angiosperms. If initial diversification of the pleurocarpous mosses was an adaptation to a forest habitat, such a habitat would have been largely dominated by gymnosperms and ferns. However, the possibility that pleurocarp diversification was a response to an unknown factor cannot be rejected. Extant lineages of pleurocarpous mosses are found in a variety of forest habitats, including coniferous forest, are both terrestrial and epiphytic, and also occur in non-forest habitats such as fens and heaths. They also form a very important component (with the acrocarpous mosses) of the ground-level flora, promoting the formation of humus, and acting to stabilize the soil surface, reducing run-off, erosion and loss of minerals. Rather than the pleurocarpous mosses diversifying in response to the development of angiosperm forests, it is possible that the increasing complexity of the ground-level flora may have contributed to the general increase of complexity of terrestrial floras, including that of the angiosperms. If diversification of the pleurocarps was a response to an unidentified extrinsic event (including abiotic events such as climate change or geological activity, a possibility also suggested for polypod ferns by Schneider et al. 2004) it is possible that this same event also promoted the early diversification of angiosperms. In conclusion, the following scenario regarding the diversification of the pleurocarpous mosses can be drawn: During the Middle Jurassic, a variety of reproductive modes existed in the ancestors of the extant lineage of pleurocarpous mosses, with the “distal-pleurocarpous” mode becoming dominant by the Late Jurassic. Increases in species diversity and morphological complexity occurred in at least the ancestors of the extant hypnalean lineages in the Early Cretaceous, at about the time that angiosperm diversification was beginning to occur. Both diversification events may have been a response to an unidentified extrinsic factor. The majority of the ancestors of the pleurocarp lineages inhabited terrestrial habitats in simple ecosystems containing both gymnosperms and angiosperms, and very likely contributed to the evolution of complexity in the terrestrial ecosystems. When the complex angiosperm forest habitats developed somewhat later, in the early Cenozoic, further diversification in the pleurocarpous lineages occurred. Although according to the results of Shaw et al. (2003), this must have been at a rather lower rate than during the earlier diversification, this phase could have resulted in the appearance of the more specialist epiphytic taxa independently in a number of groups across the pleurocarpous mosses (Huttunen et al. 2004). It is worth noting that our results show that the major lineages of the Lejeuneaceae, the vast majority of which inhabit leaf surfaces in complex wet forest, originated in the early to mid Cenozoic. It is apparent that the evolution of the pleurocarpous mosses is considerably more complex than previously thought, and possibly also of more significance for the evolution of terrestrial ecosytems. However, many questions still remain unanswered.

ACKNOWLEDGMENTS Funding for this project from the National Environmental Research Council to Angela E. Newton in 2003 and from the Swedish Research Council (VR-2003-2541) to Niklas Wikström is gratefully

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acknowledged. A number of previously unpublished gene sequences were obtained by Cymon Cox with funding from the Museum Research Fund at NHM. Other gene sequence data for a number of taxa that were unpublished when this project was in progress were provided by several colleagues: many thanks for your assistance.

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and 18 Phylogenetic Morphological Studies within the Ptychomniales, with Emphasis on the Evolution of Dwarf Males Niklas Pedersen and Angela E. Newton CONTENTS Abstract ..........................................................................................................................................367 18.1 Introduction...........................................................................................................................368 18.2 Materials and Methods .........................................................................................................369 18.2.1 Taxon and DNA Sampling .......................................................................................369 18.2.2 DNA Extraction, PCR Amplification, and Sequencing...........................................369 18.2.3 Sequence Manipulation and Alignment ...................................................................372 18.2.4 Morphological and Habitat Characters ....................................................................372 18.2.4.1 Character and State Descriptions and Coding..........................................373 18.2.5 Phylogenetic Analyses..............................................................................................374 18.2.6 Reconstruction of Morphological Character States.................................................375 18.2.7 Tests of Correlated Evolution ..................................................................................375 18.3 Results...................................................................................................................................376 18.3.1 DNA Sequence Data ................................................................................................376 18.3.2 Phylogenetic Analyses..............................................................................................376 18.3.3 Reconstruction of Morphological Character States.................................................377 18.3.4 Tests of Correlated Evolution ..................................................................................383 18.4 Discussion.............................................................................................................................383 18.4.1 Phylogenetic Relationships and Taxonomic Consequences ....................................383 18.4.2 Reconstruction of Morphological Character States.................................................384 18.4.3 Tests of Correlated Evolution ..................................................................................389 18.5 Concluding Remarks and Future Research Needs ..............................................................390 Acknowledgments ..........................................................................................................................391 References ......................................................................................................................................391

ABSTRACT Phylogenetic relationships within the Ptychomniales were evaluated using maximum likelihood and Bayesian inference of chloroplast and mitochondrial DNA sequence data. Maximum likelihood and maximum parsimony were employed to study evolution of 18 morphological characters within 367

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the Ptychomniales, and maximum likelihood was used to test whether the evolution of dwarf males is correlated with morphological evolution and the epiphytic habitat. The Ptychomniaceae are paraphyletic to a monophyletic Garovagliaceae. The genus Glyphothecium Hampe is polyphyletic and Glyphothecium gracile (Hampe) Broth. is recognized as the monospecific genus Glyphotheciopsis gen. nov. Reconstructions of morphological characters under maximum likelihood and maximum parsimony are mostly congruent although maximum likelihood reconstructions indicate high uncertainties at most internal nodes. Correlation tests using maximum likelihood suggest that the evolution of dwarf males is significantly correlated with 12 of the morphological characters studied. In addition, the correlation tests indicate that the presence of dwarf males may promote morphological evolution.

18.1 INTRODUCTION Phyllodioicy is a reproductive strategy in mosses where reduced male plants germinate from spores on female plants. This strategy was first discovered in Fissidens Hedw. and Camptothecium Schimp. by Philibert (1883) and has later been described in several unrelated groups of mosses (Allen, 1935, 1945; Brotherus, 1924, 1925; Dening, 1935; During, 1977; Fleischer, 1904–1923; Ramsay, 1979; Woesler, 1935a, 1935b). In its most extreme form, the male plants are reduced to a few leaves and antheridia, germinated from spores established on the female plants. The underlying mechanisms of phyllodioicy have been little studied, although Loveland (1956) showed that dwarf males could be produced by chemical influence of female plants on germinating spores. This is contrasted by the studies of Ernst-Schwarzenbach (1939), who showed that sexual dimorphism in Macromitrium was genetically determined. An intriguing feature is that dwarf males occur most commonly in subtropical epiphytes (Ramsay, 1979). Although it could be argued that the proximity of male and female plants increases the likelihood of sexual reproduction and allows genetic variation that may confer an evolutionary advantage, it is unclear why it should be correlated with epiphytism (Ramsay, 1979). The evolution of dwarf males has never been studied in a phylogenetic context. If the presence of dwarf males confers an evolutionary advantage on the taxa in which they occur, it should be possible to demonstrate changes in morphological variability with the presence of dwarf males using phylogenetic methodology. This needs to be explored in a monophyletic group with variation in the expression of dwarf males. The order Ptychomniales, comprising the two families Garovagliaceae and Ptychomniaceae, is of a suitable size and sufficiently well known to be appropriate. Brotherus (1924, 1925), following Fleischer (1909), recognized the Garovagliaceae as the subfamily Garovaglioideae in the Pterobryaceae, whereas both authors recognized the Ptychomniaceae at the family level. This classification prevailed until Buck and Goffinet (2000) defined the family Garovagliaceae and placed it with Ptychomniaceae in the suborder Ptychomniieae in the order Hookeriales. Most recently, phylogenetic analyses by Buck et al. (2004) based on DNA sequence data resolved the Ptychomniaceae as paraphyletic to a monophyletic Garovagliaceae within a well-supported clade that is sister to the majority of the pleurocarps (Hypnanae). They synonymized the two families and placed them in their own order, the Ptychomniales, and Goffinet and Buck (2004) adopted this taxonomic concept in their most recent classification of mosses. The genera of the Garovagliaceae are Garovaglia Endl., Euptychium Schimp., and the monospecific Endotrichellopsis During. These taxa are differentiated by their tufted habit with erect, densely foliated stems with dense rhizoidal tomentum. The genus Garovaglia contains a considerable degree of morphological plasticity, which has led to extreme over-description of taxa although During (1977) reduced the number of taxa to a manageable level. In his monographic work, During (1977) divided Garovaglia into the six sections Baeuerlenia, Garovaglia, Aristatae, Endotrichum, Compressae and Angustifoliae. Euptychium is morphologically less plastic and During (1977) divided the genus into the two sections Euptychium and Crassisubulata.

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The Ptychomniaceae comprise the genera Ptychomnion Hook. f. & Wils., Cladomniopsis Fleisch., Cladomnion Hook. f. & Wils., Glyphothecium Hampe., Hampeella C. Müll., Tetraphidopsis Broth. & Dix., and Dichelodontium Hook. f. & Wils. In general, these taxa are recognized by 8-ribbed capsules with long rostrate opercula and rigid leaves that often are plicate and/or rugose. Ptychomnion is the largest genus and Brotherus (1925) divided the genus into two subgenera, namely, the now illegitimate Eu-Ptychomnion, with eight species, and Ptychomniella, containing the single species P. ptychocarpon. The Ptychomniaceae were revised by Hattaway (1984), who reduced the number of species from 24 to 16. The phylogenetic analyses by Buck et al. (2004) show that P. ptychocarpon is not closely related to the remainder of the Ptychomnion but should be recognized as Ptychomniella ptychocarpa Schwägr. The objectives of this chapter are several: first, to resolve phylogenetic relationships within the Ptychomniales using DNA sequence data; second, to reconstruct ancestral character states within the Ptychomniales; and third, to test whether the presence of dwarf males correlates to morphological characters and the epiphytic habitat.

18.2 MATERIALS AND METHODS 18.2.1 TAXON

AND

DNA SAMPLING

Thirty-one taxa were sampled from all of the genera within the Ptychomniales except Endotrichellopsis of which no recent material was available for molecular work. The species Hampeella concavifolia, described by Hattaway (1984), was also sampled, although the name is invalid because Hattaway never published the description. A recently collected specimen from Chile exhibiting features of the Ptychomniaceae (Bell, personal communication) was also included. Since the description will be published elsewhere (Bell et al., in prep) and to avoid creating a nomen nudum, the specimen is here denoted “Chilean specimen.” Adelothecium bogotense, Lepyrodon pseudolagurus and Rhytidiadelphus triquetrus were chosen as outgroups. The taxa included in the phylogenetic analyses are listed in Table 18.1 with GenBank accession numbers, voucher information, and authors of Latin names. Sequences were obtained for four chloroplast genomic regions: rps4, rbcL, the trnL (UAA) 5 exon–trnF (GAA) region (trnL–F), and the trnG (UCC) intron (trnG), plus the mitochondrial NADH protein-coding subunit 5 (nad5).

18.2.2 DNA EXTRACTION, PCR AMPLIFICATION,

AND

SEQUENCING

Total genomic DNA was extracted using the protocol of Doyle and Doyle (1987), modified as described in Shaw (2000), cleaned using the GFX PCR DNA purification kit (Amersham Biosciences, Little Chalfont, UK), and diluted in 50 μl nanopure water. Polymerase chain reactions (PCR) were prepared using 2.5 units Taq polymerase in a 25 μl reaction volume (1× thermostable buffer, 2.5 mM MgCl2, 100 μM dNTPs, 10 μM primer). Double-stranded DNA templates were prepared with 30 to 35 cycles, preceded by an initial melting step of 5 min at 94°C and followed by a final extension period of 7 min at 72°C. For each genomic region, PCR was optimized as follows: rps4 and trnL–F — 94°C (30 sec), 50°C (30 sec), 72°C (1 min); trnG — 94°C (30 sec), 52°C (30 sec), 72°C (1 min); rbcL and nad5 — 94°C (30 sec), 48°C (30 sec), 72°C (2 min). The primer sets trnC and trnF (Taberlet et al., 1991) and rps5 and trnas (Nadot et al., 1995) were used for the amplification of the trnL–F region and the rps4 gene, respectively. Amplification products for the trnG intron were accomplished by using the primer combination trnGF and trnGR (Pacak and Szweykowska-Kulinska, 2000). The rbcL gene and the nad5 region were both amplified as two overlapping fragments using the primer combinations M34–M740 and M636–M1390 for rbcL (Manhart, 1994) and nad5K–nad5Li and nad5Ki–nad5L for nad5 (Beckert et al., 1999). Amplified fragments were cleaned using the GFX PCR DNA purification kit and eluted in 20 to 50 μl nanopure

Fife, 10610 (CHR) Buck, 41360 (NY) MacMillan, BH 99/14 (CHR) Höhe, CH00-51 (NY) Bell, 542 (BM) / Newton 5694, (BM) Newton, 5679 & 5682 (BM) Newton, 6555 (BM) Newton, 5407 (BM) Bell, 1144 (BM) Newton, 5489 (BM) Bell, 1013 (BM) Bell, 1058 (BM) Santori, 31/10/2000 (BM) Bell, 1042 (BM)

Ingroup

Pedersen, 9/04 (BM) / Bell, 798 (BM)

Outgroup Vital & Buck, 19649 (NY) / Churchill et al., 15385 (NY)

Voucher Information

AY306884 AY306883 AY449664 DQ186840 DQ186841 DQ186842 DQ186843 DQ186844 DQ186849 DQ186845 DQ186846 DQ186847 DQ186848 DQ186850

AY306856 AF143014 DQ186851

rps4

AY306718 AY306717 AY449670 DQ194220 DQ194221 DQ194222 DQ194223 DQ194224 DQ194229 DQ194225 DQ194226 DQ194227 DQ194228 DQ194230

AY306690 AF161107 AF397811

trnL

DQ196077 DQ196078 DQ196091 AY631183 AY524435 DQ196092 DQ196093 DQ196098 DQ196094 DQ196095 DQ196096 DQ196097 DQ196099

DQ194232 DQ194248 DQ194249 DQ194250 DQ194251 DQ194252 DQ194253 DQ194254 DQ194255 DQ194256 DQ194257 DQ194258

AY524436

AB103354

rbcL

DQ194231

DQ194259

trnG

DQ200896 DQ200897 DQ200898 DQ200899 DQ200904 DQ200900 DQ200901 DQ200902 DQ200903 DQ200905

AY452418 AY452335 AY452347

Z98971

AY452318

nad5

370

Ptychomniaceae Cladomnion ericoides (Hook.) Wilson Cladomniopsis crenato-obtusa Fleisch. Dichelodontium nitidum (Hook. f. & Wilson) Broth. Glyphothecium gracile (Hampe) Broth. Glyphothecium sciuroides (Hook.) Broth. Hampeella alaris (Dixon & Sainsbury) Sainsbury Hampeella concavifolia Hattaway* Hampeella pallens (Sande Lac.) M. Fleisch. Ptychomniella ptychocarpa Schwägr. Ptychomnion aciculare (Brid.) Mitt. Ptychomnion cygnisetum (Müll. Hal.) Kindb. Ptychomnion densifolium (Brid.) A. Jaeger Ptychomnion falcatulum Broth. Ptychomnion subaciculare Besch.

Adelothecium bogotense (Hampe) Mitt. Lepyrodon pseudolagurus B.H. Allen Rhytidiadelphus triquetrus (Hedw.) Warnst.

Taxon

TABLE 18.1 Taxa Sampled in this Study with GenBank Accession Numbers and Voucher Information

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Newton, 5373 (BM) Crosby, 14280 (NY) Streimann, 50150 (NY) Streimann, 56055 (CBG) Crosby, 81325 (CBG) Buck, 7255 (NY) Stephen et al., SBC6351 (SINU) Schumm & Schwarz, 4719 (SINU) Iserentant, n B-73 (NY) Raymod et al., SBC6376 (SINU) Newton, 5465 (BM) Ellis, BF9512 (BM) Newton, 6496 (BM) Sloover, 43.136 (BM) Norris, 65427 (BM)

Garovagliaceae Euptychium cuspidatum (Mitt.) Mitt. Euptychium dumosum (Besch.) Broth. Euptychium mucronatum Hampe Euptychium robustum Hampe Euptychium setigerum (Sull.) Broth. Euptychium vitiense Dixon Garovaglia angustifolia Mitt. Garovaglia baeuerlenii (Geh.) Paris Garovaglia binsteadii (Broth.) During Garovaglia compressa Mitt. Garovaglia elegans (Dozy & Molk.) Hampe Garovaglia plicata (Brid.) Bosch & Sande Lac. Garovaglia powellii Mitt. Garovaglia subelegans Broth. Garovaglia zantenii During DQ186829 DQ186830 DQ186831 AY306907 DQ186832 AY306909 DQ186833 DQ186834 AY306913 AY306914 DQ186835 DQ186836 DQ186837 DQ186838 DQ186839

DQ219413 AY307001

DQ194209 DQ194210 DQ194211 AY306741 DQ194212 AY306743 DQ194213 DQ194214 AY306747 AY306748 DQ194215 DQ194216 DQ194217 DQ194218 DQ194219

DQ219414 AY306835

DQ194233 DQ194234 DQ194235 DQ194236 DQ194237 DQ194238 DQ194239 DQ194240 DQ194241 DQ194242 DQ194243 DQ194244 DQ194245 DQ194246 DQ194247

DQ222848

DQ196090

DQ196082 DQ196083 DQ196084 DQ196085 DQ196086 DQ196087 DQ196088 DQ196089

DQ196079 DQ196080 DQ196081

DQ219412 DQ196100

DQ200894 DQ200895

DQ200892 AY452354 AY452355 DQ200893

AY452435

AY452352

DQ200890 DQ200891

DQ219411 DQ200906

Note: Sequences generated for this study are in bold text. Herbarium acronyms follow Holmgren & Holmgren (www.nybg.org/bsci/ih). An asterisk indicates that the name is not effectively published and therefore invalid.

Bell, 1247 (BM) Höhe, 775 (CHR)

Chilean specimen Tetraphidopsis pusilla (Hook. f. & Wilson) Dixon

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water, depending on the amount of amplification product obtained. Sequencing was performed using each amplification primer in conjunction with the ABI BigDye Terminator Cycle Sequencing Reaction Kit on an ABI PRISM 377 automated sequencing machine.

18.2.3 SEQUENCE MANIPULATION

AND

ALIGNMENT

Nucleotide sequences were edited and forward and reverse sequences assembled with Sequencher 3.1 (Genes Code Corporation). The assembled sequences were aligned manually using Se-Al v 2.0 (http://evolve.zoo.ot.ac.uk/software.html?id=seal). Regions of incomplete data and ambiguous alignment were identified and excluded from subsequent analyses.

18.2.4 MORPHOLOGICAL

AND

HABITAT CHARACTERS

Eighteen morphological characters and one habitat character were chosen for reconstruction of ancestral states and correlation studies. The characters included are listed below and the character matrix is presented in Table 18.2. A list of the specimens used for the anatomical and morphological

TABLE 18.2 Morphological Character Matrix for the Taxa Studied Character No.

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

Rhytidiadelphus triquetrus Cladomnion ericoides Cladomniopsis crenato-obtusa Dichelodontium nitidum Euptychium cuspidatum Euptychium dumosum Euptychium mucronatum Euptychium robustum Euptychium setigerum Euptychium vitiense Garovaglia angustifolia Garovaglia baeuerlenii Garovaglia binsteadii Garovaglia compressa Garovaglia elegans Garovaglia plicata Garovaglia powellii Garovaglia subelegans Garovaglia zantenii Glyphothecium gracile Glyphothecium sciuroides Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion densifolium Ptychomnion falcatulum Ptychomnion subaciculare Tetraphidopsis pusilla

0 1 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 1 1 1 1 1 0

0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 0 0 0 0 0 0 0

0 1 0 0 1 1 1 1 1 1 0 1 1 0 0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0

1 1 0 1 1 1 1 1 1 1 1 1 1 1 0 1 1 0 0 0 0 0 0 0 0 1 1 1 0 1 0

1 0 1 1 1 1 1 1 0 0 1 1 1 1 1 1 0 1 1 0 0 0 0 1 0 1 1 0 0 1 0

1 1 1 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 1 1 1 1 1 1 0

1 1 0 0 0 0 0 0 0 0 1 1 1 0 0 1 0 0 0 0 0 0 0 0 0 1 1 0 0 1 0

0 0 0 0 0 1 0 0 1 0 0 0 1 0 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0

1 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 0

0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 1 1 0 1 1 0

1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 1 0

0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 0 0 0 1 1 1 1 1 1 0

0 0 0 0 1 0 0 0 1 0 1 1 1 1 1 1 1 1 0 1 1 1 1 1 0 0 0 0 0 0 1

0 0 0 0 1 1 1 1 1 1 0 1 1 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1

1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 1 1 0

0 0 0 1 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 1

0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0

0 1 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1

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373

studies is available from the first author. All the morphological characters were scored as binary characters because the computer program Discrete (Pagel, 2002), which was used in the present study, is designed for reconstruction of ancestral character states and correlation studies of binary characters. Consequently, any multistate characters have to be excluded or changed into binary ones. Alternatively, the program Multistate (Pagel, 2003), which can handle characters with up to six states, can be used for reconstruction of ancestral states. Unfortunately, Multistate is not intended for studies of correlated evolution among characters and to avoid scoring some characters as multistate for the reconstruction of ancestral states, and then subsequently changing these characters into binary ones for the correlation studies, we chose to use binary characters for the reconstruction of ancestral character states. 18.2.4.1 Character and State Descriptions and Coding 1. Dwarf males absent (0) or present (1). Garovaglia has the simplest dwarf males consisting of a few leaves with antheridia and some paraphyses. In Euptychium, Ptychomnion and Cladomnion ericoides they are larger and branched. During (1977) mentions that the larger males occur in some species of Garovaglia also but this could not be confirmed. 2. Germination normal (0) or precocious (1). In Hampeella, Glyphothecium and Cladomnion, spores may germinate before they are released from the capsule. 3. Perichaetial leaves attached on lower 1/4 of vaginula (0) or along its whole length (1). During (1977) used perichaetial leaves that are attached along the whole length of the vaginula as a diagnostic feature of Euptychium and some sections of Garovaglia, but the feature is present in Cladomnion as well. 4. Leaves flaccid (0) or slightly stiff to rigid (1). In most species of Garovaglia and Ptychomnion the leaves are slightly stiffened, whereas rigid leaves are characteristic of Euptychium. 5. Leaves flat to slightly concave (0) or strongly concave to tubular (1). Tubular leaves are present in Euptychium, although E. setigerum has flat leaves. 6. Leaves not plicate (0) or plicate (1). Plicate leaves occur in all genera except Dichelodontium, Hampeella and Tetraphidopsis. 7. Leaves not rugose (0) or rugose (1). Rugose leaves are relatively rare within the Ptychomniales but are present in Cladomnion and some species of Garovaglia and Ptychomnion. 8. Leaves without (0) or with (1) dorsal teeth. This character is extremely variable, particularly within Garovaglia. The leaves of G. angustifolia lack dorsal teeth, those of G. plicata are short and rarely more than five per leaf, whereas the leaves of G. subelegans can have up to 50 dorsal teeth. Also, in some species, both dorsal and ventral teeth are present (e.g., G. binsteadii). 9. Leaf margin entire (0) or serrulate to serrate (1). Entire margins occur only in a few taxa of the Ptychomniaceae. 10. Stem without (0) or with (1) paraphyllia. Paraphyllia are present in Cladomnion, Glyphothecium and Ptychomnion, either as few patches or continuously along the stem. 11. Setae less than 5 mm long (0) or longer (1). In taxa with short setae the capsules are either immersed, with the capsules exceeded by the perichaetial leaves, or emergent, with the capsules partly projecting beyond the tips of the perichaetial leaves. These states were used by During (1977) but they reflect the length of the perichaetial leaves rather than seta length. 12. Annulus present (0) or absent (1). All taxa of the Garovagliaceae plus Dichelodontium, Ptychomniella and Ptychomnion lack an annulus. 13. Filamentous gemmae absent (0) or present (1).

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14. Calyptra cucullate (0) or mitrate (1). Mitrate calyptrae is the most common condition within the Ptychomniales, but cucullate calyptrae occur in all Euptychium and some Garovaglia species. 15. Capsule smooth (0) or with 8 longitudinal ridges (1). A furrowed capsule with eight longitudinal ridges is considered a diagnostic feature of the Ptychomniaceae. 16. Number of endostome cilia between processes 0–1 (0) or 2–3 (1). Most ingroup taxa have none or one rudimentary cilium but two to three cilia occur in species of Ptychomnion and Cladomniopsis. 17. Exostomes well developed (0) or reduced (1). The length of the exostome teeth was used to estimate the degree of exostome reduction. Taxa with exostome teeth up to 350 μm long were coded as reduced. 18. Inner perichaetial leaves smooth (0) or plicate (1). Plicate inner perichaetial leaves are rare within the Ptychomniales and only present in Garovaglia angustifolia, G. baeuerlenii, G. binsteadii and G. zantenii. 19. Species not epiphytic (0) or epiphytic (1). A species was scored as epiphytic if it occurs on living trees. This character was only used for the correlation studies.

18.2.5 PHYLOGENETIC ANALYSES Maximum parsimony (MP) and maximum likelihood (ML) analyses were conducted using PAUP 4.0b10 (Swofford, 2002). Bayesian analyses were performed using MrBayes v 3.0 (http://mrbryes.csit.fsu.edu) and P4 v 0.82 (http://www.nhm.ac.uk/research-curation/projects/ software/p4.html). To test for incongruence among the genomic partitions, nonparametric bootstrap analyses under MP were conducted for each partition. These analyses included only those taxa for which all partitions were available, using 300 replicates with one random addition sequence. The majority rule consensus trees of the analyses were compared to search for conflicting relationships supported by at least 70% (Hillis and Bull, 1993). An evolutionary model for the ML analysis was selected using MrModeltest 2.0 (Nylander, 2004). The chosen model (GTR + G + I) and its parameters were fixed in the subsequent ML analysis. Tree searches under the ML criterion were performed with the following settings: 100 replicates, TBR branch swapping, lset base=(0.3206 0.1780 0.1660), nst=6, rmat=(1.7698 5.8476 0.7901 1.4292 4.9448), rates=gamma, shape=0.7642, pinvar=0.4685. Homogeneous Bayesian analyses were conducted using four runs under the GTR + G + I model of evolution with the following settings: mcmc, startingtree=random, ngen=2000000, samplefreq=100, nchains=4, savebrlens=yes. The number of trees needed to reach stationarity (burn-in) was estimated by plotting ML scores of sampling points against generation time using the graphics program Gnuplot 3.8 (Williams and Kelley, 2002). The trees of the burn-in for each run were excluded from the tree set. Convergence between runs was checked by comparing the 95% majority rule consensus trees of each run in PAUP after the burn-in. The trees from each run were combined into one treefile and a 95% majority rule consensus tree was constructed in PAUP. Heterogeneous Bayesian analyses were also conducted. The dataset was divided into nine partitions; one for each of the trnL–F, trnG, and nad5 regions, and one partition for each of the codon positions of rps4 and rbcL. The following evolutionary models were selected by MrModeltest: trnL-F — HKY + G; trnG — GTR + G; nad5 — GTR + G; rps4 1st position — GTR + G + I; rps4 2nd and 3rd position — GTR + G; rbcL 1st position — GTR + G; rbcL 2nd and 3rd position — SYM + G. The analyses were conducted with the same settings as for the homogeneous analyses. The assessments of the burn-in and posterior probabilities were as described for the homogeneous analyses. To test if the heterogeneous model was a better fit to the data than was the homogeneous model, both models were optimized on the ML tree using p4 and compared using a likelihood ratio test statistic.

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18.2.6 RECONSTRUCTION

OF

375

MORPHOLOGICAL CHARACTER STATES

Sufficient material of Lepyrodon pseudolagurus and the “Chilean specimen” for morphological studies was not available and these taxa were pruned from the ML tree. Reconstruction of ancestral character states under MP was accomplished by mapping the morphological characters onto the pruned ML tree using MacClade 4.03 (Maddison and Maddison, 2001). An evolutionary model for the pruned ML tree was recalculated with MrModeltest. Since the molecular clock was rejected for the pruned dataset, the pruned ML tree was made ultrametric, assuming autocorrelation of rates among branches, using semiparametric rate smoothing in r8s (Sanderson, 2001). The most optimal smoothing parameter was obtained using a cross-validation procedure using penalized likelihood in conjunction with the truncated Newton algorithm. The optimization was conducted with 20 starts each with 20 perturbations, with the age of the ingroup arbitrarily set to 1. Adelothecium bogotense was initially used as the outgroup to obtain ingroup branch lengths and was subsequently pruned from the ML tree. ML reconstruction of morphological character states on the ultrametric tree was accomplished with Discrete (Pagel, 2002). Models allowing separate forward (α) and backward (β) transition rates (two-parameter model) were compared with models in which the transition rates were identical (one-parameter model). For each character, a likelihood ratio was calculated between the oneparameter and the two-parameter model and a χ2 statistic with a 0.05 confidence level and one degree of freedom was used to test if the two-parameter model was a significantly better fit to the data than was the one-parameter model. When this was not the case, the one-parameter model was used for reconstruction of ancestral states (Pagel, 1999). The transition rates of each character were fixed and used to calculate the likelihood of each node at a state 0 or 1, using local calculations (Pagel, 1999, 2002). Support for the ML estimates was accomplished by taking the ratio of the two likelihoods at each state and was considered significant if the ratio was at least 7:1 (Schluter et al., 1997).

18.2.7 TESTS

OF

CORRELATED EVOLUTION

Tests of correlated evolution of dwarf males with the remaining morphological features and the epiphytic habitat were conducted using Discrete (Pagel, 1999). This was accomplished by first fitting a model to the data in which the two characters were allowed to evolve independently. The likelihood of this model was then compared to the likelihood of a more complicated model in which the characters evolve in a correlated fashion, and a likelihood ratio was calculated between the dependent and the independent model to test if the more complicated model was a better fit to the data than was the model assuming independent evolution. A Monte Carlo simulation was run to obtain a null distribution for the test of correlated evolution (Pagel, 1994). This proceeded by first finding the ML estimates of the parameters of the model of independent evolution of the observed data. The null model was then generated by fixing these parameters and using them to evolve the two characters along the phylogeny. The null model was then analysed with the model of correlated evolution and the model of independence, and the likelihood ratio of the two models was found. The simulation procedure was run 100 times and the model of correlated evolution was accepted when less than 5% of the simulated likelihood ratios were greater than the observed ones. The hypothesis that a specific character state (the dependent Y variable in Pagel’s method) is more likely to evolve in the presence of dwarf males (the independent X variable) was also investigated. This was performed by testing whether the rate of the transition parameter (0, 0) → (0, 1) differs from the rate of the transition parameter (1, 1) → (1, 0) (q12 and q34, respectively, in Pagel, 1994)). In other words, it can be tested whether the two transition parameters differ against the null hypothesis that they are the same (Pagel, 1994). This was achieved by creating a sevenparameter model where the two parameters were set as equal and comparing this to an eight-

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parameter model in which the two parameters were free to vary. The likelihoods of the two models were then compared by means of a likelihood ratio test statistic and a χ2 statistic with a 0.05 confidence level and one degree of freedom was used to test if the full model was a significantly better fit to the data than was the null model. When the null model could not be rejected, the presence of dwarf males was set as the dependent (Y) variable to test if the presence of a specific character state (X) is likely to promote evolution of dwarf males. This was achieved by creating a seven-parameter model in which q13 = q24 (cf. Pagel, 1994) and comparing this to an eight-parameter model where the two parameters were free to vary. The likelihoods of the two models were then compared and tested as described above.

18.3 RESULTS 18.3.1 DNA SEQUENCE DATA Alignment of 35 taxa for the five genomic regions resulted in 5483 nucleotide sites (589 trnL–F, 723 rps4, 709 trnG, 1450 rbcL, 2012 nad5), of which 1355 sites were excluded due to areas of ambiguous alignment and missing data. Of the 4128 included nucleotide sites, 431 were parsimony informative (46 trnL–F, 98 rps4, 57 trnG, 136 rbcL, 94 nad5). The bootstrap analyses under MP revealed no conflict among partitions with regard to nodes supported by more than 70%, suggesting taxonomic congruence among partitions (results not presented).

18.3.2 PHYLOGENETIC ANALYSES The likelihood ratio test (LRT = –2 (ln (null/alternative)) of the homogeneous (-ln L = 19651.29688) and the heterogeneous (-ln L = 19268.7156495) model suggested that the heterogeneous model was a significantly better fit to the data than was the homogeneous model (LRT = 765.162461, d.f. = 66, p << 0.001). The topology resulting from the homogeneous analyses was identical to the heterogeneous one and is not further discussed. The single most likely tree of the ML analysis (-ln L = 19651.29688) with heterogeneous Bayesian posterior probabilities (BPP) is presented in Figure 18.1. On the first ingroup node, Hampeella is robustly supported as a monophyletic group (100% BPP). On the next node, Ptychomniella branches from the remaining taxa with high support (100% BPP). The next two nodes split Tetraphidopsis (100% BPP) and the “Chilean specimen” (97% BPP), respectively. Cladomniopsis is placed as sister to the large Glyphothecium gracile–Garovaglia subelegans clade, but without support. Glyphothecium gracile is robustly supported (100% BPP) as sister to the Cladomnion–G. subelegans clade. The latter clade is divided into one small and one large clade. The small clade is unsupported and includes Cladomnion, Dichelodontium and Ptychomnion, of which the latter two genera are resolved as sisters (100% BPP). Within Ptychomnion, P. aciculare is well supported (100% BPP) as sister to the robust P. falcatulum–P. subaciculare clade (99% BPP). A well-supported clade (100% BPP) comprising P. cygnisetum and P. subaciculare is resolved as sister to P. densifolium, but with no support. The large clade is robustly supported (97% BPP) and consists of Glyphothecium sciuroides, plus a clade comprising the monophyletic genera Euptychium (100% BPP) and Garovaglia (100% BPP). On the first node of the Euptychium clade, E. setigerum branches from the remaining taxa with high support (100% BPP). Phylogenetic relationships within the rest of Euptychium are mainly without support, but E. cuspidatum and E. vitiense form a robust clade (100% BPP) and E. dumosum is strongly supported as sister to the E. cuspidatum–E. robustum clade (97% BPP). Two clades are recognized within Garovaglia. In the first clade, G. angustifolia is strongly supported (100% BPP) as sister to a robust clade including G. plicata and G. powellii (100% BPP). In the second clade, a robust clade (100% BPP) including G. binsteadii and G. zantenii is with high support (100% BPP) resolved as sister to the G. compressa–G. subelegans clade (100% BPP). Within this latter clade, G. compressa and G. elegans are successively resolved

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Adelothecium bogotense Lepyrodon pseudolagurus Rhytidiadelphus triquetrus

98

Hampeella alaris Hampeella concavifolia

100 100

Hampeella pallens

Ptychomniella ptychocarpa

100

Tetraphidopsis pusilla ‘Chilean specimen’

100 100

Cladomniopsis crenato-obtusa Glyphothecium gracile

97

Cladomnion ericoides Dichelodontium nitidum 100

Ptychomnion aciculare

100

Ptychomnion falcatulum

100

Ptychomnion densifolium

99

Ptychomnion cygnisetum 100

100 Ptychomnion subaciculare

Glyphothecium sciuroides Euptychium setigerum Euptychium dumosum 100 97

97

100

Euptychium cuspidatum

Euptychium vitiense Euptychium mucronatum Euptychium robustum

100

Garovaglia angustifolia 100

100

Garovaglia plicata Garovaglia powellii

Garovaglia binsteadii

100 100 100 100 0.005 substitutions/site

Garovaglia zantenii Garovaglia compressa Garovaglia elegans Garovaglia baeuerlenii Garovaglia subelegans

FIGURE 18.1 Phylogram of the most likely tree (–ln L = 19561.59688) obtained from the maximum likelihood analysis. Numbers below branches, or to the right when appropriate, indicate heterogeneous Bayesian posterior probabilities (≥95%).

as sisters to a clade comprising G. baeuerlenii and G. subelegans, but none of those inferences are supported.

18.3.3 RECONSTRUCTION

OF

MORPHOLOGICAL CHARACTER STATES

Reoptimization of the parameters for the pruned dataset resulted in a tree with likelihood –ln L = 18990.88851. Enforcing a molecular clock resulted in a tree with likelihood –ln L = 19187.62925; hence the pruned tree was significantly non-clocklike (LRT = 393.48148, d.f. = 32, p << 0.001). For two characters, namely, endostome cilia (16) and epiphytism (19), a model allowing different rates of forward and backward transitions was a better fit to the data than was the oneparameter model. Character transition rates and likelihood ratio statistics are presented in Table 18.3. MP and ML reconstructions of the 18 morphological characters are shown in Figure 18.2 and Figure 18.3, respectively. For the ML reconstructions, statistically significant reconstructions

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Pleurocarpous Mosses: Systematics and Evolution

TABLE 18.3 Morphological Character Transition Rates, Likelihood Ratio Test (LRT) Statistic and Probability (p-Value) Character

Transition Rate

LRT Statistic

p-Value

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

6.88739 6.91584 18.66611 42.49512 50.01137 6.66866 50.00114 17.82647 11.51096 7.30547 4.12565 8.47056 28.04100 12.24070 4.17565 α = 6.30229, β = 50.00847 6.56471 7.05837 α = 50.00776, β = 6.22875

2.7243 1.8588 1.6845 0.3168 0.0300 0.2225 3.4922 2.9819 0.3917 3.6741 2.2604 0.5726 0.0811 0.7804 0.0231 6.5815 1.6923 1.0850 4.6119

0.0988 0.6046 0.1943 0.5735 0.9886 0.6372 0.0617 0.0842 0.3817 0.0553 0.1327 0.4492 0.7758 0.3700 0.8792 0.0103 0.1933 0.2976 0.0318

Note: Forward (α) and backward (β) transitions are identical for characters 1–15 and 17–18.

at branches are indicated in grey for state “0” and black for state “1”, whereas pie-charts indicate relative support for the two ancestral states when reconstructions are not statistically significant (Figure 18.3). Both MP and ML reconstruct the absence of dwarf males (Figure 18.2A, Figure 18.3A) as the plesiomorphic condition for the Ptychomniales. Under MP, this character is ambiguously reconstructed at the most basal nodes of the large clade comprising Cladomnion, Dichelodontium, Ptychomnion, Glyphothecium sciuroides and the Garovagliaceae (Figure 18.2A). In contrast, ML reconstructs the absence of dwarf males as the most likely plesiomorphic state for this clade and the presence of dwarf males is therefore most probably an independent synapomorphy for each of Ptychomnion and the Garovagliaceae (Figure 18.3A). MP reconstructs precocious germination as a synapomorphy for Hampeella (Figure 18.2B), which also is suggested by ML although the reconstruction at the ingroup node is not statistically significant (Figure 18.3B). MP and ML both reconstruct inner perichaetial leaves that are attached at the base of the vaginula (Figure 18.2C, Figure 18.3C) as the plesiomorphic condition for the ingroup, although the ML reconstruction is not statistically significant at the ingroup node. Under MP, inner perichaetial leaves that are attached along the whole length of the vaginula provides a synapomorphy for Euptychium, the G. plicata–G. powellii clade, and the G. baeuerlenii–G. subelegans clade (Figure 18.2C). Under ML, however, this character state is reconstructed as a synapomorphy for the Garovagliaceae with further reversals in G. angustifolia, G. zantenii, G. compressa and G. elegans, but none of those inferences are statistically significant (Figure 18.3C). Under both MP and ML, stem leaf rigidity (Figure 18.2D, Figure 18.3D) is ambiguously reconstructed at most of the deeper branches of the ingroup. Stem leaf concavity is ambiguously reconstructed under both MP and ML (Figure 18.2E, Figure 18.3E).

A

C Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnioncygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

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Phylogenetic and Morphological Studies within the Ptychomniales 379

B

D

FIGURE 18.2 Maximum parsimony reconstructions of the 18 morphological characters. For each character, unambiguous reconstructions at branches are indicated in white for state “0” and black for state “1”. Hatched lines indicate equivocal reconstructions. (A) dwarf males (character 1); (B) germination (2); (C) attachment of perichaetial leaves (3); (D) leaf rigidity (4); (E) leaf concavity (5); (F) leaf plication (6); (G) leaf rugosity (7); (H) leaf dorsal dentation (8); (I) leaf margin dentation (9); (J) paraphyllia (10); (K) setae length (11); (L) annulus (12); (M) filamentous gemmae (13); (N) calyptrae (14); (O) capsule surface (15); (P) number of endostome cilia (16); (Q) exostome development (17); (R) inner perichaetial leaf plication (18). Continued.

Based on MP, stem leaf plicae (Figure 18.2F) is reconstructed as the plesiomorphic state within the Ptychomniales and smooth leaves as a synapomorphy for Hampeella. Under ML, smooth leaves are most likely a synapomorphy for Hampeella but without statistical support (Figure 18.3F). In addition, under ML, smooth leaves are reconstructed as the most likely state (53% of total likelihood) for the node on which Tetraphidopsis branches from the remaining taxa (Figure 18.3F). Both MP and ML suggest rugose leaves as a synapomorphy for the Ptychomnion cygnisetum–P. subaciculare split (Figure 18.2G, Figure 18.3G), although with considerable ambiguity under ML due to uncertainty in the ancestral state of its immediate ancestor (Figure 18.3G). MP unambiguously reconstructs the absence of dorsal teeth on the leaf lamina as the plesiomorphic condition for the

E

G

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

380

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

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Pleurocarpous Mosses: Systematics and Evolution

F

H

FIGURE 18.2 Continued.

ingroup (Figure 18.2H). Under ML, this condition is with statistical significance reconstructed as the ancestral character state at most of the deeper nodes of the phylogeny, except on the ingroup node (85% of the total likelihood) (Figure 18.3H). Furthermore, both MP and ML reconstruct the presence of dorsal teeth as a synapomorphy for the Garovagliaceae (Figure 18.2H, Figure 18.3H), although without statistical support under ML (Figure 18.3H). MP reconstructs entire leaf margins as a synapomorphy for the Ptychomniella–G. zantenii clade, although 22 of the 27 taxa of the clade have serrulate or serrate leaf margins (Figure 18.2I). By contrast, under ML, entire leaf margins are most likely the plesiomorphic condition of the ingroup and serrate to serrulate margins a synapomorphy for the Glyphothecium gracile–G. subelegans clade, but those reconstructions are without statistical support (Figure 18.3I). Both MP and ML reconstruct the presence of paraphyllia as a synapomorphy for the large clade starting with Glyphothecium gracile, with further reversals to the plesiomorphic condition in P. densifolium and the Garovagliaceae (Figure 18.2J, Figure 18.3J). Both MP and ML unambiguously reconstruct short setae as a synapomorphy for the Garovagliaceae (Figure 18.2K, Figure 18.3K). The presence of an annulus is reconstructed as plesiomorphic for the ingroup under MP (Figure 18.2L). This is in concurrence with the ML reconstruction (Figure 18.3L), although the ML

I

K Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare P Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum E Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

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Phylogenetic and Morphological Studies within the Ptychomniales 381

J

L

FIGURE 18.2 Continued.

estimates are not statistically significant at the deeper nodes of the ingroup. On the other hand, the ML reconstruction suggests that the absence of an annulus most likely is a synapomorphy for the large Cladomnion–Garovaglia subelegans clade, but with considerable ambiguity. Based on the MP reconstruction, the absence of filamentous gemmae (Figure 18.2M) represents a synapomorphy for the Euptychium dumosum–E. cuspidatum clade, and the presence of filamentous gemmae is plesiomorphic for the Garovagliaceae. Under ML, the presence of filamentous gemmae is most likely the ancestral state for the Garovagliaceae, but with very low statistical support (Figure 18.3M). In addition, the presence of filamentous gemmae is with 52% likelihood the most probable ancestral state at the node defining Euptychium, although this is without statistical support (Figure 18.3M). The MP reconstruction suggests that cucullate calyptrae is plesiomorphic for the ingroup, whereas mitrate calyptrae represents a synapomorphy for Euptychium and the Garovaglia plicata–G. powellii clade, respectively (Figure 18.2N). Cucullate calyptrae is statistically supported as plesiomorphic under ML as well (Figure 18.3N). ML also supports mitrate calyptrae as a synapomorphy for Euptychium, although with considerable uncertainty because the immediate ancestor of this clade is ambiguously reconstructed with only 68% of the likelihood suggesting a cucullate calyptrae. Reconstructions under MP and ML both support smooth capsules as a synapomorphy for the Garovagliaceae (Figure 18.2O, Figure 18.3O). Under MP, endostomes with two to three cilia between the processes (Figure 18.2P) represents a synapomorphy for Ptychomnion,

M

O

Q

FIGURE 18.2 Continued. Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

382

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

Rhytidiadelphus triquetrus Hampeella alaris Hampeella concavifolia Hampeella pallens Ptychomniella ptychocarpa Tetraphidopsis pusilla Cladomniopsis crenato-obtusa Glyphothecium gracile Cladomnion ericoides Dichelodontium nitidum Ptychomnion aciculare Ptychomnion cygnisetum Ptychomnion subaciculare Ptychomnion densifolium Ptychomnion falcatulum Glyphothecium sciuroides Euptychium cuspidatum Euptychium vitiense Euptychium mucronatum Euptychium robustum Euptychium dumosum Euptychium setigerum Garovaglia angustifolia Garovaglia plicata Garovaglia powellii Garovaglia baeuerlenii Garovaglia subelegans Garovaglia elegans Garovaglia compressa Garovaglia binsteadii Garovaglia zantenii

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Pleurocarpous Mosses: Systematics and Evolution

N

P

R

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383

although the cilia have been lost in P. densifolium. The ML reconstruction agrees with MP even though the immediate ancestor of Ptychomnion is equivocally reconstructed (Figure 18.3P). Both MP and ML reconstruct reduced exostomes as a synapomorphy for Garovaglia (Figure 18.2Q, Figure 18.3Q) and plicate inner perichaetial leaves as a synapomorphy for the G. binsteadii–G. zantenii split (Figure 18.2R, Figure 18.3R).

18.3.4 TESTS

OF

CORRELATED EVOLUTION

The evolution of dwarf males was significantly correlated with most of the morphological characters except seta length (Character 11), gemmae (13), endostome cilia (16), exostome development (17), and inner perichaetial leaf plication (18). In addition, there is no statistical support for correlated evolution of dwarf males with the epiphytic habit. The statistics of the correlation tests are presented in Table 18.4. Three character states were found to be significantly more likely to evolve in the presence of dwarf males, namely, teeth on dorsal leaf lamina (8), mitrate calyptrae (14), and furrowed capsules (15). With statistical support, the correlation tests suggest that dwarf males are more likely to evolve in the presence of rugose leaves (7) and paraphyllia (10).

18.4 DISCUSSION 18.4.1 PHYLOGENETIC RELATIONSHIPS

AND

TAXONOMIC CONSEQUENCES

The results of the phylogenetic analyses presented here support the results of Buck et al. (2004) that the Ptychomniaceae are paraphyletic to a robustly supported Garovagliaceae. The phylogenetic placement of Euptychium setigerum as suggested by Buck et al. (2004), however, is not in accord with the results presented here. In their ML tree, E. setigerum is resolved with high support as nested within Garovaglia and they transferred this species to Garovaglia. In contrast, the phylogenetic analyses presented here strongly support E. setigerum as sister to the rest of Euptychium. The gametophyte of E. setigerum has flaccid leaves that are spirally arranged along the stem, which is unique within Euptychium but typical of Garovaglia, but the peristome of E. setigerum differs markedly compared to Garovaglia. Hence, unless sporophytes are available, specimens of E. setigerum can be difficult to separate from Garovaglia. A unique feature of E. setigerum that is found neither in Garovaglia nor other Euptychium species, however, is the multistratose acumen of the inner perichaetial leaves. The voucher used by Buck et al. (2004) lacks sporophytes but young perichaetia are present and the acumen of its inner perichaetial leaves are unistratose and typical of the ones found in Garovaglia. Identification using the keys of During (1977) showed that the voucher used by Buck et al. (2004) is a misidentified Garovaglia elegans ssp. dietrichiae. Other results that are incongruent with Buck et al. (2004) are the phylogenetic placements of G. elegans and G. powellii. Their analyses place G. powellii as sister to G. subelegans and G. elegans as sister to G. binsteadii, whereas the present study places G. powellii with G. plicata and G. elegans as sister to a clade with G. subelegans and G. baeuerlenii. These conflicting results are due to misidentifications of the vouchers of G. elegans and G. powellii used by Buck et al. (2004). In his systematic treatment of Garovaglia, During (1977) recognized the section Baeuerlenii comprising the two species G. baeuerlenii and G. binsteadii. The phylogenetic analyses presented here strongly support G. binsteadii as sister to G. zantenii, suggesting that section Baeuerlenii is not monophyletic. On the other hand, the clade with G. plicata and G. powellii, both of which During placed in section Garovaglia, support monophyly of this section. A novel inference revealed by the molecular data is that the genus Glyphothecium is polyphyletic. Morphological characters that separate G. gracile from G. sciuroides are the presence of an annulus (lacking in G. sciuroides) and the absence of stomata (phaneroporous in G. sciuroides). Clearly, G. gracile is not closely related to G. sciuroides, which is sister to the Garovagliaceae.

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The type of the genus, G. muellerianum Hampe. was synonymised with G. sciuroides (Hook.) Hampe. (Mitten, 1882) and consequently G. gracile is here recognized as the monospecific genus Glyphotheciopsis. Glyphotheciopsis gen. nov. Plantae dioicae caespitosae. Folia ovato-lanceolata, apice acuminata basi plicata, margine infra medium integra supra medium serrulata, cellulis medilaminaribus 50–68 × 6–11 μm porosis. Seta 3–6 mm longa. Theca erecta, longitudinaliter 8-porcata, stomatibus carens, annulis ex 1–3 seriebus cellularum discedentium constantibus, calyptra cucullata. Sporae 10–22 μm in diametro, subtiliter papillosae. Dioicous. Plants tufted. Leaves ovate-lanceolate, acuminate, with basal plicae. Alar cells slightly auriculate. Margins entire below, serrulate above. Mid-lamina cells 50–68 × 6–11 μm, porose. Setae 3–6 mm long. Capsules erect with 8 longitudinal ridges, stomata absent, annuli of 1–3 rows of separating cells, calyptrae cucullate. Spores 10–22 μm, finely papillose.

TYPE: Glyphothecium gracile (Hampe) Broth. Glyphotheciopsis gracile (Hampe) Pedersen and Newton comb. nov. Leucodon gracilis Hampe, Icon. Musc. (Hampe) 18. 1844. ≡ Glyphothecium gracile (Hampe) Broth.

18.4.2 RECONSTRUCTION

OF

MORPHOLOGICAL CHARACTER STATES

In general, the MP reconstructions are similar to the ones under ML, although ML clearly shows that reconstructions are not as simplistic as MP might suggest. Particularly, ML estimates show that character state reconstructions are uncertain even when MP reconstructions are unambiguous. MP and ML reconstructions were most similar when character state changes are estimated to be rare, but even when this is the case the two methods might not suggest identical results. For instance, MP reconstructs leaves with dorsal teeth (Figure 18.2H) as a synapomorphy for the Garovagliaceae, but the ML estimate shows that leaves without dorsal teeth is the most likely state at the node defining the Garovagliaceae, although without statistical support (Figure 18.3H). A further example is that MP reconstructs the mitrate calyptrae as synapomorphic for Euptychium and the Garovaglia plicata–G. powellii clade, respectively (Figure 18.2N). Under ML, however, mitrate calyptrae is most likely synapomorphic for each of these clades but this is not statistically supported (Figure 18.3N). Reconstructions under both MP and ML suggest considerable ambiguity for most internal nodes. This can be explained by a high probability of change in certain characters and even single lineages might switch between character states several times, making inferences about state changes in the past unattainable (Schluter et al., 1997). As mentioned above, Discrete can analyse only binary characters and any multistate character has to be either excluded from the analyses or transformed into binary ones. For some of the characters used in the present analyses, multistate codings are possible. For instance, the presence of dwarf males (character 1; state 1) can be coded as simple and unbranched, as for Garovaglia, or larger and branched, as for Euptychium, Glyphothecium and Cladomnion. It is therefore possible that the uncertainties in ancestral character state reconstructions might be an artifact of the binary FIGURE 18.3 (See figure, facing page.) Maximum likelihood reconstructions of the 18 morphological characters. For each character, statistically significant reconstructions at branches are indicated in grey for state “0” and black for state “1”. Pie-charts indicate relative support for the two ancestral states when reconstructions are not statistically significant. (A) dwarf males (character 1); (B) germination (2); (C) attachment of perichaetial leaves (3); (D) leaf rigidity (4); (E) leaf concavity (5); (F) leaf plication (6); (G) leaf rugosity (7); (H) leaf dorsal dentation (8); (I) leaf margin dentation (9); (J) paraphyllia (10); (K) setae length (11); (L) annulus (12); (M) filamentous gemmae (13); (N) calyptrae (14); (O) capsule surface (15); (P) number of endostome cilia (16); (Q) exostome development (17); (R) inner perichaetial leaf plication (18).

3856_book.fm Page 385 Saturday, March 3, 2007 12:29 PM

Phylogenetic and Morphological Studies within the Ptychomniales

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata Garovaglia powellii

Garovaglia powellii

A

Garovaglia binsteadii

B

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

Garovaglia powellii Garovaglia binsteadii Garovaglia zantenii

FIGURE 18.3 Continued.

Garovaglia binsteadii Garovaglia zantenii

Garovaglia zantenii

C

385

D

Garovaglia powellii Garovaglia binsteadii Garovaglia zantenii

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

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386

Pleurocarpous Mosses: Systematics and Evolution

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

E

Garovaglia powellii Garovaglia binsteadii

Garovaglia powellii

F

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

Garovaglia powellii

Garovaglia powellii

G

Garovaglia binsteadii Garovaglia zantenii Garovaglia compressa Garovaglia elegans Garovaglia baeuerlenii Garovaglia subelegans

FIGURE 18.3 Continued.

Garovaglia binsteadii Garovaglia zantenii

Garovaglia zantenii

H

Garovaglia binsteadii Garovaglia zantenii Garovaglia compressa Garovaglia elegans Garovaglia baeuerlenii Garovaglia subelegans

3856_book.fm Page 387 Saturday, March 3, 2007 12:29 PM

Phylogenetic and Morphological Studies within the Ptychomniales

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

Garovaglia powellii

I

K

Garovaglia binsteadii

Garovaglia powellii

J

Garovaglia binsteadii

Garovaglia zantenii

Garovaglia zantenii

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

Garovaglia powellii

Garovaglia powellii

Garovaglia binsteadii

Garovaglia binsteadii

Garovaglia zantenii Garovaglia compressa

FIGURE 18.3 Continued.

387

L

Garovaglia zantenii Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

3856_book.fm Page 388 Saturday, March 3, 2007 12:29 PM

388

M

Pleurocarpous Mosses: Systematics and Evolution

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

Garovaglia powellii

Garovaglia powellii

Garovaglia binsteadii

N

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

Rhytidiadelphus triquetrus

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

O

Garovaglia powellii Garovaglia binsteadii Garovaglia zantenii

FIGURE 18.3 Continued.

Garovaglia binsteadii Garovaglia zantenii

Garovaglia zantenii

Garovaglia plicata

P

Garovaglia powellii Garovaglia binsteadii Garovaglia zantenii

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

3856_book.fm Page 389 Saturday, March 3, 2007 12:29 PM

Phylogenetic and Morphological Studies within the Ptychomniales

Rhytidiadelphus triquetrus

Q

389

Rhytidiadelphus triquetrus

Hampeella alaris

Hampeella alaris

Hampeella concavifolia

Hampeella concavifolia

Hampeella pallens

Hampeella pallens

Ptychomniella ptychocarpa

Ptychomniella ptychocarpa

Tetraphidopsis pusilla

Tetraphidopsis pusilla

Cladomniopsis crenato-obtusa

Cladomniopsis crenato-obtusa

Glyphothecium gracile

Glyphothecium gracile

Cladomnion ericoides

Cladomnion ericoides

Dichelodontium nitidum

Dichelodontium nitidum

Ptychomnion aciculare

Ptychomnion aciculare

Ptychomnion falcatulum

Ptychomnion falcatulum

Ptychomnion densifolium

Ptychomnion densifolium

Ptychomnion cygnisetum

Ptychomnion cygnisetum

Ptychomnion subaciculare

Ptychomnion subaciculare

Glyphothecium sciuroides

Glyphothecium sciuroides

Euptychium setigerum

Euptychium setigerum

Euptychium dumosum

Euptychium dumosum

Euptychium cuspidatum

Euptychium cuspidatum

Euptychium vitiense

Euptychium vitiense

Euptychium mucronatum

Euptychium mucronatum

Euptychium robustum

Euptychium robustum

Garovaglia angustifolia

Garovaglia angustifolia

Garovaglia plicata

Garovaglia plicata

Garovaglia powellii

Garovaglia powellii

Garovaglia binsteadii

R

Garovaglia binsteadii

Garovaglia zantenii

Garovaglia zantenii

Garovaglia compressa

Garovaglia compressa

Garovaglia elegans

Garovaglia elegans

Garovaglia baeuerlenii

Garovaglia baeuerlenii

Garovaglia subelegans

Garovaglia subelegans

FIGURE 18.3 Continued.

character coding. To test this, we recoded, if possible, the characters as multistate, mapped them onto the ML tree under MP and compared the results to the MP reconstructions of the binary coded dataset. This, however, did not reduce ambiguities in the reconstructions of ancestral character states, which suggests that the uncertainties are not an artefact of character coding. Of course, this has to be explored under ML as well using, for instance, the computer program Multistate (Pagel, 2003). Nevertheless, despite these uncertainties in ancestral character state reconstructions, the absence of paraphyllia (character 10), short setae (11), and smooth capsules (15) are unambiguously reconstructed as synapomorphies for the Garovagliaceae, whereas reduced exostomes (17) and plicate inner perichaetial leaves (18) are synapomorphies for Garovaglia and the clade with G. binsteadii and G. zantenii, respectively.

18.4.3 TESTS

OF

CORRELATED EVOLUTION

It has been suggested that specific morphological features may facilitate the evolution of dwarf males, by providing suitable establishment points for incoming spores (Ernst-Schwarzenbach, 1939; During, 1977). Although the results of the present study suggest significant correlations of the presence of dwarf males with 12 morphological features, only two of them, namely rugose leaves and the presence of paraphyllia, increase the likelihood of the evolution of dwarf males. It seems reasonable that rugose leaves, compared to smooth ones, can provide suitable, firm, establishment points for incoming spores and consequently enhance the evolution of dwarf males. Because paraphyllia are lacking in Garovaglia, it may be difficult to envisage how the presence of paraphyllia could facilitate the evolution of dwarf males. Nevertheless, by comparing how dwarf males and paraphyllia are reconstructed on the phylogeny it becomes clear that the possibility of correlated evolution might not be too implausible after all. Since the presence of paraphyllia precedes the occurrence of dwarf males on the phylogeny (e.g., compare Figure 18.2A and Figure 18.2J), an

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Pleurocarpous Mosses: Systematics and Evolution

TABLE 18.4 Likelihood Ratio Test Statistics (LRT) and Probabilities (p-Value) of Tests of Correlation of Dwarf Males with Morphological Characters and the Epiphytic Habitat Character

LRT Statistic

p-Value

Germination Perichaetial leaf attachment Leaf rigidity Leaf concavity Leaf plication Stem leaf rugosity Dorsal teeth Margin dentation Paraphyllia Seta length Annulus Gemmae Calyptra Capsule surface Endostome cilia Exostome development Inner perichaetial leaf plication Epiphytism

5.125 5.795 6.047 3.788 5.067 6.388 6.125 5.401 9.122 3.902 5.362 2.281 5.673 6.237 2.683 2.644 4.104 1.781

0.012* << 0.001* << 0.001* 0.011* << 0.001* << 0.001* << 0.001* << 0.001* << 0.001* 0.052 << 0.001* 0.417 << 0.001* << 0.001* 0.114 0.364 0.054 0.273

Note: Asterisks indicate significant correlations.

evolutionary scenario can be visualized in which the presence of paraphyllia in the ancestor of the clade comprising Cladomnion, Dichelodontium and Ptychomnion provided attachment points and protection for incoming spores, and thereby increasing the possibility of evolution of dwarf males in this clade. The results of the correlation tests suggest that the presence of teeth on the dorsal leaf lamina, mitrate calyptrae and furrowed capsules, are more likely to evolve when dwarf males are present. It seems reasonable that dorsal teeth, by providing further establishment points and protection for incoming spores, may be beneficial for taxa with dwarf males, but it is difficult to envision the benefits of mitrate calyptrae and furrowed capsules. It is worth mentioning, however, that correlation does not necessarily imply causation. The hypothesis that the presence of dwarf males is correlated with epiphytism within the Ptychomniales is rejected by the present study. Dwarf males are also found among terricolous taxa unrelated to the Ptychomniales, e.g., Dicranum, Ctenidium and Thuidium, but are in general more common among epiphytes (Ramsay, 1979). Thus, it is possible that correlation studies based on extensive taxonomic sampling across all the mosses may reveal that the presence of dwarf males correlates with the epiphytic habitat.

18.5 CONCLUDING REMARKS AND FUTURE RESEARCH NEEDS Perhaps the most striking inference gained from the current study is that the evolution of dwarf males appears to be significantly correlated with several morphological traits. In addition, dorsal teeth are more likely to evolve when dwarf males are present whereas rugose leaves promote

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evolution of dwarf males. It is noteworthy that rugose leaves occur in G. angustifolia and G. plicata, and dorsal teeth in G. powellii and G. plicata. These three species contain extreme morphological plasticity and variation, with many subspecific taxa recognized, and numerous names included in their synonymy. For instance, 5 subspecies, 7 varieties, and 35 synonyms have been recognized in G. powellii, and the corresponding numbers in G. plicata are 3, 2, and 17. This is reflected in the levels of observed character variation within these species. The number of dorsal teeth in different specimens of G. powellii, for example, can be none, as in var. taitensis, up to ten in var. brevicuspidata, and as many as 100 in var. muelleri (During, 1977). This may suggest that morphological plasticity is correlated with the expression of dwarf males, but studies based on extensive sampling of subspecific taxa and varieties are needed to assess this. The results of the phylogenetic analyses presented here strongly support that the genera Ptychomnion, Euptychium and Garovaglia are monophyletic, but relationships within these genera are generally poorly supported. In addition, the branches within Ptychomnion are very short, which may suggest recent radiations and/or high speciation rates within the genus. Although further sampling of species and subspecific taxa in Garovaglia is possible, both Euptychium and Ptychomnion have been thoroughly sampled in this study. Hopefully, analyses including genomic markers from the nuclear genome will resolve phylogenetic relationships within these genera.

ACKNOWLEDGMENTS This research was supported by the European Commission grant no. MEIF-CT-2003-501682 to N. Pedersen. We thank Cymon Cox for comments on the manuscript and assistance with the program p4 and Norman Robson for help with Latin.

REFERENCES Allen, C. E. (1935) The genetics of bryophytes, I. Botanical Review, Interpreting Botanical Progress, 1: 269–291. Allen, C. E. (1945) The genetics of bryophytes, II. Botanical Review, Interpreting Botanical Progress, 11: 260–287. Beckert, S., Steinhauser, S., Muhle, H. and Knoop, V. (1999) A molecular phylogeny of the bryophytes based on nucleotide sequences of the mitochondrial nad5 gene. Plant Systematics and Evolution, 218: 179–192. Brotherus, V. F. (1924) Musci. In Die natürlichen Pflanzenfamilien, Vol. 10., Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig. Brotherus, V. F. (1925) Musci. In Die natürlichen Pflanzenfamilien, Vol. 11., Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R., Cox, C. J., Shaw, A. J. and Goffinet, B. (2004) Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematics and Biodiversity, 2: 121–145. Dening, K. (1935) Untersuchungen über sexuellen Dimorphismus der Gametophyten bei heterotallischen Laubmosen. Flora, Jena, 30: 57–86. Doyle J. J. and Doyle J. L. (1987) A rapid DNA isolation procedure for small quantities of fresh tissue. Phytochemical Bulletin, 19: 11–15. During, H. J. (1977) A taxonomic revision of the Garovaglioideae (Pterobryaceae, Musci). Bryophytorum Bibliotheca. Lahre, Vaduz, 12: 1–244. Ernst-Schwarzenbach, M. (1939) Zur Kenntnis der sexuellen Dimorphismus der Laubmoose. Archiv der Julius Klaus-stiftung fur Vererbungsforschung, 14: 362–474. Fleischer, M. (1904–1923) Die Musci der Flora von Buitenzorg. Four volumes. E. J. Brill, Leiden. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematic of Bryophytes (ed. B. Goffinet, V. Holland and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239.

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Hattaway, R. A. (1984) A Monograph of the Ptychomniaceae (Bryophyta). Ph.D. dissertation, UMI Dissertation Services, Ann Arbor. Hillis, D. M. and Bull, J. J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42: 182–192. Loveland, H. F. (1956) Sexual dimorphism in the moss genus Dicranum Hedw. Ph.D. dissertation, University of Michigan, Ann Arbor. Maddison, D. R. and W. P. Maddison (2001) MacClade 4: Analysis of Phylogeny and Character Evolution, Version 4.03. Sinauer Associates, Sunderland, Massachusetts. Manhart, J. R. (1994) Phylogenetic analysis of green plant rbcL sequences. Molecular Phylogenetics and Evolution, 3: 114–127. Mitten, W. (1882) Australian mosses. Transactions of the Royal Society of Victoria, 19: 49–96. Nadot, S., Bittar, G., Carter, L., Lacroix, R. and Lejeune, B. (1995) A phylogenetic analysis of monocotyledons based on the chloroplast gene rps4, using parsimony and a new numerical phenetics method. Molecular Phylogenetics and Evolution, 4: 257–282. Nylander, J. A. A. (2004) MrModeltest 2.0. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Pacak, A. and Szweykowska-Kulinska, Z. (2000) Molecular data concerning alloploid character and the origin of chloroplast and mitochondrial genomes in the liverwort Pellia borealis. Journal of Plant Biotechnology, 2: 101–108. Pagel, M. (1994) Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London. Series B, Biological Sciences, 255: 37–45. Pagel, M. (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology, 48: 612–622. Pagel, M. (2002) Discrete, version 4. Available from the author. http://www.ams.rdg.ac.uk/zoology/pagel/mppubs.html. Pagel, M. (2003) Multistate, version 0.8. Available from the author. http://www.ams.rdg.ac.uk/zoology/pagel/mppubs.html. Philibert, H. (1883) Les fleurs mâles du Fissidens decipiens. Revue Bryologique. Caen, 10: 65–67. Ramsay, H. (1979) Anisospory and sexual dimorphism in the musci. In Bryophyte Systematics (ed. G. C. S. Clarke and J. G. Duckett). Academic Press, London, pp. 281–316. Sanderson, M. J. (2001) r8s, version 1.60. http://ginger.ucdavis.edu/r8s/. Schluter, D., Price, T., Mooers, A. O. and Ludwig, D. (1997) Likelihood of ancestor states in adaptive radiation. Evolution, 51: 1699–1711. Shaw, A. J. E. (2000) Molecular phylogeography and cryptic speciation in the mosses. Mielichhoferia elongata and M. mielichhoferiana. Molecular Ecology, 9: 595–608. Swofford, D. L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts. Taberlet, P., Gielly, L., Pautou, G. and Bouvet, J. (1991) Universal primers for the amplification of three noncoding regions of chloroplast DNA. Plant Molecular Biology, 17: 1105–1109. Williams, T. and Kelley, C. (2002) Gnuplot, version 3.8: Software and Documentation. http://sourceforge.net/projects/gnuplot. Woesler, A. (1935a) Zur Frage der Sexualdimorphismus bei Laubmoosen. In Proceeding VI International Botanisch Congress, Vol. 2, E. J. Brill, Leiden, pp. 143–145. Woesler, A. (1935b) Zur Zwergmännchenfrage bei Leucobryum glaucum Schpr, 1. Planta, 24: 1–13.

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of Austral 19 Biogeography Pleurocarpous Mosses: Distribution Patterns in the Australasian Region Ray Tangney CONTENTS Abstract ..........................................................................................................................................394 19.1 Introduction...........................................................................................................................394 19.2 Distribution Patterns of Austral Pleurocarps .......................................................................395 19.2.1 Distribution Tracks ...................................................................................................395 19.2.1.1 Track 1. Southern Indonesia–Melanesia–New Caledonia– Vanuatu–Fiji ..............................................................................................395 19.2.1.2 Track 2. New Guinea–East Australia–Tasmania ......................................395 19.2.1.3 Track 3. Central east Australia–Lord Howe Island–Norfolk Island–New Caledonia–Vanuatu ...............................................................395 19.2.1.4 Track 4. New Zealand–New Caledonia–Solomon Islands.......................396 19.2.1.5 Track 5. South-east Australia–Tasmania–New Zealand–Southern South America ...........................................................................................397 19.3 Generalized Distribution Pattern ..........................................................................................397 19.4 Distribution of Related Taxa ................................................................................................397 19.4.1 The Lembophyllaceae ..............................................................................................397 19.4.1.1 Distribution of Camptochaete ...................................................................399 19.4.1.2 Distribution Patterns within Camptochaete ..............................................399 19.4.2 Distribution of the Hypopterygiaceae ......................................................................399 19.4.2.1 Distribution of Cyathophorum ..................................................................399 19.4.2.2 Distribution of Lopidium...........................................................................401 19.4.3 Distributions within the Hypnodendraceae..............................................................401 19.5 Discussion.............................................................................................................................403 19.5.1 General Pattern of Allopatry ....................................................................................403 19.5.2 Distribution of the Lembophyllaceae.......................................................................403 19.5.3 Comparison with the Angiosperms..........................................................................404 19.6 Conclusions...........................................................................................................................406 Acknowledgments ..........................................................................................................................406 References ......................................................................................................................................406

393

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ABSTRACT This chapter examines the distribution patterns of pleurocarpous mosses in the Australasian region. Comparison of the details of species distributions of pleurocarps reveals several distinct patterns of distribution, each emphasizing different areas within the region. Together they form an interlocking network of general distribution tracks common to a diverse range of plants and animals and independent of the biological characteristics of individual groups. A feature of the distributions of species is spatial separation of closely related taxa. The coincidence of this vicariance with a general pattern of distribution has implications for the explanation of the distributions of individual taxa as well as for the understanding of the phylogeny of pleurocarps in the region. It highlights a relationship between taxa and localities stronger than that expected if long distance dispersal were a major determining factor in forming the distribution, suggesting a major role for allopatric evolution, the allopatric splitting of ancestral populations within their ancestral ranges. A distinction is drawn between the timing of the origin of taxa and the time of the origin of the ancestral range. Differentiation of taxa may occur at different times within ancestral ranges and therefore taxa of different ages and taxonomic levels may share the same present-day distribution through congruence of ancestral ranges and interaction with regional geological and ecological processes.

19.1 INTRODUCTION The origin of the pleurocarpous mosses is one of the intriguing problems in bryology. Pleurocarps are a speciose group that is considered to be evolutionarily successful, analogous to the angiosperms. Compared to other mosses that on the whole form well-defined groupings suggestive of a long evolutionary history, the pleurocarpous mosses form a morphologically rather diffuse group placed distally in phylogenies with poorly resolved interrelationships. Recent applications of cladistic analyses of morphological and molecular data have overturned accepted views of the evolution and classification of pleurocarps, necessitating reexamination of a wide range of aspects of their biology. This chapter examines some of these questions with respect to pleurocarpy (origins, place and time) from the perspective of biogeography. Biogeography is the study of the distributions of plants and animals. However, biogeographic studies often assume a priori a more important role for biological factors than for the spatial relations of taxa. Mosses, for example, have small, easily dispersed propagules capable of longdistance dispersal, but paradoxically often have distributions characterized by limited geographic ranges and discrete, repeated patterns, indicating a closer relationship with geographic locality than chance dispersal would be expected to produce. This paradox between the geographic mobility suggested by apparent biological vagility and the geographic stability suggested by the repeated patterns lies at the heart of biogeography as a discipline. Despite the often striking features of taxon distributions, the spatial relations of distributions are seldom studied in themselves and are often subsumed in a wider discussion that implicitly makes distribution data contingent on other considerations. A central question in biogeography is therefore the importance of the study of the area relations of taxa versus the recovery of species histories. Biogeographic studies often focus on the individual species occurring in a particular area, characterizing their distributions with respect to distribution elements that reflect the origins of the taxa. Implicit in this approach is the assumption of an important role for dispersal, movement of the species to the study area from respective centres of origin. The flora of the region is seen as an amalgam of elements with different dispersal histories. Giving priority to dispersal as the means by which distributions are formed has several undesirable effects. First, it devalues distribution data. The possibility of the reliability of pattern in distributions is lessened if dispersal is assumed to be a major determining factor. Also, if distributions are represented as ranges within element classifications the precision of distributions and their details are disguised.

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Most importantly, species are not compared with their close relatives, members of the same genus, etc., and their spatial relations to the rest of their group, their evolutionary context, is overlooked. This latter feature is critical as the spatial relations of taxa are an important and underemphasized aspect of the distributions of organisms. Here the focus is on spatial pattern and relationships. In presenting the distributions track analysis is used. This method, as developed by Croizat (e.g., 1964; see also Craw et al. (1999)), is to plot distribution records of taxa and join them to form line graphs, or tracks. Through the comparison of numerous taxa, general or standard tracks are formed from the areas of agreement of the line graphs of individual taxa (Craw et al., 1999). This approach gives priority to analysing the distributions of organisms. In this way, a spatial pattern is established that is a biogeographic context in which other evidence, e.g., biological, ecological and geological, can be considered and synthesized (Grehan, 2001).

19.2 DISTRIBUTION PATTERNS OF AUSTRAL PLEUROCARPS The distributions of a range of pleurocarpous mosses in the Australasia region were examined, comparing the areas occupied and limits of their distributions. Examples were examined from the following families: Lembophyllaceae (Tangney, 1997a, 1997b), Hypnodendraceae (Touw, 1971), and Hypopterygiaceae (Kruijer, 2002). Distinct similarities and differences are seen among the taxa, and five distribution patterns recognized. These are summarized as tracks to facilitate comparison (Figure 19.1). Each track corresponds to the distribution of one or more species and may be a boundary or limit of distribution for others. Some are distributed on part of the area highlighted and not on others.

19.2.1 DISTRIBUTION TRACKS 19.2.1.1 Track 1. Southern Indonesia–Melanesia–New Caledonia–Vanuatu–Fiji This track marks the southern limit of taxa distributed more widely to the north in southern Asia, Indonesia and Melanesia, for example, Hypopterygium flavolimbatum, Cyathophorum spinosum and Hypnodendron diversifolium. These species are distributed from southern Indonesia in the west to the Solomon Islands in the east, not including Australia. Some species with this track as limit to their distribution are also present in New Caledonia, Vanuatu, Fiji and Samoa: Hypnodendron milnei and Hypopterygium viresei. Other species have the track as their distribution. Camptochaete subporotrichoides is present in southern Indonesia (Flores), Papua New Guinea, the Solomon Islands, Vanuatu and Fiji, and Cyathophorum tahitense is present in Vanuatu, Fiji, Samoa and the Society Islands. This track is the northern limit of the genus Camptochaete. 19.2.1.2 Track 2. New Guinea–East Australia–Tasmania Camptochaete excavata and Hypnodendron vitiense ssp. australe are present in eastern Australia, while the former is present also in New Guinea and Lord Howe Island and the latter also in Tasmania. 19.2.1.3 Track 3. Central east Australia–Lord Howe Island–Norfolk Island–New Caledonia–Vanuatu This track connects eastern Australia with the New Caledonia–Vanuatu area. It sometimes also involves presence on Lord Howe and Norfolk Islands. Camptochaete curvata is endemic in central eastern Australia and Camptochaete leichhardtii has a similar distribution there and is also present in Vanuatu. Variations on this pattern are provided by Hypopterygium discolor (central eastern Australia and northern New Zealand) and Braithwaitea sulcata (eastern Australia, Lord Howe

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A

Track 1

B

Track 2

C

Track 3

D

Track 4

E

Track 5

X

F

FIGURE 19.1 (A) to (E) Distribution patterns of pleurocarpous mosses in the Australasian region summarized as tracks. (F) Generalized distribution track in the southern Pacific Ocean based on the distributions of pleurocarpous mosses; X = Macpherson–Macleay Overlap.

Island, New Caledonia and northern New Zealand). There are similarities between this pattern and Track 4, with the more widespread Camptochaete excavata also present on Lord Howe Island. 19.2.1.4 Track 4. New Zealand–New Caledonia–Solomon Islands This track links New Zealand to the north rather than to Australia as in Track 5 (see below). In the groups examined only one species has this distribution. Hypnodendron menziesii is present in New Zealand, New Caledonia and the Solomon Islands, and doubtfully recorded in Tasmania and Norfolk

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Island (Touw, 1971). The distribution of Camptochaete angustata is suggestive of this pattern, being present in New Zealand and the Kermadec Islands to the north of New Zealand. 19.2.1.5 Track 5. South-east Australia–Tasmania–New Zealand–Southern South America Several species are distributed along this track or part of it. Hypnodendron comosum, Hypnodendron spininervium and Camptochaete deflexa are present in New Zealand, south-east Australia and Tasmania, while Hypopterygium didictyon and Lopidium concinnum are present in these areas as well as in southern South America.

19.3 GENERALIZED DISTRIBUTION PATTERN The five patterns were combined to produce a generalized pattern of distribution (Figure 19.1F). This pattern reveals relationships between areas as follows. Distinct east–west relations are highlighted in the north (Track 1), central (Track 3) and south (Track 5) of the region. In addition, north–south relations are highlighted in the east (Track 4) and west (Track 3). These area relations highlighted by species distribution of pleurocarpous mosses have been found in the results of similar analyses of other taxa. An analysis based on diverse groups of mosses (Dawsonia, Macromitrium, Dicnemonaceae, and including Hypnodendron and Hypnum) (Tangney, 1990), yielded the same pattern of relationships as did analyses of vascular plants (Burbidge, 1960) and analyses of numerous and diverse groups of plants and animals (Croizat, 1964). This pattern comprises a series of intersecting generalized distribution tracks. The intersections of these tracks are recognized as nodes: areas characterized by species diversity and endemism (Heads, 1990). Croizat (1964) found that the track connecting central eastern Australia with the New Caledonia area was an important feature of the distributions in the region. He highlighted the eastern end of the Queensland–New South Wales border as an area of particular biogeographic significance. It was recognized by Burbidge (1960) as the MacPherson–Macleay Overlap, which Croizat considered a major global biogeographic feature (shown here in Figure 19.1F and Figure 19.6). Burbidge (1960) interpreted the linear series of relationships as migration routes that plants had followed into the region, whereas Croizat (1964) considered that the pattern of distribution was the result of what he called “vicariant form-making”: in situ allopatric evolution within an ancestral range. This view was based on the observation that not only do species distributions conform to a general pattern but also that related species tended to replace each other in space.

19.4 DISTRIBUTION OF RELATED TAXA 19.4.1 THE LEMBOPHYLLACEAE The Lembophyllaceae are a family of pleurocarpous mosses that are common on rocks and tree bases, and are often pendant epiphytes. The Australasian taxa form a monophyletic group of closely related species. Putative sister groups to this clade are genera distributed widely in the Northern Hemisphere, North and South America and Asia. The Australasian Lembophyllaceae (Tangney, 1997b) extend from Indonesia to Papua New Guinea and Fiji, south to Australasia and to southern South America (Figure 19.2).Within Australasia, there are centres of diversity in the north (Coral Sea), as shown by Camptochaete sect. Thamniella (Figure 19.3), and in the south (Tasman Sea), as shown by Camptochaete sect. Camptochaete (southeast Australia–New Zealand) (Figure 19.3), and Lembophyllum, Weymouthia and Fallaciella (southeast Australia–New Zealand–southern South America). Fifea is endemic to New Zealand.

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FIGURE 19.2 Distribution of Australasian Lembophyllaceae.

Camptochaete sect. Thamniella Camptochaete sect. Camptochaete

FIGURE 19.3 Distribution of Camptochaete (Lembophyllaceae). See text for details.

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19.4.1.1 Distribution of Camptochaete Camptochaete occurs in Indonesia (Flores), Papua New Guinea, Vanuatu, New Caledonia, Fiji, eastern Australia (Queensland to Tasmania), New Zealand (Figure 19.3). The distributions of the species are as follows: Sect. 1. Camptochaete C. arbuscula. Eastern Australia: Victoria, Tasmania. New Zealand: North Island, South Island, Stewart Island, Chatham Island, Snares Island, Auckland Island, Campbell Island. C. deflexa. Eastern Australia: Queensland, New South Wales, Australian Capital Territory, Victoria, Tasmania. New Zealand: North Island, South Island, Chatham Island, Snares Island, Auckland Island, Campbell Island. C. angustata. New Zealand: Kermadec Island, North Island, South Island. C. pulvinata. New Zealand: North Island, South Island. Hawaii(?). C. leichhardtii. Vanuatu: Anatom. Eastern Australia; southern Queensland, New South Wales, Victoria. Sect. 2. Thamniella C. excavata. Papua New Guinea. Eastern Australia: Queensland, New South Wales, Victoria; Lord Howe Island. C. curvata. Eastern Australia: Queensland, New South Wales. C. porotrichoides. New Caledonia. C. subporotrichoides. Indonesia: Flores. Papua New Guinea. Solomon Islands. Vanuatu: Anatom. Fiji. C. papuana. Papua New Guinea. 19.4.1.2 Distribution Patterns within Camptochaete Within the area encompassed by the sections, the species exhibit different distributions. In sect. Thamniella, C. excavata occurs from Papua New Guinea in the north, through eastern Australia to Victoria in the south. This contrasts with the distribution of C. subporotrichoides which occurs in Papua New Guinea, Vanuatu and Fiji. C. papuana is present in Papua New Guinea. C. curvata is present in eastern Australia, at and around the Queensland–New South Wales border. C. porotrichoides is found only in New Caledonia. Sect. Camptochaete has a southern Tasman Sea distribution, with four of its five species present in mainland New Zealand, and two of these also in south-eastern Australia. The distribution of the remaining species in sect. Camptochaete, C. leichhardtii corresponds to the overlap between the two sections: south-east Australia, southern Queensland to Victoria, and Vanuatu. Similar patterns of replacement highlighting the major features of distribution in the region can be seen in other groups of pleurocarps. The following provide further examples.

19.4.2 DISTRIBUTION

OF THE

HYPOPTERYGIACEAE

Kruijer (2002) provided a monograph of the Hypopterygiaceae (see also Chapter 4). Two examples are presented here, Cyathophorum and Lopidium. 19.4.2.1 Distribution of Cyathophorum The genus Cyathophorum (Hypopterygiaceae) has six species distributed as follows (Figure 19.4 and Figure 19.5): C. parvifolium (Indonesia, southern Philippines, Sumatra, Timor, Papua New Guinea), and C. spinosum (Indonesia, Borneo, Sumatra, Philippines, Timor, New Guinea, Solomon Islands) have their southern limits at the line southern Indonesia–Melanesia, and there is spatial separation of species within the genus. Based on an analysis of morphological characters (Kruijer,

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Cyathophorum adiantum Cyathophorum bulbosum Cyathophorum spinosum Cyathophorum tahitense

FIGURE 19.4 Distribution of Cyathophorum in part (Hypopterygiaceae). See text for details.

Cyathophorum hookerianum Cyathophorum parvifolium

FIGURE 19.5 Distribution of Cyathophorum in part (Hypopterygiaceae). See text for details.

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X

Lopidium concinnum Lopidium struthiopsis

FIGURE 19.6 Distribution of Lopidium (Hypopterygiaceae). See text for details. X = Macpherson–Macleay Overlap.

2002), Cyathophorum spinosum is sister to C. tahitense (Vanuatu, Fiji, Samoa, Society Islands), and these two are sister to C. bulbosum (Papua New Guinea, eastern Australia, Tasmania, Lord Howe Island and New Zealand), and together form a clade sister to C. adiantum (Himalayas, Southern India, Sri Lanka, south-east Asia, China, Korea, Japan). Cyathophorum hookerianum (Himalayas, south-east Asia, China, Korea, Japan, northern Philippines) and C. parvifolium form a clade sister to the other species, and the remaining species, C. africanum (east Africa, Ethiopia, Uganda, Kenya, Tanzania, Rwanda, Democratic Republic of Congo), is sister to the rest of the genus (not shown). A recent molecular study of the family (see Kruijer and Blocher, Chapter 4) includes four species of Cyathophorum. Of the species included in the analysis, C. africanum does not occur in Australasia, C. hookerianum is in a clade with Hypopterygium species, and C. adiantum and C. bulbosum form a monophyletic clade. 19.4.2.2 Distribution of Lopidium Lopidium has two species with wide ranging distributions (Figure 19.6). The only geographical overlap between the species is central eastern Australia, at the Macpherson–Macleay Overlap. Within the latter area the species are not sympatric, occurring in different localities (H. Kruijer, personal communication). Species distributions are as follows: L. struthiopsis, southern and east Africa, southern India, Indonesia, Melanesia, Samoa and Society Islands, Australia (north-east Queensland and the Queensland–New South Wales border); L. concinna, south-east Australia, north to the Queensland–New South Wales border, Tasmania, New Zealand, southern South America.

19.4.3 DISTRIBUTIONS

WITHIN THE

HYPNODENDRACEAE

Within the sections of Hypnodendron (Touw, 1971) taxa show spatial separation. Two examples are presented. In H. sect. Hypnodendron (Figure 19.7), H. junghuhnii (Malaysia, western Indonesia, Philippines, Papua New Guinea) and H. vitiense (Taiwan, Philippines, Papua New Guinea, Bismarck Archipelago, Solomon Islands, Vanuatu, New Caledonia, Fiji, Samoa [Savaii, Upolu], north-east Queensland, eastern Australia to Tasmania), are largely vicariant; H. spininervium (New Zealand, south-east Australia, Tasmania) overlaps with H. vitiense in south-east Australia and Tasmania; H. samoanum (Samoa [Tutuila], Society Islands, and the Marquesas); H. microstichum (southern South America); H. marginatum is endemic to New Zealand. Hypnodendron sect Comosa has six species (Figure 19.8), with a centre of diversity in New Zealand: H. comatulum (north-east Queensland); H. camptotheca (New Caledonia); H. comosum

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Hypnodendron junghuhnii Hypnodendron microstichum

Hypnodendron vitiense ssp. australe

Hypnodendron samoanum

Hypnodendron vitiense ssp. vitiense

Hypnodendron spininervium

Hypnodendron vitiense (unknown ssp.)

FIGURE 19.7 Distribution of Hypnodendron sect. Hypnodendron (Hypnodendraceae). See text for details.

Hypnodendron comosum Hypnodendron camptotheca Hypnodendron comatulum Hypnodendron dendroides Hypnodendron tahiticum

FIGURE 19.8 Distribution of Hypnodendron sect. Comosa (Hypnodendraceae). See text for details.

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(New Zealand, south-east Australia, Tasmania); H. dendroides (south-east Asia, Papua New Guinea, Solomon Islands, Vanuatu, and Fiji); H. tahiticum (Samoa, Society Islands, and the Marquesas). Hypnodendron colensoi and H. comatum are endemic to New Zealand (not shown).

19.5 DISCUSSION 19.5.1 GENERAL PATTERN

OF

ALLOPATRY

By mapping the distributions of individual species it is apparent that different species have distributions that highlight different biological relations between areas within Australasia. The addition of species reinforces the pattern by repeating distributions wholly or partly, or by the patterns marking boundaries for taxa. For example, Track 1 is a southern boundary for several species examined here and is also the distribution of other species (e.g., Camptochaete subporotrichoides). Similarly, Track 3 (central eastern Australia–New Caledonia) corresponds to the distribution of some species (Camptochaete leichhardtii). It is also a boundary within Camptochaete, and a northern or southern boundary for many other species. As noted above, the eastern end of this track is known as the Macpherson–Macleay Overlap, an important locality in the region. Examples of taxa with distributions that correspond to these tracks are readily found in other groups of mosses. For example Hypopterygium flavolimbatum (Kruijer, 2002) and Hypnodendron milnei (Touw, 1971) correspond to Track 1; Dawsonia longiseta (Van Zanten, 1973), Track 2; Hypnum chrysogaster (Ando, 1982), Eucamptodon muelleri (Allen, 1987), and Macromitrium leratii (Vitt and Ramsay, 1985), Track 3; Hypopterygium didictyon (Kruijer, 2002), Trachyloma planifolium (Miller and Manuel, 1982), Track 5. Examples of Track 4 are not common in mosses. Braithwaitea sulcata (Touw, 1971) and Hypopterygium discolor (Kruijer, 2002) are examples of species with distributions linking northern New Zealand to the north: to New Caledonia and central eastern Australia in B. sulcata and to central eastern Australia in H. discolor. These distributions highlight a connection between northern New Zealand and Track 3, the central area of overlap between Track 1 to the north and Track 5 to the south. Other examples of moss distributions in the Australasian region are found in the following: Calomnion (Vitt, 1995), Mitthyridium (Nowak, 1980), Neckeropsis (Touw, 1962), Trachypodaceae (Van Zanten, 1959), Ctenidium (Nishimura, 1985), and Thuidiaceae (Touw, 2001). This general pattern of relationships between areas is built up from the distributions of unrelated taxa, in this and previous analyses (Burbidge, 1960; Croizat, 1964; Tangney, 1990). It is independent of taxon relations as it is the sum of individual species distributions, compiled through mapping populations of different taxa at various taxonomic levels, each with different ecologies and dispersal capabilities. These biological characteristics are not correlated with the distribution patterns, and are therefore not an explanation for the pattern. Furthermore, comparison of the distributions of related taxa reveals well-developed spatial separation within groups. Within the groups examined individual taxa highlight different aspects of the general pattern of distribution, with the more closely related taxa replacing each other in space. The generality of the pattern discounts random dispersal of the individual taxa from a centre of origin, and the pattern of vicariance strongly suggests in situ allopatric evolution within a preexisting ancestral range.

19.5.2 DISTRIBUTION

OF THE

LEMBOPHYLLACEAE

These two facets of distribution (adherence to a general pattern and spatial replacement of related taxa) are readily seen in the distribution of the Lembophyllaceae. The family consists of a core of Australasian taxa with genera and sister-group relations that are global in scope, involving all the continents. Within Australasia they exhibit a pattern of replacement of substantial allopatry that is consistent with the general pattern of distribution in the region. Sister-group relations derived from

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molecular data (Quandt et al., in press) involve genera such as Rigodium (Central and South America, East Africa and Madagasca), Isothecium (widespread Northern Hemisphere), Pilotrichella (Hawaii, tropical America, Africa and Madagascar), Dolichomitra and Dolichomitropsis (south-east Asia), and Tripterocladium and Bestia (western North America), thus yielding a familial distribution spanning both hemispheres and centred on the Pacific Ocean. The combination of allopatric evolution within Australasia and global relationships suggests that the Australasian region is only one among several centres of evolution within this group of pleurocarpus mosses. The sister-group of a broadly defined Lembophyllaceae, the Neckeraceae–Thamnobryaceae clade, is also a distinct evolutionary lineage, global in distribution. This sister-group relation between two independent lineages suggests that the biogeographic relationships are the legacy of ancestral distributions of a global nature laid down at the time of the origin of the major clades of pleurocarpous mosses they represent.

19.5.3 COMPARISON

WITH THE

ANGIOSPERMS

The origin of the pleurocarps with respect to that of the angiosperms has long been of interest to bryologists (Newton et al., Chapter 17), and the distributions of angiosperms in the region provide comparisons with those of the mosses. The genus Nothofagus, for example, considered to be a key taxon in austral biogeography (Hill, 1996), has a present-day range (Figure 19.9) almost exactly that of the Australasian Lembophyllaceae (Figure 19.2). Within Nothofagus, species distributions highlight the main features of the general pattern of distribution in the region, including a northern limit at Papua New Guinea, differentiation about the line Macpherson–Macleay Overlap–New Caledonia, and strong southern Australasia–southern South America connections, as well as vicariance within the genus (Heads, 1990). The same repeated patterns of distribution were also found in Australasian flowering plants (Proteaceae) by Weston and Crisp (1996), who used track analysis to compare distributions, and their resulting patterns reinforced those outlined earlier by Burbidge (1960) and Croizat (1964). These patterns are generally considered to be related to the Cretaceous tectonic features of eastern Gondwana, ca. 80 million years ago. For example, the east–west rifting of New

FIGURE 19.9 Distribution of extant Nothofagus.

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Zealand–New Caledonia–Solomon Islands from eastern Australia has been used to explain biotic similarities between New Zealand and south-east Australia, eastern Australia and New Caledonia and across the Coral Sea to the north, and distributions extending to Fiji in the east, i.e., those exhibiting fidelity with the Gondwanic province (Weston and Crisp, 1996). The biogeographic significance of these tectonic features is here supported by the strong east–west differentiation of taxa, implying the existence of pre-rifting ancestral populations, and the north–south differentiation around the axis MacPherson–Macleay Overlap–New Caledonia implies differentiation within the ancestral range prior to rifting. The dating of the rifting event means that the ancestral populations and, perhaps already, differentiation within the ancestral populations, were established by the end of the mid to late Cretaceous. Weston and Crisp (1996) considered that the age of the Australasian Proteaceae, based on fossils, and its distribution patterns were consistent with the known extent of Gondwana, allowing the distributions to be established over land, and they saw “… no need to invoke ad hoc dispersal hypotheses to explain these patterns” (Weston and Crisp, 1996: 228). Similar arguments could be used to explain the distribution of Nothofagus, which shows a similar antiquity and the same distribution, although a literal reading of the fossil record (see Heads, 2005) required Hill (1996) to postulate long-distance dispersal for some distributions within Nothofagus. These differing explanations for the same distribution highlight a perception in biogeography that the assumed age of individual taxa is more important than correspondence to a shared pattern of evolution. Indications of recency in the age of taxa, for example from molecular data, are often used as evidence for disjunctions being the product of long-distance dispersal; the taxon is assumed to have not existed before the rifting event and therefore must have crossed the ocean after its origin. The species within the Australasian Lembophyllaceae could be considered to be recent, based on molecular data. There are low base pair differences for rbcL between species of Weymouthia (Quandt et al., 2001) and Camptochaete, as well as conspecific trans-Tasman and transSouthern Ocean disjunctions. However, these could indicate either recent differentiation within the Australasian Lembophyllaceae, very low rates of mutation in these taxa, or evolution followed by a long period of stasis. Frey et al. (1999) considered Lopidium concinnum to be an example of the latter, and McDaniel and Shaw (2003) found vicariant phylogeographic structure in the transantarctic disjunct distribution of the moss Pyrrhobryum mnioides, which they dated through calibration of their phylogeny to at least 80 mya. Thus, the same distribution pattern among these southern land masses is exhibited by mosses at different taxonomic levels. This, combined with the lack of correlation between the distribution of species and their dispersal capability and the strong relation that exists between taxa and localities, also supports the view that evolution has occurred in different groups at different times, and/or to different extents, within congruent ancestral ranges that have been disrupted by tectonic change. Increasingly, the tectonic environment of the region is being seen as much more complex than the result of the movement of several large continental plates. Correlation between microplates (terranes) and biotic distributions are becoming important in biogeographic studies (Polhemus, 1996; Heads, 2003), reflecting a concern with the fine scale details of distributions and tectonic processes. Additionally, the relation between biogeography and geology is being questioned. As more attention is paid to the facts of biotic distribution, the traditional explanatory power of geological scenarios is taken less for granted. Although orthodox reconstructions of Gondwana may explain the common disjunctions between Australasia and southern South America, transPacific disjunctions involving the central and northern Pacific cannot easily be explained by a scenario that postulates a continuously open Pacific Ocean (McCarthy, 2003). Nothofagus and the Australasian Lembophyllaceae are good examples of groups with austral distributions that are commonly perceived as Gondwanic. However, in both cases their wider relationships encompass taxa with distributions that, taken together, span both hemispheres and are centred on the Pacific Ocean (see also Craw, 1985). Such distributions are not explained by Gondwana reconstructions.

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Biogeographic explanations are needed that address both the general pattern of distribution and the vicariance of related taxa.

19.6 CONCLUSIONS The presence of a pattern of repeated distributions emphasizes the value of geographic data in biogeographic analysis and the need for careful study of the locality data of taxa. The patterns show distinct repeated features, as well as replacement of related taxa, supporting a strong relation between taxa and locality that suggests evolution in situ within the region, rather than dispersal of preexisting taxa into the region from an external centre of origin. The pattern of relationships between areas (biogeographic information) is the same for diverse taxa and independent of assumptions of taxon age and biological characteristics, for example, vagility and survivability. This general pattern of evolution provides a biogeographic context for the synthesis of geological data. The spatial pattern exhibited by the pleurocarps is correlated with that shown by angiosperms in the region. For example, Nothofagus and examples from the Proteaceae have the same distributions, and these patterns have been related to Gondwana era tectonic events in the region. Croizat (1964) considered the Australasian region to be a major centre of evolution of global importance. He called it the Polynesian Gate and a cradle of evolution in the angiosperms. Similarly, it is an important region for pleurocarps. The different groups of pleurocarpous mosses examined here span the pleurocarp phylogeny, showing that the close relation of these mosses with locality in the region is not just a local feature of one group, but is a general feature of pleurocarpy in the region. With the diversification of most major lineages of pleurocarps completed by 130 mya and the majority of the extant Hypnalean lineages by 98 mya (Newton et al., Chapter 17), at the latest, the ancestral ranges of these mosses could well have been established by the tectonic events that formed the modern geography of the region, with subsequent evolution occurring in situ.

ACKNOWLEDGMENTS I wish to thank Michael Heads for his helpful comments on this chapter, Chris Meechan for skillfully producing the figures for publication and Katherine Vint for her help in the early stages of the manuscript.

REFERENCES Allen, B. H. (1987) A revision of the Dicnemonaceae (Musci). Journal of the Hattori Botanical Laboratory, 62: 1–100. Ando, H. (1982) Hypnum in Ausralasia and the southern Pacific. Journal of the Hattori Botanical Laboratory, 52: 93–101. Burbidge, N. T. (1960) The phytogeography of the Australian region. Australian Journal of Botany, 8: 75–211. Craw, R. C. (1985) Classic problems of southern hemisphere biogeography re-examined. Zeitschrift für Zoologische Systematik und Evolutionsforschung, 23: 1–10. Craw, R. C., Grehan, J. R. and Heads, M. J. (1999) Panbiogeography:Tracking the History of Life. Oxford University Press, New York. Croizat, L. (1964) Space, Time, Form: The Biological Synthesis. Published by the author, Caracas. Frey, W., Stech, M. and Meissner, K. (1999) Chloroplast DNA relationships in palaeoaustral Lopidium concinnum (Hypopterygiaceae, Musci). An example of stenoevolution in mosses. Studies in austral temperate rainfall bryophytes 2. Plant Systematics and Evolution, 218: 67–75. Grehan, J. R. (2001) Panbiogeography from tracks to ocean basins: Evolving perspectives. Journal of Biogeography, 28: 413–429. Heads, M. J. (1990) Integrating earth and life sciences in New Zealand natural history: The parallel arcs model. New Zealand Journal of Zoology, 16: 549–585.

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Heads, M. J. (2003) Ericaceae in Melanesia: Vicariance biogeography, terrane tectonics and ecology. Telopea, 101: 311–449. Heads, M. J. (2005) Dating nodes on molecular phylogenies: A critique of molecular biogeography. Cladistics, 21: 62–78. Hill, R. S. (1996) The riddle of unique Southern Hemisphere Nothofagus on southwest Pacific islands: Its challenge to biogeographers. In The Origin and Evolution of Pacific Island Biotas, New Guinea to Eastern Polynesia: Patterns and Processes (eds A. Keast and S. E Miller). SPB Academic Publishing, Amsterdam, pp. 215–232. Keast, A. and Miller, S. E. (eds). (1996) The Origin and Evolution of Pacific Island Biotas, New Guinea to Eastern Polynesia: Patterns and Processes. SPB Academic Publishing, Amsterdam. Kruijer, H. (2002) Hypopterygiaceae of the World. Blumea, Supplement 13: 1–388. McCarthy, D. M. (2003) The trans-Pacific zipper effect: Disjunct sister taxa and matching geological outlines that link the Pacific margins. Journal of Biogeography, 30: 1545–1561. McDaniel, S. F. and Shaw, A. J. (2003) Phylogeographic structure and cryptic speciation in the trans-Antarctic moss Pyrrhobryum mnioides. Evolution, 57 (2): 205–215. Miller, N. G. and Manuel, M. (1982) Trachyloma (Bryophytina, Pterobryaceae): A taxonomic monograph. Journal of the Hattori Botanical Laboratory, 51: 273–321. Nishimura, N. (1985) A revision of the genus Ctenidium (Musci). Journal of the Hattori Botanical Laboratory, 58: 1–82. Nowak, H. (1980) Revision de Laubmoosgattung Mytthyridium (Mitten) Robinson für Ozeanien (Calymperaceae). Bryophytorum Bibliotheca, Band 20, J. Cramer, Vaduz, pp. 1–236. Polhemus, D. A. (1996) Island arcs and their influence on Indo-Pacific biogeography. In The Origin and Evolution of Pacific Island Biotas, New Guinea to Eastern Polynesia: Patterns and Processes (ed. A. Keast and S.E Miller). SPB Academic Publishing, Amsterdam, pp. 215–232. Quandt, D., Frahm, J.-P. and Frey, W. (2001) Patterns of molecular divergence within the palaeoaustral genus Weymouthia Broth. (Lembophyllaceae, Bryopsida). Studies in austral temperate rain forest bryophytes 11. Journal of Bryology, 23: 305–311. Quandt, D., Huttunen, S., Tangney, R. S. and Stech, M. A molecular generic revision of the Lembophyllaceae. Systematic Botany, in press. Tangney, R. S. (1990) Moss biogeography in the Tasman Sea region. New Zealand Journal of Zoology, 16: 665–678. Tangney, R. S. (1997a) A taxonomic revision of the genus Camptochaete Reichdt., Lembophyllaceae (Musci). Journal of the Hattori Botanical Laboratory, 81: 53–121. Tangney, R. S. (1997b) A generic revision of the Lembophyllaceae. (Musci). Journal of the Hattori Botanical Laboratory, 81: 123–153. Touw, A. (1962) Revision of the moss genus Neckeropsis (Neckeraceae). I. Asiatic and Pacific species. Blumea 11 (2): 373–425. Touw, A. (1971) A taxonomic revision of the Hypnodendraceae (Musci). Blumea, 19 (2): 211–354. Touw, A. (2001) A taxonomic revision of the Thuidiaceae (Musci) of tropical Asia, the Western Pacific and Hawaii. Journal of the Hattori Botanical Laboratory, 91: 1–136. Van Zanten, B. O. (1959) Trachypodaceae, a critical revision. Blumea, 9(2): 477–575. Van Zanten, B. O. (1973) A taxonomic revision of the genus Dawsonia R. Brown. Lindbergia, 2: 93–101. Vitt, D. H. (1995) The genus Calomnion (Bryopsida): Taxonomy, phylogeny and biogeography. Bryologist, 98 (3): 338–358. Vitt, D. H. and Ramsay, H. P. (1985) The Macromitrium complex in Australasia (Orthotrichaceae: Bryopsida). I. Taxonomy and phylogenetic relationships. Journal of the Hattori Botanical Laboratory, 59: 325–451. Weston, P. H. and Crisp, M. D. (1996) Trans-Pacific biogeographic patterns in the Proteaceae. In The Origin and Evolution of Pacific Island Biotas, New Guinea to Eastern Polynesia: Patterns and Processes (ed. A. Keast and S. E. Miller). SPB Academic Publishing, Amsterdam, pp. 215–232.

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Index χ2 statistic, 375, 376 25S rDNA, 179 26S nrDNA, 81 5.8S rDNA, 179

A Abietinella, 179, 273, 276 abscission cell, thin-walled, 112 ACCTRAN, 47, 51, 52, 61, 66 Acrocarpi, 44, 288 acrocarpous grade, 289, 338 acrocarpous lineages, well-resolved, 338 acrocarpous mosses, 322, 325, 326 determinate growth, 290 pendulous growth form, 291 acrocarpy, concept of, 287 reversal from pleurocarpy, 22, 51, 61, 288, 294 transition to pleurocarpy, 42 acrotonous growth, 302 Actinodontium, 11 Adelothecium bogotense, 369, 375 Aerobryidium, 145, 152, 153, 155, 157, 158, 159, 160 Aerobryidium–Pseudospiridentopsis–Meteoriopsis clade, 152, 158 Aerobryidium filamentosum, 157 Aerobryopsis, 147, 154, 157, 158, 159, 160, 233 Aerobryopsis longissima, 150, 158 Aerobryopsis wallichii, 150, 158, 159 Aerobryum, 146, 147 Aerolindigia, 128, 135, 153 Aerolindigia capillacea, 135 AFLP markers, 172 Africa, 135, 138, 139, 248, 255, 258, 262, 263, 265, 266, 401, 404 South, 138, 325 West, 262 age constraints, minimum, 346 age estimates, fossil-based, 340 age, minimum permitted, 346 alar cells, 166 differentiated, 159, 220, 223, 248 numerous, 258, 259 reaching costa, 259 rectangular, 159, 248 sub-quadrate, 258 undifferentiated, 224 alar region morphology, plastic, 263 alar region, in asymmetrical leaves, 258 Alignment Editor Align, 149 alignment method, 121, 127 affect on topology, 153, 160

ambiguity in ITS, 169 different positioning of nucleotides, 153 manual, 149, 150, 152, 160, 372 subjective manual, 182 alkanes, 77 Allen, Bruce Hampton, 11 allopatric evolution, 394, 397, 403, 404 Alophosia, 361 Alsia, 280, 283 Altai, 134 alternation of generations, 8 Amblystegiaceae, 13, 135, 141, 163–173, 178, 196, 199, 201, 202, 203, 216, 217, 219, 220, 222, 224, 228, 232, 233, 271, 283, 286, 334 desiccation tolerance, 168 Japanese, 167 Kindberg, 164 novel generic concepts, 168 phenotypic plasticity, 168, 169, 172 phylogenetic relationships, 166 Roth, 164 subdivisions, 167 subfamilies, 167 traditional taxonomy, 167 Amblystegiaceae s. lat., 168, 169, 170, 232 Amblystegiaceae s. str., species composition, 217 Amblystegiaceae s. str., 163, 167, 169, 170, 171, 172, 216, 217, 219, 222 Amblystegiaceae–Calliergonaceae, 169 Amblystegiaceae–Thuidiaceae, 166 Amblystegioideae, 167 Amblystegium, 164, 165, 166, 167, 168, 170, 296, 299, 302, 303 Amblystegium serpens, 45 America, 255 eastern North, 141 North, 138, 140, 141, 152, 360, 404 South, 138, 141, 150, 155, 158, 159, 160, 216, 397, 401, 494, 405 western North, 140 American Bryological and Lichenological Society, 2 amphigastria, 66, 77 amphithecium, 249 amplified fragments, 369 Anacamptodon, 13, 141, 165, 168, 170, 171, 178, 203, 271 analysis, skewed, 238 anatomical characters, see characters, anatomical ancestor, 379, 380, 381, 389 ancestral character state reconstructions, 389 ancestral range, 394, 397, 403, 405, 406 Ancistrodes, 147, 150, 159 Anderson, Lewis Edward, 10 Andreaea, 290, 325, 351

409

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410 Andreaeobryum, 351 angiosperm crown group, 359, 362 speciose, 36 angiosperm diversification, 362 preceded by pleurocarp diversification, 359 relaxed model, 357 strict model, 357 angiosperm forests, complex, 338, 359 angiosperms, appearance of, 338 first appearance, 359 fixed crown group age, 359 fossil history, 359 influence on pleurocarpous moss diversification, 359 anisophylly and heterophylly, treated as synonymous, 295 anisophylly, 295, 298, 304, 305 in Heterocladium and Neckeraceae, 200 annulus, 265, 373, 380–381, 383 absent, 203 separating, 167, 229, 236, 237, 238 anomalous taxa, 351 Anomodon, 179, 185, 194, 192, 196, 199, 200, 203, 294, 298 Anomodon giraldii, 200 Anomodon longifolius, 45, 199, 200 Anomodon rostratus, 199, 200, 203 Anomodon rugelii, 185, 199, 203 Antarctica, 324 antheridia, 368 antherozoids, transfer of, 339 anticlinal walls, autolysis, 250 Antitrichia, 178, 187, 196, 199–200 Antitrichiaceae, 187, 199–200, 271 aperistomate mosses, 351, 361 apical cell, 42, 44, 51, 270, 272 cutting faces, 42 damaged, 291 undifferentiated, 294 apical cell derivatives, 270 apical cell development, 290 apical dominance, 300 loss of, 301 apical meristem, 42 Apterygium, 164 Aptian, Early, 341 aquatic, 121, 137–138, 139, 141, 142, 216, 326, 327, 334 Arbusculohypopterygium, 66, 81, 102 Arbusculohypopterygium arbuscula, 80, 102 archegonia, 44, 45 lateral, in acrocarpous mosses, 288 architectural characters, 292 architectural elements, 303 architectural groundplan, 303 architectural models, 314 architectural unit, 309, 310, 311, 312, 313, 314, 315, 316, 317 architecture, pleurocarpous, 52 arctic-boreal gradient, 256 areolation, 44 Aristovia, 360 aromatic ring, 74

Pleurocarpous Mosses: Systematics and Evolution arthrodontous mosses, 351, 352, 361 Asia, 139, 254, 395, 397, 401, 403, 404 East, 140, 141 East + North America, 140 South East, 155, 158, 159, 160 West, 139 asymmetry, species diversity, 36, 357 atpB–rbcL, 22, 23, 30, 118, 169, 170, 218, 219, 220, 221 Aulacomniaceae, 21 acrocarpous, 21, 352 Aulacomnium, 20, 21, 22, 23, 34, 35, 36, 37, 42, 51 Aulacomnium androgynum, 51, 361 Aulacomnium heterostichoides, 361 Aulacomnium heterostichum, 36, 50–51 Aulacomnium turgidum, 361 Australasia, 49, 66 Australia, 138, 139, 155, 257, 395, 396, 397, 398, 399, 403, 405 eastern, 36 autoicous sexuality, 48, 224, 265, 274 auxins, 300 axes, orthotrophic, 112 plagiotrophic, 112 axial cavity, see cavity, axial axillary hairs, 9, 12, 72, 103, 141, 154, 157, 161, 229, 259, 260, 262, 263, 271 apical cell shape, 154 bent, 153, 159 branching, biseriate, 154, 155 brown basal cells, 155 complex, 154 short hyaline, 139 terminal cell, 103, 138 axis types, 312, 316, 317

B Bajdaievia, 322, 323, 334 Bajdaievia linearis, 322, 323 Baltic amber, 322, 326 Barbella, 147, 157, 158, 159, 160, 322 Barbella compressiramea, 158 Barbella flagellifera, 159 Barbella sect. Aerobryella, 159 Barbella sect. Elongata, 159 Barbella turgida, 158 Barbellopsis, 153, 157, 158, 160 Barbellopsis macroblasta, 158 Barbellopsis trichophora, 150, 158 Barremian, Late, 346 Bartramia, 291 Bartramiaceae, 21, 23, 32, 34, 259, 355 Bartramiineae, 21 base change, compensating, 127 Bayesian analysis, see also MrBayes Bayesian analysis, 345, 374 heterogeneous, 374 homogeneous, 374 Bayesian heterogeneous model, 376

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Index Bayesian homogeneous model, 376 Bayesian posterior distribution, 345 Bescherellia, 21 Bescherellia elegantissima, 48–49 Bestia, 404 biodiversity estimates, 356 BioEdit 7.0.1, 181 biological context of relationships, 240 Bismarck Archipelago, 401 bootstrap analysis, 28, 86, 94, 219, 374 nonparametric, 374 Borneo, 114, 399 BRA, 126 Brachymenium, 12 Brachytheciacanae, 166 Brachytheciaceae, 12, 14, 50, 118, 121, 127, 128, 129, 130, 138, 140, 141, 146, 147, 150, 179, 193, 196, 199, 200, 217, 233, 240, 249, 283, 355, 358, 359 diversification, mid-Cenozoic, 359 non-monophyletic, 200 origin, Late Cretaceous, 359 species diversity, 356 taxa poorly differentiated, 357 Brachytheciaceae clade, 200 Brachytheciaceae + Ctenidiaceae + Hylocomiaceae complex, 200 Brachytheciaceae + Meteoriaceae, 193 Brachytheciastrum, 118, 130, 140 Brachytheciastrum trachypodium, 140 Brachytheciastrum velutinum, 138 Brachythecioideae, 118, 127, 128, 130 delimitation, 130 Brachythecium, 12, 118, 141, 257, 299, 300, 355 Brachythecium cirrosum, 127 Brachythecium frigidum, 141 Brachythecium novae-angliae, 141 Brachythecium percurrens, 129, 138 Brachythecium rivulare, 141 Brachythecium rutabulum, 300, 359 Brachythecium salebrosum, 128 Braithwaitea sulcata, 395, 403 branch, see also module central strand, 103 determinate, 273 inaccurate terminology, 290 branch characters, non-independence, 297 branch development, 277, 283–284 Bryum-type, 276 Climacium-type, 260, 276 branch differentiation, control of, 342 branch formation, distal, 298 branch initial zone, 277 branch initials, see branch primordia branch initiation, basal, 114 branch lengths, short, 338 branch orientation, relative to other secondary modules, 297 relative to primary module axis, 297 relative to substrate, 298 branch origin, 289

411 branch position, 114 branch primordia, 44, 51, 66, 118, 146, 264, 272, 273, 274, 294 control by external factors, 300 development, 259, 300 differences in distibution along module, 300 differences in number between modules, 300 distribution, 300 dormant, 261, 273, 295, 300 immature, 261 pre-programmed, 300 selective development, 300 sub-perichaetial, 44 sub-perichaetial, in pleurocarpous mosses, 302 sub-perigonial, in pleurocarpous mosses, 302 suppression of development by auxins, 300 branch primordium, concave vs. convex, 276 branch support, 32, 35 branch system, new, 301 non-hierarchical, 301 branches, easily detached, 233 specialized, 44 subterminal, 274 ultimate, 101 branching, angle, 297 apical, 51, 61 basal, 45, 47–48, 49, 50, 52, 63, 66 complanate, 203, 297 fan, 103, 104 facultative, 103 obligate, 103 mode of, 289 monopodial, 114, 273, 274 non-complanate, 197 palmate, 101 pinnate, 101, 103, 195, 197 in Uskatia, 323 radial, 203, 297 reduction, 73, 74 subterminal, 274 sympodial, 114, 273, 274 umbellate, 101 vegetative, 44, 48, 49, 50, 52, 62–63 branching analysis, 309, 310 branching architecture, 44, 45, 47–49, 289, 290, 293, 306, 352, 361 branching hierarchy, 44 branching pattern, 114, 273, 289, 290 change on substrate contact, 293, 294 in acrocarps, 290 relation to primordium dormancy, 300 seasonal changes, 293 Breidleria, 187, 193, 196, 203, 216 Breidleria pratensis, 187 Bremer support, 130 Bridel-Brideri, Samuel-Elisée de, 5 broad-leafed group, in Hygrohypnum, 220, 223, 224 brood branches, 274

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412 Brothera, 141 Brotherella, 320 Brotherus, Viktor Ferdinand, 6, 9 Bryaceae, 12, 34, 249, 289, 351 species diversity, 356 Bryalean pleurocarpous mosses, see pleurocarpous mosses, bryalean Bryales, 20, 21, 72, 352, 355, 361 Bryanae, acrocarpous paraphyletic grade, 351 species diversity, 356 Bryhnia hultenii, 140 Bryhnia novae-angliae, 140 Bryhnia scabrida, 140 Bryidae, 20, 23, 34 position of rhizogonian mosses within, 32 Bryinae, acrocarpous, 355 Bryoandersonia, 129 Bryocrumia, 276 Bryokhutuliinia jurassica, 325, 326, 327, 334 Bryologia Europaea, 4 Bryonoguchia, 276 Bryopsida, 321 Bryowijkia, 291, 355 Bryum, 290 Bryum argenteum, 256 Buck, William Russel, 12 Buckley Formation, 324 Bureya River, 325, 326 burn-in, 374 “bush,” speciose, 338 Buxbaumia, 351, 352

C calibration point, 343 Callialaria, 168 Callicladium, 185, 216 Calliergon, 161,164, 165, 167, 168, 170, 172, 173, 196, 216, 217, 218, 220, 222, 223, 229, 232, 236, 271 Calliergon cordifolium, 170, 217, 218, 220 Calliergon giganteum, 170 Calliergon megalophyllum, 172 Calliergonaceae, 163, 165, 167, 169, 170, 171, 172, 173, 196, 199, 202–203, 216, 217, 220, 223, 224, 232, 271, 274 species composition, 217 Calliergonaceae clade, 199, 202–203 Calliergonella, 164, 165, 167, 168, 169, 170, 187, 194, 196, 203, 216, 236 Calliergonoideae, 167, 168 Calliergon–Warnstorfia–Hamatocaulis–Scorpidium clade, 216 Callovia–Oxfordian, 361 Calomnion, 20, 21, 22, 23, 35, 37, 42, 47, 51, 52, 352, 403 acrocarpous, 21 monophyletic, 21 peristome, 21 Calomnion brownseyi, 35

Pleurocarpous Mosses: Systematics and Evolution Calomnion complanatum, 35, 50, 51 Calomnion–Cryptopodium clade, 51 Calyptothecium, 294, 298 calyptra, anatomy, 72 cucullate, 374, 380 hairy, 204 mitrate, 101, 102, 374, 380, 383 correlated with dwarf males, 390 synapomorphy, 384 ornamentation, 72 calyptra characters, 77 calyptra structure, 12 Calyptrochaeta, 111, 112, 114, 115 Calyptrochaeta microblasta, 112 Calyptrochaeta parvireta, 114 Calyptrochaeta ramosa, 114 Calyptrochaeta remotifolia, 114 Cameroon, 255 Campanian, 360 Camptochaete, 314, 315, 316, 395, 399 Camptochaete angustata, 397, 399 Camptochaete arbuscula, 314, 315, 399 Camptochaete curvata, 399 Camptochaete deflexa, 397, 399 Camptochaete excavata, 396, 399 Camptochaete leichhardtii, 395, 399, 403 Camptochaete papuana, 399 Camptochaete porotrichoides, 399 Camptochaete pulvinata, 399 Camptochaete sect. Camptochaete, 397 Camptochaete sect. Thamniella, 399 Camptochaete subporotrichoides, 395, 399, 504 Camptothecium, 368 Campyliaceae, 167 Campyliadelphus, 164, 165, 167, 168, 170, 171 Campylidium, 202 Campylium, 163, 164, 165, 167, 168, 170, 171, 173, 232, 236, 276 Campylium + Leptodictyum, 201 ‘Campylium hispidulum’ group, 202 Campylium s. lat., 224 Campylophyllum, 164, 165, 166, 167, 168, 169, 170, 196, 201, 225, 284 Campylophyllum halleri, 164, 170, 216, 217, 218, 219, 220, 221, 224 Canalohypopterygium, 66, 73, 74, 80, 81, 94, 102 Canalohypopterygium tamariscinum, 101, 102, 105 Canonical Discriminate Analysis, 262 Capesius, Ingrid, 66 capsule, 8-ribbed, see capsule, furrowed antitropous, 240 brachythecioid, 237 cernuous, 237, 240 constriction below mouth, 166 curved cylindrical, 164, 233, 236 curved, 11, 164, 197, 198, 200 emergent, 373 erect, 141, 237, 238, 250, 249, 265

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Index furrowed, 369, 372, 373, 383 correlated with dwarf males, 390 homology, 2, 8 homotropous, 240 horizontal, 237, 238, 240 immersed, 373 inclined, 237, 240 isobryoid, 237 linear dehiscence, 351 orientation, 5, 11, 204 orientation in habitat, 237, 240 orientation relative to seta, 237, 240 orthotropous, 228, 231, 233, 237, 238, 240 pendulous, 237, 240 plagiothecioid, 237 reclinate, 240 sematophylloid, 237 seta-oriented, 240 shape, 121, 166, 229, 233 smooth, 374, 381, 389 straight, 198, 200, 237 sulcate, 36 capsule characters, conservative, 11 Carboniferous, Early, 346 Late, 346 moss fossils, 357 Caribbean, 66 Carribaeohypnum, 201 Catagoniaceae, 233 Catharomnion, 66, 72, 73, 80, 81, 94, 99, 102 Catharomnion ciliatum, 73, 101, 102, 103, 105 Catoscopiaceae, 21 cavity, axial, 101, 102 central, 73, 74, 102, 105 branch, 73 rudimentary branch, 73, 74 stem, 73, 102, 105 cortical, 73 branch, 73 stem, 73 inclusions, 73, 105 oil droplets, 74 stipe, 102 cavity system, 73 cell lineage, 44 cell shape, 12 Cenozoic, 354, 357, 359, 360, 362 Early to mid, 362 Early, 338, 359, 362 Central America, 66, 216 central cavity, see cavity, central, central strand, 103 well-developed, 224 center of diversity, tropical, 5 Chaetomitrium, 141 Chaetosphaeridium, 351 Chara, 351 character change, correlated with plant size, 167, 173 character concepts and coding, 42, 44, 45, 52, 61, 62

413 character delimitation, 147 character diversification, 339 character, key, 229, 231, 232, 233, 240 character, multistate, 373, 389 character plasticity, 146 character selection, 80 character state, ancestral, 373, 389 character state coding, 77, 80, 373 character state descriptions, 373 character state reconstructions, 389 character states, morphological, 375, 377, 389 shared derived, 228, 230 character systems, 289 characters, anatomical, 216, 228 artificial, 61 binary, 373, 389 diagnostic, 146 habitat, 372 inapplicable, 45 independent, 12 informative, 29 key, 166 morphological, 216, 372, 377 in cladistic analysis, 289 multistate, 373 peristome, 12 quantitative, 167 sporophyte, 167 Charales, 351 Chile, 138, 369 Chilean specimen, 369, 375, 376 China, 129, 136, 138, 140, 155, 401 China + North America, 140 chloroplast DNA sequences, 167, 169, 369 chronogram, 351 Chrysocladium, 147, 154, 155, 156, 160 monospecific genus, 155 Chrysocladium retrorsum, 156, 160 Chrysosquarridium, 155, 160 circumboreal, 140 Cirriphyllum, 126, 128 Cirriphyllum koponenii, 126 clade resolution, 32 clades, resolved, 33 cladistic analysis, morphological data, 164, 166, 168 cladocarp, subperichaetial innovations, 44, 61 cladocarpous mosses, indeterminate growth, 290 non-monophyletic, 305 transitional between acrocarps and pleurocarps, 288 within pleurocarp clade, 302 cladocarpy, 42, 274, 305 character state reversal, 305 concept of, 288 plesiomorphic, 305 short branch, 44 Cladomnion, 369, 374, 377, 389 Cladomnion–Dichelodontium–Ptychomnion clade, 389 Cladomnion ericoides, 373

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414 Cladomnion–Garovaglia subelegans clade, 376, 380 Cladomniopsis, 369, 374, 376 Claopodium, 179, 196, 199, 200, 203 Claopodium clade, 200 Claopodium whippleanum, 200 Clasmatodon, 135, 141, 178, 198, 194, 204 Clasmatodon parvulus, 127 classification, conflict between gametophyte and sporophyte, 3, 10 conflict between morphology and molecular data, 13–14 family, 9 Fleischer–Brotherus, 9, 147 global, 6 infrafamilial, 118 underlying philosophies, 2, 5, 13 classification of, Amblystegiaceae, new, 164 mosses, 349 pleurocarps, 2 classification on, all characters, 12 gametophyte characters, 4, 6, 9, 11, 12, 13 key characters, 232 molecular characters, 13, 14 new morphological characters, 9 peristome characters, 3, 6 sporophyte characters, 3, 6, 147 Climaciaceae, 196, 197 Climacium, 196, 200, 270, 276, 281, 282, 283, 295, 297 climate change, 362 clonal evolution, within polyploid lineages, 172 clonal variation, 266 Coleochaetales, 351 colonizers, early successional, 360 combined evidence, 22, 28, 29, 33, 65, 66, 81, 86, 94, 99, 101, 152 combined evidence tree, 29, 32, 35 complanate branching, see branching, complanate complanate leaf arrangement, see foliation, complanate complex thalloids, 357 Conardia, 165, 168, 169, 170, 194, 196, 198, 203 confidence level, 375, 376 congruence, in results of analyses, 181 coniferous forest, 340, 362 consensus tree, all compatible majority rule, 351 calibrated, 351 conservative regions, 181, 187 convergence, 374 due to environmental constraints, 305 Corollarium, 4 correlated character state complexes, 240 correlated evolution, 373, 375, 381, 389 correlation of gametophytic and sporophytic characters, 12 cortex, 42, 290 cortical cavity, see cavity, cortical costa, broad, 141 dorsally toothed, 35 double or lacking, 147

Pleurocarpous Mosses: Systematics and Evolution ending in spine, 138, 139 length, 259, 262 long single, 163, 164, 166 on lateral leaves, 101 percurrent to excurrent, 138 rhizoids from adaxial side, 195 short double, 164, 167, 248 in Hypnaceae, 164 reduction in Hypnaceae, 167 single, to mid-leaf, 147 stout single percurrent, 223 structure, 216, 223, 229 triple, 325 vegetative leaves, 229 costa development, variability, 164 Cratoneuraceae, 166 Cratoneuron, 165, 166, 167, 168, 170, 172, 201, 229, 277, 280, 283 Cratoneuropsis, 165, 168, 170, 171 Cretaceous, 322, 326, 327, 330, 334, 356, 357, 359, 360, 362 angiosperm diversification, 322 basal, 327, 334, early Late, 359 Early, 338, 358, 359, 362 late Early, 327 Late, 340, 359, 360 Lower, 325, 327, 330 mid Early, 359 mid to Late, 340 origin of pleurocarpous mosses, 322 Crosby, Marshall Robert, 9 Crosbya, 236 cross validation, 262 analysis, 346 Crum, Howard Alvin, 11 Crundwell, Alan Cyril, 9 Cryphaea, 12, 302, 303 Cryphaeaceae, 150, 271, 274, 294, 302, 325, 355, 358 acrocarpous species derived, 358 acrocarpy in, 294 cladocarpous species derived, 358 sub-perichaetial innovations derived, 358 Cryphaeophilum, 147, 150 cryptic speciation, 264, 266 Cryptopapillaria, 147, 150, 154, 155, 156, 157 polyphyletic, 156 Cryptopapillaria chrysoclada, 156 Cryptopapillaria feae, 156 Cryptopapillaria fuscescens, 154, 155, 156, 157 Cryptopapillaria helictophylla, 157 Cryptopapillaria–Toloxis clade, 150 Cryptopodium, 20, 21, 32, 34, 35, 37, 47, 50, 51, 358 Cryptopodium bartramioides, 50 Ctenidiaceae, 196, 200, 233 Ctenidium, 187, 193, 229, 260, 382, 403 Ctenidium molluscum, 193 cushions, 290 Cyathophorella, 72, 77, 103 cyathophoroid genera, 72 Cyathophoroideae, 101

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Index Cyathophorum, 66, 72, 73, 77, 78, 80, 81, 85, 86, 101, 102, 103, 104, 391, 392, 393 divergence, Early Cretaceous, 359 Cyathophorum adiantum, 78, 80, 81, 94, 99, 101, 101, 104, 401 Cyathophorum africanum, 73, 85, 94, 99, 101, 102, 104, 105, 401 Cyathophorum bulbosum, 78, 80, 81, 94, 99, 101, 104, Cyathophorum hookerianum, 81, 85, 94, 99, 102, 103,104, 401 Cyathophorum parvifolium, 103, 105, 399, 401 Cyathophorum spinosum, 101, 105, 395, 399, 401 Cyathophorum tahitense, 101, 105, 395, 401 Cyrtopodaceae, 20, 23

D Daltonia, 236, 326, 334 Daltoniaceae, 66, 73, 111, 326 Darwin, Charles Robert, 8 data, anatomical, 166 missing, 54 morphological, 166 data-based error estimators, 262 data partitions, 23, 29, 33 congruence, 33 Dawsonia, 397 Dawsonia longiseta, 403 Dawsonia superba, 291 decay index, 28, 86, see also Bremer support, delimitation, Homalothecioideae and Brachythecioideae, 130 DELTRAN, 47, 52, 61 Democratic Republic of Congo, 405 Dendrocyathophorum, 66, 72, 77, 80, 81, 85, 102 Dendrocyathophorum decolyi, 94, 99, 101, 102, 103, 104 Dendrohypopterygium, 66, 72, 80, 81, 99, 101, 102 Dendrohypopterygium arbuscula, 73, 80, 81, 99, 102, 103 Dendrohypopterygium filiculiforme, 73, 80, 99, 101, 102, 103 dendroid, facultative, 103 obligate, 103 dendroid growth form, 289 dendroid mosses, 49, 59, 103, 289, 295, 298, 302, 303, 305 determinate, 304, 305 Dendropogonella, 303 determinate habit, diagnostic of acrocarpy, 289 Devonian, Early, 349 Middle, 346 diagnostic characters, 146, 150, 154, 155 Diaphanodon, 147, 154, 155, 156 Diaphanodon blandus, 156 Dichelodontium, 369, 373, 374, 377, 389 Dichelyma, 330, 334 Dicladiella, 158 Dicnemonaceae, 397

415 dicot wood, 360 Dicranaceae, 355 Dicranales, species diversity, 354 Dicranidae, 338, 351, 354 species diversity, 356 Dicranoloma, 355 Dicranum, 3, 23, 36, 290, 390 Die Musci der Flora von Buitenzorg, 6 Die natürlichen Pflanzenfamilien, 9 Dillenius, Johann Jacob, 2 dioicous sexuality, 45, 48, 223, 224 Diphyscium, 351, 352 diplolepidous-alternate mosses, 44 diplolepidous-alternate peristomes, 352 diplolepidous peristome, formation, 249 direct optimization, 121, 149, 160, 181, 182, 204, see also POY discrete, 373, 375, 389 discriminate function (DF), 262 Distichophyllum, 182 distribution, African–Asian, 263 Gondwanan, 21, 66 divergence time analyses, 345 divergence time estimates, 351 divergence time value, mode, 351 divergence times, 351 diversification, character, 339 ecological, 339 initial, pleurocarpous mosses, 357 morphological, 339 pleurocarpous mosses, 359 species, 339 temporal variation in rates, 352 diversification of plerocarpous lineages, 357 diversification processes, 339 diversification radiation, 33 diversification rate, Hookeriales, 357 Hypnales, 357 diversification rates, shifts through time, 357 diversity, family-level, 352, 356 genetic, 13 genus-level, 352, 356 species-level, 352, 356 taxon numbers, 356 taxonomic, 14 Dixon, Hugh Neville, 9 DNA extraction, 23, 369 DNA sequence level similarity, 158 Dolichomitra, 404 Dolichomitriopsis, 147, 179, 184, 189, 192, 193, 404 Dolichomitriopsis diversiformis, 200 Donrichardsia, 121, 129, 137, 138, 141, 165, 168, 170 Donrichardsia macroneuron, 129, 141 Donrichardsia pringlei, 138 Donrichardsiaceae, 166 Drepanium, 196, 201 Drepanium recurvatum, 202

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416 Drepanocladoideae, 167, 168 Drepanocladus, 139, 164, 165, 167, 168, 169, 170, 171, 173, 223, 229, 232, 236, 256, 262 Drepanocladus aduncus, 168, 170, 174, 327 Drepanocladus aduncus species complex, 173 Drepanocladus capillifolius, 169 Drepanocladus longifolius, 169 Drepanocladus polygamus, 167, 217, 218, 219, 222, 223 Drepanocladus sendtneri, 169, 170 Duthiella, 147, 150, 152, 153, 156, 157, 158, 233 monophyly, 158 Duthiella flaccida, 158 Duthiella speciosissima, 158 Duthiella wallichii, 158 dwarf males, 368, 373, branching, 373, 384 chemical control, 368 correlation with epiphytism, 377, 390 correlation with morphological characters, 372, 373, 374, 375 evolution of, 373, 375, 389 evolutionary advantage, 368 genetic control, 368 independent synapomorphies, 378 phylogenetic context, 368 plesiomorphic, 378 presence, 375

E Echinodium, 185, 196, 203 Echinodium umbratum, 200 ecological characters, neglected, 197 ecological diversification, 339 Ectropothecium, 276 Edwards, Sean Rowan, 10 embryophyte calibration point, 450 myr, 346 embryophytes, crown group, 346 Encalyptales, 351 endemic, North American, 137 endostome, 235, 236, 238, 249, 250, 262, 264 basal membrane height, 146, 200, 204 basal membrane low, 238 basal membrane reduced, 254, 265 basal membrane, ornamentation, 252 colored and ornamented, 252 covering mouth of capsule, 260 pale, 252 reduced, 231, 252 segments, broad, 200 structure, 146 strongly perforate, 252 structure, 223 endostome cilia, 377, 383 height, 146 number, 374, 381 ornamentation, 252 reduced, 236, 238, 254, 265 well-developed, 200

Pleurocarpous Mosses: Systematics and Evolution endostome ornamentation, variation associated with gametophyte variation, 262 endostome processes, narrow, 236 perforated, 229 split, 233, 236 endostome variation, diplolepidous mosses, 249 Endotrichellopsis, 368, 369 Endotrichum, 368 England, Late Triassic, 349 Entodon, 196, 202, 203, 244, 248, 249, 250, 252, 254, 256, 257, 258, 259, 260, 261, 262, 263, 264, 265, 266, 355 monophyly, 266 Entodon cladorrhizans, 265 Entodon dregeanus, 250, 252, 255, 256, 259, 260, 261, 262, 263, 266 Entodon hampeanus, 260 Entodon jamesonii, 255, 264, 266 Entodon lacunosus, 251, 255, 256, 259, 261, 262, 264 Entodon mackaviensis, 256 Entodon macropodus, 252, 260 Entodon madagassus, 259 Entodon piovani, 254, 256, 260 Entodon plicatus, 255, 263, 265 Entodon schleicheri, 258 Entodon stereophylloides, 252, 255, 256, 259, 260, 262, 264, 265 Entodon subgenus Entodon, 250, 252, 254, 255, 259, 263 Entodon subgenus Erythropus, 250, 252, 255, 259 Entodontaceae, 8, 230, 233, 248, 249, 250, 252, 254, 256, 257, 259, 260, 262, 263, 265 key characters, 248 monophyly, 266 reduced morphology, 264 xerocastique, 254 Entodontopsis, 195 environmental modification, 289 Eocene, 322 Eopolytrichum, 361 Ephemeropsis, 322 epidermal cells, 290 epidermis, 42 epiphyllous habitats, 360 epiphytes, 49, 103, 104, 118, 141, 237, 257, 362 pendent, 141, 146, 150 epiphytic clades, multiple independent origins, 360 epiphytic habitats, 154, 360 epiphytic lineage, 200, 203 epiphytism, 374, adaptation to, 121 adaptation to in Entodontaceae, 265 correlation with dwarf males, 368, 390 facultative, 237 equatorial moist climate zone, 360 Eriodon, 140–141 Eriodon conostomus, 141 Eriopus, 111 erosion, 362 Erpodiaceae, 325

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Index Erpodium, 355 error rate, direct estimator, 262 Erythrodontium, 248, 251, 255, 256, 258, 259, 260 Erythrodontium barteri, 255 Erythrodontium julaceum, 255, 256 Erythrodontium lacoutourei, 250 Ethiopia, 255, 401 Études sur le péristome, 6 Eucamptodon muelleri, 403 Euphyllophyte, crown group, 346 Euptychium, 359, 368, 373, 374, 376, 378, 381, 383, 384, 391 monophyletic, 376, 391 Euptychium cuspidatum, 376 Euptychium cuspidatum–Euptychium robustum clade, 376 Euptychium dumosum, 376 Euptychium dumosum–Euptychium cuspidatum clade, 381 Euptychium setigerum, 373, 376, 383 Euptychium vitiense, 376 Eu-Ptychomnion, 369 Eurhynchiadelphus, 118 Eurhynchiastrum, 118, 126, 127, 130, 138 Eurhynchiastrum pulchellum, 138 Eurhynchiella acanthophylla, 138 Eurhynchiella zeyheri, 138, 139 Eurhynchioideae, 118, 121, 128, 129, 130, 133 Eurhynchium, 112, 138, 355 Eurhynchium pringlei, 138 Eurhynchium striatum, 316 Eurhyncium (Kindbergia) praelongum, 298, 359 Eurohypnum, 185, 187, 193, 196 Eurohypnum leptothallum, 196 Europe, 135, 138–139, 140, 360 central, 140 north east, 323, 324 Europe + Africa, 140 Europe + Siberia, 140 eutrophic species, 129 evidence, total, see combined evidence evolution, underlying patterns, 33 evolutionary events, extrinsic, 340 intrinsic, 340 evolutionary model, 374, 375 evolutionary reduction, parallel, 258 evolutionary relationships, 8, 14 evolutionary trends, 13–14 exostome, 249, 250, 252, 254, 255, 261, 264, 265 chemistry, 256 development, 374, 383 hypnoid shoulder in Entodontaceae, 250 internal anatomy, 254, 264 internal density differences, 254 irregular border in Entodontaceae, 250 length in Entodontaceae, 250 lower, furrowed or split, 236 massive ornamentation, in Entodontaceae, 254, 266 ornamentation, 146, 229, 255 papillae on striations, 255, 262, 264 papillae tightly packed or occluded, 250

417 papillose, 146, 153, 154, 156, 158, 236, 237, 238, 252, 256 PPL, reticulate ornamentation, 255 preperistome plates, external to OPL, 252 reduced, 265, 374, 383, 384 response to humidity, 254 smooth, 146 striae reduction and replacement by papillae, 264 striate, 146, 153, 157, 158, 167, 200, 250 striations, capillary action, 254 disruption of, 255 loosely packed, 251 tightly packed, 251 water uptake, 254 strongly ornamented, 263 structure in transverse section, 256 tapering, 255 taxonomic significance of differences in ornamentation, 252 trabeculae, height, 146, 154 in Entodontaceae, 250 strong, 236 truncated, 255 xerocastique, 254 exostome border, 166, 229, 233, 236, 238 irregular, in Entodontaceae, 250 reduced, 265 widened, 236 exostome color, 166, 195, 229, 233, 236 exostome margin, entire, 238 exostome movement, hygroscopic, 204 exostome ornamentation, infra-specific variation in Pterigynandrum filiforme, 265 not superficial, 248 exostome PPL, reduced, 236 exostome striation, fragmentation, 264 exostome structure, intra-specific variation in OPL, 255 intra-specific variation in PPL, 255 exostome teeth, hygroscopic movements, 254 length, 374 narrow, tapered, 231 exothecial cells, collenchymatous, 236 extant taxa, diversity, 346 extinction, high rates, 361 extrinsic environmental features, 339

F Fabronia, 187, 194, 195, 302 Fabronia cf. ciliaris, fossil, 322 Fabroniaceae, 118, 194, 195, 271, 326 Fallaciella, 397 family delimitation, 146 family-level diversity, 350 fatty acids, 74

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418 female plants, 45, 51 ferns, 362 fertile modules, 45, 50, 51, 52, 61, 62 fertilization distance, 265 Fifea, 397 Fiji, 395, 397, 399, 401, 403, 405 Fissidens, 6, 286, 368 Fissidens limbatus, 254 Fissidens, gametangia on lateral branches, 355 fixed age constraint, 362 flagelliform branch, plagiotropous 294 flagelliform shoots, 301, 304, 305 aerial, 301 rhizoid development on contact with substrate, 301 Fleischer–Brotherus classification, 9, 147 Fleischer, Max, 7–8 Flores, 114, 395, 399 Floribundaria, 146, 147, 153, 157, 158, 159, 160, 233 Floribundaria flaccida, 158, 159 Floribundaria floribunda, 153, 158 Floribundaria pseudofloribunda, 153, 158 Floribundaria sect. Trachycladiella, 158 Floribundaria setchwanica, 158 Floribundaria walkeri, 153, 158 Floribundaria, non-monophyletic, 158 South East Asia, monophyletic clade, 158 Florschütz, Peter A., 3 foliation, complanate, 66, 146, 153, 157, 158, 200–201, 259 dense, 156, 368 julaceous, 200, 259 terete, 146, 153, 157 Fontinalaceae, 138, 284, 330, 334 Fontinalis, 2, 194, 326, 334 forest, complex angiosperm, 359, 362 complex multilayered, 360 wet tropical montane, 111 forest floor, 103 Forsstroemia, 187, 200, 301 Forsstroemia trichomitria, 187, 305 fossil pleurocarpous mosses, 360 fossil record, 362 fossil-based age estimate, 340, 346 fossils, placement in topology, 340 founder effect, 265 Frey, Wolfgang, 69 frond, branched or leafy, 289 frondose mosses, determinate, 298 Frullania, 350 Funaria, 23, 28, 32, 290 Funariales, 351 Funaridae, 351

G g1 value, 28 gametangia distribution, environmental control, 302

Pleurocarpous Mosses: Systematics and Evolution seasonal control, 302 gametangia, position, 287, 288 gametangial position, homology of, 305 gametophore initiation, 300 gametophyte, branched, 103 simple, 103 structure, 42 gametophyte characters, range available, 258 gametophytic convergence, 13 gametophytic divergence, 4, 13 gap position, phylogenetic information, 152 gaps as missing data, 149 Garovaglia, 359, 368, 373, 374, 376, 381, 383, 384, 389, 391 divergence from Euptychium, 359 monophyletic, 376, 391 Garovaglia angustifolia, 373, 374, 376, 378, 391 Garovaglia baeuerlenii, 377, 378, 383 Garovaglia baeuerlenii–Garovaglia subelegans clade, 378 Garovaglia binsteadii, 373, 374, 376, 383, 389 Garovaglia binsteadii–Garovaglia zantenii split, 383 Garovaglia compressa, 377, 378 Garovaglia compressa–Garovaglia subelegans clade, 19 Garovaglia elegans ssp. dietrichiae, 383 Garovaglia elegans, 19, 21, 25, 378 Garovaglia plicata, 373, 376, 383, 391 Garovaglia plicata–Garovaglia powellii clade, 378, 384 Garovaglia powellii, 383, 391 Garovaglia powellii var. brevicuspidata, 391 Garovaglia powellii var. muelleri, 391 Garovaglia powellii var. taitensis, 391 Garovaglia sect. Angustifoliae, 368 Garovaglia sect. Aristatae, 368 Garovaglia sect. Baeuerlenii, 368, 383 Garovaglia sect. Baeuerlenii, monophyly, 383 Garovaglia sect. Compressae, 368 Garovaglia sect. Crassisubulata, 368 Garovaglia sect. Garovaglia, 368 Garovaglia subelegans, 373, 381, 383 Garovaglia zantenii, 374, 376, 378, 380, 389 Garovagliaceae, 236, 373, 378, 380, 381, 384 monophyletic, 368, 383 Garovaglioideae, 368 gemmae, 383 see also propagules filamentous, 112, 373, 381 gene duplication, 22, 33 genera, monotypic, 73, 80, 81, 102, 105 generic concepts, 6 genetic drift, 265 genomes, single, 230 genomic partitions, incongruence, 374 genus-level diversity, 356 geographical range, 138 Germany, 129, 138 germination, precocious, 373, 378 Glossadelphus, 187, 196, 201 Glossadelphus ogatae, 187 Glyphotheciopsis, 384 Glyphothecium, 368, 369, 373, 384 polyphyletic, 383

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Index Glyphothecium gracile, 368, 376, 380, 383 Glyphothecium gracile–Garovaglia subelegans clade, 376, 381 Glyphothecium sciuroides, 373, 383, 384 Gnuplot 3.8, 374 Goffinet, Bernard, 14 Gollania, 229 Goniobryum, 21, 32, 34, 52, 62, 63 Goniobryum subbasilare, 50, 52 grade R, 42, 45, 47, 50, 61, 62 Gradsteinia, 165, 168, 170 Grimmia, 23, 290 Grimmiaceae, 36 ground flora, increasing complexity, 362 Group I intron, 127 growth, direction, 114 duration, 114 termination of, 50, 61 growth form, 73, 101, 103, 309, 310, 313, 314 concepts, 289 determinate, 47, 48, 50, 62, 63, 112 indeterminate, 112 monopodial, 290 orthotropic, 112, 114 pendulous,49, 63, 150, 160 pinnate, 50 plagiotropic, 48, 63, 112, 114, prostrate, 44, 49, 51, 63 sympodial, 290, 294 tufted, 62 gymnosperms, 360, 362

H habit, see growth form habitat preferences, 229 habitat, 167, 168 exposed rock, 257 nutrient status, 234 variation, correlated with robustness, 257, 258 habitats, epilithic, 237 epiphyllous, 360 epiphytic, 153, 154, 179, 199, 360, 364 mineral rich, 203 habitat adaptation, 167 Habrodon, 179, 194, 196, 199, 284 Habrodontaceae, 194, 195 Hamatocaulis, 165, 167, 168, 169, 170, 171, 172, 173, 196, 203, 216, 223, 232 Hamatocaulis vernicosus, 170 Hampeella, 369, 373, 376, 378, 379 Hampeella concavifolia, 369 Hampeella, monophyletic, 376 Haplocladium, 179, 185, 187, 193, 198, 199, 277 Haplocladium angustifolium, 185, 187, 322 haplolepidous mosses, 355 Hawaii, 105, 129, 138, 140, 399, 407 Hedderson, Terry, 2

419 Hedenäs, Lars, 8, 14 Hedwig, Johann, 2, 3, 228 Hedwigia, 355 Hedwigiaceae, 355 HEL, 126, 127 Helicodontioideae, 118, 121, 126, 128, 139 Helicodontium, 10, 118, 135, 178 Helodiaceae, 166 Helodium, 179, 197, 276, 277, 283 herbarium specimens, 45 Herpetineuron, 141 Herzogiella, 194, 195, 236 heteroblastic series, 44, 49, 51, 290, 301, 313 heteroblastic transformation, 296, 301 heteroblasty, 295, 296, 298, 313 Heterocladiaceae, 196–197 Heterocladioideae, 233, 235 Heterocladium, 179, 187, 189, 200, 201, 203 Heterocladium dimorphum, 187 Heterocladium procurrens, 187 heterophylly, 295 hierarchical levels, 309, 312, 313, 314 Highest Posterior Density, 90%, 346 Himalayas, 154, 401 historical relics, 74 Hoe, William, 105 Holarctic, 216 holotype, 331 HOM, 126, 127 Homalia, 178 Homalotheciella, 135 Homalothecioideae, 118, 121, 126, 127, 128, 129, 135, 135 Homalothecioideae, delimitation, 123 Homalothecium, 130, 193, 200 Homalothecium laevisetum, 128 Homalothecium philippeanum, 126 Homalothecium sericeum, 200, 240 homology, determination of, 290 primary, 61 taxic, 36 user-defined, 152 homology assessments, 149 Homomallium, 185, 198, 202, 216 homoplasy, 77, 86 high, 230 in trnL, 169 homotropous capsule, see capsule, homotropous Hookeria, 182, 193, 194, 195, 271, 273, 284, 295 Hookeriaceae, 72, 73, 77, 271, 325 Hookeriales, 9, 11, 13, 15, 20, 23, 33, 70, 72, 84, 86, 99, 150, 182, 193, 230, 236, 237, 259, 271, 289, 322, 334, 338, 339, 351, 354, 356, 357, 358, 368 branch lengths, 356 constant diversification rate, 357 phylogenetic diversity, 356 species diversity, 356 Hookeriopsis, 334 hornworts, 351 hornworts + mosses, 351

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420 horsetails, extant, 346 HPD values, 351 humus formation, 362 Huon Peninsula, 139 Huttunen, Sanna, 15 hyalodermis, 203, 223 hybridization, interspecific, 173 hydrocarbons, apolar, 74 Hygroamblystegium, 165, 166, 167, 168, 170, 171, 172, 173, 276 Hygroamblystegium fluviatile, 170 Hygroamblystegium tenax, 167, 170, 172 Hygroamblystegium tenax, non-monophyletic, 172 Hygroamblystegium, morphological variation due to plasticity, 172 Hygrohypnella, 169, 196, 203, 216, 224 Hygrohypnella duriuscula, 169 Hygrohypnella ochracea, 169 Hygrohypnoideae, 167, 216 Hygrohypnum, 139, 164, 165, 166, 167, 168, 169, 170, 171, 173, 215–226, 276 circumscription, 216, 217 polyphyletic, 216, 220 subspecies and varieties synonymized, 216, 223 Hygrohypnum alpestre, 218, 220, 224 Hygrohypnum alpinum, 218, 220, 224 Hygrohypnum bestii, 218, 220, 222, 223, 224 Hygrohypnum bestii to H. polare clade, 222 Hygrohypnum closteri, 220 Hygrohypnum cochlearifolium, 216, 218, 220, 224 Hygrohypnum cochlearifolium–H. norvegicum clade, 224 Hygrohypnum cochlearifolium–H. smithii clade, 224 Hygrohypnum duriusculum, 203, 216, 220, 221, 223, 224 Hygrohypnum duriusculum–H. molle clade, 221, 224 Hygrohypnum eugyrium, 220, 223 Hygrohypnum eugyrium–H. subeugyrium clade, 223 Hygrohypnum luridum, 170, 215, 216, 219, 220, 222, 223 Hygrohypnum molle, 202, 220, 221, 223, 224 Hygrohypnum montanum, 170, 216, 217, 220, 221, 223, 224 Hygrohypnum montanum–Campylophyllum halleri clade, 216, 220, 221, 224 Hygrohypnum montanum–H. smithii clade, 217, 220, 223 Hygrohypnum norvegicum, 170, 201, 220, 224 Hygrohypnum ochraceum, 164, 203, 216, 220, 222, 223, 224 Hygrohypnum polare, 203, 220, 222, 223 Hygrohypnum purpurascens, 223 Hygrohypnum s. lat., 167, 169 Hygrohypnum smithii, 201, 202, 216, 217, 219, 220, 223, 224 Hygrohypnum styriacum, 219, 220, 222 Hygrohypnum styriacum–Palustriella decipiens clade, 219, 222 Hygrohypnum subeugyrium, 216, 220, 223 Hygrohypnum validum, 217 hygrophytes, 141, 203 Hylocomiaceae, 187, 196, 197, 199, 200, 228, 231, 271, 272, 283, 334 Hylocomiaceae + Antitrichiaceae, 187 Hylocomiaceae clade, 199

Pleurocarpous Mosses: Systematics and Evolution Hylocomiastrum, 270, 281, 283 Hylocomium, 197, 199, 270, 273, 276, 281, 283, 294, 295, 300 Hylocomium splendens, 240 Hymenodon, 21, 32, 35, 37, 49, 50, 51, 52, 61, 62, 352 Hymenodon pilifer, 49 Hymenodon sericeus, 47 Hymenodon, basal fruiting, 352 reduced peristome, 35 Hymenodontopsis, 20, 21, 34, 35, 37 Hymenodontopsis stresemannii, 50 Hymenodontopsis, position within Pyrrhobryum, 35 Hymenodontopsis, reduced peristome, 35 Hypnacanae, 166 Hypnaceae, 5, 11, 50, 164, 166, 216, 233, 235, 358 species diversity, 356 taxa poorly differentiated, 357 Hypnalean lineages, ancestors of in Early Cretaceous, 362 Hypnalean pleurocarps, see pleurocarps, hypnalean Hypnales, 12, 13, 15, 20, 23, 33, 34, 50, 164, 169, 170, 173, 179, 181, 183, 195, 196, 197, 198, 204, 230, 256, 276, 278, 334, 338, 339, 351, 354, 356, 357, 359, 360, 368 branch lengths, 356 family resolution lacking, 15 phylogenetic diversity, 356 rapid diversification, 339, 358 resolved phylogeny needed, 173 species diversity, 356 sporophytically uniform, 248 Hypnanae, 20, 22, 70, 289, 351, 354, 368 species diversity, 356 Hypneen, 167 Hypnidae, 20, 22, 31, 33, 34, 37, 42, 47, 50, 52, 62, 338 early diverging, 50, 62 monophyletic, 31 Hypnidae and hypnodendroid pleurocarps monophyletic, 22, 31, 33 Hypnidean pleurocarps, see pleurocarps, hypnidean Hypninae, pleurocarpous, 356 Hypnobartlettia, 165, 170, 171 Hypnobartlettiaceae, 166, 229 Hypnobryales, 15, 196, 197, 204 Hypnodendraceae, 348, 395, 401, 402 hypnodendroid mosses, origin, early Late Cretaceous, 359 hypnodendroid pleurocarps, see pleurocarps, hypnodendroid Hypnodendron, 21, 49, 289, 295, 297, 299, 300, 304, 397, 401, 402 fossil, 361 Hypnodendron sect. Comosa, 401 Hypnodendron sect. Hypnodendron, 401 Hypnodendron camptotheca, 401 Hypnodendron colensoi, 403 Hypnodendron comatulum, 399 Hypnodendron comosum, 397, 401 Hypnodendron dendroides, 403 Hypnodendron diversifolium, 77, 395 Hypnodendron junghuhnii, 401 Hypnodendron marginatum, 401

3856_IDX.fm Page 421 Friday, March 9, 2007 10:46 AM

Index

421

Hypnodendron menziesii, 45, 49, 406 Hypnodendron microstichum, 401 Hypnodendron milnei, 395, 403 Hypnodendron samoanum, 401 Hypnodendron spininervium, 397, 401 Hypnodendron tahiticum, 15 Hypnodendron vitiense, 403 Hypnodendron vitiense ssp. australe, 395 Hypno-Leskeaceae, 4–5 Hypnum, 2, 12, 185, 187, 193, 196, 197, 202, 202, 274, 284, 293, 298, 322, 397 Hypnum bambergeri, 201, 202 Hypnum chrysogaster, 403 Hypnum cupressiforme, 193, 196, 197, 202 Hypnum fluitans δ amphibium c) paludosum ††† pennulosum, 168 Hypnum imponens, 300 Hypnum molle, 202 Hypnum oldheimii, 202 Hypnum pallescens, 168, 172, 202 Hypnum plicatulum, 202 Hypnum plumaeforme, 202 Hypnum procerrimum, 202 Hypnum recurvatum, 160, 201, 202 Hypnum revolutum, 202 Hypnum sakurai, 202 Hypnum sect. Curvifolia, 1202 Hypnum sect. Hamulosa, 202 Hypnum sect. Pseudostereodon, 202 Hypnum sect. Revolutohypnum, 202 Hypnum sensu lato, 202 Hypnum vaucheri, 202 Hypnum/Eurohypnum, 185 Hypopterygiaceae, 50, 63, 66, 69, 70, 77, 84, 85, 94, 99, 101, 102, 103, 104, 105, 106, 236, 356, 395, 400 diversification, early Cenozoic, 359 monophyletic, 77, 80, 99, 351 monophyletic core, 77, 101 origin, Early Cretaceous, 359 sister to Hookeriales, 72, 84, 99 hypopterygioid genera, see pleurocarps, hypoptergyioid Hypopterygium, 59, 66, 72, 73, 77, 85, 99, 102, 103, 105, 294, 295, 298, 299, 301, 401 Hypopterygium commutatum, 73 Hypopterygium didictyon, 397, 403 Hypopterygium discolor, 104, 395, 403 Hypopterygium elatum, 105 Hypopterygium filiculiforme, 77 Hypopterygium flavolimbatum, 77, 103, 104, 395, 403 Hypopterygium sandwicense, 73, 103, 105 Hypopterygium tamarisci, 77, 84, 103, 104 Hypopterygium viresei, 105, 395

in phylogenetic reconstruction, 152 indels, see also under individual gene regions India, 66, 399 Indo Malaysia, 66, 103 Indochina, 155 indolyle-3-acetic acid, 300 Indonesia, 395, 397, 399, 401 inference from specimen observation, 300 initial diversification, pleurocarpous mosses, 362 inner peristome layer (IPL), 249 innovation, key, 42, 52, 61, 361 morphological, 339 physiological, 339 reproductive, 339 sub-perichaetial, 302 innovation shoots, 314, 318, 319 innovations, 42, 49, 50, 51, 52 apical, 61, 290 basal, 61, 112 lateral, 44 orthotropic, 112 subperichaetial, 61, 355 derived, 52 in cladocarps, 47, 61 independently derived reversal, 303 in pleurocarps, 45, 47, 49, 50, 52, 61, 62, 302, 303, 355 plesiomorphic, 52, 303 subperigonial, 49 International Commission on Stratigraphy, 360 interrupted false stem, 51 Intia, 323 introgression, 22, 33 intron group I, secondary structure, 182 Ireland, Robert Root, 9 Isobryales, 15, 196, 204, 231 see also Leucobryales Isopterygiopsis, 194, 276, 284 Isopterygium, 277 Isothecium, 294, 404 Isothecium alopecuroides, 317, 318 Isothecium stoloniferum, 257 ITS, 169, 170, 172, 173, 219, 221 indels and substitutions, 201 ITS region, high length variation, 193 ITS1, 129–130, 179, 182, 187, 193, 198, 200, 201, 204 ITS2, 80, 85, 86, 105, 118, 121, 129, 158, 179, 182, 187, 193, 204, 224 indels and substitutions, 9, 101, 102, 193 Iwatsukiella, 179, 196, 199, 203

I

jackknife, 129, 134 Jaegerina, 355 Jamieson, numerical analysis, 220, 223 Japan, 134, 140, 401 Java, 114 Jungermannia, 357

IAA, 300 identification by morphological characters, 16 Ignatov, Mikhail S., 15 indel events, 152

J

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422 Jurassic, 322, 325, 326, 330, 358, 361, 362 Late, 325, 326, 327, 330, 334, 358, 362 Middle, 362 Upper, 322, 325, 327, 330 juvenile leaves, see leaf, juvenile

K Kenya, 138, 401 Kermadec Islands, 397, 399 key character, see character, key key innovation, see innovation, key Kindbergia, 118, 129 Koponen, Timo Juhani, 9 Koponenia, 165, 168 Korea, 401 Kortselius, Joop, 105 Kulani Honor Camp, 105 Kuznetsk Coal Basin, 322, 323

L lamina cells, elongate, 258 elongate thin-walled, 158 length, 167 linear, 166 marginal, 223 papillae, number, 146 rows over lumen, 146 rows over walls, 146, 153 scattered over lumen, 146 secondary loss, 150 papillose, 146, 150, 153, 159, 198, 200, 201 pluripapillose, 153, 200 rhomboid, 146, 158 shape, 146, 236 short, 178, 198, 201, 204 short, broad, 361 short, in epiphytic lineages, 201 short distal, 138 smooth, 35, 147, 201, 258 thick-walled, 136 unipapillose, 153, 158, 159, 200 lamina, polystratose, 224 lateral bud, see branch primordium lateral perichaetia, parallel evolution, 289 see perichaetia, lateral leaf, flaccid, 373, 387 flat, 373 juvenile, 45 lamina cell shape, 167 lanceolate, 166 marginal cells enlarged, 259 number of cell layers, 166 orientation, 167, 220

Pleurocarpous Mosses: Systematics and Evolution papillae, see also lamina cells, papillose papillae dorsal, 197 papillae ventral on plicae, 197 plicate, 369, 373 rigid, 369, 373, 378 rugose, 369, 373, 389 correlated with dwarf males, 389 promotion of dwarf male evolution, 390 shape, 167, 220, 223 smooth, 374, 378 symmetry, 220, 223, 224 tubular, 373 ventral teeth, 373 leaf acumen, crispate, 153 piliferous flexuous, 159 leaf, alar cells numerous, 258 cells, sub-quadrate, 258 morphology plastic, 262 region reaching costa, 259, 263 region shape, 259 leaf apices, vegetative, 223 leaf arrangement, dorsi-ventral, 66 plastic, 146 three-ranked, 66 leaf, attached to stem only by costa, 322, 327 leaf axils, 48 leaf border, 167 bistratose, 35, 324 teeth geminate, 35 leaf, concave, 223, 224, 373 leaf corner, anodic, 277, 278, 280, 283 cathodic, 277, 278, 280, 283 leaf, costa, 164 leaf, decurrent, 258, 259, 278, 283 leaf dentation, 73 leaf development, juvenile, 45 leaf, dorsal teeth, 373, 379, 389 correlated with dwarf males, 381 evolution in presence of dwarf males, 381 synapomorphy, 379 leaf form, alternation within module, see heterophylly change along developing module, see heteroblasty differentiation between modules, see anisophylly leaf “hair-point,” pellucid, 200 leaf insertion, oblique, in lateral leaves, 259 straight, 156 transverse, in dorsal/ventral leaves, 259 leaf margin, bistratose, 326 ciliate, 96 entire, 373, 379 number of cell layers, 167 serrate, 36, 201, 263, 355, 373, 379 serrulate, 373, 379

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Index teeth, two-celled, 106 variation in curvature with hydration, 254 leaf margins, recurved, 226 leaf morphology, change on substrate contact, 294 change with pendulous growth, 294 variation between dorsal/ventral and lateral leaves, 259 variation in complanate plants, 259 leaf position, effect on alar cells, 263 effect on morphological variation, 259 superposed, 74 leaves, asymmetric, 36 asymmetric lateral, 66 auriculate, 160 carinate, 361 deciduous apical, 36 ecostate, 325, 326, 361 heteroblastic series, 273 julaceous, in exposed rock habitats, 257 juvenile, around branch primordia, 297 orientation, 156 perichaetial, see perichaetial leaves plication, 156 scaly, 69, 260, 261, 274, 275, 276, 301 spirally arranged, 383 squarrose, 158, 159 transitional series, 376 Lejeuneaceae, 357, 362 Lembophyllaceae, 118, 147, 150, 193, 199, 309, 315, 316, 395, 397, 403, 404, 405 Lembophyllum, 397 Leptobryum, 13 Leptodictyum, 165, 167, 168, 170, 171 Leptodictyum riparium, 187 Leptodon, 200, 278, 279, 282, 283 Leptodontaceae, 200, 289 Leptodontium, 324 Leptopterigynandrum, 179, 187, 196, 199, 201, 204 Leptostomataceae, 23, 34 Leptostomum, 32, 33 Leptotheca, 20, 21, 32, 34, 35, 37, 50–51, 52, 61 acrocarpous, 350 Leptotheca gaudichaudii, 45, 51, 52, 61 Lepyrodon pseudolagurus, 367, 373 Lepyrodontopsis, 147, 150 Lescuraea, 179, 185, 187, 196, 198, 279, 281, 282, 283 Lescuraea clade, 198 Lescuraea mutabilis, 187, 198 Lescuraea plicata, 187 Lescuraea saxicola, 187, 198 Lescuraea secunda, 185 Lescuraea sensu lato, 196, 197, 198 Leskea, 2, 5, 179, 185, 187, 193, 198, 199, 204, 277, 280, 283 Leskea obscura, 167 Leskea secunda, 185 Leskea + Haplocladium, 193 Leskea + Thuidiaceae clade, 199 Leskeacanae, 166, 228

423 Leskeaceae, 5, 11, 178, 179, 183, 185, 187, 196, 197, 198, 199, 201, 204 polyphyletic, 179 Leskeaceae sensu lato, 197 Leskeaceae sensu stricto + Thuidiaceae, 187 Leskeaceae sensu stricto, 201 Leskeella, 179, 197 Leucodon, 194, 196, 199 Leucodon gracilis, 388 Leucodon julaceus, 296 Leucodon sciuroides, 195, 196 Leucodontaceae, 199, 325 Leucodontales, 13, 50, 179, 197, 231, 233, 355, 360 non-monophyletic, 231 polyphyletic, 179 Leucolepis, 34, 291 Leucoloma, 291 liana-type leaves, absence of, 360 lid, see operculum life form, 309, 310 likelihood, 860, 376 maximum, 42, 45, 61, 374 likelihood ratio, 376, 390 likelihood ratio test, 374, 376, 379, 390 Limprichtia, 167, 169, 186, 203, 216, 223 Lindbergia, 179, 197, 198 Lindbergia clade, 198 Lindigia, 147, 150 lineage diversification, 339 extinction, 339 maintenance, 339 origination, low rates, 361 sorting, 22, 33 lineages-through-time plots, 340, 354 Linnaeus, Carl, 2 Liriodendron disjunction, 141 complex thalloid, 349 liverworts, 349 simple thalloid, 357 species diversity, 357 local calculations, 375 LOCFIT, 346 Loeskeobryum, 270, 281, 283 Loeskypnum, 165, 167, 168, 170, 171, 172, 173, 232 Loeskypnum–Straminergon–Warnstorfia clade, 173 log10 smoothing factor, 346 Lopidium, 66, 72, 77, 80, 81, 94, 102, 103, 172, 193, 194, 195, 359, 399, 401 Lopidium concinnum, 73, 104, 397, 401, 405 Lopidium struthiopsis, 73, 401 Lord Howe Island, 395, 396, 399, 401 lycopsid fossils, stem group, 349 lycopsids, crown group, 349

M Maastrichian, 360 Macaronesia, 138 MacClade, 47, 375

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424 MacPherson–Macleay Overlap, 389, 401, 403, 404, 405 macrofossils, 346 Macromitrium, 368, 407 Macromitrium leratii, 403 Magnoliales, 346 magnoliids, 359 majority rule consensus trees, 374 majority rule tree, all-compatible, 351 male plants, 48, 51, 104 acrocarpous, 51 reduced, 368 Malesia, 111, 112, 136, 138, 139 Mamillariella, 177, 197, 198 mammillae, 235 manual alignment, 150, 151, 160, see alignment, manual Manual of Bryology, 9 Marchantiales, 348 Marchantites cyathodoides, 348 Margadant, Willem Daniël, 2 Markov Chain Monte Carlo, 345 Mastopoma, 322 maximum likelihood see likelihood, maximum maximum likelihood tree, pruned, 375 maximum parsimony, 221, see parsimony, maximum Meesia triquetra, 256 Meesiaceae, 13, 21, 23 MegAlign, 217 Melanesia, 385, 399, 401 Menzies, Archibald, 2 Merceria augustia, 320, 322 Merillobryum cf. fabronioides, fossil, 320 meristem, in vascular plants, 290 merophytes, 290, 313 branch primordium development, 300 Mesochaete, 21, 32, 34, 35, 36, 52, 63, 352 Mesochaete and Aulacomnium, morphological similarity, 36 Mesochaete/higher pleurocarp clade, 34, 52, 63 Mesochaete taxiforme, 48 Mesonodon, 248, 250, 252, 255, 256, 259, 260, 264, 265 Mesonodon flavescens, 254 Mesozoic, 322, 324, 357 Mesozoic Gondwanic origin, 66 Mesozoic moss fossils, 346 metamers, 42, 44, 290, 272, 313 successive homology, 272 Meteoriaceae, 118, 121, 146, 147, 150, 153, 154, 156, 157, 158, 159, 160, 230, 233, 288 delimitation, 146, 147, 159 family concept, 147 monophyly, 146, 147, 150 phylogenetic relationships, 146, 147 polyphyly, 147 Meteoriaceae–Brachytheciaceae clade, 150 Meteoridium, 146, 147 Meteoriella, 147 Meteorioideae, 147, 150, 153, 154, 155, 156, 157, 160 paraphyletic, 150 synapomorphies, 154 Meteoriopsis, 153, 154, 157, 158, 159, 160

Pleurocarpous Mosses: Systematics and Evolution delimitation, 159 Meteoriopsis ancistrodes, 159 Meteoriopsoideae, 150, 153, 154, 157, 158, 160 monophyly of clades, 157 Meteorium, 147, 150, 152, 153, 154, 155, 156, 158, 159, 295 Meteorium–Chrysocladium clade, 156 Meteorium deppei, 155 Meteorium flagelliferum, 159 Meteorium nigrescens, 146, 147, 155 Meteorium–Papillaria clade, 155, 156 Meteorium pendulum, 147 Meteorium polytrichum, 155 Mexico, 137, 138 microclimate, 114 micronemata, 282 micronemata and paraphyllia, 282 Mielichhoferia, 34, 288 Mielichhoferia, gametangia on lateral branches, 355 Mielichhoferiaceae, 34 mineral concentration, 231 minimum age constraint, 359 misclassifications, 263 missing data, 152, see data, missing Mitten, William, 5 Mittenia, 22, 23, 28, 32, 35, 36 haplolepidous, 32, 36 Mitthyridium, 403 Mniaceae, 23, 32, 34, 282, 289, 323, 326, 352 Mnium, 34 model, eight-parameter, 376 GTR + G, 374 GTR + I + G, 181, 345, 374 one-parameter, 375, 377 seven-parameter, 376 SYM + G, 374 two-parameter, 375 models, diversification rates, 357 Modeltest, 86 modular structure, 42, 45, 47, 50, 51, 52, 306 module, 42, 44, 45, 50, 51, 61, 311, 312, 313, 314, 315, 316, 317, 318 female, see perichaetial module fertile, 44, 45, 51, 61, 62 elongated, 51, 61 position, 52 hierarchy, 42, 44, 45, 51, 273, 290, 299, 300 male, see perigonial module perichaetial see perichaetial module perigonial see perigonial module primary, see primary module vegetative, see vegetative module module form, alternation, 304 modules, distinction between primary and secondary, 295 molecular clock, enforced, 377 rejected, 375 molecular data, 149, 156 molecular diversity, 356 molecular gene sequence, divergence, 338

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Index molecular phylogenies, single marker, 230 molecular synapomorphies, 121, 126, 127 molecular variation, within morphologically defined species, 173 Molteno Group, 325 Mongolia, 323, 326, 327 Monilophyte, crown group, 346 stem group, 346 monocotyledons, 346, 360 monophyly, 161 Meteoriaceae, 147 monopodial growth, 50, 112, 146, 290, 293 monopodial habit, diagnostic of pleurocarpy, 289 monopodium, 310, 311, 312, 313, 314, 317 montane belt, high, 114 Monte Carlo simulation, 375 morphological character state reconstruction, 377–378, 384–389 morphological characters, 215, 220, 223, 224, 228, see also character states, morphological convergence, 215, 223 homoplasy, 153 neglected, 197 morphological circumscription, inappropriate, 173 morphological data, 149, 152, 153, 154, 156, 160 morphological diversification, 339 morphological evolution, rapid, 138 uncoupled from molecular evolution, 174 morphological homology, in direct optimization, 160 morphological innovation, 339, 361 pleurocarpy, 339 morphological plasticity, 160, 359, 368, 391 morphological synapomorphies, 157, 338 morphological terms, information content, 290 morphological transformations, 61 morphological variation, 248, 256, 259, 265, 368 in gametophyte, 259 in relation to geographical location, 256 morphology, effect of habitat, 256 effect of humidity, 256 moss fossils, Mesozoic, 346 Palaeozoic, 346 moss mats, 106 mosses + hornworts, 349 mosses, diversification in angiosperm forest, 359 mountain fens, lakes, and streams, 223 MrBayes, 86, 181, 345, 374 MrModelTest 2.0, 345, 374 Müller, Carl, 5 Multistate, 373, 389 Muscites fontinaloides, 325, 326, 334, 361 Muscites guesceliniae, 325 Myrinia, 201 Myriniaceae, 10 Myurella, 201 Myurium hochstetteri, 298 Myuroclada, 129

425

N nad5 mtDNA, 22, 23, 105, 374 NADH protein-coding subunit, 369 Naiadita lanceolata, 349 natural selection, gametophyte characters, 12 peristome characters, 11 Neckera, 2, 178, 200, 201, 274, 277, 278, 289, 294, 295, 298, 301, 305 Neckeraceae, 178, 200, 201, 274, 282, 283, 284, 404 species diversity, 356 Neckeradelphus, 276 Neckeropsis, 403 Nematocladia, 10 nematodontous mosses, 351, 360 Neobarbella, 147 Neodicladiella, 146, 147, 153, 157, 158, 159, 160 Neodicladiella pendula, 147, 159 Neodolichomitra, 187, 189, 196 Neodolichomitra + Antitrichia, 199 Neodolichomitra yannanensis, 187 Neonoguchia, 146, 157, 159 Neonoguchia auriculata, 159 Neotropical/African disjunction, 264 net venation, 323, 324, 334 New Caledonia, 258, 395, 396, 397, 399, 401, 403, 404, 405 New Guinea, 139, 141, 395, 397, 399, 401, 403, 404, see also Papua New South Wales, 139 New Zealand, 395, 396, 397, 398, 401, 403, 405 New Zealand endemics, 73 Newton algorithm, 375 Nobregaea latinervis, 141 node, constrained, 346 nodes, estimated ages, 347 nomenclature, 154 Nona, 129, 185, 187 Nona analysis, resolution, 187, 193 nonpleurocarpous mosses, 20, 21 Norfolk Island, 395, 396 Norris, Daniel Howard, 9 Northern Hemisphere, 66 Nothofagus, 404, 405, 406 nucleotide sequences, 372, 376 null distribution, 374

O Oceania, 21 Ochyraea, 168, 187, 196, 201, 202, 216, 224, 225 Ochyraea clade, 201–202 Ochyraea mollis (Hedw.) Ignatov, comb. nov., 185, 202 Ochyraea montana, 187 Ochyraea smithii, 202 Ochyraea tatrensis, 17, 20, 202, 224, 225 Oedipodium, 338, 351, 352 Okamuraea, 141, 179, 193, 199, 200 Okamuraea brachydictyon, 200 one degree of freedom, 375, 376

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426 ontogeny, 229 operculum, rostrate, 237, 265, 369 optimization, 42, 45–47, 51–52, 54, 61, 62 Ordovician, Middle, 346 orientation, orthotropous, 291 plagiotropous, 291 relative to effective substrate, 294 Origin of Species, 8 Orthodontium, 20, 21, 22, 23, 32, 35, 36, 37, 42, 51, 52, 61, 352, 358 acrocarpous, 22 anomalous branching, 352 Orthodontium lineare, 45, 51 orthogonal, 240 Orthostichella, 147 Orthostichopsis, 355 Orthothecium, 136, 194, 276 Orthotrichaceae, 23, 36, 256, 355 species diversity, 356 Orthotrichales, 351, 355 Orthotricum, 256 orthotropous capsule, see capsule, orthotropous orthotropous frond, 294 orthotropous growth, 294, 295, 297 initiated on stolon contact, 294 orthotropy, in pleurocarps, 288, 291 out-crossing, 265 outer peristome layer (OPL), 249 outgroup sampling, 77, 86 overall similarity, 228, 229, 230, 231, 232, 233 Oxyrrhynchium, 118, 121, 129, 130, 137, 138, 141 Oxyrrhynchium hians, 129 Oxyrrhynchium pumilum, 129, 135 Oxyrrhynchium savatieri, 129 Oxyrrhynchium speciosum, 138, 141 Oxyrrhynchium vagans, 129

P P4, 374 Pacific Ocean, 404, 405 Pacific Rim, 66 Pacific, southern, 155 Palaeodichelyma, 325, 327 Palaeogene, early, 360 palaeolatitudes, 360 Palaeozoic, 321, 325, 327 Palaeozoic, moss fossils, 346, 357 Palisot de Beauvois, Ambroise Marie François Joseph, 2 Palustriella, 165, 167, 168, 170, 171, 197, 277, 280, 282, 283 Palustriella decipiens, 215, 217, 219, 222 pantropical, 155 papillae, 229, 235 Papillaria, 146, 147, 150, 152, 153, 154, 155, 156, 159 Papillaria donnelii, 147 Papillaria intricata, 154, 155, 157 Papillaria nigrescens, 146 Papillaria nitens, 155

Pleurocarpous Mosses: Systematics and Evolution Papillaria penicillata, 155, 156 Papua New Guinea, 395, 397, 399, 401, 403, 404, see also New Guinea paraphyletic groups, 141 paraphyllia, 164, 166, 167, 195, 197, 201, 202, 224, 229, 236, 270, 272, 274, 373, 380, 389, 390 absent in Hypnaceae, 164 abundant, 204 branched, 277 correlated with dwarf males, 383 foliose, 166 in Campylophyllum halleri, 164 in longitudinal rows, 197, 198, 276 position, 276, 277 types, 276, 277, 283 paraphyses, 229, 272, 274, 373 leaf-like, 102 parsimony, maximum, 42, 45, 47, 52, 61, 62, 219, 374 parsimony informative sites, 376 parsimony ratchet analyses using PAUP, 86 parsimony ratchet analysis, 149 parsimony ratchet method, 129 parsimony ratchet runs, sequential, 181 partitions, codon positions, 374 gene regions, 374 PAUP 4.0b10, 28, 219, 374 PCR, 28 Pechora Coal Basin, 323 Pelyatka Formation, 323 penalized likelihood, 345, 365 pendent habit, 146 perichaetia, 102, 270, 272, see also perichaetial module enlarged, 164 lateral, 44, 51, 339, 361 terminal, 51 perichaetial branch characters, 229 perichaetial leaf development, 44, 45 perichaetial leaves, 47, 379 acumen multistratose, 383 acumen unistratose, 383 appressed to seta, 197 erect, 233, 236 Garovaglia, 383 inner, 378 orientation, 166 plicate, 166, 229, 236, 374, 389 smooth, 374 length, 373 non-plicate, 197, 233 plane or weakly plicate, 224 reduced costa, 197 reflexed, 197 smooth, 229 spreading to squarrose, 233 straight, 141, 197, 236 perichaetial module, 44, 45, 47, 48, 49, 50, 51, 52, 61, 274, 293, 302, 303, 304, 305 basal, 48, 49, 50, 52, 67, 62 distal, 47, 49, 50, 52, 62, 304

3856_IDX.fm Page 427 Friday, March 9, 2007 10:46 AM

Index independent origins of basal position, 52, 62 independent origins of distal position, 52, 62 lateral, 361 appearance of, 340 parallel evolution, 289 morphology, 258 point of origin, 302 position, 47, 52 reduced, 47, 52, 61 reversal to basal position, 52, 62 terminating long branches, 302 periclinal cell wall, autolysis, 250 perigonial module, 48, 51, 270, 274, 290, 302 distribution, 302 morphology, 258 perine deposition, 256 peristome, complete, 178, 200, 355 deposition, reductionary, 10 development, 5, 10 Euptychium setigerum, 383 hydrocastique, 265 hypnoid, 146, 178, 179, 237 internal structure and function, 248 isobryoid, 146 leskeoid, 237 Mittenia, 29, 36 modified, 141 morphology, 6, 73, 121 neckeroid, 238 OPL, massive ornamentation, 254 variation in number of cells, 255 ornamentation patterns, 248 perfect, 178, 200, 229, 237 phenotypic variation, 249 poorly developed, 72 PPL reduced, 265 PPL:OPL differential thickness, 254 PPL:OPL thickness ratio, 254 reduced and inset, in Entodontaceae, 249 reduced, 102, 103, 104, 178, 198, 200, 200 range of variation, 249 retention of function, 248 taxonomic information, 248 reduction correlated with capsule orientation, 5, 11 reduction correlated with habitat, 11, 12 reduction of ornamentation, 255 reduction series, 11 well-developed, 104 peristome characters, 6, 10, 77 conservative, 7, 8, 9, 10 in identification, 249 peristome function, experimental evidence, 254 residual, 248 peristome ornamentation, correlation with gametophyte morphology, 255 peristome ornamentation patterns, as ancestral states, 264 peristome ornamentation variation, taxonomic status, 255, 263

427 peristome reduction, evolution of, 248 in epiphytes, 204 peristome reduction and epiphytic habitat, 351 peristome reduction and xerophytic habitat, 351 peristome specialization, 229 peristome structure, 153, 155, 156, 158 Fissidens limbatus, 254 hypnalian, 155 Racopilum momentous, 254 Splachnum, 254 peristome teeth, hygrocastic movement, 154 hygroscopic movement, 121, 146 peculiar, 139 Permian, diverse bryoflora, 360 Lower, Germany, 360 moss fossils, 322, 360 Upper, 323, 324 Permian Angaraland, 360 Permian–Triassic, catastrophic vegetation die-back, 360 Permian–Triassic transition, 360 phenology, 265 phenotypic plasticity, 256, 258, 263, 265 extent in morphological characters, 263 phenotypic variation, masking genotypic variation, 256 Philibert, Henri, 6 Philippines, the, 399, 401 Philonotis, 290 phyllodioicy, 366 Phyllogoniaceae, 230 phyllotaxis, 283 phyllotaxy, octostichous, 104 tristichous, 101, 104 phylogenetic analyses, 147, 149, 150, 155, 156, 157, 158, 159, 160, 374 phylogenetic analysis, DNA sequence data, 164 phylogenetic diversity, 356 phylogenetic history, 238 phylogenetic relationships, 146, 147, 154, 383 phylogenetic signal, 29, 77 phylogenies, multiple genes, 13 single gene, 12 physiological innovation, 339 pigmentation, black, 154 cherry-red, 203 Pilosium, 355 Pilotrichella, 147, 187, 194, 196, 203, 404 Pilotrichella ampullacea, 204 Pilotrichellaceae, 147 Pilotrichelloideae, 147 Pilotrichopsis, 185 Pireella, 284, 289, 294, 296, 297, 298 Plagiochila, 357 Plagiothecium, 195, 233, 235, 256, 260, 271, 274, 284, 295, 302

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428 Plagiotheciaceae, 141, 166, 178, 194, 195, 199, 201, 203, 230, 233, 235, 238, 240, 271, 284 plagiotropous flagelliform branch, 294 plagiotropous growth in pleurocarps, 289 on vertical substrate, 294 plagiotropous module formation, 301 plagiotropous stolon, 294 plagiotropous to orthotropous transition, 292 plant size, 167, 172 small, in epiphytes, 203 Plasteurhynchium, 118 plasticity, 105 Platydictya, 194, 199 Platydictya jungermannioides, 215, 216, 217, 219, 220 Platydictya jungermannioides–Hygrohypnum smithii clade, 217, 219 Platygyrium, 11, 185, 187, 193, 196, 202, 203 Platygyrium repens, 185 Platyhypnidium, 118, 121, 129, 136, 137, 138, 139, 140, 142, 217 Platyhypnidium aquaticum, 138 Platyhypnidium austrinum, 121, 136, 139, 140 Platyhypnidium fuegianum, 129, 138, 139 Platyhypnidium hedbergii, 138 Platyhypnidium muelleri, 137, 138, 139 Platyhypnidium mutatum, 129, 138 Platyhypnidium patulifolium, 121, 136 Platyhypnidium pringlei, 137 Platyhypnidium riparioides, 129, 138, 215, 217 Platyhypnidium subrusciforme, 138 Platyhypnidium, polyphyletic, 121 Platylomella, 165, 166, 168 Platylomella lescurii, 166 pleurocarp diversification preceded angiosperm diversification, 357 pleurocarp origin, no earlier than Jurassic, 334 no later than Cretaceous, 334 Pleurocarpi, 44, 288 pleurocarpous clade, first appearance, 359 monophyletic, 338 pleurocarpous lineages, early diverging, 42, 62, 63 pleurocarpous mosses, basal-fruiting, 352 bryalean, 20 crown, 20, 21, 32, 33 distal-fruiting, 352 diversification, 339, 352, 359 higher, 42, 47, 50, 52, 62 Hypnalean, 50 hypnidaean, 338, 348, 351, 352, 354 hypnodendroid, 31, 32, 33, 34, 42, 47, 50, 52, 63, 338, 352 hypoptergyioid, 70 indeterminate growth, 290 initial diversification, 362 monophyletic, 20, 288 origin before angiosperms, 359 secondary characters, 54, 289

Pleurocarpous Mosses: Systematics and Evolution sister group, 34 “true,” 45 tufted, 295 pleurocarpous moss diversification, influence of angiosperms, 359 pleurocarpous mosses and forests, 340 pleurocarps, diagnostic characters, 322 pleurocarpy, concept of, 287, 310, 314 convergent structural innovations, 350 evolution of, 20, 33, 35, 42, 61, 290 independently derived, 22, 51, 52, 61 synapomorphic, 52, 62 transition to, 34 Pleurochaete, 288 gametangia on lateral branches, 355 Pleuroziopsidaceae, 229 Pleuroziopsis, 196, 199, 281 Pleuroziopsis + Climacium, 199 Pleurozium, 167, 295, 299 plume-mosses, 300 Pohlia, 34 polyphyly, 215, 216, 217, 220, 224 polyploid, 130 polypod ferns, diversification, 359 Polyssaievia deflexa, 322, 323 Polyssaievia spinulifolia, 322, 323 polytomy, 29, 34 Polytrichaceae, 4, 256, 338, 361 Polytrichales, 338, 361 Polytrichum, 291 populations, isolated, as single clones, 265 posterior probability, 351, 376 95%, 351 Pottiaceae, Cenozoic distal node, 345 Pottiales, species diversity, 356 POY, 187 POY alignment, 121, 126 POY analysis, 121, 126, 127, 149 PQRS regions, 127 PRAP, see parsimony ratchet analysis preperistome, 252 Pre-Permian mosses, 322 primary module, 44, 45, 47, 49, 50, 57, 190, 274 acrocarpous, 45, 51, 61 basal formation of secondary modules, 295 basal reiteration, 48, 49, 51, 62, 63 determinate, 48, 50, 62, 289 erect, 355 vegetative growth, 47, 288 distal reiteration, 49, 50, 63 indeterminate, 44, 50, 62, 63, 290, 339 initiation, 295 not terminated by gametangia, 290, 293 orientation, 294, 295 orthotropous, 48, 289, 295 plagiotropous, 289 point of origin, 292, 294 stoloniferous, 63 tufted orthotropous, 304 Primary Peristome Layer (PPL), 249

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Index primary stem, see primary module inaccurate terminology, 290 primers, 23, 369, 398 probability of character state change, high, 389 propagation, horizontal, 62 vegetative, 48 propagulae, uniseriate 2-5-celled green, 195 Proteaceae, 404, 405, 406 Protolepidodendrales, 348 protonema, 44, 51 Protosphagnum, 323 psbT, 118, 1121 Pseudobarbella, 159 Pseudobarbella attenuata, 159 Pseudocalliergon, 164, 165, 166, 167, 168, 170, 171, 173 Pseudocalliergon turgescens, 164, 166 Pseudocryphaea, 294, 295, 301, 305 Pseudohygrohypnum, 164, 196, 202, 216, 223 Pseudoleskea, 179, 196, 197, 198 Pseudoleskeaceae, 196, 197, 198, 334 Pseudoleskeella, 179, 187, 197, 198, 200, 204 Pseudoleskeella serpentinensis, 187, 197, 200 Pseudoleskeella clade, 198 Pseudoleskeellaceae, 198 Pseudoleskeopsis, 179, 185, 187, 197, 198 Pseudoleskeopsis imbricata, 197, 198 Pseudoleskeopsis zippelii, 187, 197, 198, 199 pseudoparaphyllia, 9, 118, 146, 150, 185, 201, 202, 229, 260, 263, 270, 274, 275 criteria for description, 283 definition, 280 leaf-like, 146 types, 275 pseudoparaphyllia and proximal branch leaves, 283 pseudoparaphyllia position, eleven o’clock, 283 four o’clock, 283 pseudoparaphyllia vs. paraphyllia, 284 pseudoparaphyllia vs. proximal branch leaves and paraphyllia, 283 pseudoparaphyllia vs. scaly leaves, 284 Pseudopilotrichum, 147 Pseudoscleropodium, 128, 299 Pseudospiridentopsis, 146, 147, 153, 154, 157, 158, 159, 160 Pseudotrachypus, 147, 150, 153, 157, 159, 160 monophyly, 160 Pseudotrachypus martinicensis, 159 Pseudotrachypus wallichii, 159 pteridophytes, 358 Pterigynandraceae, 196 Pterigynandrum, 2, 179, 185, 187, 193, 196, 199 Pterigynandrum filiforme, 196, 249, 265 Pterobryaceae, 284, 300, 316, 368 Pterobryellaceae, 20, 23 Pterobryon, 11 Ptilium, 194, 196, 197, 203, 216 Ptilium cristra-castrensis, 300 Ptychodium, 179, 196, 197, 198 Ptychomniaceae, 63, 86, 236, 368, 369, 383

429 paraphyletic, 368, 383 Ptychomniales, 20, 23, 33, 50, 299, 322, 334, 338, 339, 344, 348, 353, 368, 369, 374, 375, 379, 390 diversification, mid Cenozoic, 359 dwarf male absence plesiomorphic, 375 origin, Early Cretaceous, 359 Ptychomnianae, 354 Ptychomnianae monophyletic, 351 Ptychomniella, 369, 373 Ptychomniella ptychocarpa, 369 Ptychomniieae, 368 Ptychomnion, 236, 369, 373, 376, 378, 381, 383, 390 monophyletic, 391 Ptychomnion aciculare, 376 Ptychomnion cygnisetum, 86, 376 Ptychomnion cygnisetum–P. subaciculare split, 379 Ptychomnion densifolium, 376, 383, 389 Ptychomnion falcatulum–P. subaciculare, 376 Ptychomnion ptychocarpon, 369 Ptychomnion subaciculare, 376 Pylaisia, 11, 178, 202, 216 Pylaisiaceae, 202, 216, 223 Pylaisiella, 196 Pylaisiobryum, 248, 252, 254, 255, 256, 259, 260, 263, 265, 266 Pylaisiobryum abyssinicum, 254, 255, 260 Pyrrhobryum, 20, 21, 34, 37, 51, 295, 392, 303 acrocarpous, 355 distal-fruiting, 350 Pyrrhobryum bifarium, 35, 49 Pyrrhobryum dozyanum, 45, 48, 49, 52, 62, 350 Pyrrhobryum latifolium, 35 Pyrrhobryum mnioides, 35, 48, 49 Pyrrhobryum paramattense, 35, 48 Pyrrhobryum sect. Bifariella, 32, 34, 35, 49, 52, 62, 63 Pyrrhobryum sect. Pyrrhobryum, 32, 35, 45, 47, 49, 52, 62, 63, 302, 303 sub-perichaetial innovations, 296 Pyrrhobryum spiniforme, 35, 48, 49, 347 Pyrrhobryum vallis-gratiae, 48, 49

Q Quandt, Dietmar, 85 quillworts, extant, 349

R r8s 1.60, 345 rachis, 101, 102, 104 Racomitrium, 23, 291 Racopilaceae, 20, 21, 23, 63, 359 Racopilum, 21, 359 Racopilum momentous, 254 radiation, adaptive, 339 artifact, 339 recent, 264, 390 Radula, 357

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430 rainforest, closed canopy, 360 ramification, see branching random addition sequence, 374 RANDOM Bourne-Again Shell, 345 rate, autocorrelation, 375 rate smoothing, semiparametric, 375 Rauiella, 141, 185 rbcL, 22, 23, 30, 33, 230, 235, 345, 374 recent origin, 357 reclinate capsule, see capsule, reclinate reiteration, 50, 51, 62, 301, 304, 305, 312, 313, 314, 315, 316, 317 basal, 51 basal vegetative, 62, 63 distal, 58, 289 distal vegetative, 63 perichaetial, 62 Remyella, 136 representation, incomplete, 127 reproductive innovation, 339 reproductive modes, 350 reproductive module, specialized 302 reproductive viability, 339 resubstitution, 263 Rhacocarpaceae, 23, 34 rhizautoicy, 48, 51 Rhizinigerites, 360 Rhizinigerites neuburgiae, 322, 324 Rhizogoniaceae, 20, 21, 22, 23, 32, 33, 36, 37, 42, 45, 48, 52, 62 paraphyletic grade, see rhizogonian grade Rhizogoniales, 21, 36, 326, 338, 339, 343, 355 rhizogonian grade, 21, 22, 23, 32, 33, 34, 36, 37, 351, see also Grade R rhizogonian mosses, predate origins of angiosperms, 37 rhizogonian pleurocarps, reproductive modes, 352 Rhizogonianae, 20, 21, 22, 33 paraphyletic grade, see rhizogonian grade Rhizogoniineae, 21 rhizogonioids, core, 35 Rhizogonium, 20, 21, 32, 34, 35, 37, 45, 47, 48, 49, 52, 62, 302, 303, 352 basal-fruiting, 350 sub-perichaetial innovations, 303 Rhizogonium distichum, 48 rhizoidal tomentum, 48, 50, 51, 295, 368 see also tomentum rhizoids, 8, 48, 50, 51, 111, 229, 233, 271, 301 below leaf insertion, 195, 324 from adaxial side of costa, 195 initiated on substrate contact, 301 on leaf apex, 203 on seta base, 112 reddish brown, 258 scattered on stems, 203 smooth, 258 warty papillose, 136 Rhynchostegiella, 126, 134 ‘Rhynchostegiella’ durieui, 136 Rhynchostegiella macilenta, 140 Rhynchostegiella mindorensis, 136 Rhynchostegiella muricatula, 136

Pleurocarpous Mosses: Systematics and Evolution Rhynchostegiella opacifolia, 136 Rhynchostegiella pallidirostris, 136 Rhynchostegiella papuensis, 136 Rhynchostegiella santaiensis, 136 Rhynchostegiella sinensis, 136 Rhynchostegiella tenella, 127 Rhynchostegiella teneriffae, 140 Rhynchostegielloideae, 118 Rhynchostegioideae, 118 Rhynchostegium, 118, 121, 137, 138, 139, 140, 141, 275 Rhynchostegium confertum, 138 Rhynchostegium javense, 138 Rhynchostegium megapolitanum, 138 Rhynchostegium pallidifolium, 138 Rhynchostegium–Platyhypnidium clade, 139, 141 Rhynchostegium pringlei, 137, 141 Rhynchostegium riparioides, 138 Rhynchostegium serrulatum, 127 Rhynchostegium tenuifolium, 138 Rhynchostegium, paraphyletic, 118 Rhytidiaceae, 235 Rhytidiadelphus, 130, 199, 275, 355, 359 Rhytidiadelphus squarrosus, 322 Rhytidiadelphus triquetrus, 369 Rhytidiopsis, 196, 199, 203 Rhytidium, 196, 198, 299 ribozymes, self-splicing, 127 Rigodiadelphus, 179, 182, 185, 187, 196, 197, 198 Rigodiadelphus robustus, 182 Rigodium, 228, 404 riparian habitats, 360 rostrum, straight, 102 rpl16, 173 rps4, 22, 23, 30, 33, 80, 81, 85, 86, 96, 99, 101, 102, 105, 118, 345, 374 insertion, 102 substitution, 101, 102, 102, 103 rps4-trnS spacer, 86, 96, 102 rudimentary branch, 73, 74, 102 Russia, north east European, 324 Russian Far East, 316, 325 Rwanda, 401

S Saito, Kamezo, 9 Samoa, 395, 401, 403 sampling bias, systematic, 357 sampling, randomized incomplete, 357 Sanionia, 165, 167, 168, 169, 170, 196, 197, 203, 204, 216, 223, 225 Sanionia georgicouncinata, 240 Sanionia uncinata, 223 Sasaokaea, 165, 167 saxicolous plants, 103, 104 scale leaves, see leaves, scaly Schimper, Wilhelm Philipp, 4, 5 Schimperobryum splendidissimum, 85 Schistostega, 35, 36 Schoenobryum, 302

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Index Sciaromiella, 165, 168, 171 Sciaromiopsis, 165, 168 Sciuro-hypnum, 118, 128, 129, 130, 138 Sciuro-hypnum brotheri, 130, 138 Sciuro-hypnum flotovianum, 129 Sciuro-hypnum hylotapetum, 130 Sciuro-hypnum oedipodium, 130 Sciuro-hypnum plumosum, 129 Sciuro-hypnum populeum, 129 Sciuro-hypnum reflexum, 130 Scleropodium, 118, 128, 130, 138 Scleropodium caespitans, 140 Scleropodium obtusifolium, 140 Scorpidiaceae, 169, 187, 193, 196, 203, 216, 223 Scorpidiaceae + Breidleria, 203 Scorpidiaceae clade, 188, 202, 203 Scorpidium, 164, 165, 166, 167, 168, 169, 170, 171, 172, 196, 203, 216, 234, 229, 232, 236 Scorpidium scorpioides, 164, 166, 170 Scorpiurium, 128 secondary axes, see secondary module secondary module, 44, 274 branching order, 299 complanate development, 300 density, 299 determinate, 50, 293 distribution, 302 in pleurocarps, 291 length, 300 local density optimum, 300 orientation, 297 pinnate or umbellate branching, 289 point of origin, 298 reduced, 44 reproductive, 290 short determinate, 293 vegetative, 48, 49, 50, 290 secondary modules, presence of, 290 secondary stem, inaccurate terminology, 290 secondary structure, see trnL intron seed plant, crown groups, 346 self-fertilization, 265 SEM, 154 Sematophyllaceae, 236, 237, 240, 264, 358 species diversity, 356 Sematophyllaceae, taxa poorly differentiated, 356 Sematophyllum, 185, 187, 189, 196, 197 Sematophyllum homomallium, 185, 189, 195 Sematophyllum and Pylaisiadelphaceae, 193 semi-aquatic, 216 SeqMan, 217 sequence alignment, 28 sequence manipulation and alignment, 372 sequence polymorphism, 173 sequences, assembled, 372 composite, 23, 35 Serpoleskea, 164, 165, 167, 170, 171, 199, 204 seta, length, 70, 102, 164, 204, 237, 265, 361, 373, 379, 383, 389

431 mamillose, 198 wide base, 101 seta-oriented capsule, see capsule, seta-oriented Severodvinian Horizon, 324 sexual dimorphism, 368 sexual module, 274 Shaw, Arthur Jonathan, 2, 10, 13, 103, 105 shelf-forming moss, 305 shoot units, 311, 313 shoots, complanate, 229 julaceous, 224 Siberia, central, 322 eastern, 140 southern, 140, 322, 323, 327 Silurian, Middle, 346 similarities, analogous, 230 Sinitza, Sofia, 328 Sinskea, 153, 155, 157, 160 smoothing parameter, 375 Society Islands, 395, 401, 403 soils, shaded mineral mesic, 36 Solomon Islands, 395, 396, 399, 401, 403, 405 Southern hemisphere, 42, 66 speciation, active, 357 rapid, 142 speciation rate, high, 390 speciation rates, increased, 339 species diversification, 339, 340, 360 species diversity, 20, 362 asymmetry, 23, 36 Brachytheciaceae, 356 Bryaceae, 356 Dicranales, 356 Hookeriales, 356 Hypnaceae, 356 Hypnales, 356 liverworts, 357 Neckeraceae, 356 Orthotrichaceae, 356 Pottiales, 356 Sematophyllaceae, 356 Species Muscorum Frondosorum, 2, 3 species richness, see species diversity Sphaerocarpales, 349 Sphagnales, 338 Sphagnum, 13, 285, 351 gametangia on lateral branches, 355 Spiridens, 294, 299 Spiridens camusii, 48, 49 Spiridentaceae, 20, 23 Splachnales, 351 Splachnum, 254 spore maturation, summer, 234, 236 winter, 233 spore maturation time, 166, 233 spore morphology, Entodontaceae, 256

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432 inter-population variation in papillae, 256 intra-specific variation, 256 taxonomic value, 255 spore ornamentation, 121, 256 spore release, passive, 254 spore size, 121, 141, 204 spore surface sculpturing, 256 spore tetrad fossils, 346 spore wall morphology, 346 spores, large, 141, 154, 265 resistance to decay, 346 retention in tetrads, 346 sporophyte, above gametophyte, 104 beneath gametophyte, 104 character reliability, 118 characters, 139 cygneous, 104 evolutionarily conservative, 249 orientation, 70 uncinate, 34, 104 sporophyte development, effect of environmental conditions, 249 sporophyte production, 62 sporophyte structure, 240 sporophytes, basal, 355 multiple, 339 sporophytic complexes, 238 sporophytic traits, correlated with epiphytism, 265 sporopollenin, 346 Squamidium, 128, 147, 178 Squamidium brasiliense, 128 Sri Lanka, 401 Steerecleus serrulatus, 138, 139 stem, cavity, see cavity, stem central strand, 103, 167, 259 epidermal cells, 167 primary, 305 secondary, 305 stem anatomy, 12, 69, 98, 223 stem epidermal cells, 51 stem leaf, orientation, 153 stem ridge projections, 280 stem structures, 223 Stereodon, 187, 196, 202, 203, 216 Stereodon pallescens, 202, 203 Stereodon plicatulus, 187 Stereodon plumaeforme, 187 Stereodon vaucheri, 187 Stereophyllaceae, 194, 195 Stereophyllum, 187, 194, 195, 355 stipe, 49, 74, 102, 104, 289 cavity, see cavity, stipe stipe-branch modular series, 289 stipe differentiation, 303 stolon, 63, 197, 274, 301 growth pattern, 301 inaccurate terminology, 290

Pleurocarpous Mosses: Systematics and Evolution orientation, 301 plagiotropous, 301 stomata, 383, 384 long-pored, 233, 236 pore shape, 172, 197, 198, 229 round-pored, 197, 198, 201, 233 Stone, Brandon, 105 Straminergon, 165, 167, 168, 170, 171, 172, 173, 196, 232 Streimann, Heinar, 139 streptophyte algae, 351 Struckia, 141, 178, 203 sub-aquatic, 121, 138, 139, 141 sub-perichaetial branch primordia, see branch primordia, sub-perichaetial sub-perichaetial innovations, see innovations, subperichaetial substitutions/indels, 182, see also under individual genes substrate, horizontal, 294 proximity, 114 vertical, 294 substrate preference, 36, 37 subtropical areas, 66, 160 subtropical epiphytes, 368 Sumatra, 114, 399 Symphyodon, 322 Symphyodontaceae, 141, 356 Symphysodon, 284 sympodial branching, see branching, sympodial sympodium, 311, 313, 314, 317 synapomorphies, Garovagliaceae, 389 molecular, see molecular synapomorphies morphological, see morphological synapomorphies synapomorphy, 150, 240 synoicy, 274 Synopsis, 5

T Takakia, 351 Talynjan Formation, 325, 326 Tanzania, 401 Tasmania, 395, 396, 397, 399, 401, 403 taxa, over-description, 368 poorly differentiated, 357 subspecific, 391 Taxiphyllum, 196, 201, 276 taxon sampling, 21, 23, 32, 33, 99, 101, 105, 127, 221, 222, 225, 369 insufficient, 33, 193 strategy, 356 taxonomic congruence, 376 taxonomy, generic-level, 42 temperate areas, 66 temperate forests, warm, 146 terrestrial ecosystems, diversity, 362 terrestrial floras, increasing complexity, 362 terrestrial habitats, 103, 114, 154

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Index terrestrial substrates, 63 terrestrial vegetation, catastrophic die-back, 360 tertiary module, 45 tertiary or quaternary module, 299 Tetraphidales, 21 Tetraphidopsis, 369, 373, 376, 379 Tetraphis, 290, 351 Thamnobryaceae, 404 Thamnobryum, 278, 289, 294, 295, 298, 301, 304, 311 Thamnobryum alopecurum, 304, 316 Thamnobryum negrosense, 326 Thelia, 179, 187, 196, 199, 204, 293, 294, 295 Theliaceae, 233 Thuidiaceae, 10, 12, 13, 172, 179, 187, 193, 196, 197, 198, 199, 216, 228, 235, 277, 283, 284, 403 Thuidiaceae–Amblystegiaceae–temperate Hypnaceae clade, 172, 196 Thuidium, 12, 179, 270, 271, 276, 277, 283, 282, 294, 295, 298, 299, 300, 355, 390 Thuidium tamariscinum, 299, 300 Timor, 399 Toloxis, 147, 150, 154, 156, 157, 160 segregated from Papillaria, 156 Toloxis semitorta, 157, 158 tomentum, 48, 50, 51, 112, see also rhizoidal tomentum Tomentypnum, 168, 169, 170, 196, 201, 202, 216, 225 Tomentypnum nitens, 202 topological uncertainty, 61 topologies, conflicts between, 42, 45, 47, 61 topology, 376 Tortula, 256, 290 total evidence stage, 230, 236 total genomic DNA, 369 tracheophytes, extant, 346 Trachycladiella, 146, 153, 156, 157, 158, 160 Trachycystis, 34, 326 Trachyloma planifolium, 403 Trachypodaceae, 147, 150, 153, 154, 155, 156, 159, 233, 403 basal grade in Meteoriaceae, 153 circumscription, 147 polyphyletic, 153 synonymization with Meteoriaceae, 150, 155 Trachypodopsis, 147, 150, 153, 156, 157, 159, 160 Trachypodopsis serrulata, 157 Trachypus, 147, 150, 153, 154, 155, 156, 160 Trachypus bicolor, 154, 156 placement, 150 track analysis, 395, 404 Transbaikalia, 322, 325, 326, 327, 330 transformational independence, 61 transition parameter, 375 transition rates, 375, 378 transition to pleurocarpy, 351 transmission electron microscope, 248 tree congruence, 32, 33 tree fern, alpine, 141 tree ferns, 35, 36, 37, 340 tree islands, 28, 29

433 tree trunks, 118, 140 Treegraph, 91 Triassic, 324, 325 Late, 341, 360 Late, England, 349 Late, South Africa, 349 Tricostium, 325, 326, 334 Tricostium papillosum, 325 Tripterocladium, 404 tRNA-Gly, 173 trnF, 179 trnG (UCC) intron, 369 trnL (UAA) 5′exon–trnF (GAA), 369 trnL 3-exon, 86, 179 trnL intron, 86, 127, 182, 187, 195, 198, 199, 202 conservative regions, 182, 187 indels and substitutions, 101, 102, 103, 127, 129, 198, 201, 202 P6 loop, 201 secondary structure, 121, 127, 129, 182 secondary structure, in Amblystegiaceae, 201 shared substitution, 182, 187, 198 variable loop regions, 182, 187 trnL, intron, P8 region, 127, 128, 129 P8 region, ratio paired to unpaired nucleotides, 129 trnL, substitution rates, 129 trnL-F, 22, 30, 85, 86, 118, 121, 127, 138, 139, 158, 169, 170, 172, 173, 219, 220, 221 trnL–trnF, 85, 96 spacer, 86, 96, 179 trnLUAA intron, 80, 170 trnLUAA, 219, 224 trnS-rps4 spacer, substitution, 102 tropical bryophytes, microclimate effect on morphology, 256 tropical forests, humid, 146 tropical pleurocarps, 2, 8 tropical regions, 111, 135, 138, 141, 160 tufted habit, 112, 368 Tunguska Coal Basin, 323 turfs, 290 typification, 154

U Uganda, 401 ultimate branches, filiforme, 159 ultrametric, 375 ultrametric tree, 375 Ulugey Formation, 326, 327 uncertainty, artifact of binary character coding, 389 Unclejackia, 141, 142 UNIXPAUP 4.0b10, 149 Uskatia, 360 pinnate branching, 323 Uskatia conferta, 322, 323, 334 Uskatia dentata, 323

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434

V vaginula, 373 attachment of perichaetial leaves, 378 length, 101 Vanderpoorten, Alain, 129 Vanuatu, 395, 399, 401, 403 vegetative branching, see branching, vegetative vegetative leaves, 45, 47 undifferentiated, 302 vegetative module, 51 indeterminate growth, 50 Verdoorn, Frans, 9 vicariant form-making, 397 Vitt, Dale Hadley, 10 Vittia, 165, 166, 168, 170, 171 Vittia pachyloma, 166 Vittiaceae, 170 voucher, misidentification, 167, 383 vouchers, 86 Vyatkian Horizon, 324

W

Pleurocarpous Mosses: Systematics and Evolution Warnstorfia fluitans var. fluitans, 169 Warnstorfia pseudostraminea, 169, 172 Warnstorfia sarmentosa, 172 water, nutrient and gas-exchange, 339 running, adaptations to growth in, 166 weft-forming mosses, 112, 302 Wenlockian, 346 wetland habitats, inundated, 168 wetlands, calcareous, 170 mineral-rich, 170 tropical montane, 170 Weymouthia, 146, 147, 315, 317, 397, 405 Weymouthia cochlearifolia, 315, 317 Weymouthia mollis, 315, 317 Winclada, 91, 106, 130, 181 winPAUP 4.0b10, 86, 149 Winteraceae, stem group, 346 worldwide revisions needed, 160

X xerophyte, 203

Wardia, 338, 355 Warnstorfia, 165, 167, 168, 169, 170, 171, 172, 173, 187, 196, 203, 232, 271 Warnstorfia exannulata, 45, 170, 215, 217, 220 Warnstorfia fluitans, 170, 327

Z Zelometeorium, 147, 178

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Systematics Association Publications 1. Bibliography of Key Works for the Identification of the British Fauna and Flora, 3rd edition (1967)† Edited by G.J. Kerrich, R.D. Meikie and N. Tebble 2. Function and Taxonomic Importance (1959)† Edited by A.J. Cain 3. The Species Concept in Palaeontology (1956)† Edited by P.C. Sylvester-Bradley 4. Taxonomy and Geography (1962)† Edited by D. Nichols 5. Speciation in the Sea (1963)† Edited by J.P. Harding and N. Tebble 6. Phenetic and Phylogenetic Classification (1964)† Edited by V.H. Heywood and J. McNeill 7. Aspects of Tethyan biogeography (1967)† Edited by C.G. Adams and D.V. Ager 8. The Soil Ecosystem (1969)† Edited by H. Sheals 9. Organisms and Continents through Time (1973)† Edited by N.F. Hughes 10. Cladistics: A Practical Course in Systematics (1992)* P.L. Forey, C.J. Humphries, I.J. Kitching, R.W. Scotland, D.J. Siebert and D.M. Williams 11. Cladistics: The Theory and Practice of Parsimony Analysis (2nd edition)(1998)* I.J. Kitching, P.L. Forey, C.J. Humphries and D.M. Williams * †

Published by Oxford University Press for the Systematics Association Published by the Association (out of print)

SYSTEMATICS ASSOCIATION SPECIAL VOLUMES 1. The New Systematics (1940) Edited by J.S. Huxley (reprinted 1971) 2. Chemotaxonomy and Serotaxonomy (1968)* Edited by J.C. Hawkes 3. Data Processing in Biology and Geology (1971)* Edited by J.L. Cutbill

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4. Scanning Electron Microscopy (1971)* Edited by V.H. Heywood 5. Taxonomy and Ecology (1973)* Edited by V.H. Heywood 6. The Changing Flora and Fauna of Britain (1974)* Edited by D.L. Hawksworth 7. Biological Identification with Computers (1975)* Edited by R.J. Pankhurst 8. Lichenology: Progress and Problems (1976)* Edited by D.H. Brown, D.L. Hawksworth and R.H. Bailey 9. Key Works to the Fauna and Flora of the British Isles and Northwestern Europe, 4th edition (1978)* Edited by G.J. Kerrich, D.L. Hawksworth and R.W. Sims 10. Modern Approaches to the Taxonomy of Red and Brown Algae (1978) Edited by D.E.G. Irvine and J.H. Price 11. Biology and Systematics of Colonial Organisms (1979)* Edited by C. Larwood and B.R. Rosen 12. The Origin of Major Invertebrate Groups (1979)* Edited by M.R. House 13. Advances in Bryozoology (1979)* Edited by G.P. Larwood and M.B. Abbott 14. Bryophyte Systematics (1979)* Edited by G.C.S. Clarke and J.G. Duckett 15. The Terrestrial Environment and the Origin of Land Vertebrates (1980) Edited by A.L. Pachen 16 Chemosystematics: Principles and Practice (1980)* Edited by F.A. Bisby, J.G. Vaughan and C.A. Wright 17. The Shore Environment: Methods and Ecosystems (2 volumes)(1980)* Edited by J.H. Price, D.E.C. Irvine and W.F. Farnham 18. The Ammonoidea (1981)* Edited by M.R. House and J.R. Senior 19. Biosystematics of Social Insects (1981)* Edited by P.E. House and J.-L. Clement 20. Genome Evolution (1982)* Edited by G.A. Dover and R.B. Flavell 21. Problems of Phylogenetic Reconstruction (1982) Edited by K.A. Joysey and A.E. Friday 22. Concepts in Nematode Systematics (1983)* Edited by A.R. Stone, H.M. Platt and L.F. Khalil 23. Evolution, Time and Space: The Emergence of the Biosphere (1983)* Edited by R.W. Sims, J.H. Price and P.E.S. Whalley 24. Protein Polymorphism: Adaptive and Taxonomic Significance (1983)* Edited by G.S. Oxford and D. Rollinson 25. Current Concepts in Plant Taxonomy (1983)* Edited by V.H. Heywood and D.M. Moore

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26. Databases in Systematics (1984)* Edited by R. Allkin and F.A. Bisby 27. Systematics of the Green Algae (1984)* Edited by D.E.G. Irvine and D.M. John 28. The Origins and Relationships of Lower Invertebrates (1985)‡ Edited by S. Conway Morris, J.D. George, R. Gibson and H.M. Platt 29. Infraspecific Classification of Wild and Cultivated Plants (1986)‡ Edited by B.T. Styles 30. Biomineralization in Lower Plants and Animals (1986)‡ Edited by B.S.C. Leadbeater and R. Riding 31. Systematic and Taxonomic Approaches in Palaeobotany (1986)‡ Edited by R.A. Spicer and B.A. Thomas 32. Coevolution and Systematics (1986)‡ Edited by A.R. Stone and D.L. Hawksworth 33. Key Works to the Fauna and Flora of the British Isles and Northwestern Europe, 5th edition (1988)‡ Edited by R.W. Sims, P. Freeman and D.L. Hawksworth 34. Extinction and Survival in the Fossil Record (1988)‡ Edited by G.P. Larwood 35. The Phylogeny and Classification of the Tetrapods (2 volumes)(1988)‡ Edited by M.J. Benton 36. Prospects in Systematics (1988)‡ Edited by J.L. Hawksworth 37. Biosystematics of Haematophagous Insects (1988)‡ Edited by M.W. Service 38. The Chromophyte Algae: Problems and Perspective (1989)‡ Edited by J.C. Green, B.S.C. Leadbeater and W.L. Diver 39. Electrophoretic Studies on Agricultural Pests (1989)‡ Edited by H.D. Loxdale and J. den Hollander 40. Evolution, Systematics, and Fossil History of the Hamamelidae (2 volumes)(1989)‡ Edited by P.R. Crane and S. Blackmore 41. Scanning Electron Microscopy in Taxonomy and Functional Morphology (1990)‡ Edited by D. Claugher 42. Major Evolutionary Radiations (1990)‡ Edited by P.D. Taylor and G.P. Larwood 43. Tropical Lichens: Their Systematics, Conservation and Ecology (1991)‡ Edited by G.J. Galloway 44. Pollen and Spores: Patterns and Diversification (1991)‡ Edited by S. Blackmore and S.H. Barnes 45. The Biology of Free-Living Heterotrophic Flagellates (1991)‡ Edited by D.J. Patterson and J. Larsen 46. Plant–Animal Interactions in the Marine Benthos (1992)‡ Edited by D.M. John, S.J. Hawkins and J.H. Price 47. The Ammonoidea: Environment, Ecology and Evolutionary Change (1993)‡ Edited by M.R. House

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48. Designs for a Global Plant Species Information System (1993)‡ Edited by F.A. Bisby, G.F. Russell and R.J. Pankhurst 49. Plant Galls: Organisms, Interactions, Populations (1994)‡ Edited by M.A.J. Williams 50. Systematics and Conservation Evaluation (1994)‡ Edited by P.L. Forey, C.J. Humphries and R.I. Vane-Wright 51. The Haptophyte Algae (1994)‡ Edited by J.C. Green and B.S.C. Leadbeater 52. Models in Phylogeny Reconstruction (1994)‡ Edited by R. Scotland, D.I. Siebert and D.M. Williams 53. The Ecology of Agricultural Pests: Biochemical Approaches (1996)** Edited by W.O.C. Symondson and J.E. Liddell 54. Species: the Units of Diversity (1997)** Edited by M.F. Claridge, H.A. Dawah and M.R. Wilson 55. Arthropod Relationships (1998)** Edited by R.A. Fortey and R.H. Thomas 56. Evolutionary Relationships among Protozoa (1998)** Edited by G.H. Coombs, K. Vickerman, M.A. Sleigh and A. Warren 57. Molecular Systematics and Plant Evolution (1999) Edited by P.M. Hollingsworth, R.M. Bateman and R.J. Gornall 58. Homology and Systematics (2000) Edited by R. Scotland and R.T. Pennington 59. The Flagellates: Unity, Diversity and Evolution (2000) Edited by B.S.C. Leadbeater and J.C. Green 60. Interrelationships of the Platyhelminthes (2001) Edited by D.T.J. Littlewood and R.A. Bray 61. Major Events in Early Vertebrate Evolution (2001) Edited by P.E. Ahlberg 62. The Changing Wildlife of Great Britain and Ireland (2001) Edited by D.L. Hawksworth 63. Brachiopods Past and Present (2001) Edited by H. Brunton, L.R.M. Cocks and S.L. Long 64. Morphology, Shape and Phylogeny (2002) Edited by N. MacLeod and P.L. Forey 65. Developmental Genetics and Plant Evolution (2002) Edited by Q.C.B. Cronk, R.M. Bateman and J.A. Hawkins 66. Telling the Evolutionary Time: Molecular Clocks and the Fossil Record (2003) Edited by P.C.J. Donoghue and M.P. Smith 67. Milestones in Systematics (2004) Edited by D.M. Williams and P.L. Forey 68. Organelles, Genomes and Eukaryote Phylogeny (2004) Edited by R.P. Hirt and D.S. Horner

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69. Neotropical Savannas and Seasonally Dry Forests: Plant Diversity, Biogeography and Conservation (2006) Edited by R.T. Pennington, G.P. Lewis and J.A. Rattan 70. Biogeography in a Changing World (2006) Edited by M.C. Ebach and R.S. Tangney

*Published by Academic Press for the Systematics Association †Published by the Palaeontological Association in conjunction with Systematics Association ‡Published by the Oxford University Press for the Systematics Association **Published by Chapman & Hall for the Systematics Association

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