The First Four Million Years of Human Evolution

RSTB_365_1556_Cover.qxd 9/7/10 10:42 AM Page 1 volume 365 . number 1556 . pages 3263–3410 The first four million y...

Author: Alan Walker | Chris Stringer (eds.)

34 downloads 1316 Views 11MB Size Report

This content was uploaded by our users and we assume good faith they have the permission to share this book. If you own the copyright to this book and it is wrongfully on our website, we offer a simple DMCA procedure to remove your content from our site. Start by pressing the button below!

Report copyright / DMCA form

DOWNLOAD PDF

RSTB_365_1556_Cover.qxd

9/7/10

10:42 AM

Page 1

volume 365

. number 1556 . pages 3263–3410

The first four million years of human evolution Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer Introduction The first four million years of human evolution A. Walker & C. Stringer

3265

Articles In search of the last common ancestor: new findings on wild chimpanzees W. C. McGrew More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure A. C. Stone, F. U. Battistuzzi, L. S. Kubatko, G. H. Perry Jr, E. Trudeau, H. Lin & S. Kumar

3267

3277 3289

Arboreality, terrestriality and bipedalism R. H. Crompton, W. I. Sellers & S. K. S. Thorpe

3301

Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction M. Brunet

3315

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia) Y. Haile-Selassie

3323

Anterior dental evolution in the Australopithecus anamensis–afarensis lineage C. V. Ward, J. M. Plavcan & F. K. Manthi

3333

Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis P. S. Ungar, R. S. Scott, F. E. Grine & M. F. Teaford

3345

An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar to modern humans P. L. Reno, M. A. McCollum, R. S. Meindl & C. O. Lovejoy

3355

The cranial base of Australopithecus afarensis: new insights from the female skull W. H. Kimbel & Y. Rak

3365

Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000 F. Spoor, M. G. Leakey & L. N. Leakey

3377

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene J. A. Lee-Thorp, M. Sponheimer, B. H. Passey, D. J. de Ruiter & T. E. Cerling

3389

Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past M. C. Dean

Founded in 1660, the Royal Society is the independent scientific academy of the UK, dedicated to promoting excellence in science Registered Charity No 207043

3397

volume 365

number 1556

pages 3263–3410

In this Issue

The first four million years of human evolution Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer

The first four million years of human evolution

Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip–bent-knee gait C. O. Lovejoy & M. A. McCollum

Phil. Trans. R. Soc. B | vol. 365 no. 1556 pp. 3263–3410 | 27 Oct 2010

27 October 2010

ISSN 0962-8436

The world’s first science journal

rstb.royalsocietypublishing.org 27 October 2010

Published in Great Britain by the Royal Society, 6–9 Carlton House Terrace, London SW1Y 5AG See further with the Royal Society in 2010 – celebrate 350 years

RSTB_365_1556_Cover.qxd

9/7/10

10:42 AM

Page 2

GUIDANCE FOR AUTHORS

Editor Professor Georgina Mace Publishing Editor Joanna Bolesworth Editorial Board Neuroscience and Cognition Dr Brian Billups Dr Andrew Glennerster Professor Bill Harris Professor Trevor Lamb Professor Tetsuro Matsuzawa Professor Andrew Whiten Cell and developmental biology Professor Makoto Asashima Dr Buzz Baum Professor Martin Buck Dr Louise Cramer Dr Anne Donaldson Professor Laurence Hurst Professor Fotis Kafatos Professor Elliot Meyerowitz Professor Dale Sanders Dr Stephen Tucker

Publishing Editor: Joanna Bolesworth (tel: +44 (0)20 7451 2602; fax: +44 (0)20 7976 1837; [email protected]) Production Editor: Jessica Mnatzaganian 6–9 Carlton House Terrace, London SW1Y 5AG, UK rstb.royalsocietypublishing.org

Organismal, environmental and evolutionary biology Professor Spencer Barrett Professor Nick Barton Dr Will Cresswell Professor Georgina Mace Professor Yadvinder Malhi Professor Manfred Milinski Professor Peter Mumby Professor Karl Sigmund Health and Disease Professor Zhu Chen Professor Mark Enright Professor Michael Malim Professor Angela McLean Professor Nicholas Wald Professor Joanne Webster

Publishing format Phil. Trans. R. Soc. B articles are published regularly online and in print issues twice a month. Along with all Royal Society journals, we are committed to archiving and providing perpetual access. The journal also offers the facility for including Electronic Supplementary Material (ESM) to papers. Contents of the ESM might include details of methods, derivations of equations, large tables of data, DNA sequences and computer programs. However, the printed version must include enough detail

to satisfy most non-specialist readers. Supplementary data up to 10Mb is placed on the Society's website free of charge. Larger datasets must be deposited in recognised public domain databases by the author.

Conditions of publication Articles must not have been published previously, nor be under consideration for publication elsewhere. The main findings of the article should not have been reported in the mass media. Like many journals, Phil. Trans. R. Soc. B employs a strict embargo policy where the reporting of a scientific article by the media is embargoed until a specific time. The Executive Editor has final authority in all matters relating to publication.

Electronic Submission details For full submission guidelines and access to all journal content please visit the Phil. Trans. R. Soc. B website at rstb.royalsocietypublishing.org.

AIMS AND SCOPE Each issue of Phil. Trans. R. Soc. B is devoted to a specific area of the biological sciences. This area will define a research frontier that is advancing rapidly, often bridging traditional disciplines. Phil. Trans. R. Soc. B is essential reading for scientists working across the biological sciences. In particular, the journal is focused on the following four cluster areas: neuroscience and cognition; organismal and evolutionary biology; cell and developmental biology; and health and disease. As well as theme issues, the journal publishes papers from the Royal Society’s biological discussion meetings. For information on submitting a proposal for a theme issue, consult the journal‘s website at rstb.royalsocietypublishing.org.

ISBN: 978-0-85403-847-3

Copyright © 2010 The Royal Society Except as otherwise permitted under the Copyright, Designs and Patents Act, 1988, this publication may only be reproduced, stored or transmitted, in any form or by any other means, with the prior permission in writing of the publisher, or in the case of reprographic reproduction, in accordance with the terms of a licence issued by the Copyright Licensing Agency. In particular, the Society permits the making of a single photocopy of an article from this issue (under Sections 29 and 38 of this Act) for an individual for the purposes of research or private study. SUBSCRIPTIONS In 2011 Phil. Trans. R. Soc. B (ISSN 0962-8436) will be published twice a month. Full details of subscriptions and single issue sales may be obtained either by contacting our journal fulfilment agent, Portland Customer Services, Commerce Way, Colchester CO2 8HP; tel: +44 (0)1206 796351; fax: +44 (0)1206 799331; email: [email protected] or by visiting our website at http://royalsocietypublishing.org/info/subscriptions. The Royal Society is a Registered Charity No. 207043.

Selection criteria The criteria for selection are scientific excellence, originality and interest across disciplines within biology. The Editors are responsible for all editorial decisions and they make these decisions based on the reports received from the referees and/or Editorial Board members. Many more good proposals and articles are submitted to us than we have space to print, we give preference to those that are of broad interest and of high scientific quality.

The Royal Society, the national academy of science of the UK and the Commonwealth, is at the cutting edge of scientific progress. We support many top young scientists, engineers and technologists, influence science policy, debate scientific issues with the public and much more. We are an independent, charitable body and derive our authoritative status from over 1400 Fellows and Foreign Members. During 2010, we are celebrating the Royal Society’s 350th anniversary. As part of this, there will be an exciting programme of activities – exhibitions, lectures, conferences, a new book, a vast science festival on the South Bank in London, television and radio broadcasting and much more besides. Our mission: to expand knowledge and further the role of science and engineering in making the world a better place.

Subscription prices 2011 calendar year

Europe

USA & Canada

All other countries

Electronic access only

£2145/€2788

$4058

£2317/US$4153

• invest in future scientific leaders and in

Printed version plus electronic access

£2574/€3345

$4869

£2780/US$4983

• influence policymaking with the best scientific

For further information on the Society’s activities, please contact the following departments on the extensions listed by dialling +44 (0)20 7839 5561, or visit the Society’s Web site (www.royalsociety.org). Research Support (UK grants and fellowships) Research Appointments (Fellowships): 2542 Research Grants: 2223 International travel Grants: 2555 Newton International Fellowships: 2559 Science Advice Science Policy Centre: 2550 Science Communication General enquiries: 2573 Library and Information Services Library/archive enquiries: 2606

The Royal Society’s strategic priorities are to: innovation, advice,

• invigorate science and mathematics education, • increase access to the best science internationally, and

Typeset in India by Techset Composition Limited, Salisbury, UK. Printed by Latimer Trend, Plymouth. This paper meets the requirements of ISO 9706:1994(E) and ANSI/NISO Z39.48-1992 (Permanence of Paper) effective with volume 335, issue 1273, 1992. Philosophical Transactions of the Royal Society B (ISSN: 0962-8436) is published twice a month for $4058 per year by the Royal Society, and is distributed in the USA by Agent named Air Business, C/O Worldnet Shipping USA Inc., 149-35 177th Street, Jamaica, New York, NY11434, USA. US Postmaster: Send address changes to Philosophical Transactions of the Royal Society B, C/O Air Business Ltd, C/O Worldnet Shipping USA Inc, 149-35 177th Street Jamaica, New York, NY11414.

• inspire an interest in the joy, wonder and excitement of scientific discovery.

Cover image: Sahelanthropus tchadensis: Toumaï chest, drawing (by S. Riffaut) of the sculpture (by E. Daynes); copyright MPFT.

The first four million years of human evolution Papers of a Discussion Meeting held at the Royal Society on 19 and 20 October 2009. Organized and edited by Alan Walker and Chris Stringer

Contents

Introduction 3265

The first four million years of human evolution A. Walker and C. Stringer

Articles In search of the last common ancestor: new findings on wild chimpanzees W. C. McGrew

3267

More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure A. C. Stone, F. U. Battistuzzi, L. S. Kubatko, G. H. Perry Jr, E. Trudeau, H. Lin and S. Kumar

3277

Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip – bent-knee gait C. O. Lovejoy and M. A. McCollum

3289

Arboreality, terrestriality and bipedalism R. H. Crompton, W. I. Sellers and S. K. S. Thorpe

3301

Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction M. Brunet

3315

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia) Y. Haile-Selassie

3323

Anterior dental evolution in the Australopithecus anamensis – afarensis lineage C. V. Ward, J. M. Plavcan and F. K. Manthi

3333

Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis P. S. Ungar, R. S. Scott, F. E. Grine and M. F. Teaford

3345

An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar to modern humans P. L. Reno, M. A. McCollum, R. S. Meindl and C. O. Lovejoy

3355

The cranial base of Australopithecus afarensis: new insights from the female skull W. H. Kimbel and Y. Rak

3365

Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000 F. Spoor, M. G. Leakey and L. N. Leakey

3377

3263

3264

Contents

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene J. A. Lee-Thorp, M. Sponheimer, B. H. Passey, D. J. de Ruiter and T. E. Cerling

3389

Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past M. C. Dean

3397

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3265–3266 doi:10.1098/rstb.2010.0179

Introduction

The first four million years of human evolution In one of the last paragraphs of The origin of species (1859), Darwin famously suggested that ‘Much light will be thrown on the origin of man and his history’. When he published The descent of man 12 years later, there was still no fossil evidence of our earliest evolutionary history, and nothing at all from the African continent. Yet our close biological relationship to the great apes, and especially the African apes, the gorilla (Gorilla gorilla) and chimpanzees, had long been recognized, even by scientists who were ignorant of, or unsympathetic to, evolutionary thinking. Nevertheless, when we remember his cautious nature and the continuing powerful opposition to his ideas, it still required fortitude for Darwin to venture ‘It is therefore probable that Africa was formerly inhabited by extinct apes closely allied to the gorilla and chimpanzee; and as these two species are now man’s nearest allies, it is somewhat more probable that our early progenitors lived on the African continent than elsewhere’. In explaining why the fossil evidence of our origins was slow to appear, he prophetically stated ‘Nor should it be forgotten that those regions which are the most likely to afford remains connecting man with some extinct ape-like creature, have not as yet been searched by geologists’. In fact it was to take another 50 years before such fossil evidence began to emerge in Africa itself, and Darwin would have been amazed by the remarkable evidence which has accumulated since then concerning the earliest stages of human evolution. Spectacular discoveries of early members of the human lineage, including nearly complete skeletons and dozens of other 6 to 2 Ma fossils have been made in the last 10 – 20 years. Single complete skeletons are much more useful analytically than separate parts of many individuals, yet until recently, few had been found from the period before 2 Ma. Even Australopithecus, discovered in South Africa in 1924, and published and named in 1925, is still relatively incompletely known. For instance, the famous ‘Lucy’ skeleton from Ethiopia is only about 20 per cent intact. But new and more complete early hominin skeletons from different parts of the African continent now promise to give us a much more complete picture of the early phases in the history of the human lineage.

One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

As discussed in one of the first contributions to this volume, molecular estimates of the divergence time between humans and chimpanzees presently converge on approximately 5– 7 Ma, although we two are old enough to remember the pre-molecular days, when the supposed uniqueness of humans seemed to require a time-span 2– 3 times those figures to account for the evolution of special features like bipedalism and high encephalization. But now, fossils of putative human lineage members have been reported from approximately 6 Ma deposits in Chad and Kenya, and fossils of the genus Ardipithecus from approximately 4.4 Ma sediments in Ethiopia include about 40 per cent of a complete skeleton. Views differ on the relationship of these forms to each other, and to the succeeding and better-known genus Australopithecus. Several skeletons of the latter have been found in the last few years. These include an adult from Sterkfontein cave, South Africa, not yet certainly dated, another adult from 3.8 Ma deposits in Woranso-Mille, Ethiopia, a 3.3 Ma child’s skeleton from Dikika, Ethiopia and four partial skeletons from Malapa Cave, South Africa, dated to about 1.9 Ma. Dozens of other less complete hominin fossils from approximately 6 to 2 Ma have been found, as well as these skeletons. Our meeting was timed to coincide with the double celebration of Darwin’s 200th birthday and the 150th anniversary of the publication of The Origin of Species, and to take the first opportunity to bring together as much as possible of the rich, newly published data concerning the earliest-known members of the human lineage. Through the generosity of the participants, our hope that detailed images and casts of the new material would be brought together for the first time during the meeting was amply met, although in the event only one of us could be there to see the outcome. The meeting was also planned to showcase the interdisciplinary nature of palaeoanthropology, by highlighting the new methods that have been developed to extract behavioural and life history information from fossils. These included computer modelling of locomotor capabilities, finite element modelling of stresses in bone, laser scanning comparisons of joint surfaces, quantification of semicircular canal morphology and its relationship to head motion, isotope analysis of teeth for dietary and climate reconstruction, confocal microscopy and texture analysis of tooth wear to indicate diet, and reconstruction of life history parameters from

3265

This journal is # 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3266

A. Walker & C. Stringer

Introduction

incremental lines in tooth enamel and dentine. The analytical sessions highlighted what could be accomplished by the careful reconstruction, study and analysis of the new fossils. By concentrating on the early part of the record of human evolution, the meeting was also able to document the essential ecological, behavioural, and morphological stages that underpinned the subsequent emergence of the genus Homo. Field workers reported on studies of the behaviour of wild chimpanzees as possible models for early hominin behaviour, and on the geological and environmental setting of the fossils, as well as their anatomy and preservation. Context for the discoveries was provided by colleagues who, for example, used tephrostratigraphy, argon – argon radiometric dating, faunal and floral analysis, GIS satellite imagery and taphonomy. Our hope was to bring about a new understanding of early hominin evolution by bringing together the newest fossils and the latest analytical methods, and we think the meeting at least helped progress towards that ambitious goal. But the meeting also provided the first opportunity to present many of the newest discoveries to scientific and public audiences alike. A memorable conference dinner was accompanied by a display of replicas of spectacular

Phil. Trans. R. Soc. B (2010)

new material such as the just-published Ardipithecus skeleton, and the reconstructed Sahelanthropus cranium. In the event, we have not been able to publish all of the contributions made at the meeting, and this unfortunately included a description of the very complete australopithecine skeleton from Sterkfontein mentioned earlier. Nevertheless we feel that The first four million years of human evolution was an appropriate measure of how much progress the field of palaeoanthropology (a term unknown 150 years ago) has made in meeting Charles Darwin’s expectations. We would like to thank all the staff of the Royal Society who worked on the planning and running of the meeting, and the editorial team who has worked so hard to bring this volume to fruition.

Alan Walker1 Chris Stringer2,* 1

June 2010

Anthropology & Biology, Penn State University, University Park, PA 16802, USA 2 Dept of Palaeontology, The Natural History Museum, London SW7 5BD, UK *Author for correspondence ([email protected]).

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3267–3276 doi:10.1098/rstb.2010.0067

In search of the last common ancestor: new findings on wild chimpanzees W. C. McGrew* Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK Modelling the behaviour of extinct hominins is essential in order to devise useful hypotheses of our species’ evolutionary origins for testing in the palaeontological and archaeological records. One approach is to model the last common ancestor (LCA) of living apes and humans, based on current ethological and ecological knowledge of our closest living relations. Such referential modelling is based on rigorous, ongoing field studies of the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus). This paper reviews recent findings from nature, focusing on those with direct implications for hominin evolution, e.g. apes, using elementary technology to access basic resources such as food and water, or sheltering in caves or bathing as thermoregulatory adaptations. I give preference to studies that directly address key issues, such as whether stone artefacts are detectible before the Oldowan, based on the percussive technology of hammer and anvil use by living apes. Detailed comparative studies of chimpanzees living in varied habitats, from rainforest to savannah, reveal that some behavioural patterns are universal (e.g. shelter construction), while others show marked (e.g. extractive foraging) or nuanced (e.g. courtship) cross-populational variation. These findings allow us to distinguish between retained, primitive traits of the LCA versus derived ones in the human lineage. Keywords: tool use; shelter; diet; ranging; last common ancestor; chimpanzee

1. INTRODUCTION This paper aims to synthesize and to update recent (from 2005 onwards) findings from studies of the ethology and ecology of wild chimpanzees (Pan troglodytes) that are relevant to modelling human origins. Given space constraints, this exercise will be limited to field studies, and therefore mostly to observational data on the spontaneous behaviour of apes in situ, cited selectively. It emphasizes primary reports, usually journal articles, on the assumption that older secondary reviews (e.g. Mitani et al. 2002; McGrew 2004) provide access to earlier material. It concentrates on the eight study sites with fully habituated subjects, here listed in the order of seniority: Gombe (Tanzania), Budongo (Uganda), Mahale (Tanzania), Kanyawara (Uganda), Bossou (Guinea), Taı¨ (Ivory Coast), Ngogo (Uganda) and Fongoli (Senegal). However, given the geographical bias to eastern and western Africa, other sites with partly habituated subjects, especially in central Africa, such as Goualougo (Republic of Congo), are necessarily invoked too. Most importantly, it focuses on topics that are relevant to modelling the behaviour of the last common ancestor (LCA) of the divergent lines that led to living humans and living chimpanzees. These topics are presented in terms of their ‘directness’ in comparisons between what primatologists see now in living apes, and what palaeoanthropologists seek to infer about

*[email protected] One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

the extinct LCA, based on indirect evidence. Thus, this synthesis covers technology, diet, shelter and ranging and foraging. Attempts to use findings from ethological and ecological (as opposed to morphological) research on chimpanzees to model the behaviour of ancestral humans are relatively recent, dating from the rise of primatological field studies in the last 50 years. Although most early field workers were interested in apes in their own right, their mentors often had in mind the potential applicability of the exciting new findings to human issues (e.g. Goodall & Hamburg 1974). Many of the early attempts now look crude and simplistic (e.g. McGrew 1981). For example, most were content to talk about extinct hominids as a single unspecified class, but as the hominin evolutionary record became more and more diverse, with more and more taxa unearthed, this monolithic exercise was less and less satisfactory. Furthermore, as data began to emerge on wild bonobos, Pan paniscus (Kano 1992), who are as equally closely related as chimpanzees to hominins, and as cross-populational variation began to emerge in chimpanzees (McGrew 1992), easy generalizations grew harder to make. Ecological studies of chimpanzees in a variety of ecotypes, from rainforest to savannah, forced more precise modelling (Moore 1996). Finally, debate over the best way to model human origins and evolution, that is, via referential versus strategic models, or by homology versus analogy, muddied the waters (e.g. Tooby & DeVore 1987). Sayers & Lovejoy (2008) took the extreme position that chimpanzees may be no more useful as models than other, more ecologically,

3267

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3268

W. C. McGrew Chimpanzees and the last common ancestor

zoogeographically and phylogenetically distant taxa, such as capuchin monkeys (Cebus spp.). More recently, Lovejoy (2009) has asserted that extant African apebased models are no longer appropriate (for a contrary view, see Whiten et al. 2010). However, for focused studies, such as of Oldowan lithic industries, apes may still be the model of choice (Toth & Schick 2009). This paper takes the conservative line that lacking a fossil record for apes since the Miocene (cf. McBrearty & Jablonski 2005), and having only a shallow archaeological record for apes, all that we sensibly can hope to model is the LCA. In doing so, I make several simplifying assumptions, such as that anything that a chimpanzee can do today, the LCA could have done 6 – 7 Myr ago. Another pragmatic assumption is that although the LCA could have resembled the living chimpanzee, or bonobo, or neither, or some combination of the two, most of what we have to work with on grounds of homology comes from P. troglodytes. Therefore, until comparable breadth and depth of data are available for P. paniscus, the chimpanzee must carry the load.

(a) Technology Most of what behavioural primatologists have to offer to palaeoanthropology relies on artefacts, as these objects are comparable to what is found in the archaeological record. However, artefacts are the products of behaviour, and sometimes archaeological data are a further step removed: butchery cutmarks on bones are the products of the ephemeral acts that produced them. Whatever the caveats, primatologists can offer something that no archaeologist will ever see, that is, BOTH the product AND the behaviour, directly recorded. When a glancing blow of a stone hammer being used to crack a nut hits instead the stone anvil, producing a conchoidally fractured flake, the observer can see whether this was an accident. An archaeologist given only that same single flake could draw no valid inference about the percussionist’s intentions. Studies of tool use by apes in nature have come a long way from piecemeal natural history notes collected opportunistically and descriptively, to comprehensive, systematic, hypothesis-driven empirical efforts, some of which are experimental. Comparative analyses of chimpanzee material culture are done at every level, of individuals, lineages, communities, populations, subspecies and species (McGrew 2004). The chimpanzee ethnographic record now spans so many study sites across equatorial Africa that even chimpologists have trouble keeping them straight. Although only eight sites consistently allow all-day, close-up observation, there are five times as many other sites with varying degrees of habituation. In the 5 years, long-term sites studying the central (Hicks et al. 2005; Sanz & Morgan 2007) and Nigerian (Fowler & Sommer 2007) subspecies have joined the longer term studies in eastern and western Africa. Even sites that have yet to habituate their subjects have yielded new behavioural patterns, e.g. rootdigging at Ugalla, Tanzania (Hernandez-Aguilar et al. 2007), fruit-cleaving at Nimba, Guinea (Koops et al. 2010), etc. The only comprehensive study of Phil. Trans. R. Soc. B (2010)

innovation in wild chimpanzees, at Mahale, shows inventiveness to be common, but the chance that a novel behavioural pattern will be propagated and become established in a population is rare (Nishida et al. 2009). No longer is it enough just to list the types of tool found at a given site, as nominal (presence/absence) data. Now attention to relative frequency and competence of performance across age and sex classes is expected, along with data on context, variation in form and function of the tools’ manufacture and use (e.g. Sanz et al. 2009a). Functional (e.g. extractive foraging), biomechanical (e.g. percussive) and cognitive (e.g. artefact complexity) aspects of technology are stressed. Anecdotal versus idiosyncratic versus habitual use of tools is differentiated. Distinction is drawn between a tool kit (i.e. the whole repertoire of a community’s collective range of tools) and a tool set (i.e. the obligate sequence of two or more tools used to achieve a single goal). Composite tools (i.e. when two or more objects are used simultaneously and complementarily to achieve a goal), such as hammer and anvil (Carvalho et al. 2009), are distinguished from compound tools (i.e. when two or more elements of different types are combined into a single unit), such as a wedge used to level an anvil’s working surface (Biro et al. in press). Typology is now part of chimpanzee technology. Tool kits show both uniformity and variety across populations. Sanz & Morgan (2007) presented quantitative and qualitative findings from the Goualougo, Republic of Congo, chimpanzees, whose tool kit numbers 22 types, of which nine are used habitually (customary). In contrast, Watts (2008b) published comparable data from Ngogo, Uganda, where the total tool kit numbers only 10 types, with four of these being habitual. Such variation suggests the possibility of a normally distributed spectrum, but this is not the case. As with Goualougo, all habituated populations show about the same-sized tool kits: Gombe (22), Bossou (21), Taı¨ (21) and Mahale (16). However, along with Ngogo, the other Ugandan sites show small tool kits: Budongo (8) and Kanyawara (10) (Sanz & Morgan 2007, table 3). Even more striking is the contrast between Goualougo and Ngogo with regard to the predominate types of tools: the top three at Goualougo are used in subsistence, that is, extractive foraging of termites, honey and water; the top three at Ngogo are used in hygiene, especially wiping the penis after copulation, and in courtship. (The reverse is equally true: Goualougo chimpanzees very rarely use napkins, and Ngogo chimpanzees rarely harvest insects.) However, some types of tool use are chimpanzee universals, being found in all long-studied populations across Africa, such as leaf sponge (drinking water), aimed throw (weapon), play start (toy), branch drag (display), etc. Of particular importance is percussive technology, that is, the application of ballistic force via one object to another to achieve a goal (Ling et al. 2009). In chimpanzees, this most famously takes the form of hammer and anvil used to crack nuts, but it also occurs in smashing hard-shelled objects directly against anvils, in agonistic clubbing of adversaries or

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chimpanzees and the last common ancestor W. C. McGrew in display, or in specialized extractive foraging such as pestle-pounding (Yamakoshi & Sugiyama 1995). In the latter case, the pestle is a detached palm frond, the mortar is the apical growth tip of an oil palm (Elaeis guineensis) and the result is a cavity full of mashed-up slurry, which is eaten. Anvil use without hammers occurs when a hand-held, hard-shelled fruit is bashed directly against a boulder or root, as with baobabs (Adansonia digitata). Marchant & McGrew (2004) hypothesized an evolutionary scenario that led from anvil use to stone-knapping. Tool sets in apes were first recognized in honey extraction (Brewer & McGrew 1990). In seeking to harvest nature’s most calorific food, the minimal tool set requires a tool to break into the bees’ storage reservoir and another tool to extract the liquid. That is, some kind of percussive tool, such as hammer or chisel, plus some kind of dip-stick, are needed to secure the food item (for the most complete treatment of this resource’s exploitation, see Sanz & Morgan 2009). Tool sets may be more complex: Boesch et al. (2009) recently described tool sets used by the chimpanzees of Loango, Gabon, in which up to five tools were needed, e.g. pounder, perforator, enlarger, collector and swab. Tool sets also are used to exploit other animal prey, e.g. termites (Deblauwe et al. 2006; Sanz & Morgan 2007), ants (Sanz et al. 2009b) and even when getting honey, the proteinaceous bonus of bee brood may be important too. The key point about a tool set is that it is sequential task: if an A –B – C – D is necessary, then A – C– B – D will not do; you cannot check the oil level in your car’s engine via the dip-stick, until you have opened the car’s bonnet. Although tool sets may suggest advanced cognitive abilities, many such mandatory sequences are shown by creatures with modest brains (Hansell 2004), especially in shelter construction (see below). What is impressive (and possibly unique) about chimpanzee tool sets is that alternative versions may be used flexibly by different apes to solve the same problem. In human elementary technology, composite tools are well known: Mortar and pestle, bow and arrow, etc. Each element may stand alone, but is almost useless without its partner. (Tool composites differ from tool sets in that they are used simultaneously, rather than sequentially.) Tool composites are known for apes (see summary in Sugiyama 1997), and some are widespread, for example, in all populations where chimpanzees use long wands to dip for driver ants, they also use bent-over saplings as a perch while doing so, to avoid the painful bites of the ants swarming on the ground below (McGrew 1974). However, only recently have tool composites been systematically studied: Carvalho et al. (2009) showed that certain combinations of stone hammers and anvils were used over and over again by the chimpanzees of Bossou, even taking into account the apes’ separate, independent preferences for hammer or anvil. Compound tools are harder to find in living apes in nature, although their production is readily induced under contrived captive conditions. Combination of multiple items of the same type, e.g. leaves compressed together in leaf-sponging for water, is the simplest kind Phil. Trans. R. Soc. B (2010)

3269

of compound tool (Sousa et al. 2009), but it barely qualifies, being iterative. The most obvious example of compound technology (albeit not tool use) in non-human primates in nature is the sleeping platforms/nests/beds that are woven daily by great apes (see below). The best-known example in the extractive foraging of chimpanzees is the anvil– wedge, known only from the nut-cracking of the Bossou chimpanzees (Matsuzawa 2006). Bossou’s stone anvils are movable, and so their positioning can be adjusted; anvils with near-horizontal working surfaces are the most efficient, as the yielded nut-meat is readily picked up. An angular anvil can be levelled by inserting a smaller stone as a wedge underneath, to make the working surface less tilted. To what extent is the technological repertoire of the chimpanzee now known? The steepness of the cumulative ethnographic curve may be less than in the last century, but it has not flattened out. New habitual patterns continue to be described: chimpanzees use spears to skewer small mammals (Pruetz & Bertolani 2007) and digging sticks to unearth roots (Hernandez-Aguilar et al. 2007). Furthermore, new modes of tool use continue to emerge, such as the chimpanzees of Nimba, Guinea, using cleavers to break apart large, fibrous Treculia fruits (Koops et al. 2010). Much progress has also been made on how individual apes in nature learn to use elementary technology. Previous studies were descriptive or qualitative, whereas modern ones use sophisticated multivariate analyses (e.g. general linear mixed model) to tease out the influences of independent variables. Lonsdorf ’s (2006) study of termite fishing at Gombe showed that although all chimpanzees in the Kasakela community show this tool use by 5.5 years of age, daughters acquire the skills earlier, and this acquisition is a function of the mother’s overall time spent in the activity. Humle et al. (2009) showed that chimpanzee infants at Bossou who had more opportunities to observe their mothers started ant-dipping sooner and were more proficient than their low-opportunity counterparts. However, in neither case were individual differences in mother’s performance reflected in individual differences in their offspring, nor was there any direct teaching by mothers. Youngsters learned to fish or to dip by passive observational learning of tolerant models. Matsuzawa et al. (2001) have termed this dyadic conduit of information from one ape to another as ‘education by master–apprenticeship’. Some primatologists now apply archaeological methods to the study of chimpanzee technology in nature. Mercader et al. (2002, 2007) have shown that the past nut-cracking activities of the Taı¨ chimpanzees leave behind a record of stone artefacts. These can be distinguished from human artefacts or naturally splintered rocks by ‘blind’ assessors, dated by standard radiometric techniques (C14), and yield organic residues (starch grains) that reveal their function. We can now speak of a chimpanzee ‘stone age’ with time depth. Carvalho et al. (2008) applied one of the core concepts of archaeology, the chaine operatoire, to the nut-cracking of Bossou’s chimpanzees, showing that from start to finish, this analytical technique is equally applicable to apes as to humans. Even retrospective

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3270

W. C. McGrew Chimpanzees and the last common ancestor

analyses of chimpanzee artefacts, in this case the brush-sticks used to fish for termites, as found in a museum, may explain how they were made (Heaton & Pickering 2006; cf. Sanz & Morgan 2007). The extent to which the archaeology of non-humans can be pushed back in time remains to be seen, but a new field is now underway (Haslam et al. 2009). Finally, here is a sobering thought: of all the tools named so far, only some of the hammers and anvils, and some of the missiles thrown, will have a chance of persisting in the archaeological record, taphonomy willing, because they are made of stone. All of the others are made of organic raw materials, e.g. plant or animal matter, and so will perish over time. There are other lithic objects used, e.g. stones in self-tickle, pebbles in play start, boulders in splash display, etc., but it is unlikely that these will be archaeologically recognizable.

(b) Diet The chimpanzee is an omnivore, as all well-studied populations show a mix of herbivory and faunivory. The former is dominated by ripe fruit, but also includes leaves, pith, seeds, flowers, bark, gum, etc. The latter focuses on social insects (ants, bees, termites) and small- to medium-sized mammals, especially monkeys. Invertebrates usually are taken by tool-assisted extractive foraging, such as ant-dipping, ant-fishing, honey-dipping and termite-fishing, that is, by gathering. Until recently, vertebrate prey were known to be captured and dispatched only by hand, without technology. Pruetz & Bertolani (2007) showed that the chimpanzees of Fongoli, Senegal, use a weapon-assisted hunting technique to disable or kill bushbabies while they sleep during the day in tree holes. The weapon is a sharpened stick (spear), jammed into the prosimian’s sleeping chamber. (Some sceptics have questioned whether the technique qualifies as hunting, or the instrument as a spear. When an Inuit waits beside a seal’s air-hole in the ice, then thrusts a sharp-ended linear object into it, skewering the prey, we are happy to call it hunting, so why not for apes?). Notably absent from the diets of most chimpanzee populations are the underground storage organs (USO) of plants, that is, bulbs, roots, tubers, corms, rhizomes, etc. This absence was thought to reflect the generalized, non-digging hands of primates, plus the apes’ lack of the appropriate technology, that is, the digging stick. Hernandez-Aguilar et al. (2007) recently described how the chimpanzees of Ugalla, Tanzania, dig up roots, using sticks and pieces of bark that show the abraded wear patterns of repeatedly used digging tools. Spat-out wadges of fibrous roots show them to be chewed and sucked, then discarded. A similar processing technique is used by the chimpanzees of Tongo, Democratic Republic of Congo, to get drinking water from subterranean tubers, but these are dug up by hand from friable, volcanic soils (Lanjouw 2002). Across the continent, from Tanzania to Ivory Coast, chimpanzee hunters take more monkeys as prey than all other types of vertebrates combined, especially favouring the red colobus (Piliocolobus badius) (e.g. Watts & Mitani 2002). Others also hunt ungulates, Phil. Trans. R. Soc. B (2010)

but one of the keenest hunting populations, the chimpanzees of Taı¨, does not hunt the small forest antelopes (Cephalophus spp.) that are plentiful there. At the same time, several populations of bonobos avidly hunt antelope, but were said to show no interest in primate prey; this apparent species difference evaporated with Surbeck & Hohmann’s (2008) report that the bonobos of Lui Kotale, Democratic Republic of Congo, also hunt guenons (Cercopithecus spp.). What differs between the two sibling species of chimpanzee and bonobo is the sexual politics of meat-sharing. In bonobos, females control the carcass and distribute the meat, and their collective dominance over males sometimes leaves the males with none, even if individually a male can dominate a female (Hohmann & Fruth 2008). In chimpanzees, males often control carcasses, and there has been much debate about how the sharing of the meat functions in chimpanzee society. Now come solid data to test Stanford’s (1999) hypothesis of meat-for-sex, that is, that males selectively give meat to females in exchange for sexual favours. Gomes & Boesch (2009) report that females copulate more often with males who share meat with them in the long term. Thus, the female need not be in oestrus at the time of the hunt, but rather forms a relationship that mutually enhances the lifetime reproductive success of male (insemination probability) and female (nutritional enhancement). However, meat-sharing in some chimpanzee populations, e.g. Gombe in Tanzania (Gilby 2006), appears to be driven by different mechanisms: intimidation, harassment, reciprocity, etc. Less likely is Tennie et al.’s (2009) ‘meat-scrap’ hypothesis that meat-sharing can be explained by the micro-nutrients found in even small amounts of meat. Meat-eating is only one kind of faunivory, and the same nutrients can be easily obtained from invertebrates, which chimpanzees eat daily. Male sharing of prized foodstuffs with females also occurs with plant foods, which otherwise is rare in apes, usually occurring only between mother and infant. However, Hockings et al. (2007) showed that when males at Bossou raided crops, especially papaya (Carica papaya), they almost always shared the proceeds with females of reproductive age, even when the latter were not in oestrus. These sharing patterns reflected patterns of later sexual consortship. What about scavenging? Scattered, anecdotal reports of chimpanzee scavenging mammalian prey have appeared from time to time, but no systematic study was done until Watts (2008a) documented all known scavenging opportunities at Ngogo over 11 years of observations totalling over 10 000 h. In that period, he saw only four scavenging events, and opportunities were rare, occurring on average only every 100 h. This contrasts mightily with over 650 kills made in over 270 hunts in the same period (Watts & Mitani 2002). Similar pictures of rarity emerge from Gombe, Mahale and Taı¨. Chimpanzees are not scavengers, it seems.

(c) Shelter Shelter can be defined as the use of any material object to buffer the effects of the elements. A universal

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chimpanzees and the last common ancestor W. C. McGrew behavioural pattern among great apes is their daily construction of arboreal sleeping platforms: every weaned individual builds an overnight nest and many also build day nests for napping. These compound artefacts are scattered over the landscape and may endure for months, leaving a record of points in space where chimpanzees spend most of their lives. (Chimpanzees typically retire at dusk and arise at dawn, and so spend half of each tropical circadian cycle in their beds.) Hernandez-Aguilar (2009) found 5354 nests over a 20 month period at Issa, an open-country, savannah area in western Tanzania. These shelters were highly clumped on woodland hillsides, in particular sites that were re-used over and over again. The chimpanzees’ ranging and consequent nest distribution varied predictably over wet and dry seasons, reflecting an annual cycle of movement that reflects availability of surface water and ripe fruit. However prominent a part these shelters play in their daily lives, these constructions later will be archaeologically invisible, being made entirely of woody vegetation. At the same time, studies of individual nests and their making have yielded insights: Koops et al. (2007) showed that at Nimba, surprisingly many nests were built on the ground. From the patterning and size of nests, they hypothesized that this reflected a pattern of male overnight mateguarding, that is, when an oestrous female nested in a tree, a male seemed to nest on the ground at its base, to sequester her from the nocturnal attention of other males. Various functions for nests have been proposed: anti-predator, anti-parasite, anti-disease vector, thermoregulation, etc., but there has yet been no comprehensive study of these hypotheses. Meanwhile, Stewart et al. (2007) studied the proximal characteristics of nests, in terms of their architecture and materials. First-hand empirical data showed that chimpanzees prefer comfortable nests, presumably to gain restorative sleep for their big brains. The species’ name for the chimpanzee implies a cave dweller, yet until recently, there was no record of chimpanzees using caves as shelter. Pruetz (2007) reported that the Fongoli chimpanzees, who occupy one of the hottest and driest areas in the species’ distribution, regularly use a cave during the hottest season of the year. They retreat to its cooler environment during the heat of the day for ‘siestas’ and picnics; overnight, they sleep in arboreal nests, just like other great ape populations. Chimpanzees are notoriously hydrophobic, as they do not swim, which makes watercourses notable barriers to their geographical distribution. However, they enter surface water in certain circumstances: at Fongoli, they immerse themselves in temporary rain-filled pools at the beginning of the rainy season, when it is still hot and humid; there they rest, groom and play (Pruetz & Bertolani 2009). Thus, water becomes a thermoregulatory device, even when potentially risky.

(d) Ranging Although some authors (e.g. Lovejoy 2009) stubbornly continue to characterize evergreen rainforest Phil. Trans. R. Soc. B (2010)

3271

as the typical ecotype for wild chimpanzees, and so contrast their ecological context with that of hominins who lived in more seasonal, mosaic habitats, this restrictive picture is less and less tenable. Most of the study sites at which chimpanzees have been studied, and at least (depending on definition) three (Fongoli, Gombe and Mahale) of the eight where the apes have been fully habituated to close-range observation, are not evergreen rainforest. More accurately, chimpanzees subsist in a range of ecotypes, from woodland savannah (not steppe) to rainforest, with mean annual rainfall that range from about 800 to more than 2000 mm per year. Many of these landscapes are vegetationally heterogenous, and chimpanzee use of this array of habitat types varies greatly. At the other extreme, chimpanzees (unlike baboons, Papio spp.) do not survive in places that lack surface water for drinking or that lack the riverine forests that follow these watercourses, although only a tiny fraction of such gallery forest will suffice. Copeland’s (2007, 2009) detailed comparison of several open and arid African habitats shows that landscapes with annual rainfall in the 500 – 750 mm range cannot support chimpanzees. Early hominins apparently relied on eating C4 plants and USOs, both of which have yet to be shown to be important in the diets of chimpanzees, despite recent prominent findings (Hernandez-Aguilar et al. 2007). When drinking water runs short, that is, during the dry season when water table drops below the surface, chimpanzees turn to digging wells when riverbeds are sandy enough to allow this (Hunt & McGrew 2002). Although the wells are dug by hand, leaf sponges are used to extract water from the wells; it would not be surprising to find digging tools used to dig wells in other substrates, e.g. mud, gravel, etc. On a day-to-day basis, chimpanzees must find ephemeral food. Frugivores in particular must find and monitor clumps of food that should be eaten at peak ripeness and which varies from year to year in availability. The same grove that yielded a bumper crop last year may not fruit at all this year. The biodiverse array of trees, shrubs and lianas, much less nonwoody plants, may present a potential cornucopia of food, but the daily challenge is how to be in the right place at the right time. Various hypotheses have been put forward as to how chimpanzees achieve this, but the strategy turns out to be simple: Normand et al. (2009) showed that chimpanzees in the Taı¨ Forest memorize the locations of thousands of individual trees. Modelling of the apes’ powerful spatial memory allows for their ‘rules’ of foraging to be inferred, e.g. travel longer distances to resources that allow longer feeding bouts, revisit more often sources where you last ate for long periods. But how to acquire such information? Murray et al. (2008) showed at Gombe that even in adulthood and long after their mothers have died, males return to the core ranges used by their mothers, especially in lean times. Resource locations learned during dependent infancy are harvested lifelong. It is all very well to know what resources are in the home range, but how to know where they are, that is, how to navigate optimally between them? Again, various hypotheses have been proposed, e.g. spatial

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3272

W. C. McGrew Chimpanzees and the last common ancestor

orientation by means of landmarks. Normand & Boesch (2009) show from data on travel directions and distances that Taı¨ chimpanzees have sophisticated mental maps, that is, cognitive two-dimensional representations of the landscape that allow them to travel from resource to resource in straight lines.

2. DISCUSSION What can now be said about the LCA, based on what has been learned over the past 5 years from field studies of wild chimpanzees? Technology is the obvious starting point: — Given the large and varied tool kits of the chimpanzee, we can expect that of the LCA to be similar. That is, tools were made and used not just for food acquisition and processing, but also in selfmaintenance and shelter, as well as in social and sexual life (not covered here). However, just as the size of tool repertoire in chimpanzees is a function of research effort, so it will be in recovering the material culture of the LCA. — Most of the presumed technology of the LCA is archaeologically unrecoverable, given its perishable, organic nature; thus the archaeological record is biased towards lithics. Short of a time machine, this problem is insoluble, but aspects of chimpanzee behaviour that are universal, such as bed-making or leaf-sponging, are hard to deny to the LCA. — As with chimpanzees, the material culture of the LCA will show inter- and intra-regional differences (e.g. Schoening et al. 2008). Just as nut-cracking differs between East and West Africa (Morgan & Abwe 2006), despite the common presence of both prey and raw materials (McGrew et al. 1997), so it is for the LCA. Similarly, just as extractive foraging for social insects is central to Tanzanian populations of chimpanzees, but is largely absent in the neighbouring country of Uganda, so we should not be surprised to find such differences in e.g. Kenyan and Ethiopian populations of a species of hominin. — Subsistence technology in chimpanzees involves reuse of artefacts, whether these are nut-cracking hammers or ant-dipping wands. Especially given that the extent of reuse seems to be a function of availability of raw materials (and some African forests afford no surface stones bigger than a walnut, e.g. Lui Kotale, W. C. McGrew & L. F. Marchant 2006, unpublished data), the same is expected of the LCA. Just as at Bossou, reuse of stone tools may increase the probability of predictable fracture or amplified use – wear that would leave archaeological signatures in the resulting artefacts. Lack of data on curation of tools by apes in nature may reflect lack of precise study, as evidence exists of such premeditated storage in captivity (Osvath 2009). — Given tool sets in chimpanzees, we should expect the same in the LCA. But how to recognize sequential use from a static assemblage? This is further complicated by findings that anvils may Phil. Trans. R. Soc. B (2010)

—

—

—

—

become hammers, as they are modified by use (Carvalho et al. 2009). That is, tools may change functional categories. (Studies of refitting may help to distinguish reduction products from tool sets; e.g. Delagnes & Roche 2005). Moreover, application of knowledge from ape tool sets may help make sense of patterned heterogeneity in archaeological assemblages, as revealed by multivariate statistical analyses. Composite tools probably were used by the LCA, but the challenge is to recognize such combinations in recovered lithic assemblages. It is not always clear what was the goal of reduction sequences in knapping, such as core or flake. The best candidate still may be pounding technology, as it seems likely that flaked stone did not spring de novo with the Oldowan, but more probably evolved from earlier lithic percussion for other reasons. Perhaps the analogues to chimpanzee hammers and anvils are there to be found in deposits older than 2.6 Ma? Primatologists should be able to help in seeking the pre-Oldowan (Haslam et al. 2009), based on reliably recognized modifications from chimpanzee hammers and anvils. This may help to clarify persisting confusion and controversy (e.g. Mora & de la Torre (2005) versus Diez-Martin et al. (2009)) among archaeologists. Apart from their nest-building, chimpanzees have few compound artefacts. In the evolution of human elementary technology, much is made of the first evidence of hafted weapons, that is, a compound tool of shaft, point and fixative. However, arguably, the earliest known compound technology was necklaces of snail shells, as found in Blombos Cave, South Africa (Henshilwood et al. 2004). Whether or not the LCA had compound tools is unclear, especially as not all components survive equally well, e.g. the spear’s shaft versus its point, the necklace’s string versus its shells. Studies of the acquisition and development of chimpanzee technology remind us that some proportion of what is found archaeologically is probably the immature version of the polished adult form of material culture. How much debitage reflects ‘honest’ mistakes by youthful learners versus clumsy or misguided efforts by adults? This problem probably applies as well to the LCA. Actualistic studies of children of various ages learning to knap stone might be useful. Finally, we must repeatedly remind ourselves that the LCA was almost certainly not a chimpanzee, and vice versa. Just as living apes continue to reveal new kinds of technology, so should we expect the same from the LCA. If chimpanzees turn out not to use tools to make other tools, or lack important but basic material cultural items like the container, or do not transport objects over long distances, we may have found important hominin watersheds (cf. Wynn & McGrew 1989).

Regarding diet: — Chimpanzee opportunistic omnivory is clear, and so it is probably in the LCA. The same inference

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chimpanzees and the last common ancestor W. C. McGrew derives from increasing evidence of dietary overlap (e.g. monkey-hunting) between chimpanzee and bonobo, although important differences remain between these taxa (e.g. extractive foraging for insects). — Recent findings of chimpanzee use of USOs paradoxically show apes to be capable of harvesting these foodstuffs, yet in no known population are they a staple (cf. Hockings et al. 2009, for data on USOs as fallback foods). Experimental studies need to be done on the limits of chimpanzeedigging. Similarly, chimpanzees commonly consume the pith of C4 plants, yet not the seeds or corms, and so their stable isotope data are confusing (Sponheimer et al. 2006). (It seems likely that staple exploitation of cereals requires grinding technology, which seems to be absent in wild chimpanzees, but apparently has not been tested with apes in captivity.) Or, it may be that profitable use of USOs and cereals requires treatment by fire, that is, cooking, which came much later in human evolution (Carmody & Wrangham 2009). Here, studies of wild chimpanzees are not yet helpful in hypothesizing about the LCA. — Chimpanzees are wide-ranging foragers, and their patterns of ranging map onto the distribution of their resources, as in any other organism. What we now are beginning to know is the extent of their intelligent foraging, and it exceeds our expectations, e.g. about spatial memory. This upgrades our estimation of the LCA, but inferring the timing and spacing of resources in the archaeological record is problematic. — Recent findings on chimpanzee hunting confirm its seductiveness for evolutionary scenarios. (Conversely, scavenging’s role seems less and less important, at least until after the LCA, in the hominin lineage.) However, estimations of the importance of hunting, based on chimpanzees, must be tempered: Most chimpanzee hunting is done arboreally, by ‘four-handed’ hunters who can leap about in the canopy, pursuing monkeys. This is not likely to be instructive about hunting by terrestrial bipeds, even if it applies to the LCA, who may have practised ambush hunting on the ground, as well as pursuit hunting in the treetops. More significantly, the function of carnivory is revealed to be much richer than expected: sharing meat may drive social and sexual life, almost as a currency (although many of the same arguments probably apply also to honey).

3273

most chimpanzee field sites do not offer caves, although this has never been systematically studied. — We now know that chimpanzee nests are more complex structures than hitherto realized, and this may imply that beyond a certain point of investment of time and effort, they began to be reused. This raises the possibility of home bases, already hinted at in the non-random distribution of chimpanzee nest sites on the landscape. But until we know the fitness-enhancing function of beds, it would be rash to infer the same for the LCA. Anti-predation is assumed, but equally attractive alternative hypotheses are there to be tested. The presence of ground nests is sometimes presumed to be based on local release from predation, but no correlative study of sympatric large carnivores and apes has been done. On ranging and foraging: — Chimpanzees are nomadic over areas that can be large, that is, tens or even hundreds of square kilometres. If the singlemost obvious influence on this ranging is food availability, the more crucial limiting factors may be drinking water and cover. Well-digging, especially with the technological assistance of digging tools and containers, appears to allow an expanded ecological niche. (Unlike temperature or humidity, which turn out not to be so important.) Similarly, no matter how dry and open the eco-type inhabited, every known population of great apes seems to require access to trees for shelter construction. Even savannahdwelling chimpanzees need their ribbons of gallery forest. The same was probably true of the LCA. In conclusion, even if one-tenth of what has been learned in the last five years about wild chimpanzees is applicable to the LCA of living apes and humans, then the case has been made for preserving them. Referential modelling requires living proxies upon which to base the models, and current expectations are that wild populations of great apes may be gone by the middle of the current century. Both primatologists and palaeoanthropologists should work together to save them. Most of the author’s data and ideas were supported by the US National Science Foundation, Researching Hominid Origins Initiative (Award no. BCS-0321893) grant awarded to Tim White and to the late Clark Howell. I am grateful to S. Carvalho, L. F. Marchant, P. Mellars and A. Walker for comments on the manuscript.

On shelter: REFERENCES — Based on the near-uniformity of arboreal overnight sleeping off the ground in great apes, it seems likely that the LCA did the same. It may be that safe terrestrial sleeping came much later, with the domestication of fire (Pruetz & LaDuke 2010). But we now know that cave use, at least during the day, did not depend on fire, and that thermoregulation needs could have been for diurnal cooling, rather than nocturnal heat retention. However, Phil. Trans. R. Soc. B (2010)

Biro, D., Carvalho, S. & Matsuzawa, T. In press. Tools, traditions, and technologies: interdisciplinary approaches to chimpanzee nut-cracking. In The mind of the chimpanzee: ecological and experimental perspectives (eds E. V. Lonsdorf, S. R. Ross & T. Matsuzawa). Chicago, IL: University of Chicago Press. Boesch, C., Head, J. & Robbins, M. M. 2009 Complex tool sets for honey extraction among chimpanzees in Loango National Park, Gabon. J. Hum. Evol. 56, 560 –569. (doi:10.1016/j.jhevol.2009.04.001)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3274

W. C. McGrew Chimpanzees and the last common ancestor

Brewer, S. M. & McGrew, W. C. 1990 Chimpanzee use of a tool-set to get honey. Folia Primatol. 54, 100 –104. (doi:10.1159/000156429) Carmody, R. & Wrangham, R. W. 2009 The energetic significance of cooking. J. Hum. Evol. 57, 379 –391. (doi:10.1016/j.jhevol.2009.02.011) Carvalho, S., Cunha, E., Sousa, C. & Matsuzawa, T. 2008 Chaines operatoires and resource-exploitation strategies in chimpanzee (Pan troglodytes) nut-cracking. J. Hum. Evol. 55, 148–163. (doi:10.1016/j.jhevol.2008. 02.005) Carvalho, S., Biro, D., McGrew, W. C. & Matsuzawa, T. 2009 Tool-composite reuse in wild chimpanzees (Pan troglodytes): archaeologically invisible steps in the technological evolution of early hominins? Anim. Cogn. 12(Suppl. 1), 103–114. (doi:10.1007/s10071-009-0271-7) Copeland, S. 2007 Vegetation and plant reconstruction of lowermost Bed II, Oldovai Gorge, using modern analogs. J. Hum. Evol. 53, 146–175. (doi:10.1016/j.jhevol.2007. 03.002) Copeland, S. 2009 Potential hominin plants foods in northern Tanzania: semi-arid savannas versus savanna chimpanzee sites. J. Hum. Evol. 57, 365 –378. (doi:10. 1016/j.jhevol.2009.06.007) Deblauwe, I., Guislain, P., Dupain, J. & van Elsacker, L. 2006 Use of a tool-set by Pan troglodytes troglodytes to obtain termites (Macrotermes) in the periphery of the Dja Biosphere Reserve, southeast Cameroon. Am. J. Primatol. 68, 1191– 1196. (doi:10.1002/ajp.20318) Delagnes, A. & Roche, H. 2005 Late Pliocene hominid knapping skills: the case of Lokalalei 2C, West Turkana, Kenya. J. Hum. Evol. 48, 435–472. (doi:10.1016/j. jhevol.2004.12.005) Diez-Martin, F., Sanchez, P., Dominguez-Rodrigo, M., Mabulla, A. & Barba, R. 2009 Were Olduvai hominins making butchering tools or battering tools? Analysis of a recently excavated lithic assemblage from BK (Bed II, Olduvai Gorge, Tanzania). J. Anthropol. Archaeol. 28, 274 –289. (doi:10.1016/j.jaa.2009.03.001) Fowler, A. & Sommer, V. 2007 Subsistence technology of Nigerian chimpanzees. Int. J. Primatol. 28, 997–1023. (doi:10.1007/s10764-007-9166-0) Gilby, I. C. 2006 Meat sharing among Gombe chimpanzees: harassment and reciprocal exchange. Anim. Behav. 71, 953 –963. (doi:10.1016/j.anbehav.2005.09.009) Gomes, C. M. & Boesch, C. 2009 Wild chimpanzees exchange meat for sex on a long-term basis. PLoS ONE 4, e5116. (doi:10.1371/journal.pone.0005116) Goodall, J. & Hamburg, D. A. 1974 Chimpanzee behavior as a model for the behavior of early man. New evidence on possible origins of human behavior. Am. Handb. Psychiat. 6, 14–43. Hansell, M. H. 2004 Animal architecture. Oxford, UK: Oxford University Press. Haslam, M. et al. 2009 Primate archaeology. Nature 460, 339 –344. (doi:10.1038/nature08188) Heaton, J. L. & Pickering, T. R. 2006 Archaeological analysis does not support intentionality in the production of brushed ends on chimpanzee termiting tools. Int. J. Primatol. 27, 1619–1633. (doi:10.1007/s10764-006-9091-7) Henshilwood, C. A., d’Errico, F., Vanhaeren, M., van Niekerk, K. & Jacobs, Z. 2004 Middle Stone Age shell beads from South Africa. Science 304, 404. (doi:10.1126/science. 1095905) Hernandez-Aguilar, A. 2009 Chimpanzee nest distribution and site re-use in a dry habitat: implications for early hominin ranging. J. Hum. Evol. 57, 350–364. (doi:10. 1016/j.jhevol.2009.03.007) Hernandez-Aguilar, A., Moore, J. & Pickering, T. R. 2007 Savanna chimpanzees use tools to harvest the Phil. Trans. R. Soc. B (2010)

underground storage organs of plants. Proc. Natl Acad. Sci. USA 104, 19 210 –19 213. (doi:10.1073/pnas. 0707929104) Hicks, T. C., Fouts, R. S. & Fouts, D. H. 2005 Chimpanzee (Pan troglodytes troglodytes) tool use in the Ngotto Forest, Central African Republic. Am. J. Primatol. 65, 221 –237. (doi:10.1002/ajp.20111) Hockings, K. J., Humle, T., Anderson, J. R., Biro, D., Sousa, C., Ohashi, G. & Matsuzawa, T. 2007 Chimpanzees share forbidden fruit. PLoS ONE 2, e886. (doi:10.1371/journal.pone.0000886) Hockings, K. J., Anderson, J. R. & Matsuzawa, T. 2009 Flexible feeding on cultivated underground storage organs by rainforest-dwelling chimpanzees at Bossou, West Africa. J. Hum. Evol. 58, 227 –233 (doi:10.1016/j.jhevol.2009. 11.004) Hohmann, G. & Fruth, B. 2008 New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Folia Primatol. 79, 103–110. (doi:10.1159/000110679) Humle, T., Snowdon, C. T. & Matsuzawa, T. 2009 Social influences on ant-dipping acquisition in the wild chimpanzees (Pan troglodytes verus) of Bossou, Guinea, West Africa. Anim. Cogn. 12, 37–48. (doi:10.1007/ s10071-009-0272-6) Hunt, K. D. & McGrew, W. C. 2002 Chimpanzees in the dry areas of Assirik, Senegal, and Semliki Wildlife Reserve, Uganda. In Behavioural diversity in chimpanzees and bonobos (eds C. Boesch, G. Hohmann & L. F. Marchant), pp. 35–51. Cambridge, UK: Cambridge University Press. Kano, T. 1992 The last ape: pygmy chimpanzee behavior and ecology. Stanford, CA: Stanford University Press. Koops, K., Humle, T., Sterck, E. H. M. & Matsuzawa, T. 2007 Ground-nesting by the chimpanzees of the Nimba Mountains, Guinea: Environmentally or socially determined? Am. J. Primatol. 69, 407–419. (doi:10. 1002/ajp.20358) Koops, K., McGrew, W. C. & Matsuzawa, T. 2010 Do chimpanzees (Pan troglodytes) use cleavers and anvils to fracture Treculia africana fruits? Preliminary data on a new form of percussive technology. Primates 51, 175 –178. (doi:10.1007/s.10329-009-0178-6) Lanjouw, A. 2002 Behavioural adaptations to water scarcity in Tongo chimpanzees. In Behavioural diversity in chimpanzees and bonobos (eds C. Boesch, G. Hohmann & L. F. Marchant), pp. 52–60. Cambridge, UK: Cambridge University Press. Ling, V., Hernandez-Aguilar, A., Haslam, M. & Carvalho, S. 2009 The origins of percussive technology; a smashing time at Cambridge. Evol. Anthropol. 18, 48–49. (doi:10. 1002/evan.20197) Lonsdorf, E. V. 2006 What is the role of mothers in the acquisition of termite-fishing behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? Anim. Cogn. 9, 36–46. (doi:10.1007/s10071-005-0002-7) Lovejoy, C. O. 2009 Reexamining human origins in light of Ardipithecus ramidus. Science 326, 74e1–74e8. (doi:10. 1126/science.1175834) Marchant, L. F. & McGrew, W. C. 2004 Percussive technology: chimpanzee baobab smashing and the evolutionary modeling of hominid knapping. In Stone knapping: the necessary conditions for a uniquely hominin behaviour? (eds V. Roux & B. Bril), pp. 341 –350. Cambridge, UK: McDonald Institute for Archaeological Research. Matsuzawa, T. 2006 Sociocognitive development in chimpanzees: a synthesis of laboratory work and fieldwork. In Cognitive development in chimpanzees (eds T. Matsuzawa, M. Tomonaga & M. Tanaka), pp. 3 –33. Tokyo, Japan: Springer.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chimpanzees and the last common ancestor W. C. McGrew Matsuzawa, T., Biro, D., Humle, T., Inoue-Nakamura, N., Tonooka, R. & Yamakoshi, G. 2001 Emergence of culture in wild chimpanzees: education by master-apprenticeship. In Primate origins of human cognition and behavior (ed. T. Matsuzawa), pp. 557– 574. Tokyo, Japan: Springer. McBrearty, S. & Jablonski, N. G. 2005 First fossil chimpanzee. Nature 437, 105– 108. (doi:10.1038/nature.04008) McGrew, W. C. 1974 Tool use by wild chimpanzees in feeding upon driver ants. J. Hum. Evol. 3, 501–508. (doi:10.1016/0047-2484(74)90010-4) McGrew, W. C. 1981 The female chimpanzee as a human evolutionary prototype. In Woman the gatherer (ed. F. Dahlberg), pp. 35–73. New Haven, CT: Yale University Press. McGrew, W. C. 1992 Chimpanzee material culture: implications for human evolution. Cambridge, UK: Cambridge University Press. McGrew, W. C. 2004 The cultured chimpanzee: reflections on cultural primatology. Cambridge, UK: Cambridge University Press. McGrew, W. C., Ham, R. M., White, L. T. J., Tutin, C. E. G. & Fernandez, M. 1997 Why don’t chimpanzees in Gabon crack nuts? Int. J. Primatol. 18, 353–374. (doi:10.1023/A:1026382316131) Mercader, J., Panger, M. & Boesch, C. 2002 Excavation of a chimpanzee stone tool site in the African rainforest. Science 296, 1452–1455. (doi:10.1126/science.1070268) Mercader, J., Barton, H., Gillespie, J., Harris, J., Kuhn, S., Tyler, R. & Boesch, C. 2007 4,300-year-old chimpanzee sites and the origins of percussive stone technology. Proc. Natl Acad. Sci. USA 104, 3043–3048. (doi:10. 1073/pnas/0607909104) Mitani, J. C., Watts, D. P. & Muller, M. N. 2002 Recent developments in the study of wild chimpanzee behavior. Evol. Anthropol. 11, 9–25. (doi:10.1002/evan.10008) Moore, J. J. 1996 Savanna chimpanzees, referential models and the last common ancestor. In Great ape societies (eds W. C. McGrew, L. F. Marchant & T. Nishida), pp. 275 –292. Cambridge, UK: Cambridge University Press. Mora, R. & de la Torre, I. 2005 Percussion tools in Olduvai Beds I and II (Tanzania): implications for early human activities. J. Anthropol. Archaeol. 24, 179 –192. (doi:10. 1016/j.jaa.2004.12.001) Morgan, B. J. & Abwe, E. E. 2006 Chimpanzees use stone hammers in Cameroon. Curr. Biol. 16, R632–R633. (doi:10.1016/j.cub.2006.07.045) Murray, C. M., Gilby, I. C., Mane, S. V. & Pusey, A. E. 2008 Adult males inherit maternal ranging patterns. Curr. Biol. 18, 20–24. (doi:10.1016/j.cub.2007.11.044) Nishida, T., Matsusaka, T. & McGrew, W. C. 2009 Emergence, propagation or disappearance of novel behavioral patterns in the habituated chimpanzees of Mahale: a review. Primates 50, 23–36. (doi:10.1007/ s10329-008-0109-y) Normand, E. & Boesch, C. 2009 Sophisticated Euclidean maps in forest chimpanzees. Anim. Behav. 77, 1195– 1201. (doi:10.1016/anbehav2009.01.025) Normand, E., Ban, S. D. & Boesch, C. 2009 Forest chimpanzees (Pan troglodytes verus) remember the location of numerous fruit trees. Anim. Cogn. 12, 797 –807. (doi:10.1007/s10071-009-0239-7) Osvath, M. 2009 Spontaneous planning for future stone throwing by a male chimpanzee. Curr. Biol. 19, R190 –R191. (doi:10.1016/j.cub.2009.01.010) Pruetz, J. D. 2007 Evidence of cave use by savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal: implications for thermoregulatory behavior. Primates 48, 316 –319. (doi:10.1007/s10329-007-0038-1)

Phil. Trans. R. Soc. B (2010)

3275

Pruetz, J. D. & Bertolani, P. 2007 Savanna chimpanzees, Pan troglodytes verus, hunt with tools. Curr. Biol. 17, 412–417. (doi:10.1016/j.cub.2006.12.042) Pruetz, J. D. & Bertolani, P. 2009 Chimpanzee (Pan troglodytes verus) behavioral responses to stresses associated with living in a savanna-mosaic environment: implications for hominin adaptations to open habitats. Palaeoanthropology 2009, 252–262. (doi:10.4207/PA.2009.ART33) Pruetz, J. D. & LaDuke, T. C. 2010 Reaction to fire by savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal: conceptualization of ‘fire behavior’ and the case for a chimpanzee model. Am. J. Phys. Anthropol. 141, 646–650. (doi:10.1002/ajpa.21245) Sanz, C. M. & Morgan, D. B. 2007 Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo. J. Hum. Evol. 52, 420 –433. (doi:10.1016/j. jhevol.2006.11.001) Sanz, C. M. & Morgan, D. B. 2009 Flexible and persistent tool-using strategies in honey-gathering by wild chimpanzees. Int. J. Primatol. 30, 411 –427. (doi:10. 1007/s10764-009-9359-5) Sanz, C., Call, J. & Morgan, D. 2009a Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes). Biol. Lett. 5, 293 –296. (doi:10.1098/rsbl.2008.0786) Sanz, C. M., Schoening, C. & Morgan, D. B. 2009b Chimpanzees prey on driver ants with specialized tool set. Am. J. Primatol. 71, 1 –8. (doi:10.1002/ajp.20744) Sayers, K. & Lovejoy, C. O. 2008 The chimpanzee has no clothes. A critical examination of Pan troglodytes in models of human evolution. Curr. Anthropol. 49, 87–114. (doi:10.1086.523765) Schoening, C., Humle, T., Moebius, Y. & McGrew, W. C. 2008 The nature of culture: technological variation in chimpanzee predation on army ants revisited. J. Hum. Evol. 55, 48–59. (doi:10.1016/j.jhevol.2007.12.002) Sousa, C., Biro, D. & Matsuzawa, T. 2009 Leaf-tool use for drinking water by wild chimpanzees (Pan troglodytes): acquisition patterns and handedness. Anim. Cogn. 12, S115– S125. (doi:10.1007/s.10071-009-0278-0) Sponheimer, M., Loudon, J. E., Codron, C., Howells, M. E., Pruetz, J. D., Codron, J., de Ruiter, D. J. & LeeThorp, J. A. 2006 Do ‘savanna’ chimpanzees consume C4 resources? J. Hum. Evol. 51, 128–133. (doi:10.1016/ j.jhevol.2006.02.002) Stanford, C. B. 1999 The hunting apes. Meat eating and the origins of human behavior. Princeton, NJ: Princeton University Press. Stewart, F. A., Pruetz, J. D. & Hansell, M. H. 2007 Do chimpanzees build comfortable nests? Am. J. Primatol. 69, 930 –939. (doi:10.1002/ajp20432) Sugiyama, Y. 1997 Social tradition and the use of toolcomposites by wild chimpanzees. Evol. Anthropol. 6, 23–27. (doi:10.1002/(SICI)1520-6505(1997)6:1,23:: AID-EVAN7.3.0.CO;2-X) Surbeck, M. & Hohmann, G. 2008 Primate hunting by bonobos at LuiKotale, Salonga National Park. Curr. Biol. 18, R906 –R907. (doi:10.1016/j.cub.2008.08.040) Tennie, C., Gilby, I. C. & Mundry, R. 2009 The meat-scrap hypothesis: small quantities of meat may promote cooperative hunting in wild chimpanzees (Pan troglodytes). Behav. Ecol. Sociobiol. 63, 421 –431. (doi:10.1007/ s00265-008-0676-3) Tooby, J. & DeVore, I. 1987 The reconstruction of hominid behavioral evolution through strategic modeling. In The evolution of human behavior: primate models (ed. W. G. Kinzey), pp. 183 –237. Albany, NY: State University of New York Press. Toth, N. & Schick, K. 2009 The Oldowan: the tool making of early hominins chimpanzees compared.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3276

W. C. McGrew Chimpanzees and the last common ancestor

Ann. Rev. Anthropol. 38, 289– 305. (doi:10.1146/ annurev-anthro-091908-164521) Watts, D. P. 2008a Scavenging by chimpanzees at Ngogo and the relevance of chimpanzee scavenging to early hominin behavioral ecology. J. Hum. Evol. 54, 125– 133. (doi:10. 1016/j.jhevol.2007.07.008) Watts, D. P. 2008b Tool use by chimpanzees at Ngogo, Kibale National Park, Uganda. Int. J. Primatol. 29, 83–94. (doi:10.1007/s10764-007-9227-4) Watts, D. P. & Mitani, J. C. 2002 Hunting behavior of chimpanzees at Ngogo, Kibale National Park,

Phil. Trans. R. Soc. B (2010)

Uganda. Int. J. Primatol. 23, 1 –28. (doi:10.1023/A: 1013270606320) Whiten, A. et al. 2010 Studying extant species to model our past. Science 327, 410. (doi:10.1126/science.327.5964. 410-a) Wynn, T. G. & McGrew, W. C. 1989 An ape’s view of the Oldowan. Man 24, 383 –398. (doi:10.2307/2802697) Yamakoshi, G. & Sugiyama, Y. 1995 Pestle-pounding behavior of wild chimpanzees at Bossou, Guinea: a newly observed tool-using behavior. Primates 36, 489 –500. (doi:10.1007/BF02382871)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3277–3288 doi:10.1098/rstb.2010.0096

More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure Anne C. Stone1,*, Fabia U. Battistuzzi2, Laura S. Kubatko4, George H. Perry Jr1, Evan Trudeau6, Hsiuman Lin5 and Sudhir Kumar2,3 1

School of Human Evolution and Social Change, 2Center for Evolutionary Medicine and Informatics, Biodesign Insitute, and 3School of Life Sciences, Arizona State University, Tempe, AZ, USA 4 Department of Mathematics and Statistics, and 5Department of Anthropology, University of New Mexico, Albuquerque, NM, USA 6 Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO, USA Here, we report the sequencing and analysis of eight complete mitochondrial genomes of chimpanzees (Pan troglodytes) from each of the three established subspecies (P. t. troglodytes, P. t. schweinfurthii and P. t. verus) and the proposed fourth subspecies (P. t. ellioti ). Our population genetic analyses are consistent with neutral patterns of evolution that have been shaped by demography. The high levels of mtDNA diversity in western chimpanzees are unlike those seen at nuclear loci, which may reflect a demographic history of greater female to male effective population sizes possibly owing to the characteristics of the founding population. By using relaxed-clock methods, we have inferred a timetree of chimpanzee species and subspecies. The absolute divergence times vary based on the methods and calibration used, but relative divergence times show extensive uniformity. Overall, mtDNA produces consistently older times than those known from nuclear markers, a discrepancy that is reduced significantly by explicitly accounting for chimpanzee population structures in time estimation. Assuming the human – chimpanzee split to be between 7 and 5 Ma, chimpanzee time estimates are 2.1 – 1.5, 1.1 – 0.76 and 0.25– 0.18 Ma for the chimpanzee/bonobo, western/ (eastern þ central) and eastern/central chimpanzee divergences, respectively. Keywords: mitochondrial genome; Pan troglodytes; Pan paniscus; divergence time

1. INTRODUCTION Mitochondrial DNA has long been used to investigate questions about primate taxonomy and demography (e.g. Morin et al. 1994; Horai et al. 1995; Gagneux et al. 1999; Schrago & Russo 2003; Eriksson et al. 2004; Raaum et al. 2005). The ability to sequence the complete mtDNA genome relatively quickly and inexpensively has resulted in a number of studies in humans that investigate population history (Ingman et al. 2000; Maca-Meyer et al. 2001; Herrnstadt et al. 2002; Ingman & Gyllensten 2003; Macaulay et al. 2005; Thangaraj et al. 2005; Sun et al. 2006) and selection (Nachman et al. 1996; Mishmar et al. 2003; Elson et al. 2004). However, the application of complete mtDNA sequence data to questions about population history and selection within other species has not been common. Chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are our sister species, and studies of

* Author for correspondence ([email protected]). Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rstb.2010.0096 or via http://rstb.royalsocietypublishing.org. One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

genetic variation in these species shed light on their evolutionary histories as well as serve as a comparison to our own history. Both paleoanthropological and genetic studies indicate that that the human and chimpanzee þ bonobo lineages diverged 6.5– 4.2 Ma (Sarich & Wilson 1973; White et al. 1994; Chen & Li 2001; Glazko & Nei 2003; Kumar et al. 2005), while chimpanzees and bonobos diverged more recently with estimates ranging from 2.5 to 0.8 Ma (Horai et al. 1992; Kaessmann et al. 1999; Stone et al. 2002; Yu et al. 2003; Fisher et al. 2004; Won & Hey 2005; Caswell et al. 2008). Genetic data, as well as some morphological data, suggest strong population structuring within chimpanzees that correlates with subspecies boundaries, and this structure appears to be demarcated by river and habitat boundaries and reinforced by dispersal patterns (Gagneux et al. 2001; Guy et al. 2003; Lockwood et al. 2004; Gonder et al. 2006; Becquet et al. 2007). Currently, three subspecies, distributed across the central part of Africa, are recognized within chimpanzees. Pan t. schweinfurthii is the easternmost subspecies, located in Tanzania, Burundi, Rwanda, Uganda and the Democratic Republic of Congo. The central subspecies, P. t. troglodytes, is found in Congo, Gabon, the Central African Republic, Equatorial

3277

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3278

A. C. Stone et al.

Divergence times in Pan

Guinea and Cameroon, and P. t. verus, the westernmost subspecies, is found in Senegal, Guinea-Bissau, Guinea, Sierra Leone, Liberia, Mali and Ivory Coast. MtDNA research has also suggested a potential fourth subspecies, P. t. ellioti (Oates et al. 2009), formerly known as P. t. vellerosus, in Nigeria (Gonder et al. 1997, 2006; Gagneux et al. 1999), although the limited Y-chromosome evidence has failed to support this claim (Stone et al. 2002). Demographic inferences about chimpanzee subspecies are limited but mostly indicate a larger effective population size in the central subspecies, and an initial split between the western and central/eastern subspecies (Deinard & Kidd 1999; Kaessmann et al. 1999; Stone et al. 2002; Fisher et al. 2004; Won & Hey 2005; Becquet et al. 2007). There has also been a distinction between haploid markers (both mtDNA and Y-chromosome studies) that have shown high levels of structure (corresponding to subspecies designations) and autosomal nuclear data that have suggested significant gene flow, differences in male and female effective population sizes and/or incomplete sorting of lineages. On the one hand, this has led to some researchers nominating new subspecies based on results from haploid markers (Gonder et al. 1997; Gonder Disotell & Oates 2006), while others have proposed elimination of subspecies designations altogether based on the nuclear data (Fisher et al. 2006). In addition, some experts suggest that the western and Nigerian chimpanzees should form one subspecies (P. t. vellerosus), while the central and eastern chimpanzees should belong to a second subspecies (P. t. troglodytes; Gonder Disotell & Oates 2006). More recently, a large autosomal microsatellite dataset has supported substructure within chimpanzees that corresponds to the subspecies designations (Becquet et al. 2007). Comparisons of levels of intraspecific variability have important implications for understanding the evolution of hominoid genomes and clarifying the demographic history of contemporary populations of humans and great apes (Stone & Verrelli 2006). Because of the different signals regarding population history as well as the conflicting estimates of divergence times based on different loci, a better sampling of markers and populations is needed. In this study, we report complete mtDNA sequences in eight chimpanzees including individuals from all of the three currently recognized subspecies as well as an individual with a P. t. ellioti mtDNA haplotype to assess the neutrality of evolutionary patterns of the mtDNA genome and to examine intraspecific diversity. A major emphasis of our mtDNA analysis is to investigate why the timing of divergence between chimpanzees and bonobos and among the subspecies of chimpanzees that have been reported from previous mtDNA studies are much older than those obtained using the nuclear DNA (e.g. Horai et al. 1995; Stone et al. 2002; Fisher et al. 2004; Won & Hey 2005).

2. MATERIAL AND METHODS (a) Materials The complete mitochondrial genomes from seven wild-born chimpanzees (four P. troglodytes verus, two Phil. Trans. R. Soc. B (2010)

P. t. schweinfurthii and one P. t. ellioti ) and one captive born chimpanzee (haplotype corresponds to P. t. troglodytes) were sequenced for this study. When unknown, subspecies status was determined based on a comparison of the mtDNA HVI region sequence to those from chimpanzees of known subspecies (Morin et al. 1994; Gonder et al. 1997; Stone et al. 2002). Two P. t. verus samples, Pt115 and Pt120 (ISIS no. 2738 and 2216), and the P. t. ellioti sample, Pt114 (ISIS no. 2412), were from the New Iberia Primate Center. The remaining two P. t. verus samples, Pt82 and Pt105 (North American regional studbook for the chimpanzee no. 341 and ISIS no. 2435), were from the Riverside Zoo in Scottsbluff, NE, and the Southwest Foundation for Biomedical Research, respectively. The two P. t. schweinfurthii samples, Pt96 and Pt161 (ISIS no. 3020 and 925), and the P. t. troglodytes sample, Pt13 (ISIS no. 4441), were from the Primate Foundation of Arizona. Whole blood samples (5 –10 ml) were taken during routine veterinary examinations, and DNA was isolated using a standard phenol/chloroform-based extraction (Sambrook & Russell 2001).

(b) Polymerase chain reaction and nucleotide sequencing The complete mtDNA genome was amplified in 28 overlapping segments using the polymerase chain reaction (PCR) in a PTC-200 thermal cycler (MJ Research). PCR primers for each segment are listed in the electronic supplementary material. For most segments, PCR conditions were: 948C for 5 min (948C, 30 s; annealing temperature specified in table S1 in the electronic supplementary material, 30 s; 728C, 30 s) for 35 cycles, followed by a single final extension of 728C for 5 min. A touchdown PCR protocol was used for segments amplified with primers L846 and H1620, L4589 and H5276 and L14110 and H14900. For these segments, PCR conditions were: 948C for 5 min (948C, 30 s; 108C above annealing temperature specified in table S1 in the electronic supplementary material minus 0.58C per cycle, 30 s; 728C, 30 s) for 20 cycles, (948C, 30 sec; annealing temperature specified in table S1 in the electronic supplementary material, 30 s; 728C, 30 s) for another 20 cycles, then 728C for 5 min. PCR products were purified with the QIAquick Purification Kit (Qiagen) and sequenced in two directions, using the BigDye terminator cycle sequencing kit v. 3.1 (Applied Biosystems) and an Applied Biosystems 3730 capillary sequencer. Sequence trace files were assembled using the SEQMAN program (DNAStar), and then manually checked and aligned. MtDNA insertions into the nuclear genome (numts) can complicate analyses and invalidate conclusions if they are mistakenly amplified in the place of authentic mtDNA sequence (Bensasson et al. 2001; Thalmann et al. 2004). Although there was no direct evidence that numts had been amplified here (i.e. there were no ‘heterozygous’ positions and no nucleotide mismatches between overlapping fragments), we checked the authenticity of our sequences with the long-range PCR method described by

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Divergence times in Pan Thalmann et al. (2004) using Platinum Taq HiFi (Invitrogen). Briefly, for each chimpanzee individual, we amplified two large fragments, A (approx. 9 kb) and B (approx. 10 kb), which overlap each other at both ends to cover the entire mtDNA genome using primers listed in table S1 in the electronic supplementary material. Five microlitres of the PCR product was electrophoresed through a 2 per cent NuSieve GTG low-melting agarose (Cambrex) gel. Bands were excised and melted in 100 ml Molecular Biology Reagent Water (Sigma) at 558C for 1 h, and then vortexed thoroughly. Four microlitres of this mixture was then used to amplify and sequence three of our original segments, using the methods specified above. One of these segments (primers L15255 and H107, 1214 bp) was amplified from both fragments A and B. Additionally, we amplified a 687 bp segment (L4589 and H5276) from fragment A and an 862 bp segment (L8333 and H9195) from fragment B. The resulting sequences were compared with each other and with the original sequence for each individual. There were no observed discrepancies, supporting the authenticity of the complete mtDNA genome sequences generated for these eight individuals. These data were submitted to GenBank and are listed under accession numbers GU112738 – GU112745.

(c) Data analysis We compared our sequences with those from previous studies, including two P. t. verus (Jenny, GenBank accession number X93335 and the chimpanzee mtDNA reference sequence no. NC 001643), one P. paniscus (no. NC 001644), one gorilla (Gorilla gorilla, no. NC 001645), one orangutan from each of the two subspecies (Pongo pygmaeus, no. NC 001646 and Pongo pygmaeus abelii, no. NC002083), one gibbon (Hylobates lar, no. NC 002082), the Cambridge human reference sequence (Homo sapiens, no. AC000021) and 53 additional humans (Anderson et al. 1981; Horai et al. 1992, 1995; Arnason et al. 1996; Xu & Arnason 1996; Andrews et al. 1999; Ingman et al. 2000). The hypervariable region or D-loop is non-coding and was excluded from most analyses because it is known to have a very different mutational pattern. Two estimates of diversity were calculated for each locus: p is based on the average number of nucleotide differences per site between two sequences randomly drawn from a sample and us is based on the sample size-corrected proportion of segregating sites (Watterson 1975; Nei 1987). The Jukes & Cantor (1969) correction was applied to all sequence comparisons involving interspecific variation and divergence (Lynch & Crease 1990). Under equilibrium conditions with respect to mutation and drift, both p and us estimate the neutral parameters: 2Nem for mtDNA, where Ne is the effective population size and m is the neutral mutation rate. Tajima’s D-statistic was calculated to test for deviations from neutral frequency distribution (Tajima 1989). The measures of diversity and tests of neutrality were performed with the program DNASP 4.0 (Rozas et al. 2003). Phil. Trans. R. Soc. B (2010)

A. C. Stone et al.

3279

The mutation rate for the complete genome, excluding the D-loop region, was calculated from the data as follows: mutation rate per site per year ¼ (k/2Tsplit) l, where k is the mean genetic distance, l the length of the sequence and Tsplit the time in years since the human and chimpanzee divergence. Tsplit is assumed to be 6 Ma. The mean genetic distance was estimated between the 10 chimpanzees examined in this study and the 53 humans from Ingman et al. (2000) using the Tamura– Nei distance (Tamura & Nei 1993) with the evolutionary rates among sites modelled using the gamma distribution in MEGA 4 (Tamura et al. 2007). The shape parameter for the gamma distribution was calculated using MODELTEST as noted below. MODELTEST (Posada & Crandall 1998) was used to select the most appropriate evolutionary model for each dataset. For the 13 protein-coding genes, the general time-reversible (GTR) model with a proportion of the sites invariable (I) and gammadistributed rates among sites (G ) was selected by the AIC criterion. For the complete genome without the D-loop, the GTR þ G model was selected by the AIC. Phylogenetic analyses were then performed using PAUP* (Swofford 2003) using the model and parameters estimated by MODELTEST. Ten random addition sequences with TBR branch swapping were used to obtain the maximum-likelihood estimates of the phylogenies. Bootstrap analyses were subsequently performed using 100 bootstrap replicates and TBR searches for each replicate for each dataset. We calculated divergence times between species and subspecies using two relaxed-clock methods: MULTIDIVTIME (MDT) and BEAST (Thorne & Kishino 2002; Drummond & Rambaut 2007). In these methods, a Markov Chain Monte Carlo (MCMC) procedure is used within a Bayesian analysis framework to estimate the posterior distributions of evolutionary rates and divergence times, given priors on phylogenetic relationships and calibration nodes. These analyses were performed using DNA sequence alignment of the complete mitochondrial genome, except the D-loop region, and for 13 protein-coding genes separately. The protein-coding genes were analysed at amino acid and DNA sequence level as a super-alignment. We also analysed the fourfold (4F) degenerate sites by themselves, as their evolutionary patterns are expected to be the closest to the strict neutrality (Kumar et al. 2005). In MDT, branch lengths of the amino acid dataset (16 taxa, 3772 sites) were estimated with the mitochondrial mammal (mtmam.dat) model of substitution, while for nucleotides (genome and 4F sites) the F84 þ gamma model was used within the PAML program package (Yang 2007). Initial number of sites analysed for whole genome and 4F degenerate sites were 15 514 and 1843, respectively. All sites containing gaps and ambiguous nucleotides were excluded from the analyses. Other parameters used in MDT were: 10 000 sampling of the Markov chain, with sampling frequency every 100, burn-in of 100 000, and bigtime was set to 50 Ma. The root to tip distance (rttm) was set at 25 Ma with identical standard deviation (rttmsd).

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3280

A. C. Stone et al.

Divergence times in Pan

Table 1. Diversity statistics for mtDNA. Length is excluding gaps. *Significance: p , 0.05. taxa

n

length

s

p (%)

u (%)

Tajima’s D

complete genome P. troglodytes P. t. schweinfurthii P. t. s. and P. t. t. P. t. verus (w/Nigeria) P. t. verus H. sapiens a

10 2 3 7 6 53

16 543 16 556 16 556 16 548 16 548 16 553

695 38 134 413 320 657

1.48 0.23 0.54 0.95 0.84 0.37

1. 49 0.23 0.54 1.02 0.85 0.87

20.16

without D-loop P. troglodytes P. t. schweinfurthii P. t. s. and P. t. t. P. t. verus (w/Nigeria) P. t. verus H. sapiens a

10 2 3 7 6 53

15 441 15 443 15 443 15 441 15 441 15 430

544 26 95 298 224 516

1.23 0.17 0.41 0.72 0.62 0.29

1.25 0.17 0.41 0.79 0.64 0.74

20.16

a

20.49 20.1 22.12*

20.59 20.17 22.23*

Ingman et al. (2000).

The same data sets were analyzed also in BEAST with an uncorrelated lognormal relaxed clock. Substitution model used were the mtREV þ gamma þ invariant sites model for amino acids and the GTR þ gamma þ invariant sites for nucleotides. We also separated models for population and species divergences by using two populations based on the geographical distribution of the western and eastern þ central chimpanzee subspecies (two populations plus one species model). The remaining divergences were estimated under a Yule speciation process. The length of the chain for each analysis was adjusted to the dataset in order to obtain effective sample sizes above 200 for all parameters. The same prior information on times (lower and upper bounds) was used for the two molecular clock methods. These included the times of the following species divergences: gorilla versus chimpanzee þ human divergence (10 – 6.5 Ma) and the chimpanzee and human divergence (6.5 – 4.2 Ma) times defined as uniform distributions. These calibrations were used together or separately depending on the dataset and the hypothesis to test. MDT and BEAST yielded divergence times and their 95% credibility intervals (CrIs). In addition to species and subspecies divergences, BEAST also produces the age of the most recent common ancestor (TMRCA) based on the population sample included. We compared these estimates with those obtained using the GENETREE program, which simulates a coalescent process including time information conditional on a specific haplotype tree with a given value of u (Griffiths & Tavare´ 1994; Bahlo & Griffiths 2000). We estimated u for each dataset by GENETREE using the maximum-likelihood method. Indels and the D-loop were not included in the analyses, and constant population sizes and panmixia were assumed. Simulation results are based on 10 million replicate runs. To calculate the TMRCA in years, a chimpanzee generation time of 15 years was used and the divergence between chimpanzees and humans was set at 6 Ma. Phil. Trans. R. Soc. B (2010)

3. RESULTS The complete mtDNA genomes (16 541 bp) of 10 chimpanzees contain 695 segregating sites (table 1). We also observe insertion/deletion (indel) polymorphisms in both the 12S rRNA gene and the D-loop. In the 12S rRNA gene, an insertion of a guanine (G) after nucleotide position 138 was present in all sequences except the chimpanzee reference sequence. This G is also present in humans (Anderson et al. 1981; Ingman et al. 2000) where it is found in stem 7 of the secondary structure model of Neefs et al. (1993). In addition, a length polymorphism was found in the 12S rRNA gene in the loop between stems 23 and 24. Here, at nucleotide positions 378 – 384, an unstable run of cytocines resulted in significant variation with at least 6 –15 cytocines present. This region was difficult to PCR and produced a heteroplasmic sequence. In the D-loop, a total of 12 indels was found. Because it is difficult to properly incorporate indels into models of sequence evolution for estimating divergence times, these were removed from further analyses. Non-synonymous polymorphisms were found in all 13 protein-coding genes. On average, chimpanzee sequences contained 28.8 non-synonymous differences when compared with 8.91 observed in humans. The estimates of synonymous and nonsynonymous substitution diversities for each mitochondrial gene as well as comparative data from humans are shown in table 2. When examining silent and replacement sites separately (table 2), Tajima’s test rejected strict neutrality at a 5 per cent significance level in chimpanzees only for non-synonymous sites at CO3 and ND4L. Humans show many significantly negative Tajima’s D-statistic for both synonymous and non-synonymous sites. When data from only P. t. verus (without Pt114) was examined, three genes (ND1, CO2 and ND6) showed significantly negative Tajima’s D-values at replacement sites. When Pt114 was included in P. t. verus, only replacement sites at CO3 produced a significantly negative value (data not shown).

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Divergence times in Pan

A. C. Stone et al.

3281

Table 2. Population diversity estimates and tests of neutrality at mtDNA protein-coding genes in humans (n ¼ 53, Ingman et al. 2000) and chimpanzees (n ¼ 10). *p , 0.05. replacement taxa and genes

lengtha

Pan troglodytes ND1 ND2 CO1 CO2 ATP8 ATP6 CO3 ND3 ND4L ND4 ND5 ND6 CYTB all genes

954 1041 1539 681 204 678 783 345 294 1377 1809 522 1140 11 316

Homo sapiens ND1 ND2 CO1 CO2 ATP8 ATP6 CO3 ND3 ND4L ND4 ND5 ND6 CYTB all genes

954 1041 1539 681 204 678 783 345 294 1377 1809 522 1140 11 316

silent

pb

TDc

S

p

TD

3 16 4 2 4 7 6 5 2 12 17 3 8 88

0.0016 0.0066 0.0016 0.0013 0.0097 0.0054 0.0021 0.0055 0.0019 0.0032 0.0046 0.0022 0.0035 0.0034

0.13 20.46 1.32 20.03 0.23 0.39 21.8* 20.83 21.4* 21 0.23 0.54 0.11 20.34

41 33 42 14 4 25 28 10 9 46 63 16 54 385

0.0539 0.046 0.042 0.026 0.025 0.051 0.058 0.045 0.048 0.045 0.05 0.045 0.069 0.049

20.27 0.18 0.51 20.46 20.45 0.11 0.68 0.41 0.81 20.05 0.07 0.33 0.18 0.14

8 13 8 3 2 8 4 3 1 12 23 5 16 106

0.0007 0.0012 0.0008 0.0007 0.0014 0.002 0.0003 0.0028 0.0002 0.0007 0.0015 0.0013 0.0011 0.0011

21.93* 22.04* 21.32 21.11 20.96 21.17 21.73* 0.12 21.32* 22.15* 21.95 21.31 22.2* 22.19*

19 29 40 19 6 22 25 10 9 43 51 20 26 318

0.0087 0.0071 0.0083 0.0067 0.0158 0.0096 0.0105 0.0108 0.015 0.0116 0.0095 0.0118 0.0099 0.0096

21.49* 22.31* 22.15* 22.32* 21.18 22.08* 22.01* 21.67* 21.09 21.89* 22.12* 22.01* 21.66* 22.17*

S

a

Length does not include the stop codon, for ‘all genes’, ATP8 and ND4L were truncated so that overlapping regions with other genes were not counted twice. b Nucleotide diversity. c Tajima’s D-test.

Our analysis shows that chimpanzees harbour approximately four times more nucleotide diversity ( p) than humans (table 1), while us is 1.7 times greater. Within chimpanzees, P. t. verus exhibited the most variation; however, multiple samples of the central subspecies were not included in this study and only two P. t. schweinfurthii were sampled. Despite the population structure within chimpanzees, Tajima’s test of the complete genome and also of only the protein-coding genes did not show a significant departure from neutrality, while it is significantly negative in humans (tables 1 and 2). These results support the assumption of constant population size in chimpanzees used in the GENETREE analysis. For a reduced dataset including only the chimpanzees, the best evolutionary model selected by MODELTEST using both likelihood ratio tests and the AIC was the GTR þ G model with the shape parameter in the gamma distribution, a, estimated to be 0.066. PAUP* was then used to estimate the ML tree and bootstrap support. Using the entire dataset, the phylogenetic analyses of both the complete genome without the D-loop and using only the protein-coding genes produced similar results Phil. Trans. R. Soc. B (2010)

(figure 1). Bootstrap support was high (greater than 97%) for all nodes. The western chimpanzee sequences, Pt82, Pt105, Pt115 and Pt120, the chimpanzee mtDNA reference sequence and the sequence for the chimpanzee Jenny cluster together with the Nigerian sequence, Pt114, as their most closely related taxon. The eastern chimpanzees, Pt96 and Pt161, cluster with the central chimpanzee sequence, Pt13. We first inferred a time tree of chimpanzee and bonobo evolution by using the MDT software. In this case, we used two primary time constrains: 10.0 –6.5 Ma for gorilla/(human þ chimpanzee) divergence and 6.5 – 4.2 for human/chimpanzee divergence. Using this calibration for full mitochondrial genome (excluding the D-loop), only amino acid alignments of 13 protein-coding genes and only 4F degenerate sites produced similar estimates (table 3). The chimpanzee/bonobo split was estimated to be 3.2 – 2.3 Ma. The time estimates for western/ (eastern þ central) and eastern/central splits were dated to 1.68– 1.13 and 0.46 – 0.34 Ma, respectively (table 3). Interestingly, MDT analysis yielded a human/chimpanzee divergence date of approximately 5.7 Ma, which would be considered young by some

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3282

A. C. Stone et al.

Divergence times in Pan Pt161

100

eastern + central

Pt96 100

Pt13 Pt114

100

Pt115 100 100 97 100

Pt82

100 100 100

100

western

Pt105 Pt120 Jenny Pt reference P. paniscus H. sapiens G. gorilla

0.01 Figure 1. Maximum-likelihood phylogeny of chimpanzees, human and gorilla. Full mitochondrial genome (excluding the D-loop) and 13 mitochondrial protein-coding genes gave similar results. The geographical location of the chimpanzee populations is shown. Bootstrap values are shown near each node.

Table 3. Time estimates and 95% CrIs (in million years) for major divergences in the phylogeny obtained using MDT and BEAST for three datasets (mitochondrial genome, amino acids, and 4F degenerate sites). MDT and BEAST coalescent model do not model population structure within chimpanzees, which, instead, is accounted for in BEAST 2 þ 1 model. MDT divergence times in parenthesis for the 4F degenerate sites are obtained with the human/chimpanzee calibration fixed at 6.5 Ma. All other times are estimated using gorilla/human þ chimpanzee (10.0–6.5 Ma) and human/chimpanzee (6.5 –4.2 Ma).

Mt genomea

amino acidsb

4Fc

time

95% CrI

time

95% CrI

time

95% CrI

MDT human/chimpanzee chimpanzee/bonobo western/eastern þ central Nigerian/western eastern/central

5.69 2.33 1.13 0.55 0.34

4.76– 6.46 1.75– 3.14 0.80– 1.70 0.37– 0.86 0.22– 0.58

5.73 3.17 1.5 0.78 0.43

4.72 –6.46 2.23 –4.24 0.86 –2.47 0.4–1.48 0.16 –0.93

5.65 (6.5) 2.81 (3.35) 1.68 (2.04) 0.811 (1) 0.458 (0.57)

4.49 –6.46 1.68 –4.19 0.84 –3 0.35 –1.66 0.7–1.11

BEAST (coalescent model) human/chimpanzee chimpanzee/bonobo western/eastern þ central Nigerian/western eastern/central

5.48 2.02 0.96 0.48 0.27

4.63– 6.5 1.53– 2.57 0.70– 1.22 0.35– 0.61 0.18– 0.37

5.43 2.79 1.13 0.72 0.35

4.46 –6.5 1.88 –3.72 0.84 –1.85 0.45 –1.03 0.15 –0.58

5.28 1.79 0.92 0.42 0.21

4.24 –6.35 1.23 –2.42 0.62 –1.27 0.27 –0.60 0.11 –0.33

BEAST (2 þ 1 model)d human/chimpanzee chimpanzee/bonobo western/eastern þ central Nigerian/western eastern/central

4.94 1.76 0.83 0.41 0.23

4.2–5.68 1.35– 2.19 0.64– 1.04 0.32– 0.52 0.16– 0.31

4.87 2.28 1.05 0.57 0.27

4.2–5.73 1.5–3.16 0.67 –1.45 0.36 –0.80 0.1–0.44

4.7 1.49 0.76 0.35 0.18

4.2–5.43 1.05 –1.99 0.51 –1.01 0.23 –0.47 0.095–0.27

a

Mitochondrial genome excluding the D-loop. Thirteen mitochondrial protein-coding genes. c 4F degenerate sites of the 13 protein-coding genes. d Two populations (western and eastern þ central) and one speciation model (Yule). b

experts. Therefore, we re-estimated divergence times in MDT by assuming the human/chimpanzee divergence to be 6.5 and found that all the resulting time estimates increased proportionally (table 3). Because MDT assumes that evolutionary rates among lineages are autocorrelated, we also estimated Phil. Trans. R. Soc. B (2010)

divergence times using the BEAST software, which allows rates among lineages to vary independently. For genomic DNA and amino acid sequence analysis, BEAST analyses produced estimates very similar to those from MDT for the same sequences (table 3). However, the BEAST analysis of 4F degenerate sites

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Divergence times in Pan

3283

respectively. These results were similar to those found by BEAST in the 4F dataset.

3.5 time estimates (Ma)

A. C. Stone et al.

3.0 2.5 2.0 1.5 1.0 0.5 0 chimpanzee/ bonobo

western/ eastern + central

eastern /central

Figure 2. Compilation of estimated divergence times between chimpanzees and bonobos and within chimpanzees from literature (autosomal loci only, filled circle) and this study (MDT, cross; BEAST (2 þ 1), square).

yielded much younger estimates (table 3). The above analyses, however, did not take into account the population structure of chimpanzees. In order to incorporate this biological reality, we conducted BEAST analysis by assuming that each P. t. subspecies constitutes a population (western subspecies and eastern þ central subspecies). This leads to a two populations plus one speciation model (2 þ 1 model), which yields younger divergence times than those obtained from MDT or from other BEAST analyses (table 3). Although the use of 2 þ 1 model in BEAST makes results younger compared with the estimates obtained without considering population structure within chimpanzees, the time estimates based on amino acid sequences are 50 per cent older than those from the analysis of DNA sequences (genome as well as 4F degenerate sites). Kumar et al. (2005) have previously shown that amino acid time estimates are often older and not preferred for relatively recent divergences. Overall, the 2 þ 1 model produces time estimates that are more similar to those reported from nuclear autosomal loci (figure 2). Based on the 2 þ 1 BEAST analysis, the average divergence times within the chimpanzees across three datasets are 2.28 – 1.49, 1.05– 0.76 and 0.27– 0.18 Ma for the chimpanzee/ bonobo, western/(eastern þ central) and the eastern/ central divergences, respectively (table 3). These results highlight the need for modelling populations correctly while estimating times of closely related species and subspecies divergences when using relaxed-clock methods. The time to the MRCA (TMRCA) for each chimpanzee population in the BEAST analysis was 0.35 and 0.18 (table 3). We compared these estimates of TMRCA with those obtained from GENETREE, which employs a coalescence process and estimates of diversity to generate time estimates. The estimate of sequence diversity for the complete genome, excluding the D-loop, was 1.38 1028 substitutions per site per year assuming a chimpanzee – human divergence time of 6 Ma. Using this estimate and applying GENETREE separately to each subspecies (western and eastern þ central), we obtained TMRCA of 202 000 (+14 000) and 180 000 (+19 000) years, Phil. Trans. R. Soc. B (2010)

4. DISCUSSION Studies of diversity and divergence times in chimpanzees, and primates in general, have frequently used mtDNA. Similar to some previous studies (Morin et al. 1994; Gagneux et al. 1999), our new data indicate that diversity within chimpanzees is greatest in the western subspecies ( p ¼ 0.94% for all or 0.84% without the Nigerian individual), although the sample size for the eastern/central subspecies ( p ¼ 0.54%) is rather small (n ¼ 3). This pattern of diversity is contrary to those found at nuclear loci where diversity estimates are higher in the central subspecies. For example, analyses of NRY data showed that central chimpanzees had higher levels of diversity, because five different haplotypes were observed when compared with only one observed in a much larger sample of western chimpanzees (Stone et al. 2002). In a survey of approximately 10 kb at Xq13.3 from 30 chimpanzees (17 P. t. verus, 12 P. t. troglodytes and 1 P. t. schweinfurthii), Kaessmann et al. (1999) found that P. t. troglodytes were the most diverse. The mean pairwise sequence diversity at this locus among chimpanzees was 0.13 per cent, which is about four times greater than that in humans (0.037%). We also found a similar difference. Kaessmann et al. (1999) also noted that the subspecies were not monophyletic for X-chromosome haplotypes (one western and one central chimpanzee shared the same haplotype). However, Verrelli et al. (2006) found that haplotypes were not shared between subspecies for the X-chromosome locus G6PD. At this locus, diversity was also greatest among central chimpanzees in a survey of 56 chimpanzees (6 P. t. troglodytes and 48 P. t. verus). Because the X-chromosome has three times the effective population size (Ne) of mtDNA, it should take three times as long as mtDNA to achieve monophyly. So it is not surprising that some of the X-chromosome lineages are not completely sorted among the subspecies given their likely divergence times. Autosomal sequences also indicate higher diversity in central chimpanzees followed by eastern and western chimpanzees (Deinard & Kidd 1999; Yu et al. 2003; Fisher et al. 2004, 2006). Fisher et al. (2004) found that central chimpanzees are 2.0 – 2.5 times more diverse than western chimps and worldwide samples of humans. Central chimpanzees also show a relatively high proportion of rare alleles that could be the result of an old bottleneck or fine-scale population structure. Won & Hey (2005) found evidence for oneway gene flow from P. t. verus to P. t. troglodytes and suggest that this may be the result of interactions between the Nigerian chimpanzees and the central subspecies. The distinct pattern of higher mtDNA diversity and lower diversity at other loci found in western chimpanzees suggests that the founding population of this subspecies may have been skewed with a larger number of females and a smaller group of closely related males. This pattern is perhaps not surprising

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3284

A. C. Stone et al.

Divergence times in Pan

Table 4. Divergence times (in million years) and ratios among major divergences for 4F degenerate sites from BEAST 2 þ 1 model. The human/chimpanzee (H/C) time is used as the reference in calculating the time ratios. The gorilla/human þ chimpanzee divergence was used as calibration (10.0–6.5 Ma) in all the estimations. The human/chimpanzee calibration was used either as a range (6.5–4.2 Ma) or fixed (6.5 Ma). Absolute times with H/C at 5 or at 7 Ma were scaled according to the ratios calculated. BEAST (2 þ 1)a absolute times (4F)

human/chimpanzee chimpanzee/bonobo western/(eastern þ central) eastern/central a

time ratios (4F)

absolute times

H/C ¼ (4.2 –6.5)

H/C ¼ 6.5

H/C ¼ (4.2–6.5)

H/C ¼ 6.5

H/C ¼ 5

H/C ¼ 7

4.70 1.49 0.76 0.18

6.50 1.94 0.98 0.23

— 32% 16% 4%

— 30% 15% 4%

5.00 1.49 0.76 0.18

7.00 2.09 1.06 0.25

Two populations (western and eastern þ central) and one speciation model (Yule).

given the philopatric mating patterns of chimpanzees where females disperse at adolescence, and males remain within their natal group (Nishida 1979; Pusey 1979; Wrangham 1979; Goodall 1986; Pusey & Packer 1986; Langergraber et al. 2007; Inoue et al. 2008). However, the pattern of higher mtDNA diversity/lower nuclear diversity in western chimpanzees compared with central þ eastern chimpanzees indicate that the finding and/or subsequent demography of the western subspecies was somehow different from that found in the other subspecies. Genetic studies confirm that the males within many chimpanzee groups are typically more closely related than females; however, this is not true in all groups, particularly those where habitat fragmentation, disease or poaching affect group demography (Morin et al. 1994; Vigilant et al. 2001; Lukas et al. 2005; Inoue et al. 2008). The mtDNA data generated in this study indicate that chimpanzee female effective population size has been large (Ne ¼ approx. 36 000 for all chimpanzees and approx. 20 000 for P. t. verus) with no evidence of population bottleneck or expansion. MtDNA data may also be affected by selection, and several studies suggest that many mtDNA protein polymorphisms are slightly deleterious in humans (e.g. Nachman et al. 1996; Rand & Kann 1996; Kivisild et al. 2006). In this study, we also found evidence for a significantly negative value of Tajima’s D for most mitochondrial protein-coding genes in humans (and for the genome as a whole) which can be indicative of population expansion and/or selection. However, in these chimpanzee data, a significant departure from neutrality was only found for CO3 and ND4L at replacement sites and there was no evidence for a departure from neutrality for the genome as a whole (table 2). In molecular phylogenetics analysis of the complete mtDNA of chimpanzees, bonobos, humans and other great apes, human lineages are the most recent closest relative of Pan, in agreement with the scores of previous studies. A more controversial issue in chimpanzee evolutionary genomics has been the timing of divergence between chimpanzees and bonobos and among the subspecies of chimpanzees owing to the discrepancy between nuclear and mitochondrial results. The results from our mtDNA analysis provide Phil. Trans. R. Soc. B (2010)

partial resolution for this discrepancy. We find that the lack of consideration of population substructure of the chimpanzee subspecies when using mtDNA is a major cause of this difference. Therefore, we consider the time estimates from the use of two populations þ one speciation model for analysing 4F degenerate sites data in BEAST to be the least biased and most appropriate for estimating chimpanzee divergence times. However, the absolute divergence times are strongly influenced by the calibration points used. For example, when using two calibration ranges (10.0–6.5 and 6.5 – 4.2 for gorilla/(human þ chimpanzee) and human/chimpanzee splits, respectively), we obtain chimpanzee/bonobo divergence of 1.49 Ma. However, the human/chimpanzee divergence predicted by BEAST in this case is only 4.70 Ma, which is significantly lower than the current expectation. By constraining the human/chimpanzee divergence to be 6.5, the chimpanzee/bonobo time increases to 1.94 Ma. Interestingly, the ratio of the estimates of human/chimpanzee and chimpanzee/bonobo divergences is very similar (0.30–0.32) in different BEAST analyses under 2 þ 1 model (table 4). Therefore, the estimate of chimpanzee/bonobo divergence times scales proportionally with the human/chimpanzee calibration. In this case, mtDNA analyses suggest a range of 2.09–1.49 Ma for chimpanzee/bonobo divergence, because the best estimates of human/ chimpanzee divergence are in the range of 7–5 Ma (Kumar et al. 2005; Hedges et al. 2006; figure 3). These mtDNA estimates for chimpanzee/bonobo are consistent with the range of 1.8 – 0.93 Ma based on the earlier analysis of Y-chromosomes, noncoding and non-repetitive genomic segments and X-chromosomes (Xq13.3; Kaessmann et al. 1999; Stone et al. 2002; Yu et al. 2003). However, more recent nuclear genome analyses have typically yielded a much younger date for this divergence (0.93 – 0.79 Ma). For example, Fisher et al. (2004) estimated a divergence time of 0.80 Ma for this divergence using a moment estimator method that examines the numbers of segregating sites at particular frequencies (Wakeley & Hey 1997). Won & Hey (2005) obtained an estimate of 0.89– 0.86 Ma from multiple datasets (Deinard & Kidd 1999; Kaessmann et al. 1999; Stone et al. 2002; Yu et al. 2003) using an isolation

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Divergence times in Pan

Jenny Pt reference Pt120 Pt105 Pt82 Pt115 Pt114 Pt13 Pt96 Pt161 P. paniscus H. sapiens G. gorilla Pongo pygmaues pygmaeus Pongo pygmaeus abelii Hylobates lar

H/C: 6.5 – 4.2 Ma

Jenny Pt reference Pt120 Pt105 Pt82 Pt115 Pt114 Pt13 Pt96 Pt161 P. Paniscus H. sapiens G. gorilla Pongo pygmaeus pygmaeus Pongo pygmaeus abelii Hylobates lar

H/C: 6.5 Ma

25

A. C. Stone et al.

20

15

10

5

3285

western

central + eastern

western

central + eastern

0 Ma

Figure 3. Timetrees obtained from BEAST (2 þ 1 model) from 4F degenerate sites. The time scale is in million years (Ma). Both trees used the gorilla/human þ chimpanzee calibration (10.0–6.5 Ma). Additionally, the upper tree used the human/ chimpanzee (H/C) calibration range of 6.5 –4.2 Ma while the lower tree fixed it at 6.5 Ma.

with migration (IM) model, as did Becquet & Przeworski (2007) who estimated a split of 0.92– 0.79 Ma from two datasets using an MCMC method to estimate the parameters of an IM model. Recently, Hey (2010) estimated a split of 0.68– 1.54 Ma using a multi-population IM model, while Wegmann & Excoffier (2010) used an approximate Bayesian computation approach to estimate a divergence time of 1.6 Ma. These previous studies and our analysis show how the time estimates are sensitive not only to the choice of dataset, but also to the models used to describe the chimpanzee’s population structure. Within chimpanzees, the western and central þ eastern clades diverged between 1.06 –0.76 Ma according to our mtDNA analyses. This is younger than previous estimates from mtDNA (1.6 – 1.3 Ma; Morin et al. 1994), but older than other estimates based on nuclear loci. Fisher et al. (2004) examined 5.4 kb of autosomal sequence in 14 central and 16 western chimpanzees, and they propose a time of 0.65– 0.43 Ma for the divergence of western and central þ eastern groups. Won & Hey (2005) also calculated a divergence time estimate of 0.43 Ma for the central and western subspecies, while Becquet & Przeworski (2007) obtained much younger time Phil. Trans. R. Soc. B (2010)

estimates (0.28 Ma for western/eastern split and 0.44 Ma western/central divergence). More recent estimates range from 0.34 – 0.91 Ma (Caswell et al. 2008; Wegmann & Excoffier 2010). Therefore, nuclear DNA time estimates are again much younger than those indicated by mtDNA. The eastern and central subspecies of chimpanzee are estimated to have diverged recently. Although these two subspecies do not appear to share either mtDNA or NRY haplotypes, these haplotypes are not monophyletic (Gagneux et al. 2001; Stone et al. 2002). From the limited number of sequences in this study, we estimate the divergence of eastern and central subspecies to be approximately 0.25– 0.18 Ma. The Nigerian lineage appears to have diverged significantly earlier (approx. 0.4 Ma). Even though the single Nigerian lineage potentially diverged much earlier than its closest relatives, there is yet no evidence from Y-chromosome and autosomal STR markers to elevate the Nigerian chimpanzees to a separate subspecies (Stone et al. 2002; Becquet et al. 2007). The consistent discrepancy among the different divergence estimates, both within chimpanzees and between chimpanzees and bonobos, are probably due to the different population histories reflected by different parts of the genome. The older divergence times

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3286

A. C. Stone et al.

Divergence times in Pan

based on mtDNA data may reflect a demographic history of greater female effective population size in Pan compared with the male effective population size (Stone et al. 2002; Eriksson et al. 2006). Despite the wealth of information gleaned from complete mtDNA genome sequences to provide insight into the maternal history and patterning of humans (e.g. Ingman et al. 2000; Macaulay et al. 2005), such population genetic data have not been available for other primates. In chimpanzees, complete mitochondrial DNA sequences have previously been published for only one of the three subspecies (Horai et al. 1995; Arnason et al. 1996). Analysis of these sequences along with eight additional sequences representing all of the recognized subspecies, including one individual from the proposed subspecies P. t. ellioti, add to the picture of diversity and population history in this species; however, these data also illustrate the need for additional sampling of chimpanzees throughout their range. In addition, mtDNA data may be affected by certain demographic scenarios (sexbiased dispersal and bottlenecks), as suggested in this study, as well as selection, and thus may not provide an accurate time scale of evolutionary or population events unless population structure is considered (Nachman et al. 1996; Ballard & Rand 2005). Much of the primate diversity and taxonomic data published to date relies solely on mtDNA data. These studies should be eyed with caution until additional data are available. We thank Cecil Lewis, Vinod Swarna and Brian Verrelli for helpful discussions and comments pertaining to this study and/or manuscript. This study would not have been possible without the samples generously provided by the New Iberia Primate Center (supported by an NCRR grant no. U42 RR015087 to the University of Louisiana at Lafayette, New Iberia Research Center), the Primate Foundation of Arizona, the Southwest Foundation for Biomedical Research and Riverside Zoo, Scottsbluff, Nebraska. This research was supported by the National Science Foundation to A.S. (BCS-0073871), the National Institutes of Health to S.K. (HG002096) and the Arizona State University.

REFERENCES Anderson, S. et al. 1981 Sequence and organization of the human mitochondrial genome. Nature 290, 457 –465. (doi:10.1038/290457a0) Andrews, R. M., Kubacka, I., Chinnery, P. F., Lightowlers, R. N., Turnbull, D. M. & Howell, N. 1999 Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 23, 147. Arnason, U., Gullberg, A. & Xu, X. 1996 A complete mitochondrial DNA molecule of the white-handed gibbon, Hylobates lar, and comparison among individual mitochondrial genes of all hominoid genera. Hereditas 124, 185 –189. (doi:10.1111/j.1601-5223.1996.00185.x) Bahlo, M. & Griffiths, R. C. 2000 Inference from genetrees in a subdivided population. Theor. Popul. Biol. 57, 79–95. (doi:10.1006/tpbi.1999.1447) Ballard, J. W. O. & Rand, D. M. 2005 The population biology of mitochondrial DNA and its phylogenetic implications. Annu. Rev. Ecol. Evol. Syst. 36, 621 –642. (doi:10.1146/annurev.ecolsys.36.091704.175513) Becquet, C. & Przeworski, M. 2007 A new approach to estimate parameters of speciation models with application to Phil. Trans. R. Soc. B (2010)

apes. Genome Res. 17, 1505–1519. (doi:10.1101/gr. 6409707) Becquet, C., Patterson, N., Stone, A. C., Przeworski, M. & Reich, D. 2007 Genetic structure of chimpanzee populations. PLoS Genet. 3, e66. (doi:10.1371/journal.pgen. 0030066) Bensasson, D., Zhang, D., Hartl, D. L. & Hewitt, G. M. 2001 Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol. Evol. 16, 314–321. (doi:10.1016/ S0169-5347(01)02151-6) Caswell, J. L., Mallick, S., Richter, D. L., Neubauer, J., Schirmer, C., Gnerre, S. & Reich, D. 2008 Analysis of chimpanzee history based on genome sequence alignments. PLoS Genet. 4, e1000057. (doi:10.1371/journal. pgen.1000057) Chen, F.-C. & Li, H. 2001 Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68, 444 –456. (doi:10.1086/318206) Deinard, A. & Kidd, K. 1999 Evolution of a HOXB6 intergenic region within the great apes and humans. J. Hum. Evol. 36, 687–703. (doi:10.1006/jhev.1999. 0298) Drummond, A. J. & Rambaut, A. 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214. (doi:10.1186/1471-2148-7-214) Elson, J. L., Turnbull, D. M. & Howell, N. 2004 Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am. J. Hum. Genet. 74, 229 –238. (doi:10.1086/381505) Eriksson, J., Hohmann, G., Boesch, C. & Vigilant, L. 2004 Rivers influence the population genetic structure of bonobos (Pan paniscus). Mol. Ecol. 13, 3425 –3435. (doi:10. 1111/j.1365-294X.2004.02332.x) Eriksson, J., Siedel, H., Lukas, D., Kayser, M., Erler, A., Hashimoto, C., Hohmann, G., Boesch, C. & Vigilant, L. 2006 Y-chromosome analysis confirms highly sexbiased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Mol. Ecol. 15, 939–949. (doi:10.1111/j.1365-294X.2006.02845.x) Fischer, A., Wiebe, V., Paabo, S. & Przeworski, M. 2004 Evidence for a complex demographic history of chimpanzees. Mol. Biol. Evol. 21, 799 –808. (doi:10.1093/molbev/ msh083) Fischer, A., Pollack, J., Thalmann, O., Nickel, B. & Paabo, S. 2006 Demographic history and genetic differentiation in apes. Curr. Biol. 16, 1133–1138. (doi:10.1016/j.cub. 2006.04.033) Gagneux, P. et al. 1999 Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc. Natl Acad. Sci. USA 96, 5077–5082. (doi:10. 1073/pnas.96.9.5077) Gagneux, P., Gonder, M. K., Goldberg, T. L. & Morin, P. A. 2001 Gene flow in wild chimpanzee populations: what genetic data tell us about chimpanzee movement over space and time. Phil. Trans. R. Soc. Lond. B 356, 889 –897. (doi:10.1098/rstb.2001.0865) Glazko, G. V. & Nei, M. 2003 Estimation of divergence times for major lineages of primate species. Mol. Biol. Evol. 20, 424–434. (doi:10.1093/molbev/msg050) Gonder, M. K., Oates, J. F., Disotell, T. R., Forstner, M. R. J., Morales, J. C. & Melnick, D. J. 1997 A new west African chimpanzee subspecies? Nature 388, 337. (doi:10.1038/41005) Gonder, M. K., Disotell, T. R. & Oates, J. F. 2006 New genetic evidence on the evolution of chimpanzee populations and implications for taxonomy. Int. J. Primatol. 27, 1103–1127. (doi:10.1007/s10764-006-9063-y) Goodall, J. 1986 The chimpanzees of Gombe: patterns of behavior. Cambridge, UK: Harvard University Press.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Divergence times in Pan Griffiths, R. C. & Tavare´, S. 1994 Simulating probability distributions in the coalescent. Theor. Popul. Biol. 46, 131 –159. (doi:10.1006/tpbi.1994.1023) Guy, F., Brunet, M., Schmittbuhl, M. & Viriot, L. 2003 New approaches in hominoid taxonomy: morphometrics. Am. J. Phys. Anthropol. 121, 198– 218. (doi:10.1002/ajpa. 10261) Hedges, S. B., Dudley, J. & Kumar, S. 2006 TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971 –2972. (doi:10.1093/ bioinformatics/btl505) Herrnstadt, C. et al. 2002 Reduced-median-network analysis of complete mitochondrial DNA coding-region sequences for the major African, Asian, and European haplogroups. Am. J. Hum. Genet. 70, 1152–1171. (doi:10.1086/339933) Hey, J. 2010 The divergence of chimpanzee species and subspecies as revealed in multi-population isolationwith-migration analyses. Mol. Biol. Evol. 27, 921–933. (doi:10.1093/molbev/msp298) Horai, S., Satta, Y., Hayasaka, K., Kondo, R., Inoue, T., Ishida, T., Hayashi, S. & Takahata, N. 1992 Man’s place in the hominoidea revealed by mitochondrial DNA genealogy. J. Mol. Evol. 35, 32–43. (doi:10.1007/ BF00160258) Horai, S., Hayasaka, K., Kondo, R., Tsugane, K. & Takahata, N. 1995 Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc. Natl Acad. Sci. USA 92, 532 –536. (doi:10.1073/pnas.92.2.532) Ingman, M. & Gyllensten, U. 2003 Mitochondrial genome variation and evolutionary history of Australian and New Guinean aborigines. Genome Res. 13, 1600 –1606. (doi:10.1101/gr.686603) Ingman, M., Kaessmann, H., Pa¨a¨bo, S. & Gyllensten, U. 2000 Mitochondrial genome variation and the origin of modern humans. Nature 408, 708–713. (doi:10.1038/ 35047064) Inoue, E., Inoue-Murayama, M., Vigilant, L., Takenaka, O. & Nishida, T. 2008 Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors. Am. J. Phys. Anthropol. 137, 256–262. (doi:10. 1002/ajpa.20865) Jukes, T. H. & Cantor, C. R. 1969 Evolution of protein molecules. In Mammalian protein metabolism (ed. H. N. Munro), pp. 21– 132. New York, NY: Academic Press. Kaessmann, H., Wiebe, V. & Pa¨a¨bo, S. 1999 Extensive nuclear DNA sequence diversity among chimpanzees. Science 286, 1159– 1162. (doi:10.1126/science.286. 5442.1159) Kivisild, T. et al. 2006 The role of selection in the evolution of human mitochondrial genomes. Genetics 172, 373 –387. (doi:10.1534/genetics.105.043901) Kumar, S., Filipski, A., Swarna, V., Walker, A. & Hedges, S. B. 2005 Placing confidence limits on the molecular age of the human –chimpanzee divergence. Proc. Natl Acad. Sci. USA 102, 18 842 –18 847. (doi:10.1073/pnas. 0509585102) Langergraber, K. E., Siedel, H., Mitani, J. C., Wrangham, R. W., Reynolds, V., Hunt, K. & Vigilant, L. 2007 The genetic signature of sex-biased migration in patrilocal chimpanzees and humans. PLoS ONE 2, e973. (doi:10. 1371/journal.pone.0000973) Lockwood, C. A., Kimbel, W. H. & Lynch, J. M. 2004 Morphometrics and hominoid phylogeny: support for a chimpanzee –human clade and differentiation among great ape subspecies. Proc. Natl Acad. Sci. USA 101, 4356– 4360. (doi:10.1073/pnas.0306235101) Lukas, D., Reynolds, V., Boesch, C. & Vigilant, L. 2005 To what extent does living in a group mean living with kin? Phil. Trans. R. Soc. B (2010)

A. C. Stone et al.

3287

Mol. Ecol. 14, 2181–2196. (doi:10.1111/j.1365-294X. 2005.02560.x) Lynch, M. & Crease, T. J. 1990 The analysis of population survey data on DNA sequence variation. Mol. Biol. Evol. 7, 377 –394. Maca-Meyer, N., Gonzalez, A. M., Larruga, J. M., Flores, C. & Cabrera, V. M. 2001 Major genomic mitochondrial lineages delineate early human expansions. BMC Genet. 2, 13. (doi:10.1186/1471-2156-2-13) Macaulay, V. et al. 2005 Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308, 1034–1036. (doi:10.1126/ science.1109792) Mishmar, D. et al. 2003 Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100, 171–176. (doi:10.1073/pnas.0136972100) Morin, P. A., Moore, J. J., Chakraborty, R., Jin, L., Goodall, J. & Woodruff, D. S. 1994 Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265, 1193–1201. (doi:10.1126/ science.7915048) Nachman, M. W., Brown, W. M., Stoneking, M. & Aquadro, C. F. 1996 Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142, 953 –963. Neefs, J. M., Van de Peer, Y., De Rijk, P., Chapelle, S. & De Wachter, R. 1993 Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res. 21, 3025– 3049. (doi:10.1093/nar/21.13.3025) Nei, M. 1987 Molecular evolutionary genetics. New York, NY: Columbia University Press. Nishida, T. 1979 The social structure of chimpanzees of the Mahale Mountains. In The great apes (eds D. A. Hamburg & E. R. McCown), pp. 73–121. Menlo Park, CA: Benjamin/Cummings. Oates, J. F., Groves, C. P. & Jenkins, P. D. 2009 The type locality of Pan troglodytes vellerosus (Gray 1862), and implications for the nomenclature of west African chimpanzees. Primates 50, 78–80. (doi:10.1007/s10329008-0116-z) Posada, D. & Crandall, K. A. 1998 MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817 –818. (doi:10.1093/bioinformatics/14.9.817) Pusey, A. 1979 Intercommunity transfer of chimpanzees in Gombe National Park. In The great apes (eds D. A. Hamburg & E. R. McCown), pp. 465–479. Menlo Park, CA: Benjamin/Cummings. Pusey, A. E. & Packer, C. 1986 Dispersal and philopatry. In Primate societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 250–266. Chicago, IL: University of Chicago Press. Raaum, R. L., Sterner, K. N., Noviello, C. M., Stewart, C. B. & Disotell, T. R. 2005 Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. J. Hum. Evol. 48, 237 –257. (doi:10.1016/j. jhevol.2004.11.007) Rand, D. M. & Kann, L. M. 1996 Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol. Biol. Evol. 13, 735–748. Rozas, J., Sanchez-DelBarrio, J. C., Messeguer, X. & Rozas, R. 2003 DNASP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496– 2497. (doi:10.1093/bioinformatics/btg359) Sambrook, J. & Russell, D. 2001 Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. Sarich, V. M. & Wilson, A. C. 1973 Generation time and genomic evolution in primates. Science 179, 1144–1147. (doi:10.1126/science.179.4078.1144)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3288

A. C. Stone et al.

Divergence times in Pan

Schrago, C. G. & Russo, C. A. 2003 Timing the origin of New World monkeys. Mol. Biol. Evol. 20, 1620–1625. (doi:10.1093/molbev/msg172) Stone, A. C. & Verrelli, B. C. 2006 Focusing on comparative ape population genetics in the post-genomic age. Curr. Opin. Genet. Dev. 16, 586–591. (doi:10.1016/j.gde.2006. 09.003) Stone, A. C., Griffiths, R. C., Zegura, S. L. & Hammer, M. F. 2002 High levels of Y-chromosome nucleotide diversity in the genus Pan. Proc. Natl Acad. Sci. USA 99, 43– 48. (doi:10.1073/pnas.012364999) Sun, C. et al. 2006 The dazzling array of basal branches in the mtDNA macrohaplogroup M from India as inferred from complete genomes. Mol. Biol. Evol. 23, 683 –690. (doi:10.1093/molbev/msj078) Swofford, D. L. 2003 PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sunderland, MA: Sinaur Associates. Tajima, F. 1989 Statistical method for testing the neutral muation hypothesis by DNA polymorphism. Genetics 123, 585 –595. Tamura, K. & Nei, M. 1993 Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512 –526. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007 Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599. (doi:10. 1093/molbev/msm092) Thalmann, O., Hebler, J., Poinar, H. N., Paabo, S. & Vigilant, L. 2004 Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol. Ecol. 13, 321 –335. (doi:10.1046/j. 1365-294X.2003.02070.x) Thangaraj, K., Chaubey, G., Kivisild, T., Reddy, A. G., Singh, V. K., Rasalkar, A. A. & Singh, L. 2005 Reconstructing the origin of Andaman Islanders. Science 308, 996. (doi:10.1126/science.1109987) Thorne, J. L. & Kishino, H. 2002 Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. 51, 689–702. (doi:10.1080/10635150290102456)

Phil. Trans. R. Soc. B (2010)

Verrelli, B. C., Tishkoff, S. A., Stone, A. C. & Touchman, J. W. 2006 Contrasting histories of G6PD molecular evolution and malarial resistance in humans and chimpanzees. Mol. Biol. Evol. 23, 1592–1601. (doi:10. 1093/molbev/msl024) Vigilant, L., Hofreiter, M., Siedel, H. & Boesch, C. 2001 Paternity and relatedness in wild chimpanzee communities. Proc. Natl Acad. Sci. USA 98, 12 890–12 895. (doi:10.1073/pnas.231320498) Wakeley, J. & Hey, J. 1997 Estimating ancestral population parameters. Genetics 145, 847–855. Watterson, G. A. 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276. (doi:10.1016/00405809(75)90020-9) Wegmann, D. & Excoffier, L. 2010 Bayesian inference of the demographic history of chimpanzees. Mol. Biol. Evol. 27, 1425– 1435. (doi:10.1093/molbev/msq028) White, T. D., Suwa, G. & Asfaw, B. 1994 Australopithicus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371, 306–312. (doi:10.1038/ 371306a0) Won, Y. J. & Hey, J. 2005 Divergence population genetics of chimpanzees. Mol. Biol. Evol. 22, 297–307. (doi:10. 1093/molbev/msi017) Wrangham, R. W. 1979 Sex differences in chimpanzee dispersion. In The great apes (eds D. A. Hamburg & E. R. McCown), pp. 481–489. Menlo Park, CA: Benjamin/ Cummings. Xu, X. & Arnason, U. 1996 The mitochondrial DNA molecule of Sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan. J. Mol. Evol. 43, 431– 437. (doi:10.1007/ BF02337514) Yang, Z. 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591. (doi:10.1093/ molbev/msm088) Yu, N., Jensen-Seaman, M. I., Chemnick, L., Kidd, J. R., Deinard, A. S., Ryder, O., Kidd, K. K. & Li, W. H. 2003 Low nucleotide diversity in chimpanzees and bonobos. Genetics 164, 1511–1518.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3289–3299 doi:10.1098/rstb.2010.0112

Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip – bent-knee gait C. Owen Lovejoy1,* and Melanie A. McCollum2 1

Department of Anthropology, School of Biomedical Sciences, Kent State University, OH, USA 2 Department of Cell Biology, University of Virginia, VA, USA

Until recently, the last common ancestor of African apes and humans was presumed to resemble living chimpanzees and bonobos. This was frequently extended to their locomotor pattern leading to the presumption that knuckle-walking was a likely ancestral pattern, requiring bipedality to have emerged as a modification of their bent-hip-bent-knee gait used during erect walking. Research on the development and anatomy of the vertebral column, coupled with new revelations from the fossil record (in particular, Ardipithecus ramidus), now demonstrate that these presumptions have been in error. Reassessment of the potential pathway to early hominid bipedality now reveals an entirely novel sequence of likely morphological events leading to the emergence of upright walking. Keywords: Australopithecus; bipedality; bent-hip – bent-knee; Ardipithecus; human evolution

1. INTRODUCTION For several decades, largely subsequent to the recovery of A.L.288-1 (‘Lucy’) ( Johanson et al. 1982), upright walking in early hominids was argued to have relied on a bent-hip – bent-knee (BHBK) gait (see, e.g. Stern & Susman 1983; Susman et al. 1984; Stern 2000). This argument rested on observations of locomotion in chimpanzees and gorillas, coupled with the presumption that the post-cranium of our last common ancestor (LCA) of Pan and Homo was fundamentally similar to those of extant African apes (but see Filler 1981). Despite the fact that early hominids such as A.L.288-1 (and other members of Australopithecus afarensis and Australopithecus anamensis) exhibit pelves, knees and feet with highly advanced adaptations to a striding, bipedal gait (Latimer & Lovejoy 1989; Lovejoy 2005a,b, 2007), the BHBK hypothesis has remained largely unchallenged save arguments based on energy consumption (e.g. Crompton et al. 1998; Carey & Crompton 2005; Sellers et al. 2005). The BHBK gait of Pan and Gorilla, however, is not a function of limitations imposed by hip or knee anatomy, but is instead a direct consequence of an absence of lumbar spine mobility. African apes are unable to lordose their lumbar spines, and therefore must flex both the hip and knee joints in order to position their centre of mass over the point of ground contact (Lovejoy 2005a). Lumbar immobility in Pan and Gorilla is a consequence of their possession of only three to four lumbar vertebrae and the ‘entrapment’ of the most caudal lumbar vertebra(e) between cranially extended ilia (Stevens 2004; Stevens & Lovejoy 2004; Lovejoy 2005a; McCollum et al. 2009). Although all three African ape species share these features, there is * Author for correspondence ([email protected]). One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

now considerable evidence indicating that they have not been retained from the common ancestor shared with the human clade. Instead, a more detailed study of the vertebral formulae and the lumbar column of African apes and early hominids indicates that the LCA of Pan and Homo most probably possessed a long (six to seven segments) mobile lumbar spine similar in number to those of Old World monkeys (OWMs), Proconsul and Nacholapithecus (McCollum et al. 2009). Because such columns would have been capable of near-full lordosis, these new findings in and of themselves contraindicate pronounced African ape-like BHBK bipedality in early hominids. New revelations about LCA structure provided by Ardipithecus ramidus (especially ARA-VP-6/500; Lovejoy et al. 2009a–d; White et al. 2009) further establish that hominids never displayed any of the numerous African ape-like specializations that have reduced lumbar mobility and thus required an unusually restricted BHBK gait. Here we review this new evidence.

2. THE AXIAL PATTERN OF THE LCA As is discussed more fully in McCollum et al. (2009), it is reasonable to assume that the modal vertebral formula of basal hominoids and the LCA of Pan and Homo to have been 7-13-6/7-4–one that differs from those of OWMs merely by the addition of a fourth sacral vertebra, and replacement of the external tail by a short coccyx. Two lines of evidence support this view. First is evidence provided by the vertebral formulae of Australopithecus and early Homo (Sanders 1995). Although complete axial data are unavailable for any single early hominid specimen, a number of partial specimens, including A.L. 288-1 (complete sacrum) and KNM-WT 15000 (interpretable lumbar column), indicate a pre-coccygeal vertebral formula of 7-12/13-6-4 (Pilbeam 2004; McCollum et al. 2009).

3289

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3290

C. O. Lovejoy & M. A. McCollum Gorilla 7-13-4-5 7-13-4-6 7-13-3-6 T11 T12 T13 L1 L2 L3 L4 S1 S2 S3 S4 S5

P. troglodytes 7-13-4-6 7-13-4-5 7-13-3-6

Spinopelvic pathways to bipedality P. paniscus 7-13-4-7 7-13-4-6 7-14-4-6

T11 T12 T13 L1 L2 L3 L4 S1 S2 S3 S4 S5

T11 T12 T13 T14/L1 L2 L3 L4 S1 S2 S3 S4 S5 S6 LCA 7-12-6-5 7-13-6-4 7-13-6-5 T11 T12 T13 L1 L2 L3 L4 L5 L6 S1 S2 S3 S4

H. sapiens 7-12-5-5 7-12-5-6

Australopithecus 7-12-6-4 7-12-6-5 7-13-6-4 T11 T12 L1 L2 L3 L4 L5 L6 S1 S2 S3 S4

T10 T11 T12 L1 L2 L3 L4 L5 S1 S2 S3 S4 S5

Figure 1. Probable pathways of lumbar reduction in African apes and hominids as deduced from extant vertebral formulae for each taxon. All axial formulae that exceed 10% of the total sample for each taxon are shown here, along with presumed modal formulae (those of highest probable frequencies) for the LCA and early hominids. A horizontal arrow indicates loss of a body segment (i.e. a reduction in the number of somites contributing to the pre-coccygeal vertebral column). A vertical arrow signifies changes in the positions of the anterior boundaries of Hox gene expression domains underlying the indicated transformations of vertebral identities. Note the differences in extant Pan species. For details, see McCollum et al. (2009). Axial formula data from Pilbeam (2004) and McCollum et al. (2009). (q M.A. McCollum).

The second source of evidence is the axial morphology of bonobos (Pan paniscus). Unlike chimpanzees (Pan troglodytes) and modern humans, whose modal number of pre-coccygeal vertebrae is 29/30, bonobos possess an axial column typically composed of 30/31 vertebrae, identical to that inferred for the basal hominoid. Although it is certainly possible that the long axial column of bonobos re-evolved from an ancestor with an abbreviated column similar to that of chimpanzees and modern humans, such modification has no obvious selective advantage and runs counter to the trend towards axial length reduction observed in all suspensory anthropoids (Benton 1967; McCollum et al. 2009). Rather, the long axial column of bonobos, along with the significantly different combinations of sacral, lumbar and thoracic vertebrae that are characteristic of common chimpanzees (seven cervical, 13 thoracic, three to four lumbar, five to six sacral) and bonobos (seven cervical, 13– 14 thoracic, four lumbar, six to seven sacral), suggest instead that the two species of Pan evolved their short lumbar spines from an ancestor with a long axial column (n ¼ 30/31 pre-coccygeal vertebrae) and a long lumbar spine after division from their own LCA. This receives support from data which suggest that lumbar spine reduction in chimpanzees apparently occurred through sacralization of the Phil. Trans. R. Soc. B (2010)

caudal-most lumbar vertebrae plus reduction in the number of somites (figure 1). Bonobos, conversely, appear to have reduced their lumbar column purely through transformations of segment identity, i.e. by transforming lumbar vertebrae into sacral and thoracic vertebrae (McCollum et al. 2009).

3. THE LOCOMOTOR SKELETON OF ARDIPTHECUS RAMIDUS The Ar. ramidus limb skeleton indicates that much of extant African ape locomotor anatomy has been independently derived for vertical climbing, suspension and a feeding habitus that probably included high canopy access in relatively large-bodied hominoids (Lovejoy et al. 2009a). While OWMs also frequently climb vertically, they nevertheless retain adaptations that are primarily for more active, above-branch pronograde running and leaping. Such acrobatics appear to have become much more limited in hominoids, presumably inter alia, because of their significantly larger body mass (Cartmill 1985). The locomotor skeleton of Ar. ramidus establishes that the LCA, unlike modern apes, retained many OWM-like features sufficiently primitive to assure a primary gait pattern of above-branch pronograde palmigrady (Lovejoy et al. 2009a– c). To be sure,

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Spinopelvic pathways to bipedality numerous modifications of OWM-like anatomy had become more like that of extant hominoids in the LCA (Lovejoy et al. 2009c)—alterations known to have been initiated in likely exemplars of its remote ancestors, especially various species of Proconsul (Ward 1991, 1993; Ward et al. 1991, 1993; Nakatsukasa et al. 2003). However, the Ar. ramidus foot still retained a relatively elongated mid-tarsus, a robust os peroneum complex and presumably numerous soft tissue features associable with an inherently stiff plantar structure more typical of the above-branch propulsion seen in OWMs. These latter features can be reliably extended to the LCA by parsimony, since they are still present in the feet of modern humans (quadratus plantae, plantaris, os peroneum, elongated cuboid, etc.), but have been largely eclipsed by specializations in the feet and ankles of more highly specialized, extant African apes (Desilva 2009; Lovejoy et al. 2009a). Similar observations of the Ar. ramidus forelimb suggest that it also shares a number of primitive features with humans. These include a very primitive and unreinforced central joint complex (CJC) (capitate, trapezoid, metacarpals 2 and 3), a relatively substantial pollex, a short metacarpus, a lack of significant Mc4/Mc5 – hamulus contact, a narrow trapezoid, a palmarly displaced capitate head and an unmodified, markedly rugose, deltopectoral crest. Each of these has since been modified in extant large-bodied African apes in favour of ones associable with knuckle-walking, suspension and/or vertical climbing (Lovejoy et al. 2009c).

4. THORACOABDOMINAL STRUCTURE AND FORELIMB MOBILITY IN THE LCA At the same time, it is equally clear that the LCA differed fundamentally from its likely ancestors (including Proconsul) in several major ways, none more important than the structure of its vertebral column and its position within the thorax (Lovejoy et al. 2009c). In comparison with Proconsul and OWMs, in which the pectoral girdle is positioned more anteriorly on the thoracic cage, the hominoid pectoral girdle is located more dorsolaterally, in a manner that causes its glenoid fossa to face more laterally than is typical of more primitive taxa (Waterman 1929; Schultz 1961; Erikson 1963; Ward 2007). Such ‘posterolateralization’ places the girdle into a more favourable position for circumduction, which in turn permits relatively large-bodied primates to successfully negotiate the canopy via clambering, bridging and suspension. What has gone almost entirely unrecognized until the recovery of Ar. ramidus, however, is that repositioning of the scapula (so as to make the glenoid face more laterally and less anteriorly) in hominoids was achieved by thoracic reorganization which relied on invagination of the post-cervical spine ventrally into the thorax. This resulted in dorsal repositioning of the lumbar transverse processes (LTPs), a change in bauplan that apparently occurred independently and repeatedly even in some early Miocene hominoid taxa (e.g. in Morotopithecus by 17 Ma; MacLatchy et al. 2000; Phil. Trans. R. Soc. B (2010)

C. O. Lovejoy & M. A. McCollum

3291

Filler 2007a,b), and was significantly progressing in a number of forms by the Mid-Miocene (e.g. in Pierolapithecus by at least 10 Ma; Moya-Sola et al. 2004; Almecija et al. 2009). This shift appears to have accompanied other forelimb modifications, especially ulnar withdrawal and olecranon abbreviation. These modifications increased potential wrist adduction, enhanced stability during complete elbow extension and greatly increased the forelimb’s range of motion at the shoulder girdle (Rose 1988; Lewis 1989). However, as this change in bauplan also resulted in the sacrifice of substantial erector spinae mass (Benton 1967; Lovejoy 2005a), increasing the range of motion of the shoulder came at the expense of dynamic stabilization of the lower back. Consequently, African ape suspension and vertical climbing required compensatory lumbar column reduction—virtually to the point of inherent (i.e. osteological) rather than dynamic (i.e. muscular) rigidity. Thus, LTP position, rather than being the primary target of selection during lumbar column shortening, as has long been argued (e.g. Benton 1967), was instead a product of the fundamental change in the hominoid bauplan that centred about a general restructuring of the thorax.

5. LOCOMOTION IN THE LCA Features assignable to the LCA, therefore, now point to a pattern of cautious climbing that combined above-branch palmigrady with occasional belowbranch suspension, enhanced by a highly mobile, lateralized shoulder girdle in combination with marked wrist adduction (Cartmill & Milton 1977; Lewis 1989) and elbow extension (Rose 1988). Belowbranch suspension, however, must not have been so frequently employed (and/or so vigorously performed) as to require emergence of the considerably more advanced metacarpal, carpal, elbow and shoulder modifications seen only extant African apes. This suggests that much of the LCA’s activities may have been largely low-canopy, and might have been combined, possibly extensively, with terrestrial travel between food patches (White et al. 2009). The latter supposition receives support from the fact that the adaptations to terrestrial travel present in extant African apes (knuckle-walking) and fossil hominids (bipedality) are extensive, fundamentally divergent, and therefore likely to be of substantial antiquity. It is also likely that reliance on terrestrial travel between food patches was driven by increasing competition with radiating OWMs in the Mid-Miocene (Andrews 1981). That the post-crania of Pongo and the lesser apes (Hylobates, Symphalangus) differ substantially from those of the African apes is probably largely due to the absence of a significant terrestrial component in their respective adaptive strategies, and their entirely independent evolution from much more primitive ancestors. If the above hypothesis is correct, what was the LCA’s terrestrial locomotor habitus prior to the emergence of either knuckle-walking in apes or bipedality in hominids? One possible pattern ‘of choice’ might have been a simple extension of its primary arboreal pattern

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3292

C. O. Lovejoy & M. A. McCollum

Spinopelvic pathways to bipedality

to ground travel, i.e. palmigrade quadrupedality. In fact, some of the more unusual characters present in Ar. ramidus are strongly suggestive that hominids once exhibited such an ancestral gait pattern. These include its primitive intermembral index, relatively short metacarpus, allowance of substantial metacarpal – phalangeal dorsiflexion and especially the strongly palmar positioning of the head of its capitate (Lovejoy et al. 2009b). Indeed, the latter can be viewed as being particularly advantageous to palmigrade terrestrial quadrupedality, and this would now seem to be a possible explanation for this unusual peculiarity in Ar. ramidus, i.e. it inherited it from a habitually terrestrial palmigrade LCA. Unlike OWMs, quadrupedal terrestrial gait in large-bodied hominoids (including the LCA) may have required a much more compliant wrist, i.e. palmigrady that included more extreme dorsiflexion. Absence of such extreme adaptations in OWMs is likely explicable by their retention of primary above-branch adaptations at the radiocarpal, elbow and shoulder joints. Palmar disposition of the capitate head as seen in Ar. ramidus (Lovejoy et al. 2009b) may even now serve, given further fossil evidence, as an indicator of palmigrade/plantigrade terrestrial quadrupedality in yet undiscovered, largebodied, Miocene forms. In combination with the retention of a long mid-tarsus, a robust os peroneal complex and other primitive aspects of its foot (retained M. quadratus plantae, retained M. plantaris and associated dense palmar fascial aponeurosis (see earlier)), palmigrade/plantigrade quadrupedality seems to have been, at the least, a likely terrestrial locomotor habitus in the African ape/hominid LCA (Lovejoy et al. 2009c).

6. LOCOMOTOR SPECIALIZATIONS IN EXTANT HOMINOIDS If so, from whence came the relatively highly specialized gait patterns of the LCA’s descendants: bipedality in hominids and knuckle-walking in the African apes? The latter is reasonably explicable in these taxa as a relatively facile means of modifying palmigrade/plantigrade terrestrial travel into a form that could be successfully combined with their highly specialized modifications of the pelvis, thorax and limb skeletons for suspension and vertical climbing. Such changes included (independently in each taxon) elongation of the forelimb, abbreviation of the hindlimb, elongation of the metacarpus, stabilization of several major carpal joints either by ligamentous reinforcement or joint enlargement or both (especially in the CJC), major revisions of overall scapular morphology (predominantly in Pan as opposed to Gorilla), cranial retroflexion of the ulnar trochlear notch, modification of the deltopectoral enthesis and especially, virtual fusion of the thorax and pelvis via abbreviation and iliac fixation of the lumbar column (see earlier) (Lovejoy et al. 2009c,d ). All of the modifications to the forelimb would have reduced its inherent stability and increasingly restricted its energy-dissipating capacity during prolonged terrestrial travel. These difficulties appear to have been Phil. Trans. R. Soc. B (2010)

resolved by adoption of knuckle-walking, which permits reliance on substrate-forced dorsiflexion of the wrist that can be eccentrically resisted by powerful wrist flexors as well as both the connective tissue envelopes and contractile components of the long digital flexors. The uniqueness of these long flexors is evidenced by development of a distinctive flexor tubercle on the proximal ulna in both Pan and Gorilla (Lovejoy et al. 2009b). The most salient question remaining, of course, is the issue of the eventual adoption of bipedality in hominids. Why did hominids exchange palmigrade/ plantigrade quadrupedality for upright walking? While there have been many theories advanced for this locomotor shift, most have been made untenable by evidence now provided by Ar. ramidus (White et al. 2009). The recent suggestion that bipedality is a sequel to an arboreal upright stance stabilized by overhead forelimb grasping (Thorpe et al. 2007a,b, 2009) is untenable because the practice has emerged in Pongo as a consequence of that taxon’s extreme adaptations to suspension, none of which were ever present in hominids or their ancestors (Lovejoy et al. 2009c). The most likely explanation for the adoption of terrestrial bipedality, in our view, continues to involve novel adaptations in hominid social structure that required upright locomotion for carrying. These have been discussed extensively elsewhere (Lovejoy 1981, 1993, 2009).

7. SOME ADDITIONAL ANATOMICAL CORRELATES OF BIPEDALITY IN HOMINIDS AND ADVANCED ARBOREALITY IN EXTANT APES As noted above, still equipped with a mobile lumbar spine, the LCA was probably capable of at least facultative lordosis, sufficient to place its hip and knee either directly below its centre of mass or sufficiently close to that centre so as not to generate excessive ground-reactive torques so large as to require debilitating muscle recruitment during terrestrial travel. While the earliest hominid gait pattern probably required some degree of hip and knee flexion, research on bipedality in OWMs now suggests that it would not have been nearly as excessive as it is in extant apes, so long as the lumbar column remained long and mobile (as it is in OWMs). Studies of OWMs have now greatly illuminated our understanding of its origins in hominids (Nakatsukasa et al. 1995, 2004, 2006; Hirasaki et al. 2004). Macaques trained to walk bipedally expend less energy than do those in which the behaviour is novel, so much so that the animal’s long flexible spine is permissive for convergence with ‘human-style’ walking in the former. While those using bipedality ‘in the wild’ exhibit upright gaits that differ kinesiologically from human walking, those exposed to long-term training for bipedality walk ‘with longer, less-frequent strides, more extended hindlimb joints, double-phase joint motion at the knee joint, and most importantly, efficient energy transformation by using inverted pendulum mechanics’ (Hirasaki et al. 2004: 748). While lordosis was certainly facilitated by the presence of six to seven lumbar vertebrae in the LCA

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

4.25

4.25

4.00

4.00

3.75

3.50

Homo Pan Gorilla A.L. 288-1 BSN49/P27 KSD-VP-1/1 STS-14 human mean

3.25

3.00 4.20

4.50 4.80 log total sacral breadth

Figure 2. Components of sacral breadth in African apes and early hominids. Scatter plot of log total sacral breadth versus log alar breadth. The findings of a strong correlation (r ¼ 0.901) between sacral breadth and alar breadth, and an absence of any significant correlation between alar breadth and centrum area (figure 3) indicate that total sacral breadth in African apes and early hominids is largely a consequence of alar breadth. Note especially the exceedingly broad alae in the early hominid specimens. This is consistent with their having mediolaterally expanded the sacrum as an adaptation to free the most caudal lumbar from contact with the iliac crest, and fully accounts for the unusual platypelloidy in A.L.288-1 and Sts-14. Later, a caudally directed gradient of increasing centrum size and interfacet distance (see text) appears in Homo, and probably accounts for the unusually large human centrum. Note the much narrower alae in the two African apes compared with those of all hominids.

(most probably six; figure 1), even in most OWMs lordosis is not as complete as it is in five-lumbared humans (Nakatsukasa et al. 1995; Hirasaki et al. 2004). One probable and very important reason is that complementary motion in the most caudal lumbar vertebra in OWMs is usually restricted by its proximity to the posterosuperior portion of each iliac blade. Such iliac– lumbar propinquity is usually sufficient to probably assure at least some degree of ligamentous restriction of potential motion. Two characters that are uniquely associated with hominid pelvic adaptations to bipedality are therefore of particular interest: (i) an exceptionally short superoinferior iliac height (coupled with both anterior extension of the anterior inferior iliac spine (AIIS) and development of the greater sciatic notch) and (ii) an extremely wide sacrum generated largely by exceptionally broad sacral alae (figures 2 and 3). Both of these characters eliminate contact between the posteromost iliac crest and the most caudal lumbar vertebra, and are therefore likely to have appeared early in hominids as a means of increasing the lordotic capacity of the lumbar spine during terrestrial bipedality. Indeed, these changes are likely to have been the earliest in the evolution of bipedality in hominids, Phil. Trans. R. Soc. B (2010)

log alar breadth

log alar breadth

Spinopelvic pathways to bipedality

C. O. Lovejoy & M. A. McCollum

3293

3.75

3.50

Homo Pan Gorilla A.L. 288-1 BSN49/P27 KSD-VP-1/1 STS-14 human mean

3.25

3.00 6.00

6.25 6.50 6.75 7.00 7.25 7.50 7.75 log centrum area

Figure 3. Components of sacral breadth in African apes and early hominids. Scatter plot of log centrum area (length breadth) versus log alar breadth. For discussion, see legend of figure 2.

and largely exaptive for increased abductor capacity during the single-support phase of upright walking (Lovejoy et al. 2009c). Moreover, three features of ape sacra appear to have directly opposite polarity compared with those of hominids (figures 2– 4): (i) their strongly abbreviated sacral alae, (ii) their reduced lumbar number, and (iii) their greater number of fused sacral elements, the latter almost certainly achieved by progressive sacralization of the most caudal lumbar element(s) (McCollum et al. 2009). Alar reduction reduces the space between the two ilia so as to promote contact with the most caudal lumbar vertebra(e). In combination with the additional extension of the ilia superiorly (especially by elongation of the iliac isthmus at least in Pan; Lovejoy et al. 2009c), the African apes achieved stabilization of the entire lower spine by its fixation to the thorax—creating a rigid pelvothoracic ‘block’ in which the pelvis and thorax are separated by a distance of only a single intercostal space (Schultz 1961). Both mechanisms compensate for the loss of erector spinae mass (see earlier). Thus, both sacral structure and superoinferior iliac length directly reflect hominoid post-cranial natural history. Panids and gorillids independently elongated their ilia, narrowed their bi-iliac spaces and reduced the number of lumbar vertebrae (often by sequestration as additional sacral segments), all mechanisms that stiffened the lower back and eliminated any possibility of lordosis. Hominids, per contra, remained almost entirely plesiomorphic, retaining both the primitive number of lumbar (mode ¼ six) and sacral vertebrae (mode ¼ four), and in addition, expanded the sacral alae so as to assure the full independence of the most caudal lumbar, assuring its freedom to participate in lordosis as well.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3294

C. O. Lovejoy & M. A. McCollum

Spinopelvic pathways to bipedality

2 2

3

3 1

1

Figure 4. Hominid and pongid mechanisms of emancipation or fixation of the most caudal lumbar(s). A human pelvis (left) compared with that of a chimpanzee (right). Note the following numbered characters in each. The iliac isthmus (1) and the ilium itself (3) have both been greatly shortened in the human, so much so that a greater sciatic notch has been created (entirely absent in the chimpanzee), and there is no potential contact between the iliac crest and the most caudal lumbar. In the chimpanzee, the opposite change has occurred, i.e. the iliac isthmus (1) and the iliac blade (3) have both been superoinferiorly elongated, encouraging such contact. In addition, the sacral alae have been greatly broadened in the human and narrowed in the chimpanzee (cf. figure 2). As a consequence, there is now a very substantial horizontal distance between the iliac crest and the most caudal vertebra in the human (2), but a greatly narrowed bi-iliac gulf in the chimpanzee. In combination with (1) and (3), such narrowing in the chimpanzee (via reduced alar breadth; cf. figure 2) results in full restrictive contact between the iliac crest and the most caudal lumbar vertebra(e). In the earliest phases of this morphological shift in hominids, the pelvis became decidedly platypelloid, and the enhanced iliac breadth encouraged a more effective use of the anterior gluteal muscles as abductors during upright gait (Lovejoy 2005a; Lovejoy et al. 2009d ). The latter was thus an exaptation, rather than the primary adaptation.

8. THE QUESTION OF OREOPITHECUS Delineation of the vertebral evolutionary pattern of African apes and hominids throws considerable new light on the troublesome issue of both the locomotor pattern and phylogeny of perhaps the most enigmatic hominoid of the later Miocene, Oreopithecus. Arguments as to its potential phylogenetic relationships and locomotor patterns have been many (reviewed in Harrison 1986, 1991; Kohler & MoyaSola 1997; Rook et al. 1999). However, all have been hampered by its extremely poor condition, largely the consequence of its extreme compression during fossilization. This has frequently led to excessively liberal interpretations of its badly compromised structure. A case in point is the attribution of a lordotic spine to this taxon based on a sagittal section of specimen BA72, a crushed and compressed amalgam of three lumbar vertebrae (Kohler & Moya-Sola 1997). It seems inconceivable to us that such sectioning can reliably indicate the presence/absence of wedging in centra after they have been compressed to less than one half of their dorsoventral diameter. A far more conservative approach is to rely on more Phil. Trans. R. Soc. B (2010)

straightforward morphological characters of greater inherent reliability, and which are more resistant to misinterpretation from crushing defects. Not all of these appear to have been considered. One of the most important is the vertebral formula of Oreopithecus. There is general agreement, based on the ‘1958 specimen’ (IGF 11 778), that Oreopithecus had five lumbar vertebrae (Harrison 1986, 1991; Kohler & Moya-Sola 1997; Rook et al. 1999). A largely overlooked vital statistic, however, is that it also had six sacral vertebrae (Straus 1963; method of Schultz 1961; for details, see McCollum et al. 2009). This can be safely concluded from specimen BA-50, which preserves five sacral foramina on the left side, and at least four on the right. Moreover, the masses of the right and left halves of the sixth sacral vertebra appear to be fully symmetrical (therefore the right side presumably had five full foramina as well). We have demonstrated elsewhere that the basal hominoid column almost certainly exhibited 13 thoracics (among living taxa, only Homo and Pongo have any significant incidences of fewer). Thus, the minimum pre-coccygeal vertebral number in Oreopithecus was 31, which, as noted above, is the likely pre-coccygeal vertebral number for basal hominoids and was probably modal for Early and Mid-Miocene apes as well. Except for P. paniscus, a modal vertebral number as high as 31 is extremely rare in extant species, occurring in only 2.8 per cent of P. troglodytes and 0.06 per cent of Homo (McCollum et al. 2009). Much has been made of the putative ‘short, broad, ilium’ of Oreopithecus and of its relatively broad retroauricular segment (Hu¨rzeler 1958). However, a substantial reduction in the size of the postauricular region of the pelvis appears to have accompanied the spinal invagination underlying scapular relocation in all hominoids (see earlier). That reduction was in turn accompanied by a broadening of the pre-auricular portion of the pelvis and is therefore expected in any clade in which shoulder reorganization occurred (Lovejoy et al. 2009c). This same developmental process is likely to have reoccurred a number of times in hominoid evolution, and is almost certainly universally responsible for the dorsal migration of the LTPs. Broadening of the ilium well beyond comparable dimensions in Proconsul is therefore fully expected in virtually any large-bodied Miocene hominoid that exhibits posterolateralization of the shoulder. The fifth lumbar vertebra of the ‘1958 specimen’ lies (in situ) directly within its bi-iliac space, sharing the same functional position as the trapped (immobilized) L7 of a typical Presbytis and the L3 or L4 of Pan (see Straus 1963; figure 5). Therefore, Oreopithecus exhibits a maximum of only four potentially mobile lumbar vertebrae. This is fully consistent with its ‘classic’ adaptive regimen for suspension as also seen in Gorilla, Pan and Pongo, and with directly opposite polarity compared with their homologues in bipedal hominids in a host of major adaptive characters (table 1). These included transformation of lumbars via their sacralization, direct reduction in lumbar number from the primitive condition and entrapment (immobilization) of at least one lumbar

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Spinopelvic pathways to bipedality

(a)

(b)

C. O. Lovejoy & M. A. McCollum

3295

(c)

Figure 5. (a) Sacra of a chimpanzee, (b) A.L. 288-1 and (c) a modern human. Note the extremely narrow sacrum of the chimpanzee compared with the two hominids. Note also the much broader alae in A.L. 288-1 compared with its centrum. Compare this with the similar dimensions in the human specimen (figure 2).

(a)

(b)

(c)

(d)

1 2

Figure 6. Comparison of interfacet distances in the third lumbars and sacra of African apes and hominids. The drawing on the left demonstrates the comparison being made. In this drawing, the third lumbar has been rotated 1808 from its normal anatomical position (its superior zygapophyses now point inferiorly) for comparison with those of the sacrum. Double-headed arrows indicate the interfacet distance in each specimen. (a) chimpanzee; (b) gorilla; (c) A.L. 288-1 and (d ) human. Note that in (a) and (b) the interfacet distance is greater in the lumbar vertebra than it is in the sacrum, whereas the opposite is true of the two hominids. The increasing gradient of centrum size and interfacet distance in Homo may be an adaptation that facilitated increased lordosis and thereby enabled lumbar column reduction. The opposite gradient in chimpanzees is the likely source of reduction of the bi-iliac space. For discussion, see text. Redrawn from Lovejoy (2005a).

by contact with a posterodorsally extended iliac crest. Given its primitive vertebral number, and a series of others, such as its retention of an anterior keel on its lumbar vertebrae (Straus 1963), Oreopithecus appears to have acquired extensive adaptations to suspension entirely independently of other Miocene clades (as did Nacholapithecus; Nakatsukasa et al. 2007). It is thereby unrelated to hominids, its similarities (which are few; table 1) being largely minor convergences. Any bipedality would have been largely driven by the same context that does so in hylobatids—excessively long forelimbs combined with highly abbreviated hindlimbs (table 1). Phil. Trans. R. Soc. B (2010)

One additional supposedly hominid character in Oreopithecus is worthy of brief note. The degree of protuberance of its AIIS is not unusual for a non-hominid. What distinguishes the AIIS in hominids from those in apes is not its protuberance (those of Gorilla are often very prominent), but rather its emergence from a novel, separate physis, a hominid adaptation that is almost certainly associated with dramatic expansion of iliac isthmus breadth (Lovejoy et al. 2009b). There is no evidence of a similar degree of broadening in Oreopithecus (note its relative pelvic breadth in table 1) and certainly none suggesting its origin by means of a separate physis.

Phil. Trans. R. Soc. B (2010)

5 –6 3 –4 5 6 –7

5 5 –6 4 –5 [4]

5 2 –3 4 6

4e 2 –3 2–3 2 –3 [6] [6] 6 135 192 278 (131 –134)

170e 160 159g 152 [131– 143] 143 145

forelimb length/ body mass(0.33)b

65–79 138 130 87

119 106 101g 114 [87–91] 89–91 84

intermembral indexb

125 74 49 50

92 ? 113 137

80 66

iliac width/length index (relative iliac breadth)c

c

b

Method of Schultz (1961). Data from sample described in Lovejoy et al. (2009c) or additional sources therein unless otherwise noted. Data from Straus (1963), except for Proconsul, Ar. ramidus and Au. afarensis, which were obtained from casts. d Data for Oreopithecus from Susman (2004). e Oreopithecus data from Straus (1963) and examination of BA-50; other data from Pilbeam (2004) and McCollum et al. (2009). f See Kohler & Moya-Sola (1997). g Data from Morbeck & Zihlman (1989). h Data in brackets hypothesized for LCA of African apes and humans and/or Proconsul based on Ar. ramidus and living hominoids.

5e 3 –4 4 3 –4 [6] [6] 6

6e 5 –6 6–7 5 –6 [4] [4] 4

no. of functional lumbars

65 147 145 88

120 111 107g 113 [88 –95] 95 93

radius/ tibia indexb

71 130 116 77

117 101 108g 116 [77 –87] 87 84

humerus/ femur indexb

very long very short short [long]

very shortf short short short [long] long ?

medial cuboid lengthb

15.8 27.6 34.1 ?

18.9 ? ? ?

20.5 24.7

third Mc length/ body mass(0.33)b,d

C. O. Lovejoy & M. A. McCollum

a

Oreopithecus P. troglodytes P. paniscus Gorilla LCAh Ar. ramidus Au. afarensis H. sapiens Pongo Hylobates Proconsul

taxon

no. of lumbar vertebra

3296

no. of sacral vertebraa

Table 1. Principal characters of Oreopithecus compared with those of other hominoids.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Spinopelvic pathways to bipedality

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Spinopelvic pathways to bipedality 9. A NOTE ON POTENTIAL MECHANISMS IN LUMBAR COLUMN MODIFICATION In considering the anatomy of the lumbosacral spine, it is of some interest that whereas in humans both the overall size of the centrum and the distances separating the articular facets (zygapophyses) increase in each successively more caudal lumbar vertebrae, centrum size and interfacet distances in extant African apes instead decrease caudally (Latimer & Ward 1993; figure 6). Lumbar centrum dimensions do not appear to differ substantially in the only column that permits their observation in Australopithecus (Sts-14; Robinson 1972). There is, however, an increase in the interfacet distance between the putative L3 and sacrum of A.L. 288-1 (Lovejoy 2005a). The latter findings suggest that the progressive caudal expansion of both the interfacet distances and centrum dimensions evident in Homo, but only partially adumbrated in Australopithecus (i.e. no increase in lumbar centrum dimensions, a retention of six lumbar vertebrae, but a partial increase in interfacet distance), may be an adaptation that permits a more intense lordosis in humans, ultimately enhancing lumbar column stability by allowing a reduction in total lumbar number. If so, emergence of this gradient must have postdated Homo erectus at 1.6 ma, since the lumbar column in KNM-WT-15000 still numbers six with four sacral vertebrae (Latimer & Ward 1993; Pilbeam 2004; McCollum et al. 2009).

10. SUMMARY AND CONCLUSIONS New evidence from the fossil record and from observations of extant hominoid skeletal anatomy leads to several conclusions. Among the most important is that hominids never acquired the numerous specializations seen in extant apes for vertical climbing, suspension or knuckle-walking. This demonstrable divergence between the natural histories of hominids and those of all living apes renders most observations of locomotor behaviour in the latter, whether conducted in the laboratory or observed in the wild, no longer directly relevant to the reconstruction of the earliest locomotion of hominids. Bipedality in hominids can instead now be seen to have emerged from a predominantly primitive locomotor skeleton with a long lumbar spine capable of at least partial lordosis, and one never restrictively modified for suspension, vertical climbing or knuckle-walking. Suspension (e.g. Pongo, Hylobates) and vertical climbing (e.g. extant African apes) have repeatedly induced a rigid lower spine, especially as body mass increased. This has been accomplished in a variety of taxa in several ways, but always by a combination of reduction in lumbar number (by reduction in somite vertebral number and/or transformation of lumbar identity) via modification of hox regulation and further entrapment of a portion of the remaining lumbar vertebrae by narrowing of the bi-iliac space. The latter has been accomplished either by sacral narrowing or dorsal extension of the iliac crest (e.g. Pan and Gorilla), or both. The failure of hylobatids (but not symphalangids (i.e. modal lumbar number ¼ 4) to achieve the extreme lumbar column reductions seen Phil. Trans. R. Soc. B (2010)

C. O. Lovejoy & M. A. McCollum

3297

in African apes is probably a product of their modest body size and the unique nature of suspension in these lesser apes. The earliest hominids were able to functionally achieve bipedality because they had never rigidified their lumbar spines. Instead, they evolved an opposite morphology—a reduction in iliac height and a broadening of the sacrum, both of which assured sufficient lordosis to reduce and eventually eliminate what were probably only moderate vertical moments about the knee and hip. Were hominids to have first engaged in African ape-like behaviours, the ‘Rubicon’ to bipedality may have become too great to cross. Our decades-long assumption that the abducent capacity of the early hominid pelvis was its primary selective agent (e.g. Lovejoy et al. 1973) was, in retrospect, entirely misdirected. The favourable position of the anterior gluteal muscles in hominids that allows them to control pelvic tilt during single support can now be seen to have been largely a refinement that followed the initial primary adoption of a lordotic spine with an emancipated caudal-most lumbar vertebra. The generalized structure of earliest hominids that permitted this sequence of events is almost certainly extendable to the LCA. At least initially in pre-divergence hominoids, it now suggests a combination of cautious, palmigrade, plantigrade climbing with a long flexible back during arboreal travel, and possibly, palmigrade quadrupedality during terrestrial travel as well. We thank Alan Walker and Chris Stringer for organizing the discussion meeting and the staff of the Royal Society for ensuring its success. We thank David Pilbeam for extensive help in constructing the bonobo sample used in this paper. We thank Wim Wendelen and the staff and administration of the Royal Museum for Central Africa, Tervuren, Belgium for access to the primate collections in their care and for the valuable assistance during our examination of their specimens, and Yohannes Haile-Selassie and Lyman Jellema for aid with examination of specimens housed at the Cleveland Museum of Natural History.

REFERENCES Almecija, S., Alba, D. M. & Moya-Sola, S. 2009 Pierolapithecus and the functional morphology of Miocene ape hand phalanges: paleobiological and evolutionary implications. J. Hum. Evol. 57, 284 –297. (doi:10.1016/j.jhevol.2009. 02.008) Andrews, P. 1981 Species diversity and diet in monkeys and apes during the Miocene. In Aspects of human evolution (ed. C. Stringer), pp. 25–61. London, UK: Taylor and Francis. Benton, R. S. 1967 Morphological evidence for adaptations within the epaxial region of the primates. In The baboon in medical research: Vol. II (ed. F. van der Hoeven), pp. 201 – 216. Austin, TX: University of Texas Press. Carey, T. S. & Crompton, R. 2005 The metabolic costs of bent-hip, bent-knee walking in humans. J. Hum. Evol. 48, 25–44. (doi:10.1016/j.jhevol.2004.10.001) Cartmill, M. 1985 Climbing. Functional vertebrate morphology (eds M. Hildebrand, D. M. Bramble, K. F. Liem & D. B. Wake), pp. 73–88. Cambridge, MA: Belknap Press. Cartmill, M. & Milton, K. 1977 The lorisiform wrist joint and the evolution of ‘brachiating’ adaptations in the Hominoidea. Am. J. Phys. Anthropol. 47, 249– 272. (doi:10.1002/ajpa.1330470206)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3298

C. O. Lovejoy & M. A. McCollum

Spinopelvic pathways to bipedality

Crompton, R. H., Li, Y., Wang, W., Gu¨nther, M. M. & Savage, R. 1998 The mechanical effectiveness of erect and ‘bent-hip, bent-knee’ bipedal walking in Australopithecus afarensis. J. Hum. Evol. 35, 55–74. (doi:10.1006/jhev.1998.0222) Desilva, J. M. 2009 Functional morphology of the ankle and the likelihood of climbing in early hominins. Proc. Natl Acad. Sci. USA 106, 6567–6572. (doi:10.1073/pnas. 0900270106) Erikson, G. E. 1963 Brachiation in New World monkeys and in anthropoid apes. Symp. Zool. Soc. Lond. 10, 135 –164. Filler, A. G. 1981 Anatomical specializations in the hominoid lumbar region. Am. J. Phys. Anthropol. 54, 218. Filler, A. G. 2007a Homeotic evolution in the mammalia: diversification of therian axial seriation and the morphogenetic basis of human origins. PLoS ONE 2, e1019. (doi:10.1371/journal.pone.0001019) Filler, A. G. 2007b Emergence and optimization of upright posture among hominiform hominoids and the evolutionary pathophysiology of back pain. Neurosurg. Focus 23, E4. Harrison, T. 1991 The implications of Oreopithecus bambolii for the origins of bipedalism. In Origine(s) de la bipedie chez les hominides, Cahiers de Pale´oanthropologie (eds Y. Coppens & B. Senut), pp. 235 –244. Paris, France: Editions du CNRS. Harrison, T. 1986 A reassessment of the phylogenetic relationships of Oreopithecus bambolii gervais. J. Hum. Evol. 15, 541–583. (doi:10.1016/S0047-2484(86)80073-2) Hirasaki, E., Ogihara, N., Hamada, Y., Kumakura, H. & Nakatsukasa, M. 2004 Do highly trained monkeys walk like humans? A kinematic study of bipedal locomotion in bipedally trained Japanese macaques. J. Hum. Evol. 46, 739 –750. (doi:10.1016/j.jhevol.2004.04.004) Hu¨rzeler, J. 1958 Oreopithecus bambolii Gervais, a preliminary report. Verh. Naturforsch. Ges. 69, 1 –48. Johanson, D. C., Lovejoy, C. O., Kimbel, W. H., White, T. D., Ward, S. C., Bush, M. E., Latimer, B. M. & Coppens, Y. 1982 Morphology of the Pliocene partial hominid skeleton (A.L. 288-1) from the Hadar Formation, Ethiopia. Am. J. Phys. Anthropol. 57, 403 –452. (doi:10.1002/ajpa.1330570403) Kohler, M. & Moya-Sola, S. 1997 Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. Proc. Natl Acad. Sci. USA 94, 11 747 –11 750. (doi:10.1073/pnas.94.21.11747) Latimer, B. & Lovejoy, C. O. 1989 The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality. Am. J. Phys. Anthropol. 78, 369–386. (doi:10. 1002/ajpa.1330780306) Latimer, B. & Ward, C. V. 1993 The thoracic and lumbar vertebrae. In The Nariokotome Homo erectus skeleton (eds A. Walker & R. Leakey), pp. 266 –293. Cambridge, MA: Harvard University Press. Lewis, O. J. 1989 Functional morphology of the evolving hand and foot. Oxford, UK: Clarendon Press. Lovejoy, C. O. 1981 The origin of man. Science 211, 341 –350. (doi:10.1126/science.211.4480.341) Lovejoy, C. O. 1993 Are we sexy because we’re smart or smart because we’re sexy? In The origin and evolution of humans and humanness (ed. D. T. Rasmussen), pp. 1–28. New York, NY: Jones and Bartlett. Lovejoy, C. O. 2005a The natural history of human gait and posture I: spine and pelvis. Gait Posture 21, 113–128. Lovejoy, C. O. 2005b The natural history of human gait and posture II: hip and thigh. Gait Posture 21, 129 –151. Lovejoy, C. O. 2007 The natural history of human gait and posture III: knee. Gait Posture 25, 325 –341. (doi:10. 1016/j.gaitpost.2006.05.001) Lovejoy, C. O. 2009 Reexamining human origins in the light of Ardipithecus ramidus. Science 326, 74e1–74e8. (doi:10. 1126/science.1175834) Phil. Trans. R. Soc. B (2010)

Lovejoy, C. O., Heiple, K. G. & Burstein, A. H. 1973 The gait of Australopithecus. Am. J. Phys. Anthropol. 38, 757 –779. (doi:10.1002/ajpa.1330380315) Lovejoy, C. O., Latimer, B., Suwa, G., Asfaw, B. & White, T. D. 2009a Combining prehension and propulsion: the foot of Ardipithecus ramidus. Science 326, 72e1– 72e8. Lovejoy, C. O., Simpson, S. W., White, T. D., Asfaw, B. & Suwa, G. 2009b Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326, 70e1–70e8. Lovejoy, C. O., Suwa, G., Simpson, S. W., Matternes, J. H. & White, T. D. 2009c The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326, 100–106. Lovejoy, C. O., Suwa, G., Spurlock, L., Asfaw, B. & White, T. D. 2009d The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science 326, 71e1–71e6. MacLatchy, L., Gebo, D., Kityo, R. & Pilbeam, D. 2000 Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion. J. Hum. Evol. 39, 159 –183. (doi:10. 1006/jhev.2000.0407) McCollum, M. A., Rosenman, B. A., Suwa, G., Meindl, R. S. & Lovejoy, C. O. 2009 The vertebral formula of the last common ancestor of African apes and humans. J. Exp. Zool. B Mol. Dev. Evol. 314B, 123–134. Morbeck, M. E. & Zihlman, A. L. 1989 Body size and proportions in chimpanzees, with special reference to Pan troglodytes schweinfurthii from Gombe National Park, Tanzania. Primates 30, 369 –382. (doi:10.1007/BF02381260) Moya-Sola, S., Kohler, M., Alba, D. M., Casanovas-Vilar, I. & Galindo, J. 2004 Pierolapithecus catalaunicus, a new Middle Miocene great ape from Spain. Science 306, 1339–1344. (doi:10.1126/science.1103094) Nakatsukasa, M. 2004 Acquisition of bipedalism: the Miocene hominoid record and modern analogues for bipedal protohominids. J. Anat. 204, 385 –402. (doi:10. 1111/j.0021-8782.2004.00290.x) Nakatsukasa, M., Hayama, S. & Preuschoft, H. 1995 Postcranial skeleton of a macaque trained for bipedal standing and walking and implications for functional adaptation. Folia Primatol. (Basel) 64, 1 –29. (doi:10. 1159/000156828) Nakatsukasa, M., Tsujikawa, H., Shimizu, D., Takano, T., Kunimatsu, Y., Nakano, Y. & Ishida, H. 2003 Definitive evidence for tail loss in Nacholapithecus, an East African Miocene hominoid. J. Hum. Evol. 45, 179 –186. (doi:10.1016/S0047-2484(03)00092-7) Nakatsukasa, M., Ogihara, N., Hamada, Y., Goto, Y., Yamada, M., Hirakawa, T. & Hirasaki, E. 2004 Energetic costs of bipedal and quadrupedal walking in Japanese macaques. Am. J. Phys. Anthropol. 124, 248–256. (doi:10.1002/ajpa.10352) Nakatsukasa, M., Hirasaki, E. & Ogihara, N. 2006 Energy expenditure of bipedal walking is higher than that of quadrupedal walking in Japanese macaques. Am. J. Phys. Anthropol. 131, 33–37. (doi:10.1002/ajpa.20403) Nakatsukasa, M., Kunimatsu, Y., Nakano, Y. & Ishida, H. 2007 Vertebral morphology of Nacholapithecus kerioi based on KNM-BG 35250. J. Hum. Evol. 52, 347–369. (doi:10.1016/j.jhevol.2006.08.008) Pilbeam, D. 2004 The anthropoid postcranial axial skeleton: comments on development, variation, and evolution. J. Exp. Zoolog. B Mol. Dev. Evol. 302, 241 –267. Robinson, J. T. 1972 Early hominid posture and locomotion. Chicago, IL: University of Chicago Press. Rook, L., Bondioli, L., Kohler, M., Moya-Sola, S. & Macchiarelli, R. 1999 Oreopithecus was a bipedal ape after all: evidence from the iliac cancellous architecture.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Spinopelvic pathways to bipedality Proc. Natl Acad. Sci. USA 96, 8795–8799. (doi:10.1073/ pnas.96.15.8795) Rose, M. 1988 Another look at the anthropoid elbow. J. Hum. Evol. 17, 193–224. (doi:10.1016/0047-2484(88)90054-1) Sanders, W. J. 1995 Function, allometry and evolution of the australopithecine lower precaudal spine. New York, NY: New York University. Schultz, A. H. 1961 Vertebral column and thorax. Primatologia 4, 1–66. Sellers, W., Cain, G., Wang, W. & Cromton, R. H. 2005 Stride lengths, speed and energy costs in walking of Australopithecus afarensis: using evolutionary robotics to predict locomotion of early human ancestors. J. R. Soc. Interface 2, 431– 441. (doi:10.1098/rsif.2005.0060) Stern Jr, J. T. 2000 Climbing to the top: a personal memoir of Australopithecus afarensis. Evol. Anthropol. 9, 113–133. (doi:10.1002/1520-6505(2000)9:3,113::AIDEVAN2.3.0.CO;2-W) Stern Jr, J. T. & Susman, R. L. 1983 The locomotor anatomy of Australopithecus afarensis. Am. J. Phys. Anthropol. 60, 279 –317. Stevens, L. S. 2004 Morphological varition in the hominoid vertebral column. PhD thesis, Kent State University, Kent, OH. Stevens, L. S. & Lovejoy, C. O. 2004 Morphological variation in the hominoid vertebral column: implications for the evolution of human locomotion. Am. J. Phys. Anthropol. 123 S38, 187 –188. Strauss Jr, W. L. 1963 The classification of Oreopithecus. In Classification and human evolution (ed. S. L. Washburn), pp. 146 –177. Chicago, IL: Aldine. Susman, R. L. 2004 Oreopithecus bambolii an unlikely case of hominidlike grip capability in a Miocene. J. Hum. Evol. 46, 105– 117. (doi:10.1016/j.jhevol.2003.10.002) Susman, R. L., Stern Jr, J. T. & Jungers, W. L. 1984 Arboreality and bipedality in the Hadar hominids. Folia Primatol. (Basel) 43, 113–156. (doi:10.1159/000156176)

Phil. Trans. R. Soc. B (2010)

C. O. Lovejoy & M. A. McCollum

3299

Thorpe, S. K., Crompton, R. H. & Alexander, R. M. 2007a Orangutans use compliant branches to lower the energetic cost of locomotion. Biol. Lett. 3, 253 –256. (doi:10.1098/rsbl.2007.0049) Thorpe, S. K., Holder, R. L. & Crompton, R. H. 2007b Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316, 1328–1331. (doi:10.1126/science.1140799) Thorpe, S. K., Holder, R. & Crompton, R. H. 2009 Orangutans employ unique strategies to control branch flexibility. Proc. Natl Acad. Sci. USA 106, 12 646–12 651. (doi:10. 1073/pnas.0811537106) Ward, C. V. 1991 Functional anatomy of the lower back and pelvis of the Miocene hominoid Proconsul nyanze from Mfangano Island, Kenya, pp. 1– 379. Baltimore, MD: Johns Hopkins University. Ward, C. V. 1993 Torso morphology and locomotion in Proconsul nyanzae. Am. J. Phys. Anthropol. 92, 291 –328. (doi:10.1002/ajpa.1330920306) Ward, C. V. 2007 Postcranial and locomotor adaptations of hominoids. In Handbook of paleoanthropology (eds W. Henke & I. Tattersall), pp. 1011–1030. Heidelberg, Germany: Springer. Ward, C. V., Walker, A. & Teaford, M. 1991 Proconsul did not have a tail. J. Hum. Evol. 21, 215–220. (doi:10. 1016/0047-2484(91)90062-Z) Ward, C. V., Walker, A., Teaford, M. F. & Odhiambo, I. 1993 Partial skeleton of Proconsul nyanzae from Mfangano Island, Kenya. Am. J. Phys. Anthropol. 90, 77–112. (doi:10.1002/ajpa.1330900106) Waterman, H. C. 1929 Studies on the evolution of the pelves of man and other primates. Am. Mus. Nat. Hist. Bull. 58, 585–642. White, T. D., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, C. O., Suwa, G. & WoldeGabriel, G. 2009 Ardipithecus ramidus and the paleobiology of early hominids. Science 326, 75– 86.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3301–3314 doi:10.1098/rstb.2010.0035

Review

Arboreality, terrestriality and bipedalism Robin Huw Crompton1,*,†, William I. Sellers2,† and Susannah K. S. Thorpe3,† 1

Primate Evolution and Morphology Research Group, School of Biomedical Sciences, The University of Liverpool, Sherrington Buildings, Ashton Street, Liverpool L69 3GE, UK 2 Faculty of Life Sciences, The University of Manchester, 3.614 Stopford Building, Oxford Road, Manchester M13 9PT, UK 3 School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

The full publication of Ardipithecus ramidus has particular importance for the origins of hominin bipedality, and strengthens the growing case for an arboreal origin. Palaeontological techniques however inevitably concentrate on details of fragmentary postcranial bones and can benefit from a whole-animal perspective. This can be provided by field studies of locomotor behaviour, which provide a real-world perspective of adaptive context, against which conclusions drawn from palaeontology and comparative osteology may be assessed and honed. Increasingly sophisticated dynamic modelling techniques, validated against experimental data for living animals, offer a different perspective where evolutionary and virtual ablation experiments, impossible for living mammals, may be run in silico, and these can analyse not only the interactions and behaviour of rigid segments but increasingly the effects of compliance, which are of crucial importance in guiding the evolution of an arboreally derived lineage. Keywords: bipedalism; biomechanics; evolution; field studies

1. INTRODUCTION Darwin’s (1871) argument on human origins has never appeared stronger than now, when molecular evidence suggests a divergence time of only 5– 8 Ma for humans and their extinct relatives (the tribe Hominini), from the chimpanzees and bonobos (tribe Panini; Bradley 2008). But as pointed out by Tuttle et al. (1974) in their excellent review, Darwin, while he did not present a detailed model of the last common ancestor of humans and other African apes, made an important point that is too often ignored: that we should not expect the last common ancestor to resemble either living humans or other living apes particularly closely. 2. BIPEDALISM: AN ARBOREAL OR TERRESTRIAL ORIGIN? In the first four decades of the twentieth century, it was generally accepted that bipedalism had an arboreal origin (e.g. Keith 1903, 1923; Morton 1922; Schultz 1936). But for the last 60 years, since the first field study of mountain gorillas by Schaller (1963), the field studies of chimpanzees by Goodall (1998), and the ensuing recognition (e.g. Zihlman et al. 1978) of a special and genetically very close relationship between the hominins (humans and their ancestors) * Author for correspondence ([email protected]). † All authors contributed equally to this manuscript. One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

and the panins (bonobos and common chimpanzees), the prevailing paradigm for the origins of human bipedalism has been the knucklewalking quadrupedalism model (first proposed by Washburn (1967) and reviewed by Tuttle et al. (1974)). This model holds that the common ancestor of hominins and panins would have looked much like chimpanzees do today, and so bipedalism would have arisen in an ancestor which was a terrestrial, quadrupedal knucklewalker, like the panins, and the remaining African apes, the gorillines. This paradigm was developed in some detail by Gebo (1992, 1996), who identified heel-strike plantigrady as a common, shared-acquired character of African apes linked closely to knucklewalking quadrupedalism, and to the hominin acquisition of a terrestrially adapted foot. However, heel-strike plantigrady is not limited to the African apes (Meldrum 1993; Crompton et al. 2003); also, heel-strike is actually particularly clearly expressed in an Asian ape, the most arboreal of great apes, the orangutan, subfamily Ponginae (Crompton et al. 2003, 2008). All great apes can and do walk bipedally, and most do so in an arboreal context. Again, it is the most arboreal, the orangutan, which uses bipedal locomotion most often (Thorpe & Crompton 2005, 2006). While bipedal locomotion supported by the hindlimbs alone makes up only about 2 per cent of arboreal locomotion of orangutans, a further 6 per cent consists of bipedalism where one or both forelimbs are used for balance. But this small percentage of locomotor bipedalism (or compressive orthogrady, if preferred) plays an

3301

This journal is # 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3302

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

ecologically crucial role in movement on the fine peripheral branches, where fruits are located. It further allows orangutans to bridge from tree to tree at canopy level, avoiding the very high costs (Thorpe et al. 2007a) and predation risk associated with crossing on the ground. It is again the orangutan which of all living apes approaches closest to us in one of the most important of the biomechanical features identified by Alexander (1991) as characteristic of human walking: namely stiff-legged, upright gait. As a consequence of its stiff-legged gait, the orangutan produces, in a fifth of its bipedalism, double-humped vertical ground reaction force curves (vGRF) which, alone among apes, overlap with those produced by human walking (Crompton et al. 2003), and which allow a high degree of pendular energy conversion. Our calculations indicate that while in untrained common chimpanzees energy conversion in bipedalism reaches little more than 8 per cent, it approaches some 50 per cent in untrained orangutans, still well short, of course, of the 70 per cent possible in humans (Wang et al. 2003). But while it has recently been argued that the elongated, inverted foot of the orangutan does not at all closely resemble our own (Sayers & Lovejoy 2008), orangutan foot function in bipedal walking, expressed in the pattern of foot pressure, is actually very similar (Crompton et al. 2008) to that of the bonobo (Vereecke et al. 2003), often suggested by others as a model for the common panin –hominin ancestor (e.g. Zihlman et al. 1978 and reviewed in Vereecke et al. 2003). It has been apparent for the last few years that a growing number of scientists have found cause to doubt whether firm evidence exists in the fossil record for a knucklewalking origin: see, e.g. Stern & Susman (1983) for Australopithecus afarensis; Ward et al. (1999) for the South Turkwel handbones and Clarke (1999, 2002) for the StW-573 hand. A range of purported ‘knucklewalking features’, dorsal ridges on the distal aspect of the metacarpals, os centrale – scaphoid fusion or extension of the proximal articular surface of the capitulum onto its dorsum, have been sought in the hominin fossil record, but have either not been found or found only inconsistently. Dainton & Macho (1999) raised doubts about whether knucklewalking was a homologous phenomenon even in chimpanzees and gorillas. However, Richmond & Strait (2000) argued that the distal radial morphology of Au. afarensis was evidence for a knucklewalking phase in evolution some time between 3.6 Ma and the commonly accepted 5 – 8 Ma limits for genetic separation of hominins and panins. It is therefore noteworthy that the morphology plotted by Richmond & Strait (2000) lies well within the orangutan range of variation. Only large male Bornean orangutan make much use of the ground, the Sumatran tiger being a major discouragement to terrestriality on that island, the clouded leopard posing a threat to small or juvenile orangutan on Borneo. Large Bornean males have too much unstable mass above the hip to sustain unassisted bipedalism, and so tend to cross the ground quadrupedally. But when crossing the ground they do not walk on the middle phalanx, as chimpanzees or gorillas do, but on their proximal phalanges or on Phil. Trans. R. Soc. B (2010)

the side of their hand. Richmond et al. (2001), however, stoutly defended a knucklewalking origin in an extensive review, and Richmond & Jungers (2008) claimed that similarities in curvature of a single phalanx of the late Miocene protohominin Orrorin to that in chimpanzees represented evidence of knucklewalking, although Orrorin is regarded by its discoverers as arboreally adapted, orthograde and bipedal when moving on the ground (Senut et al. 2001). Kivell & Begun (2007) however found no clear functional link between os centrale–scaphoid fusion and knucklewalking and Kivell & Schmitt (2009) argue that there are two functionally distinct modes of knucklewalking in African apes: that in chimpanzees being associated with extended wrist postures in an arboreal environment (directly addressing Richmond & Jungers 2008), and that in gorillas with a neutral wrist posture in a terrestrial environment. Kivell & Schmitt (2009) go on to argue that the purported knucklewalking features of hominins are instead adaptations to arboreality, and thus that bipedalism indeed arose in the arboreal ecological niche common to living apes. While the absence of purported knucklewalking features in the hand of Au. afarensis (e.g. Stern & Susman 1983) leaves little time for hominins to lose any such features after the separation of hominins and panins 5– 8 Ma, the publication of a full description of Ardipithecus ramidus shows that knucklewalking features, including dorsal distal metacarpal ridges are also absent in Ar. ramidus (Lovejoy et al. 2009a), with the exception of os centrale– scaphoid fusion. However, recall that Kivell & Begun (2007) found no functional link to knucklewalking for this feature. This extends the lack of evidence for a terrestrial knucklewalking phase in the evolution of human bipedalism to 4.4 Ma. Equally, in linking terrestrial bipedalism to arboreality (Lovejoy et al. 2009a,b), publication of Ar. ramidus has greatly strengthened the positive case for an arboreal origin for the core hominin adaptation. In doing so, it challenges us to develop a convincing arboreal alternative to a terrestrial knucklewalking model of the origins of human bipedalism. While still based on the concept that we should look for the origins of human bipedalism among activities of living African apes, the most supported arboreal challenger for the terrestrial knucklewalking model is the ‘vertical climbing’ hypothesis of Fleagle et al. (1981). This was derived primarily from electromyographic similarities between hip, buttock and thigh musculature activity of African apes during climbing on large, vertical supports, and that of humans walking bipedally. However, the kinematics of vertical climbing (Isler 2002, 2003; Isler & Thorpe 2003) and knucklewalking (Watson et al. 2009) are rather similar, involving highly flexed postures of the hip and knee (Crompton et al. 2003), which are quite unlike the extended postures seen in human walking and which underlie its efficiency (Alexander 1991). Running does involve more flexed limb postures, but this is linked to the use of elastic recoil, as the spring-mass mechanism requires substantial elastic energy stores. The most well known of these elastic energy stores, a marked Achilles tendon, is absent in both the African

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Arboreal origins of hominin bipedalism apes and the orangutan, which all have large distal muscle masses (Thorpe et al. 1999; Payne et al. 2006a,b), which help the more powerful forelimbs (Thorpe et al. 1999; Oishi et al. 2009) in climbing but probably also act to tune the limbs to deal with variations in support compliance in an arboreal context. Interestingly, the gibbons and siamangs do have a large Achilles tendon: its mechanical role is currently under investigation in our laboratory (Channon et al. 2009). The absence of a medial longitudinal arch (MLA) in the non-human great apes and its reported absence in Ar. ramidus (Lovejoy et al. 2009a) appears to rule out that possible location of the required mass of elastic tissue. So the existence of one or both of the most likely possible elastic energy stores, a large mass of plantar soft tissue housed within a MLA (Ker et al. 1987) or a large Achilles tendon, is required to be demonstrated before a mechanically effective compliant, rather than stiff-legged, gait can reasonably be posited for early hominins. While energetic efficiency and mechanical performance are by no means the only parameters subject to natural selection (as fieldworkers know better than most), they are very often directly or indirectly important, and can be assessed and predicted relatively readily. Several laboratories, including our own, have therefore used computer simulation to assess the effectiveness of alternative gaits in Au. afarensis and other hominins. Independent studies by at least three separate laboratories (Crompton et al. 1998; Kramer 1999; Kramer & Eck 2000; Sellers et al. 2003, 2004, 2005; Nagano et al. 2005) demonstrate that Au. afarensis could have been an effective stiff-legged upright biped, particularly over relatively short distances and walking unloaded (Wang & Crompton 2004; Wang et al. 2004). Using forwards dynamic modelling, metabolic cost can be predicted. Predicted costs for human models have been verified against experimental values for human adults and come within 10– 15% of these values. Predicted values for upright walking by Au. afarensis in independent studies by Sellers et al. (2004, 2005) and Nagano et al. (2005) are in good accord and come quite close to the experimental values for human children of equivalent size. If Au. afarensis could thus have been an effective stifflegged, upright biped, and if moving in a compliant gait would have incurred both substantial increases in the mechanical cost of locomotion (Crompton et al. 1998) and physiological costs including increased heat load (Carey & Crompton 2005), an origin for bipedalism in locomotor modes associated with highly flexed limb postures, such as vertical climbing, seems unlikely. A different objection to the vertical climbing model has recently been raised by DeSilva (2009). He argues that early hominin ankle joint morphology is distinct from that of vertical-climbing African apes, and incompatible with the kinematics required for vertical climbing. Lovejoy et al. (2009b) argue that anatomical features of the hand associated with vertical climbing, such as elongated metacarpals, are absent in Ar. ramidus, and they follow Thorpe et al. (2007b) in proposing that both knucklewalking and a strong Phil. Trans. R. Soc. B (2010)

R. H. Crompton et al.

3303

adaptive commitment to vertical climbing were acquired independently in panins, after the divergence from hominins, although Lovejoy et al. (2009b) do not appear to make a functional link between the two. Lovejoy et al. (2009a,b,c) identify a number of features in which the hands and feet of Ardipithecus resemble those of the root hominoid Proconsul and some living arboreal monkeys, rather than living great apes. These include evidence for short hands with an extensive dorsiflexion range in the metacarpophalangeal joints that is absent in living great apes apart from humans (individuals in some human populations, such as the Han Chinese can often dorsiflex to more than 908 when young; personal observation, R. H. Crompton 1982). Following earlier arguments (Moya`Sola` et al. 2004) that the presence of the same feature in the Miocene hominoid Pierolapithecus catalaunicus suggested that it was an arboreal quadruped, they suggest, although acknowledging that it is a curious combination, that while bipedal on the ground (Lovejoy et al. 2009c), Ar. ramidus was primarily quadrupedal in the trees (Lovejoy et al. 2009b), while using some ‘careful climbing and bridging’, presumably at the periphery of trees (Lovejoy et al. 2009b). The feet of Ar. ramidus, like those of monkeys, apparently retained a thick plantar layer of fibrous tissue, and were thus rather stiff when compared with those of the panins, gorillines and pongines (Lovejoy et al. 2009a). This implies lesser ability to conform to branch diameter, and thus relatively poor grip for what was apparently a large-bodied (50 kg, Lovejoy et al. 2009c) hominin, nearly twice the mass of the largest cercopithecine monkey, the mandrill, and more than 10 kg greater than the largest individuals of the largest monkey, the Sichuan snub-nosed monkey Rhinopithecus roxellana (Rowe 1996). It is argued that panins, gorillines and pongines also acquired their compliant feet independently (Lovejoy et al. 2009a). With no tail, but equally little pedal gripping power, as well as short hands, there can have been little or no capability to exert balancing counter-torques on the support. Then how did Ar. ramidus balance their body mass above branches during pronograde quadrupedalism? Quadrupedal monkeys, lacking the wide and powerful grasp of the living non-human great apes, improve stability by deep flexion of the limbs. Stability in flexion is very often aided by anteflexion of the olecranon process in arboreal monkeys (Fleagle 1998), but there is apparently no evidence of anteflexion of the olecranon in the Ardipithecus proximal ulnae (Lovejoy et al. 2009b). Further, habitual deep flexion of the limbs as an arboreal quadruped would increase mismatch (in the power capacity of muscles at different joint angles) between the requirements of terrestrial bipedalism and those of arboreal quadrupedalism.

3. THE ARBOREAL ORIGINS OF BIPEDALISM: COMPRESSIVE ORTHOGRADY? A more parsimonious explanation of the metacarpophalangeal dorsiflexion seen in Ar. ramidus is surely desirable. It exists, in part, in consideration of elements of arboreal behaviour of all the great apes,

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3304

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

namely in the use of arboreal hand-assisted bipedalism, or if preferred, compressive orthogrady, both postural and locomotor, to move around the forest canopy. Again, in part, the explanation is to be found in consideration of the similarity, in shared lack of digital elongation and in morphological conservatism, between the human hand and that of Ar. ramidus, demonstrated by Lovejoy et al. (2009a). Together with the suggestion of Thorpe et al. (2007b) that vertical climbing and knucklewalking were both acquired independently in panins (after the separation from hominins) and in gorillins, and its confirmation by the description of Ar. ramidus (Lovejoy et al. 2009b,c), there is increasing evidence (e.g. Larson 1998) that suspensory adaptations did not evolve at the same time as other features of orthogrady, but rather homoplastically. While it is difficult to obtain definitive figures from all studies and for all species, table 1 shows that, together, terrestrial knucklewalking quadrupedalism, vertical climbing and forelimb suspension make up some 67 per cent of bonobo locomotion, 93 per cent of common chimpanzee locomotion and 97 per cent of mountain gorilla locomotion, but only 39 per cent of orangutan locomotion. A figure for lowland gorilla knucklewalking versus non-knucklewalking quadrupedalism is more difficult to determine, but based on proportions of arboreal and terrestrial activity, we have assigned a tentative figure which allows a total proportion of novel locomotor modes in the repertoire to be set pro tempore at 62 per cent. Thus, from the reported evidence of Ardipithecus, the great majority of the panin and gorilline locomotor repertoire employs novel adaptations since the divergence from hominins. This observation has significance for both palaeontologists and fieldworkers, and underlines Darwin’s (1871) warning, with which we began this paper, that we should not expect the common ancestor to resemble either humans or living apes particularly closely. This suggests that what is now the relatively small compressive component of great ape orthograde locomotion may be the oldest, and human locomotion thus relatively conservative. (Whether compressive orthogrady is as old as orthogrady itself, or whether orthograde body posture arose earlier from a random homeotic event (Filler 2007), we currently have no way of knowing). Importantly however, this behaviour offers a reasonable alternative for locomotion in a species not yet in possession of vertical climbing and suspensory adaptations. We suggest that in an arboreal context, hominin species such as Ar. ramidus (as well as ourselves) which do not have elongated hands, powerful in suspension, may tend more often to climb upwards (which they must have done relatively frequently if they were exploiting both terrestrial and arboreal niches) by pushing themselves up by pressure of the hands below shoulder level, so that the ulnar four metacarpophalangeal joints pass into deep dorsiflexion. This adds much of the length of the metacarpals to the potential lift. This is of course exactly how humans usually climb large-trunked trees when they lack climbing equipment to help them move on the main trunk, with the human lack of ‘vertical climbing’ adaptations (primarily very powerful arms; see Thorpe et al. 1999; Payne et al. Phil. Trans. R. Soc. B (2010)

2006a,b; Oishi et al. 2009): we climb up bough by bough, further out in the tree. In the absence of climbing aids, humans find it difficult and of course dangerous (Pontzer & Wrangham 2004) to climb up trees where long, naked trunks occur before any side branches. Gorillas and chimpanzees are readily able to do so, using the vertical climbing adaptations, which Ardipithecus suggests (Lovejoy et al. 2009a,b,c) arose independently and in parallel in the two lineages. Similarly, hand-assisted compressive orthogrady has been shown to allow orangutans to move on very flexible branches at the periphery of tree crowns where the most abundant supply of fruit is generally situated (Thorpe et al. 2007b) and it may play a similar role in the behaviour of lowland gorillas (see table 11 in Remis 1994). Analogy with the largest cercopithecine, the mandrill (Lahm 1986), less than 27 kg, and consideration of the behaviour of the largest of all monkeys, Sichuan snub-nosed monkeys Rhinopithecus roxellana (Kirkpatrick et al. 1999; Li 2001; Li et al. 2002), less than 37 kg, suggests that the 50 kg body weight claimed for Ar. ramidus (Lovejoy et al. 2009c) may exceed mass limits of effective monkey-like arboreal plantigrade quadrupedalism. However, compressive orthogrady is exhibited by similar-sized apes and could facilitate both access into trees and movement within them. Further, Miocene crownhominoid body weight begins above that of mandrills, and equals or exceeds that of R. roxellana: 30 – 54 kg for Morotopithecus (MacLatchy et al. 2000), 30 kg for Pierolapithecus (Culotta 2004; Moya`-Sola` et al. 2004), 30– 37 kg for Hispanopithecus (Moya`-Sola` & Ko¨hler 1996) and 32 kg for Oreopithecus (Ko¨hler & Moya`Sola` 1997). We suggest that it is unlikely that the consistently larger size of Miocene crown hominoids was not accompanied by a shift from monkey-like arboreal locomotion. Thus, we argue that a hominin which had not acquired suspensory/vertical climbing features in the forelimb would have accessed the trees and moved within them primarily by palmigrade compressive orthogrady. In the absence of vertical climbing capabilities and a powerful hand grip, access to trees would of course favour use of more stable supports, which can be loaded under compression without excessive deflection. In the absence of suspensory features, hand-assisted bipedalism could have facilitated movement among the finer supports at the periphery of trees, employing strategies similar to those we have reported in the orangutan (Thorpe et al. 2007b, 2009). Quadrupedalism would be used when absolutely necessary—as of course it is by ourselves when we no longer trust our balance or stability—but palmigrade hand postures would be inappropriate among finer supports. Many anthropoids are able to employ some degree of suspension, vertical climbing and quadrupedalism regardless of their primary adaptation, although perhaps rarely, and at some additional cost, so suspension is also likely to have been used under certain conditions. It may be argued that this is referential modelling (Sayers & Lovejoy 2008): but at least we are using multiple referents, and we are able to test the predictions of our models by simulation. We predict, for example, that

Phil. Trans. R. Soc. B (2010)

26.7

4.5 27.5 8

38.5

86.1 7.8 0

6.5 50.4 26

19.7

,1

,1

95

0.8 8.9 13

3.6

0.1

brachiate

0.5 0 22

3.3

0

orthograde clamber/transfer

0.7 1.5 7

6.1

0.8

0.2 3.1 ,1

0

0

bipedal leap

0.3 0 9

0

.0

pronograde scramble

0.1 0 11

1.3

0

otherb

93 67 39

62

97

% loco evolved since separationc

c

b

Note that all values are ballpark figures as differences in methodology and subject profiles preclude detailed comparison. For example, tree sway, pronograde suspension. This value assumes that the common ancestor at all levels was a monkey-like above branch quadruped. The value includes knucklewalking, vertical climb/descent, brachiation and orthograde clamber/ transfer. d Modified after Hunt (2004) and based on data from Tuttle & Watts (1985), Doran (1996), Hunt (1992) and Remis (1995). e Adapted from Tuttle & Watts (1985). f Knucklewalking/non-knucklewalking values are not available for lowland gorillas at present. However, 59% of their time is spent terrestrially and 41% arboreally (adapted from Hunt 1996). Consequently, as a rough estimate, we have allocated 51% of quadrupedalism to be terrestrial knucklewalking and the remainder to be arboreal non-knucklewalking quadrupedalism. g Adapted from Hunt (1992) following personal communication (K. D. Hunt, 2009). h Bonobos are more arboreal than chimpanzees but no conclusive data exist, neither for the per cent of time they are arboreal nor for how much of their quadrupedalism is knucklewalking. However, Susman (1984) observed that of 532 bouts of arboreal quadrupedalism, only 20 (3.8%) were knucklewalking and of Susman’s (1984) 89 first sightings of bonobos, 17 (19%) were terrestrial. Thus, we have weighted Doran’s (1996) frequency data with these values to calculate proportions for knucklewalking and non-knucklewalking quadrupedalism. i Modified from Thorpe & Crompton (2006).

a

mountain gorilla d,e lowland gorillad,f chimpanzeed,g bonobod,h orangutani

vertical climb/descent

other quadrupedal (terrestrial and arboreal)

knucklewalk/run (terrestrial and arboreal)

Table 1. Frequencies of locomotor behaviour in the great apes and ‘ballpark estimates’ of the per cent of their locomotion that has evolved since divergence from their last common ape ancestora.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Arboreal origins of hominin bipedalism R. H. Crompton et al. 3305

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3306

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

a dynamic model of quadrupedalism in Ardipithecus would show that quadrupedalism would be possible, if unstable, and very expensive, if perhaps less so than it would be for longer-legged humans. A parallel case has very recently been discussed in the literature. Pierolapithecus is described by Alme´cija et al. (2009) as orthograde, but as lacking the obvious suspensory adaptations seen in the rather later Iberian crown hominoid, Hispanopithecus (D.) laietanus. The metacarpophalangeal joints are described as adapted for use in dorsiflexion in palmigrade postures (Alme´cija et al. 2009). Reference to monkeys would suggest that it was an arboreal quadruped (Moya`Sola` et al. 2004), but these authors now regard it as orthograde in body plan (Alme´cija et al. 2009) but moving by palmigrade quadrupedalism. The authors also suggest that the description of the Miocene pongine Sivapithecus by Madar et al. (2002) may suggest similar behaviour. It is very difficult to reconcile an orthograde body plan with quadrupedal locomotion, even when there are no claims that Pierolapithecus was a terrestrial biped. The obvious, simple solution is again the one we propose here, that it (and perhaps even Sivapithecus) was an orthograde clamberer which, in the absence of marked suspensory adaptations, used hand-compressive climbing techniques below shoulder level, in other words, hand-assisted bipedalism and other components of the compressive-orthogrady continuum best exemplified today in orangutans. 4. THE LEGACY OF ARBOREAL ORIGINS FOR HUMAN BIPEDALITY The arboreal habitat differs markedly in one major mechanical respect from the terrestrial: it is compliant (Alexander 2003) and thus unstable, as it can be set vibrating by imposed forces. Arboreal mammals need to have strategies for dealing with this compliance. Schmitt (1999) has shown that limb flexion (limb compliance) is one such response, but limb flexion requires muscle power to maintain stable flexed postures. For this reason, most probably, muscle masses tend to be higher in arboreal animals (Degabriele & Dawson 1979), while terrestrial cursor limbs have short muscle bellies and long tendons (Alexander 2003). To what extent has this legacy of compliance influenced early hominin evolution? (a) A compliant foot? Lovejoy et al. (2009a) argue that whereas the living non-human great apes have acquired compliant feet, to enable them to grip branches more effectively, and humans have of course acquired a MLA, Ardipithecus is again conservative in the plantar foot, lacking a MLA, but retaining a thick and fibrous layer on the plantar aspect of the foot, like that of cercopithecines, contrasting with the loss of such a thick aponeurotic layer in the non-human apes, which gain thereby in foot adaptability to irregular substrates. Following Bojsen-Møller (1979), it is common in the hominin palaeontology literature (e.g. Lewis 1980; Berillon 2000; Harcourt-Smith & Aiello 2004; Jungers et al. 2009) to assess the presence or absence of a MLA by the degree of development and Phil. Trans. R. Soc. B (2010)

asymmetry of the cuboid peg for the calcaneus (figure 1a), and Lovejoy et al. (2009a) appear to follow this practice. The asymmetry and size of the cuboid peg is not, however, entirely a reliable guide to the existence or absence of a functional MLA: as can be seen in figure 1a, the peg is not overlapped ventrally by the calcaneus. While it is usual to associate this development with loss of the mid-tarsal break (axis of plantarflexion), which is present in other living apes (Lewis 1980), the absence of a mid-tarsal break is not universal in humans. Setting aside conditions such as Charcot foot, where soft-tissue failure arising from diabetes or directly from neurological conditions results in collapse of the lateral midfoot and in some cases a midfoot pressure peak under, or near, the calcaneocuboid joint, figure 1b (unfortunately from uncalibrated pressure plate data, but qualitatively reliable) shows that clinically normal individuals may also show a lateral midfoot pressure peak. It is interesting that this individual also shows absence of a lateral-to-medial path of the centre of pressure and, in figure 1c, a single-peaked vGRF, with a nonhuman-ape-like slow tailing-off of vGRF at ‘toe-off ’. While the absence of the mid-tarsal break does seem functionally linked with an extended toe-off, neither are therefore universal features of hominins. Nevertheless, if Ardipithecus lacked a human-like cuboid peg, lateral-foot stability would be limited. In both cases, a certain degree of rigidity provided by retention of a thick plantar fibrous layer would improve the capacity of the lateral metatarsals to deliver accelerative force from a more effective, relatively anterior, position. We (Pataky et al. 2008) recently demonstrated a negative correlation of plantar pressure with walking speed in humans, which implies reduced collapse of the MLA, and thus increased stiffness. This may be directly beneficial to force transmission to the ground. It is also important in enabling control of gear ratios, and thus in tuning muscles to enhance performance during constant-speed running by applying pre-tension during landing, while optimizing them also for efficiency or power at toe-off (Carrier et al. 1994). Perhaps most importantly, we can optimize muscle properties during rapid changes in speed and changes in incline in both running and walking (Lichtwark & Wilson 2006, 2007, 2008). We have suggested that increased stiffness results from pre-tension applied to the plantar aponeurosis (PA) by heel-strike or earlystance muscle activity (in triceps, tibialis anterior and the digital dorsiflexors; Pataky et al. 2008; Caravaggi et al. 2009). The windlass mechanism created as the PA wraps round the heads of the metatarsals (figure 1a) is known to contribute to stiffen the foot in late stance (Hicks 1954) by pulling on the calcaneus, causing inversion of the subtalar joint and hence ‘locking’ the midtarsal joint (Tansey & Briggs 2001). A dynamic model of the plantar foot constructed in our laboratory (Caravaggi et al. 2009) however shows that the PA is also pre-tensioned in early stance, from heel-strike onwards, as proposed by Pataky et al. (2008), and the tension appears to increase with walking speed. The predicted tension (verified against cadaveric data from Gefen (2003)) increases from lateral to medial, and ranges from 0.47 body weight at

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Arboreal origins of hominin bipedalism (a)

R. H. Crompton et al.

3307

(b)

metatarsal heads

spring ligament talonavicular joint, with calcaneocuboid joint forms ‘midtarsal’ or transverse tarsal joint head of the talus

cuboid peg calcaneocuboid joint the 5 slips of the plantar aponeurosis

(c) 1600 1400

force (N)

1200 1000 800 600 400 200 0 0

50

100

150 time (ms)

200

250

300

Figure 1. (a) Diagram of the plantar aspect of the human foot, showing the position of the cuboid peg and illustrating the ‘windlass mechanism’, whereby the five slips of the PA are tensed by the curvature of the metatarsal heads as the metatarsophalangeal joint dorsiflexes. Similarly, the spring ligament is tensed by plantad motion of the head of the talus. Both mechanisms act to stiffen the median longitudinal arch during stance. (Figure modified from image from Primal’s ‘Anatomy TV’). (b) Peak pressures, in false greyscale, where lighter tone indicates higher pressure, during bipedalism of a clinically normal subject recorded by Nike Inc., courtesy of J.-P. Wilssens of RSscan International. Dots indicate the path of the centre of pressure under the foot. (c) vGRF curve calculated from the same data for the individual featured in (a).

heel-strike to a peak 1.5 BW, generating vertical forces which sustain the MLA and metatarsals. Thus, the MLA is supported through much of stance by soft tissue: stiffening of the PA, as well as bone shape, contributes directly and very substantially to the existence of the MLA. An assumption that lack of a human-like cuboid peg (figure 1a) implies lack of a MLA is unsafe without extensive investigation of the possibility of soft-tissue stiffening. The case of human individuals with a mid-tarsal break suggests that sustained vGRFs and a substantial hallucal toe-off depend on stiffening of both the medial and lateral foot by soft-tissue tensioning throughout stance. It is notable that Vereecke et al. (2003) have shown that foot pressure records of human bipedalism are much less variable between strides and between individuals than those of the bipedalism of other hominoids. In humans, forces are applied in a more consistent manner, particularly by the hallux, which plays a limited propulsive role in most non-human apes, and may act more as a balancing structure during bipedalism. If the hallux of Ardipithecus is as Phil. Trans. R. Soc. B (2010)

abducted as Lovejoy et al. (2009a) report, the degree of abduction is comparable to that in living gibbons (e.g. Vereecke et al. 2005; Crompton et al. 2008) and perhaps Oreopithecus. While Moya`-Sola` et al. (1999) suggested that the extent of hallucal abduction in Oreopithecus would not have been compatible with other than postural bipedalism, Vereecke et al. (2006a,b) have shown that gibbons, despite compliant feet with widely abducted halluces, can sustain running on the ground for some hundred yards and attain absolute speeds equalling the human walk–run transition. Neither do compliant feet prevent the non-human great apes from walking bipedally, terrestrially or arboreally. High robusticity of metatarsals two and three is also a feature of Ar. ramidus (Lovejoy et al. 2009a) and suggests that these digits may have been more important in applying accelerative parasagittal force than the hallux, while the abducted hallux provided grip on branches. However, even in human bipedal walking, plantar pressure tends to be lower under the hallux, and greater under metatarsal heads two and three, in flat-footed humans or humans who

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3308

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism (a) 1.4

(b)

1.2

hindlimb length (m)

forelimb length (m)

1.0 0.8 0.6 0.4 0.2 0 (d)

hindlimb moment of inertia (kg m2)

forelimb moment of inertia (kg m2)

(c) 1.5

1.0

0.5

0 Gorilla

Pan

Pongo Hylobates Homo Equus

Gorilla

Pan

Pongo Hylobates Homo Equus

Figure 2. (a,b) Chart showing the limb lengths and (c,d) moments of inertia for hominoids and horse. Forelimb moments of inertia are about the shoulder joint and hindlimb moments of inertia are about the hip joint. Great ape data are from Isler et al. (2006), human data are from Winter (1990) using a median male height and weight from the GEBOD database (Cheng et al. 1994), horse data from Buchner et al. (1997).

have been brought up as barefoot walkers (D’Aouˆt et al. 2009). Thus, the human foot is less distinct than is often thought from that of other great apes. It has built on the compliant arboreal legacy (whether prior to or after the separation from panins we submit is not yet clear, given the mixed message of Ardipithecus; Lovejoy et al. 2009a) by becoming a variable-gear organ, able to change its stiffness to accommodate to speed, as well as to support compliance and irregularity.

(b) Limb mass proportions Another likely legacy from a recently arboreal past is the partial retention of arboreal limb mass proportions. A cursorial animal needs to accelerate its limbs rapidly. Rapid acceleration can be achieved with less energy if the moments of inertia are reduced, and this is commonly achieved by a reduction in distal limb elements (Hildebrand 1995). Figure 2 shows a comparison of the inertial properties and limb dimensions of hominoids in comparison with a Phil. Trans. R. Soc. B (2010)

dedicated terrestrial cursor (horse). All dimensions have been geometrically scaled to the estimated mass of Ar. ramidus, 50 kg, using mass1/3 for lengths and mass5/3 for moments of inertia. All the arboreal species have longer than expected forelimbs, but, except for humans and gibbons, hindlimb length is not greatly different from that of the specialist cursor. However, when looking at the moments of inertia it can clearly be seen how elongated limbs with heavy autopodia lead to extremely large moments of inertia when compared with the values seen in horses. This has inevitable but complex effects in terms of top speed and efficiency. Long, high-inertia legs are perfectly efficient for the pendular mechanics of slow walking, but the high-speed spring mechanics of running require low moments of inertia to minimize the internal energy lost per step. Hylobates seems to some extent to have dealt with the inertial problem of very long legs by reducing distal muscle mass. We suggest, following Channon et al. (2009), that several aspects of gibbon anatomy may relate to an unrecognized importance of leaping in the gibbon locomotor repertoire.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Arboreal origins of hominin bipedalism

(c) Proportion of mass as tendon Another area where there is still a considerable legacy from the recent arboreal past is in the amount of tendon in the hindlimbs of hominoids compared with cursorial animals. Figure 3 shows the mass of hindlimb tendon in both hindlimbs as a proportion of body mass. This parameter is informative since its biomechanical interpretation is independent of moment arm data, of which there is very little available for comparison in non-primates. Tendon acts as a simple damped spring during locomotion, so the amount of energy that can be stored depends on the mass. The strain energy storage of tendon is 2500 J kg21 at 8 per cent strain (Vogel 2003), which is therefore the limit of the amount of elastic strain energy that is potentially available per gait cycle— whether for power amplification or energy saving. For the hominoids, tendon mass was estimated using published tendon length and muscle physiological cross-section area data. Tendon cross-section area was estimated by assuming 6 per cent strain at maximal isometric contractile force and muscle contraction stress of 300 kN m22 (Sellers & Manning Phil. Trans. R. Soc. B (2010)

3309

tendon mass fraction (%)

10

1

10−1

ho

un

d

re ha

ey gr

er de

an

in re

m hu

on bb

n ta gu

gi

la ril go

an or

im

pa

nz

ee

10−2

ch

However, upper limb – lower limb proportions and the distribution of lengths and mass within limbs also affect their swing frequency. Part of the efficiency of long distance human walking at least depends on a forward swing of the contralateral arm to counteract the horizontal torque applied to the body by the swing leg (e.g. Li et al. 2001) which, among other effects, interferes with lateral stability. These swings occur even in short-distance walking of young children of similar stature/mass to Au. afarensis, and increase in magnitude with walking speed (Li et al. 2001), so they are of relevance to any consideration of early hominin locomotion. Match between the natural pendular period (NPP), and hence swing-time of upper and lower limbs, affects efficiency of all gaits, bipedal and quadrupedal; and distribution of mass within the limb affects the NPP (Isler et al. 2006). The distal position of the centre of mass of the forelimb of most great apes, with the exception of the chimpanzee, means that there is a considerable mismatch with forelimb NPP, and segment proportions are thus not well optimized for quadrupedal gaits (Isler et al. 2006). Chimpanzees may have modified their limb mass distribution for more efficient quadrupedalism, suggesting that the last common African ape ancestor was not a proficient quadruped (Isler et al. 2006). However, experimental work on the oxygen consumption of both bipedal and quadrupedal locomotion in chimpanzees confirms that they are relatively inefficient in both modalities (Sockol et al. 2007), compared with both modern humans and quadrupeds of equivalent body size. This may indicate that maximum terrestrial speed, rather than minimal terrestrial energy cost, may be the target of selective pressure for chimpanzees. (By contrast, preliminary data from the same research group suggest that metabolic costs of bipedalism in the orangutan are some of the lowest recorded locomotor costs for the body size; personal communication from H. Pontzer (2009)).

R. H. Crompton et al.

Figure 3. Total tendon in both hind limbs as a fraction of body mass. Data are based on information from Pierrynowski (1995), Payne et al. (2006), Williams et al. (2007, 2008) and Wareing et al. (submitted).

2007). Resulting volumes were converted to tendon mass using a density of 1100 kg m23 (Watson & Wilson 2007). It is clear that tendon mass is highly variable and more often related to high speed and high acceleration than to efficiency. It is also clear that while humans have appreciably increased their hindlimb tendon proportion when compared with the other apes, they are still a long way from the much higher proportions in more specialized cursorial quadrupeds—particularly those specializing in explosive acceleration rather than long-distance efficiency. This is emphasized if we multiply through by 2500 J kg21 to express elastic storage capacity in terms of energy. Most hominoids have about 1 J kg21 of elastic energy storage, humans nearly three times that, reindeer 10 J kg21 but greyhounds fully 100 J kg21. Thus, while humans have adjusted tendon mass somewhat to enhance terrestrial running, perhaps retaining a relatively large muscle mass to allow for adjustments to optimize the hindlimb for terrain, speed and support characteristics, the African apes have not. Bonobos and lowland gorillas may not require to do so because of limited terrestriality; mountain gorillas may be protected by size, but chimpanzees may simply have modified mass proportions to match hindlimb – forelimb swing frequencies better, suggesting that the selective pressures associated with movement in an unstable arboreal milieu remain strong. We can further investigate the role of elasticity in human locomotion by simulation. In recent simulation work (Sellers et al. 2010), the role of tendon elasticity was quantified by ‘virtual ablation’. In this paradigm, simulations are repeated with identical anatomical models except for the structure of interest, which is

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

6 5 4 3 2 1 0

T al rm no

nd

nd

sa

sa

on

on

nd sti

ff

te

nd

te al rm no

A

T A sti

ff

sti ff te nd

al no

rm

on

on

s

s

4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0

te

net cost of locomotion (J kg−1m−1)

(b)

nd

(a)

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

velocity (m s−1)

3310

Figure 4. (a) Chart showing the maximum velocity and (b) the cost of locomotion of human running simulations where the elastic properties of the hindlimb tendons are manipulated. AT, Achilles tendon. (Sellers et al. 2010).

removed or altered in some versions of the model. This allows the effect of a specific structure to be isolated in much the same way as classical ablation experiments but without the danger of side effects (let alone ethical difficulties) associated with performing such experiments surgically. In this case, the elastic effect of tendons was removed by making them 100 times their normal stiffness, so that the simulated tendons were unable to store appreciable amounts of energy in the simulation. Four experimental conditions were compared: normal hindlimb tendons; all hindlimb tendons stiff; all normal hindlimb tendons except for a stiff Achilles tendon; all tendons stiff except for a normal Achilles tendon. Figure 4 shows that for humans, the presence of tendon has only a moderate effect on the maximum running speed of the simulation but a very marked effect on the net cost of locomotion, and that this effect was mostly produced by the Achilles tendon. This confirms the critical role in efficient, high-performance running of a substantial Achilles tendon, which is missing from all hominoids except humans, gibbons and siamangs. Whether such a structure is present in fossil hominins (and which) is currently unknown but evidence of its presence, perhaps by analysis of calcaneal microstructure, would probably be diagnostic of running ability.

5. CONCLUSIONS We argue that, given the large body mass of Ar. ramidus, typical of both living and extinct hominoids, it is more likely that when it moved in the trees it made use of compressive orthogrady, which we suggest may be the oldest crown-hominoid locomotor adaptation, than that it adopted a monkey-like quadrupedalism. This would run counter not only to Phil. Trans. R. Soc. B (2010)

expectations from body size but also to Ar. ramidus’ clear adaptations for one form of compressive orthogrady, terrestrial bipedal walking. Secondly, we argue that from our arboreal ancestors humans have inherited feet and legs that can adapt to a large variety of terrains, support compliances and speeds. However, at some stage in our evolution we have departed some way from other hominoids in adaptation for energy-efficient running. This combination probably has a lot to do with our ability to outrun horses in trials such as those over 22 miles of hilly mid-Wales or 50 miles of sand-dunes in the United Arab Emirates. But we are not fast runners (see Bramble & Lieberman 2004), and in terms of energy storage have a very long way to go to catch up with dogs bred for hunting. Early human ancestors would clearly have been no match for a cursorial predator, so that it is perhaps fortunate that along with late retention of long forearms (Dunsworth et al. 2003), which would improve throwing distance if not accuracy, part of our arboreal inheritance was powerful leg muscles, which remain very helpful for climbing trees! R.H.C. thanks Alan Walker and Chris Stringer for the invitation to participate in this meeting. We thank the Royal Society, the Leverhulme Trust and the Natural Environment Research Council, the Biotechnology and Biological Sciences Research Council and the Engineering and Physical Sciences Research Council for supporting our research, and Chester and Twycross Zoos for permission to study the hominoids under their care. R.H.C. and W.I.S. also thank the NorthWest Grid and the Science and Technology Facilities Council Daresbury Laboratory for access to high-performance computing facilities.

REFERENCES Alexander, R. McN. 1991 Characteristics and advantages of human bipedalism. In Biomechanics in evolution (eds J. M. V. Rayner & R. J. Wooton), pp. 225 –266. Cambridge, UK: Cambridge University Press. Alexander, R. McN. 2003 Principles of animal locomotion. Princeton, NJ: Princeton University Press. Alme´cija, A., Alba, D. M. & Moya`-Sola`, S. 2009 Pierolapithecus and the functional morphology of Miocene ape hand phalanges: paleobiological and evolutionary implications. J. Hum. Evol. 57, 284– 297. (doi:10.1016/j.jhevol.2009. 02.008) Berillon, G. 2000 Le Pied des Hominoı¨des Mioce`nes et des Hominides Fossiles. Paris, France: E´ditions du CRNS. Bojsen-Møller, F. 1979 Calcaneocuboid joint and stability of the longitudinal archof the foot at high and low gear push off. J. Anat. 129, 165–176. Bradley, B. J. 2008 Reconstructing phylogenies and phenotypes: a molecular view of human evolution. J. Anat. 212, 337 –353. (doi:10.1111/j.1469-7580.2007.00840.x) Bramble, D. M. & Lieberman, D. L. 2004 Endurance running and the evolution of Homo. Nature 432, 345 –352. (doi:10.1038/nature03052) Buchner, H., Savelberg, H., Schamhardt, H. & Barneveld, A. 1997 Inertial properties of Dutch Warmblood horses. J. Biomech. 30, 653 –658. (doi:10.1016/S00219290(97)00005-5) Caravaggi, P., Pataky, T. C., Goulermas, J. Y., Savage, R. & Crompton, R. H. 2009 A dynamic model of the windlass mechanism of the foot: evidence for early stance phase

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Arboreal origins of hominin bipedalism preloading of the plantar aponeurosis. J. Exp. Biol. 212, 2491– 2499. (doi:10.1242/jeb.025767) Carey, T. S. & Crompton, R. H. 2005 The metabolic costs of ‘bent hip, bent knee’ walking in humans. J. Hum. Evol. 48, 25–44. (doi:10.1016/j.jhevol.2004.10.001) Carrier, D. R., Heglund, N. C. & Earls, K. D. 1994 Variable gearing during locomotion in the human musculoskeletal system. Science 265, 651 –653. (doi:10.1126/science. 8036513) Channon, A. J., Gu¨nther, M. M., Crompton, R. H. & Vereecke, E. E. 2009 Mechanical constraints on the functional morphology of the gibbon hind limb. J. Anat. 215, 383–400. (doi:10.1111/j.1469-7580.2009.01123.x) Cheng, H., Obergefell, L. & Rizer, A. 1994 Generator of body data (GEBOD) manual. Report no. AL/CF-TR-19940051, Armstrong Lab, Wright-Patterson Air Force Base. Clarke, R. J. 1999 Discovery of a complete arm and hand of the 3.3 million-year-old Australopithecus skeleton from Sterkfontein. S. Afr. J. Sci. 95, 477 –480. Clarke, R. J. 2002 Newly revealed information on the Sterkfontein Member 2 Australopithecus skeleton from Sterkfontein. S. Afr. J. Sci. 98, 523 –526. Crompton, R. H., Li, Y., Wang, W., Gu¨nther, M. M. & Savage, R. 1998 The mechanical effectiveness of erect and ‘bent-hip, bent-knee’ bipedal walking in Australopithecus afarensis. J. Hum. Evol. 35, 55–74. (doi:10.1006/jhev.1998.0222) Crompton, R. H. et al. 2003 The biomechanical evolution of erect bipedality. Cour. Forsch.-Inst. Senckenberg 243, 115 –126. Crompton, R. H., Vereecke, E. E. & Thorpe, S. K. S. 2008 Locomotion and posture from the common hominoid ancestor to fully modern hominins with special reference to the common panin/hominin ancestor. J. Anat. 212, 501 –543. (doi:10.1111/j.1469-7580.2008.00870.x) Culotta, E. 2004 Spanish fossil sheds new light on the oldest Great apes. Science 306, 1273– 1274. Dainton, M. & Macho, G. A. 1999 Did knuckle walking evolve twice? J. Hum. Evol. 36, 171–194. (doi:10.1006/ jhev.1998.0265) D’Aouˆt, K., Pataky, T. C., De Clercq, D. & Aerts, P. 2009 The effects of habitual footwear use: foot shape and function in native barefoot walkers. Footwear Science 1, 81–94. Darwin, C. 1871 The descent of man and selection in relation to sex. London, UK: John Murray. Degabriele, R. & Dawson, T. J. 1979 Metabolism and heat balance in an arboreal marsupial, the koala (Phascolarctos cinereus). J. Comp. Physiol. B 134, 293–301. (doi:10.1007/ BF00709996) DeSilva, J. M. 2009 Functional morphology of the ankle and the likelihood of climbing in early hominins. Proc. Natl Acad. Sci. USA 106, 6567 –6572. (doi:10.1073/pnas. 0900270106) Doran, D. M. 1996 The comparative positional behaviour of the African apes. In Great ape societies (eds W. McGrew & T. Nishida), pp. 213–224. Cambridge, UK: Cambridge University Press. Dunsworth, H., Challis, J. H. & Walker, A. 2003 Throwing and bipedalism: a new look at an old idea. Cour. Forsch.Inst. Senckenberg 243, 105 –110. Filler, A. 2007 Homeotic evolution in the Mammalia: diversification of Therian axial seriation and the morphogenetic basis of human origins. PLoS ONE 2, 10, e1019. (doi:10.1371/journal.pone.0001019) Fleagle, J. G. 1998 Primate adaptation and evolution. New York, NY: Elsevier. Fleagle, J. G., Stern, J. T., Jungers, W. L., Susman, R. L., Vangor, A. K. & Wells, J. P. 1981 Climbing: a biomechanical link with brachiation and with bipedalism. Symp. Zool. Soc. Lond. 48, 359 –375. Phil. Trans. R. Soc. B (2010)

R. H. Crompton et al.

3311

Gebo, D. L. 1992 Plantigrady and foot adaptation in African apes: implications for hominid origins. Am. J. Phys. Anthropol. 89, 29–58. (doi:10.1002/ajpa.1330890105) Gebo, D. L. 1996 Climbing, brachiation, and terrestrial quadrupedalism: historical precursors of hominid bipedalism. Am. J. Phys. Anthropol. 101, 55–92. (doi:10.1002/(SICI)1096-8644(199609)101:1,55::AIDAJPA5.3.0.CO;2-C) Gefen, A. 2003 The in vivo elastic properties of the plantar fascia during the contact phase of walking. Foot Ankle Int. 24, 238–244. Goodall, J. 1998 Through a window: my thirty years with the chimpanzees of Gombe. Boston, MA: Houghton Mifflin. Harcourt-Smith, W. E. H. & Aiello, L. C. 2004 Fossils, feet and the evolution of human bipedal locomotion. J. Anat. 204, 403–416. (doi:10.1111/j.0021-8782.2004.00296.x) Hicks, J. H. 1954 The mechanics of the foot. II. The plantar aponeurosis and the arch. J. Anat. 88, 25–30. Hildebrand, M. 1995 Analysis of vertebrate structure. New York, NY: Wiley. Hunt, K. D. 1992 Positional behavior of Pan troglodytes in the Mahale Mountains and Gombe Stream National Parks, Tanzania. Am. J. Phys. Anthropol. 87, 83–105. (doi:10. 1002/ajpa.1330870108) Hunt, K. D. 2004 The special demands of great ape locomotion and posture. In The evolution of thought: evolutionary origins of great ape intelligence (eds A. E. Russon & D. R. Begun), pp. 172– 189. Cambridge, UK: Cambridge University Press. Isler, K. 2002 Characteristics of vertical climbing in African apes. Senckenbergiana Lethaea 82, 115–124. (doi:10. 1007/BF03043777) Isler, K. 2003 Aspects of vertical climbing in gorillas. Cour. Forsch-Inst. Senckenberg 243, 71–78. Isler, K. & Thorpe, S. K. S. 2003 Gait parameters in vertical climbing of captive, rehabilitant and wild Sumatran orang-utans (Pongo pygmaeus abelii ). J. Exp. Biol. 206, 4081–4096. (doi:10.1242/jeb.00651) Isler, K., Payne, R. C., Gu¨nther, M. M., Thorpe, S. K. S., Li, Y., Savage, R. & Crompton, R. H. 2006 Inertial properties of hominoid limb segments. J. Anat. 209, 201–218. (doi:10.1111/j.1469-7580.2006.00588.x) Jungers, W. L., Harcourt-Smith, W. E. H., Wunderlich, R. E., Tocheri, M. W., Larson, S. G., Sutikna, T., Rhokus Awe Due & Morwood, M. J. 2009 The foot of Homo floresiensis. Nature 459, 81– 84. (doi:10.1038/ nature07989) Keith, A. 1903 The extent to which the posterior segments of the body have been transmuted and suppressed in the evolution of man and related primates. J. Anat. Physiol. 37, 18–40. Keith, A. 1923 Man’s posture: its evolution and disorders. Br. Med. J. 1, 451 –454, 499 –502, 545–548, 587– 590, 624–626, 669 –672. (doi:10.1136/bmj.1.3246.451) Ker, R. F., Bennet, M. B., Bibby, S. R., Kester, R. C. & Alexander, R. McN. 1987 The spring in the arch of the human foot. Nature 325, 147 –149. (doi:10.1038/ 325147a0) Kirkpatrick, R. C., Gu, H. J. & Zhou, X. P. 1999 A preliminary report on Sichuan snub-nosed monkeys (Rhinopithecus roxellana) at Baihe nature reserve. Folia Primatol. 70, 117 –120. (doi:10.1159/000021683) Kivell, T. L. & Begun, D. R. 2007 Frequency and timing of scaphoid-centrale fusion in hominoids. J. Hum. Evol. 52, 321–340. (doi:10.1016/j.jhevol.2006.10.002) Kivell, T. L. & Schmitt, D. 2009 Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor. Proc. Natl Acad. Sci. USA 106, 14 241–14 246. (doi:10.1073/pnas. 0901280106)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3312

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

Ko¨hler, M. & Moya`-Sola`, S. 1997 Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. Proc. Natl Acad. Sci. USA 94, 11 747 –11 750. (doi:10.1073/pnas.94.21.11747) Kramer, P. A. 1999 Modeling the locomotor energetics of extinct hominids. J. Exp. Biol. 202, 2807–2818. Kramer, P. A. & Eck, G. G. 2000 Locomotor energetics and leg length in hominid bipedality. J. Hum. Evol. 38, 651 –666. (doi:10.1006/jhev.1999.0375) Lahm, A. A. 1986 Diet and habitat preference of Mandrillus sphinx in Gabon: implications of foraging strategy. Am. J. Primatol. 11, 9–26. (doi:10.1002/ajp. 1350110103) Larson, S. G. 1998 Parallel evolution in the hominoid trunk and forelimb. Evol. Anthropol. 6, 87– 89. (doi:10. 1002/(SICI)1520-6505(1998)6:3,87::AID-EVAN3.3.0. CO;2-T) Lewis, O. J. 1980 The joints of the evolving foot part II, the intrinsic joints. J. Anat. 131, 275 –298. Li, Y. 2001 The seasonal diet of the Sichuan snub-nosed monkey (Pygathrix roxellana) in Shennongjia Nature Reserve, China. Folia Primatol. 72, 40–43. (doi:10. 1159/000049919) Li, Y., Wang, W., Crompton, R. H. & Gunther, M. M. 2001 Free vertical moments and transverse forces in human walking and their role in relation to arm-swing. J. Exp. Biol. 204, 47–58. Li, Y., Stanford, C. B. & Yang, Y. 2002 Winter feeding tree choice in Sichuan snub-nosed monkeys (Rhinopithecus roxellanae) in Shennongjia Nature Reserve, China. Int. J. Primatol. 23, 657 –675. Lichtwark, G. A. & Wilson, A. M. 2006 Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion. J. Exp. Biol. 209, 4379–4388. (doi:10.1242/jeb.02434) Lichtwark, G. A. & Wilson, A. M. 2007 Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? J. Biomech. 40, 1768–1775. (doi:10.1016/j.jbiomech.2006.07.025) Lichtwark, G. A. & Wilson, A. M. 2008 Optimal muscle fascicle length and tendon stiffness for maximising gastrocnemius efficiency during human walking and running. J. Theor. Biol. 252, 662 –673. (doi:10.1016/j. jtbi.2008.01.018) Lovejoy, C. O., Latimer, B., Suwa, G., Asfaw, B. & White, T. D. 2009a Combining prehension and propulsion: the foot of Ardipithecus ramidus. Science 326, 72e1–72e8. (doi:10.1126/science.1175832) Lovejoy, C. O., Simpson, S. W., White, T. D., Asfaw, B. & Suwa, G. 2009b Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326, 70e1–70e8. (doi:10.1126/science. 1175827) Lovejoy, C. O., Suwa, G., Simpson, S. W., Matternes, J. H. & White, T. D. 2009c The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326, 100–106. (doi:10.1126/science. 1175833) MacLatchy, L., Gebo, D., Kityo, R. & Pilbeam, D. 2000 Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion. J. Hum. Evol. 39, 159 –183. (doi:10. 1006/jhev.2000.0407) Madar, S. I., Rose, M. D., Kelley, J., MacLatchy, L. & Pilbeam, D. 2002 New Sivapithecus postcranial specimens from the Siwaliks of Pakistan. J. Hum. Evol. 42, 705 –752. (doi:10.1006/jhev.2002.0554) Meldrum, D. J. 1993 On plantigrady and quadrupedalism. Am. J. Phys. Anthropol. 91, 379–385. (doi:10.1002/ajpa. 1330910310) Phil. Trans. R. Soc. B (2010)

Morton, D. J. 1922 Evolution of the human foot I. Am. J. Phys. Anthropol. 5, 305 –336. (doi:10.1002/ajpa. 1330050409) Moya`-Sola`, S. & Ko¨hler, M. 1996 The first Dryopithecus skeleton: origins of great-ape locomotion. Nature 379, 156 –159. (doi:10.1038/379156a0) Moya`-Sola`, S., Ko¨hler, M. & Rook, L. 1999 Evidence of a hominid-like precision grip capability in the hand of the Miocene ape Oreopithecus. Proc. Natl Acad. Sci. USA 96, 313 –317. (doi:10.1073/pnas.96.1.313) Moya`-Sola`, S., Ko¨hler, M., Alba, D. M., Casanovas-Vilar, I. & Galindo, J. 2004 Pierolapithecus catalaunicus, a new Middle Miocene great ape from Spain. Science 306, 1339–1344. (doi:10.1126/science.1103094) Nagano, A., Umberger, B. R., Marzke, M. W. & Gerritsen, K. G. M. 2005 Neuromusculoskeletal computer modeling and simulation of upright, straight-legged, bipedal locomotion of Australopithecus afarensis (A.L. 288-1). Am. J. Phys. Anthropol. 126, 2 –13. (doi:10.1002/ajpa. 10408) Oishi, M., Ogihara, N., Endo, H., Ichihara, N. & Asari, M. 2009 Dimensions of forelimb muscles in orangutans and chimpanzees. J. Anat. 215, 373 –382. (doi:10.1111/j. 1469-7580.2009.01125.x) Pataky, T. C., Caravaggi, P., Savage, R., Parker, D., Goulermas, J. Y., Sellers, W. I. & Crompton, R. H. 2008 New insights into the plantar pressure correlates of walking speed using pedobarographic statistical parametric mapping (pSPM). J. Biomech. 41, 1987–1994. (doi:10.1016/j.jbiomech.2008.03.034) Payne, R. C., Crompton, R. H., Isler, K., Savage, R., Vereecke, E. E., Gu¨nther, M. M., Thorpe, S. K. S. & D’Aouˆt, K. 2006a Morphological analysis of the hindlimb in apes and humans. I. Muscle architecture. J. Anat. 208, 709 –724. (doi:10.1111/j.1469-7580.2006. 00563.x) Payne, R. C., Crompton, R. H., Isler, K., Savage, R., Vereecke, E. E., Gu¨nther, M. M., Thorpe, S. K. S. & D’Aouˆt, K. 2006b Morphological analysis of the hindlimb in apes and humans. II. Moment arms. J. Anat. 208, 725 –742. (doi:10.1111/j.1469-7580.2006. 00564.x) Pierrynowski, M. R. 1995 Analytical representation of muscle line of action and geometry. In Three-dimensional analysis of human movement (eds P. Allard, I. A. F. Stokes & J. P. Blanch), pp. 215 –256. Champaign, IL: Human Kinetic Publishers. Pontzer, H. & Wrangham, R. W. 2004 Climbing and the daily energy cost of locomotion in wild chimpanzees: implications for hominoid locomotor evolution. J. Hum. Evol. 46, 315– 333. (doi:10.1016/j.jhevol.2003. 12.006) Remis, M. 1994 Feeding ecology and positional behavior of western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic. PhD thesis, Yale University, New Haven, CT. Remis, M. 1995 Effects of body size and social context on the arboreal activities of lowland gorillas in the Central African Republic. Am. J. Phys. Anthropol. 97, 413–433. (doi:10.1002/ajpa.1330970408) Richmond, B. G. & Strait, D. S. 2000 Evidence that humans evolved from a knuckle-walking ancestor. Nature 404, 382 –385. (doi:10.1038/35006045) Richmond, B. G. & Jungers, W. L. 2008 Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319, 1662–1665. (doi:10.1126/ science.1154197) Richmond, B. G., Begun, D. R. & Strait, D. S. 2001 Origin of human bipedalism: the knuckle-walking hypothesis revisited. Yrbk. Phys. Anthropol. 44, 70–105.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Arboreal origins of hominin bipedalism Rowe, N. 1996 The pictorial guide to the living primates. Charlestown, RI: Pogonias Press. Sayers, K. & Lovejoy, C. O. 2008 The chimpanzee has no clothes. Curr. Anthropol. 49, 87–114. (doi:10.1086/ 523675) Schaller, G. B. 1963 The mountain gorilla. Chicago, IL: University of Chicago Press. Schmitt, D. 1999 Compliant walking in primates. J. Zool. (Lond.) 248, 149– 160. (doi:10.1111/j.1469-7998.1999. tb01191.x) Schultz, A. H. 1936 Characters common to higher primates and characters specific for man. Quart. Rev. Biol. 11, 259 –283, 425 –455. Sellers, W. I. & Manning, P. L. 2007 Estimating dinosaur maximum running speeds using evolutionary robotics. Proc. R. Soc. B 274, 2711–2716. (doi:10.1098/rspb. 2007.0846) Sellers, W. I., Dennis, L. A. & Crompton, R. H. 2003 Predicting the metabolic energy costs of bipedalism using evolutionary robotics. J. Exp. Biol. 206, 1127– 1136. (doi:10.1242/jeb.00205) Sellers, W. I., Dennis, L. A., Wang, W. & Crompton, R. H. 2004 Evaluating alternative gait strategies using evolutionary robotics. J. Anat. 204, 343– 351. (doi:10. 1111/j.0021-8782.2004.00294.x) Sellers, W. I., Cain, G., Wang, W. J. & Crompton, R. H. 2005 Stride lengths, speed and energy costs in walking of Australopithecus afarensis: using evolutionary robotics to predict locomotion of early human ancestors. J. R. Soc. Interface 2, 431 –442. (doi:10.1098/rsif.2005. 0060) Sellers, W. I., Pataky, T. C., Caravaggi, P. & Crompton, R. H. 2010 Evolutionary robotic approaches in primate gait analysis. Int. J. Primatol. 31, 321–338. (doi:10. 1007/s10764-010-9396-4) Senut, B., Pickford, M., Gommery, D., Mein, P., Cheboi, K. & Coppens, Y. 2001 First hominid from the Miocene (Lukeino formation, Kenya). CR. Acad. Sci. Paris Ser. IIA 332, 137–144. Sockol, M. D., Raichlen, A. & Pontzer, H. 2007 Chimpanzee locomotor energetics and the origin of bipedalism. Proc. Natl Acad. Sci. USA 104, 12 265 –12 266. (doi:10. 1073/pnas.0703267104) Stern, J. T. & Susman, R. L. 1993 The locomotor anatomy of Australopithecus afarensis. Am. J. Phys. Anthropol. 60, 279 –317. (doi:10.1002/ajpa.1330600302) Susman, R. L. 1984 The locomotor behavior of Pan paniscus in the Lomako forest. In The Pygmy Chimpanzee (ed. R. L. Susman), pp. 369 –394. New York, NY: Plenum Press. Tansey, P. A. & Briggs, P. J. 2001 Active and passive mechanisms in the control of heel supination. Foot Ankle Surg. 7, 131 –136. (doi:10.1046/j.1460-9584.2001. 00264.x) Thorpe, S. K. S. & Crompton, R. H. 2005 The locomotor ecology of wild orangutans (Pongo pygmaeus abelii) in the Gunung Leuser Ecosystem, Sumatra, Indonesia: a multivariate analysis using log-linear modelling. Am. J. Phys. Anthropol. 127, 58–78. (doi:10.1002/ajpa. 20151) Thorpe, S. K. S. & Crompton, R. H. 2006 Orang-utan positional behavior and the nature of arboreal locomotion in Hominoidea. Am. J. Phys. Anthropol. 131, 384–401. (doi:10.1002/ajpa.20422) Thorpe, S. K. S., Crompton, R. H., Gunther, M. M., Ker, R. F. & Alexander, R. M. cN. 1999 Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees (Pan troglodytes). Am. J. Phys. Anthropol. 110, 179–199. (doi:10.1002/(SICI)10968644(199910)110:2,179::AID-AJPA5.3.0.CO;2-Z)

Phil. Trans. R. Soc. B (2010)

R. H. Crompton et al.

3313

Thorpe, S. K. S., Crompton, R. H. & Alexander, R. M. cN. 2007a Orangutans use compliant branches to lower the energetic cost of locomotion. Biol. Lett. 3, 253 –256. (doi:10.1098/rsbl.2007.0049) Thorpe, S. K. S., Holder, R. L. & Crompton, R. H. 2007b Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316, 1328– 1331. (doi:10.1126/science.1140799) Thorpe, S. K. S., Hodder, R. & Crompton, R. H. 2009 Orangutans employ unique strategies to control branch flexibility. Proc. Natl Acad. Sci. USA 106, 12 646 – 12 651. (doi:10.1073/pnas.0811537106) Tuttle, R. H. & Watts, D. P. 1985 The positional behavior and adaptive complexes of Pan gorilla. In Primate morphophysiology, locomotor analysis and human bipedalism (ed. S. Kondo), pp. 261–288. Tokyo, Japan: Tokyo University Press. Tuttle, R. H., Butzer, K. W. & Blumenberg, B. 1974 Darwin’s apes, dental apes, and the descent of man: normal science in evolutionary anthropology. Curr. Anthropol. 15, 389– 426. (doi:10.1086/201494) Vereecke, E. E., D’Aout, K., De Clercq, D., Van Elsacker, L. & Aerts, P. 2003 Dynamic plantar pressure distribution during terrestrial locomotion of Bonobos (Pan paniscus). Am. J. Phys. Anthropol. 120, 373–383. (doi:10.1002/ajpa. 10163) Vereecke, E. E., D’Aouˆt, K., De Clercq, D., Van Elsacker, L. & Aerts, P. 2005 Functional analysis of the gibbon foot during terrestrial bipedal walking: plantar pressure distributions and 3D ground reaction forces. Am. J. Phys. Anthropol. 128, 659–669. (doi:10.1002/ajpa.20158) Vereecke, E. E., D’Aouˆt, K. & Aerts, P. 2006a Speed modulation in hylobatid bipedalism: a kinematical analysis. J. Hum. Evol. 51, 513 –526. (doi:10.1016/j.jhevol.2006. 07.005) Vereecke, E. E., D’Aouˆt, K. & Aerts, P. 2006b The dynamics of hylobatid bipedalism: evidence for an energy-saving mechanism? J. Exp. Biol. 209, 2829–2838. (doi:10. 1242/jeb.02316) Vogel, S. 2003 Comparative biomechanics, life’s physical world. Princeton, NJ: Princeton University Press. Wang, W. J. & Crompton, R. H. 2004 The role of load-carrying in the evolution of modern body proportions. J. Anat. 204, 417–430. (doi:10.1111/j.0021-8782.2004.00295.x) Wang, W. J., Crompton, R. H., Li, Y. & Gu¨nther, M. M. 2003 Energy transformation during erect and benthip-bent-knee walking by humans with implications for the evolution of bipedalism. J. Hum. Evol. 44, 563– 580. (doi:10.1016/S0047-2484(03)00045-9) Wang, W. J., Crompton, R. H., Carey, T. C., Gu¨nther, M. M., Li, Y., Savage, R. & Sellers, W. I. 2004 Comparison of inverse-dynamics musculo-skeletal models of AL 288-1 Australopithecus afarensis and KNM-WT 15000 Homo ergaster to modern humans, with implications for the evolution of bipedalism. J. Hum. Evol. 47, 453– 478. (doi:10.1016/j.jhevol.2004.08.007) Ward, C. V., Leakey, M. G., Brown, B., Brown, F., Harris, H. & Walker, A. 1999 South Turkwel: a new Pliocene hominid site in Kenya. J. Hum. Evol. 36, 69–95. (doi:10.1006/jhev.1998.0262) Washburn, S. L. 1967 Behaviour and the origin of man (The Huxley Memorial Lecture 1967). Proc. Roy. Anthropol. Inst. Great Brit. Ireland, pp. 21–27. Watson, J. C. & Wilson, A. M. 2007 Muscle architecture of biceps brachii, triceps brachii and supraspinatus in the horse. J. Anat. 210, 32–40. (doi:10.1111/j.1469-7580. 2006.00669.x) Watson, J., Payne, R., Chamberlain, A., Jones, R. & Sellers, W. I. 2009 The kinematics of load carrying in humans

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3314

R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

and great apes: implications for the evolution of human bipedalism. Folia Primatol. 80, 309–328. (doi:10.1159/ 000258646) Wareing, K., Tickle, P. G., Stokkan, K.-A., Codd, J. R. & Sellers, W. I. Submitted. The musculoskeletal anatomy of the reindeer (Rangifer tarandus): fore- and hindlimb. Williams, S. B., Payne, R. C. & Wilson, A. M. 2007 Functional specialisation of the pelvic limb of the hare (Lepus europeus). J. Anat. 210, 472 –490. (doi:10.1111/j.14697580.2007.00704.x)

Phil. Trans. R. Soc. B (2010)

Williams, S. B., Wilson, A. M., Rhodes, L., andrews, J. & Payne, R. C. 2008 Functional anatomy and muscle moment arm of the pelvic limb of an elite sprinting athlete, the racing greyhound (Canis familiaris). J. Anat. 213, 361 –372. (doi:10.1111/j.1469-7580.2008.00961.x) Winter, D. A. 1990 Biomechanics and motor control of human movement. New York, NY: John Wiley and Sons. Zihlman, A. L., Cronin, J. E., Cramer, D. L. & Sarich, V. M. 1978 Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and gorillas. Nature 275, 744–746. (doi:10.1038/275744a0)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3315–3321 doi:10.1098/rstb.2010.0069

Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction Michel Brunet1,2, * 1

Colle`ge de France, Chaire de Pale´ontologie Humaine, F75231 Paris Cedex 05, France Institut International de Pale´oprimatologie et Pale´ontologie Humaine, IPHEP UMR 6046 CNRS/Universite´ de Poitiers, F86022 Poitiers Cedex, France

2

The idea of an evolutionary sequence for humans is quite recent. Over the last 150 years, we have discovered unexpected ancestors, numerous close relatives and our deep evolutionary roots in Africa. In the last decade, three Late Miocene hominids have been described, two about 6 Ma (Ardipithecus and Orrorin) in East Africa and the third dated to about 7 Ma (Sahelanthropus) in Central Africa. The specimens are too few to propose definite relationship to other species, but clearly these belong to a new evolutive grade distinct from Australopithecus and Homo. Moreover, all of them were probably habitual bipeds and lived in woodlands, thus falsifying the savannah hypothesis of human origins. In light of all this recent knowledge, Charles Darwin predicted correctly in 1871 that Africa is the birthplace of humans, chimpanzees and our close relatives. Keywords: earliest hominids; central Africa; evolutionary grade; woodland origin 1. INTRODUCTION Who our ancestors were, and when and how they arose, are questions that are always topical. The notion of fossil humans is quite recent: the first Neanderthal specimen from the Neander Valley of Germany was first described only in 1856 (Fuhlrott 1859, 1865) and Darwin’s masterpiece ‘On the Origin of Species’ only published in the middle of the nineteenth century (Darwin 1859). By the 1980s early hominids were known just from south and east Africa (figure 1). But from 1994 in the Djurab desert of Northern Chad the M.P.F.T.1 unearthed successively a new australopithecine dated to 3.5 Ma (Brunet et al. 1995; Lebatard et al. 2008), Australopithecus bahrelghazali (Brunet et al. 1996; figure 2), the first ever found west of the Rift Valley; and a new hominid, Sahelanthropus tchadensis (Brunet et al. 2002a,b), from the Late Miocene (figures 3 – 6), dated to 7 Ma (Vignaud et al. 2002; Lebatard et al. 2008). This earliest known hominid is a new milestone suggesting that an exclusively southern or eastern African distribution of the early hominids is unlikely to be correct. And so in the last 15 years our roots have been shown to be deeper, from the Lower Pliocene (4.4 Ma) to the Late Miocene (7 Ma), with three new species: Ardipithecus kadabba (Haile-Selassie 2001; Haile-Selassie & Woldegabriel 2009; 5.2–5.8 Ma, Middle Awash, Ethiopia), Orrorin tugenensis (Senut et al. 2001; ca 6 Ma, Lukeino, Kenya) and, the earliest one, S. tchadensis (Brunet et al. 2002a,b; 7 Ma, Chad). Sahelanthropus tchadensis (figures 3– 6) displays a unique combination of plesiomorphic and apomorphic characters that clearly illustrate its hominid affinities *[email protected], [email protected] One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

temporally close to the last common ancestor of chimpanzees and humans, and also that it cannot be related to chimpanzees or gorillas (Brunet et al. 2002a,b, 2004, 2005; Vignaud et al. 2002; Guy et al. 2005; Zollikofer et al. 2005; Brunet 2006, 2009a,b; Lebatard et al. 2008). In Chad, the Late Miocene sedimentological and palaeobiological data are consistent with mosaic landscapes probably very similar to the present Okavango Delta (Central Kalahari, Bostwana; Brunet et al. 2005). As with the other Late Miocene hominids, S. tchadensis represents a new evolutionary grade (Brunet 2009b), surely a habitual biped with its usual habitat probably a wooded one. So, now, it is completely clear that the earliest hominids are not dependent on savannah and were not living just in south and east Africa. Accordingly, this early hominid history enlightens the Charles Darwin prediction of 1871 (Darwin 1871) and must be reconsidered from a completely new viewpoint.

2. A NEW STORY . . . WEST OF THE RIFT VALLEY In the 1980s, the distribution of hominid remains in Africa, with the earliest being in east Africa (Ethiopia and Tanzania) (figure 1), led Coppens (1983) to propose an ‘East Side Story’ scenario in which early hominids appeared and evolved in the Pliocene primary savannah east of the Rift Valley, while the tropical forest, west of the Rift Valley, was thought to represent the early African ape habitat. In 1994, I received a research permit from the Chadian authorities to conduct geological and palaeontological survey in the Djurab desert of northern Chad. With the M.P.F.T., one year later ( January 1995), at a site east of Koro-Toro, we found a Lower Pliocene vertebrate fauna with a partial lower jaw belonging to a new australopithecine that we nicknamed ‘Abel’, the first ever found west of the

3315

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3316

M. Brunet

Chadian hominids and Darwin’s prediction

LIBYA

NIGER

Toumaï 25

Abel

24

CHAD

SUDAN Lucy 23

NIGERIA

CAMEROON

ETHIOPIA CENTRAL AFRICAN REPUBLIC

22 21

20 19 18 16 17 14 15 13 12 KENYA 11 10 89 TANZANIA 7

45 6 SOUTH 32 AFRICA 1

Figure 1. Map of Africa showing the main Mio-Pliocene hominid localities. 1, Taung; 2, Drimolen; 3, Sterkfontein; 4, Swartkrans, 5, Kromdraai; 6, Makapansgat; 7, Malema; 8, Laetoli; 9, Olduvai; 10, Peninj; 11, Lukeino; 12, Chesowanja; 13, Lothagam; 14, Kanapoi; 15, Chemeron; 16, W. Turkana; 17, Koobi Fora; 18, Allia Bay; 19, Omo; 20, Konso; 21, Maka; 22, Aramis; 23, Hadar; 24, Koro-Toro; 25, Toros-Menalla.

Rift Valley (Brunet et al. 1995). We named it A. bahrelghazali (Brunet et al. 1996; figure 2). Other australopithecine sites have been discovered in the Koro-Toro area since 1995 (Brunet et al. 1997), all having the same fauna with mammals (proboscidians, suids, rhinocerotids and equids) indicating a biochronological age of 3.5 Ma, congruent with more recent 10beryllium cosmonuclid dating (Lebatard et al. 2008). Geological and palaeontological survey in the Djurab desert from 1994 to 1997 yielded three new fossiliferous areas, biochronologically dated to: (i) the Early Pliocene (4–4.5 Ma), at Kolle´ (Brunet et al. 1998); (ii) the Mio-Pliocene boundary (5–5.5 Ma), at Kossoum Bougoudi (Brunet et al. 2000); and (iii) the Late Miocene (ca 7 Ma), at Toros-Menalla (TM) (Brunet et al. 2002a,b). To date, more than 500 fossiliferous localities have been discovered in the Djurab desert, representing upto now around 20 000 vertebrate (mammals, reptiles, birds and fish) specimens. Phil. Trans. R. Soc. B (2010)

Figure 2. Mandible holotype specimen (KT12-95-H1) of A. bahrelghazali (Brunet et al. 1996).

In 2001, the M.P.F.T. unearthed a new hominid, S. tchadensis (Brunet et al. 2002a,b), from the locality TM 266. The holotype cranium (figure 3), nicknamed

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chadian hominids and Darwin’s prediction

Figure 3. Cranium holotype specimen (TM 266-01-060-1) of S. tchadensis (Brunet et al. 2002a,b). Scale bar, 1 cm.

M. Brunet

3317

Figure 5. Stereolithocast of the S. tchadensis cranium, threedimensional reconstruction. Scale bar, 1 cm.

Figure 4. Right lower jaw paratype specimen (TM 266-02154-1) of S. tchadensis. Scale bar, 1 cm.

‘Toumaı¨’, is associated with a fauna (more than 70 species) of which the mammalian component indicates a biochronological age estimate congruent with the 10 beryllium dating, close to 7 Ma (Vignaud et al. 2002; Lebatard et al. 2008). This earliest known hominid, S. tchadensis, unearthed at least 2600 km west of the Rift valley, is a new milestone suggesting that an exclusively eastern or southern African origin of the hominid clade is unlikely to be correct. The discovery of S. tchadensis occurred in a particular scientific context. With three new Late Miocene species, Ar. kadabba (5.2 – 5.8 Ma, Ethiopia), Or. tugenensis (ca 6 Ma, Kenya) and S. tchadensis (ca 7 Ma, Chad), our roots went deeper, from 3.6 Ma in the 1970s to about 7 Ma today. Since 1994, all these discoveries have had a scientific impact equivalent to that of Dart’s naming of Australopithecus africanus (Dart 1925). During the last 10 years the framework of the hominid evolutionary story has changed markedly. Now, we have a new understanding of the environments inhabited by early hominids, and the models established in the 1980s must be reconsidered. Potential representatives of the earliest members of the human clade are now twice as old and are shown to be spread much wider over the African continent. Moreover, the hominids described during the last 15 years, while extending the geographical and temporal limits of our family, Phil. Trans. R. Soc. B (2010)

Figure 6. Illustration of the Toumaı¨ head.

show original associations of characters and morphotypes that lead us to revise our definitions of the Hominidae per se. In fact, we have to study our evolutionary history within completely new paradigms. But, as palaeontologists and palaeoanthropologists, we have always to remember that our interpretations have, at most, a life expectancy that usually does not go beyond the next new major fossil discovery.

3. THE CHADIAN EARLY HOMINIDS The material referred to as the Chadian australopithecine ‘Abel’ is an anterior lower jaw (figure 2), with the body missing beyond the P4 level, and to a right P3. This pre-human has a new mosaic of derived and primitive anatomical characters such as: a flat mental

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3318

M. Brunet

Chadian hominids and Darwin’s prediction

surface of the lower jaw; a subvertical symphysis, bulbous in its outline with a shallow genioglossal fossa; and an incisiform and very asymmetric canine with a strong bifid lingual crest. Each premolar exhibits a three pulp canal rooting pattern and the P4s are submolariform with a large talonid. This original combination of anatomical features has been interpreted as being sufficiently distinct to name a new species: Australopithecus barhelghazali (Brunet et al. 1996). To date, only three Late Miocene species may claim the ‘enviable status’ of being among the earliest hominids. Two of them are from eastern Africa: Ar. kadabba (5.8 – 5.2 Ma, Ethiopia; Haile-Selassie 2001; Haile-Selassie et al. 2004; Haile-Selassie & Woldegabriel 2009) and Or. tugenensis (ca 6 Ma, Kenya; Senut et al. 2001; Galik et al. 2004; Ohman et al. 2005; White 2006); the third one, the oldest known hominid, is from central Africa: S. tchadensis (7 Ma, Chad; Brunet et al. 2002a,b, 2005). The geographical location of S. tchadensis, 2600 km west of the Rift Valley, along with its great antiquity, suggests an early (at least by 6 Ma) widespread hominid distribution (Sahel and eastern Africa). The material referred to as the Chadian hominid ‘Toumaı¨’ consists of a distorted but nearly complete cranium (figure 3), as reconstructed in three-dimensions (figures 5 and 6), associated with several mandibular specimens (figure 4) and isolated teeth. Sahelanthropus tchadensis displays a unique combination of primitive and derived characters. Identifiable derived features of S. tchadensis are: an anteriorly-positioned foramen magnum linked to a rather short basioccipital and a sub-horizontal nuchal plane; a downward lipping of the nuchal crest; lower jaw with a vertical symphysis with weak transverse tori; and for the dentition, the anatomical characters are: a non-honing C/P3 complex; no diastema between C and P3; small-crowned canines with a long root, the upper one without any honing distal crest and the lower one with a large distal tubercle, both shoulders being very low; a P3 with a strongly sloping buccal surface; postcanine teeth with maximum radial enamel thickness intermediate between chimpanzees and australopithecines; and bulbous, slightly crenulated postcanine occlusal morphology. It is interesting to note that all the hominid mandibular specimens from TM have the same root pattern in the postcanine teeth, with two roots and three separate pulp canals for each premolar (Brunet et al. 2002a,b, 2004, 2005; Vignaud et al. 2002; Guy et al. 2005; Zollikofer et al. 2005; Brunet 2006, 2009a,b). As known since Darwin, all these derived characters show that S. tchadensis cannot be related to an ape (chimpanzees or gorillas) but clearly suggest that it must be related to later bipedal hominids, and may be temporally close to the common ancestor of chimpanzees and humans (Brunet et al. 2002a,b, 2005; Guy et al. 2005; Zollikofer et al. 2005). Scientifically it is impossible to understand why some authors ignore these derived characters and concentrate on primitive ones to reach the conclusion that S. tchadensis is related to modern apes and even more precisely to a palaeogorilla (Wolpoff et al. 2002, 2006; Pickford 2005). This attempt to undermine the clear affinity of the Chadian hominid is curious mainly Phil. Trans. R. Soc. B (2010)

when it is coming from, among others, two who have not yet had the opportunity to check Toumaı¨ casts in their laboratory. Is it what they believe, or is it only because they want to keep Orrorin as the earliest hominid? The East Side scenario of Coppens (1983) emphasized the major role of savannah in early hominid evolution. Are the earliest known hominid environments in agreement with such a model?

4. THE LATE MIOCENE HOMINID ENVIRONMENTS AS WE KNOW THEM In Chad, the sedimentological evidence from the Late Miocene TM fossiliferous area demonstrates that, at least since 7 Ma, successive wet (mega-lake Chad events) and arid periods (desertic events) occurred. These successive events are identified by a sedimentological series comprising aeolian sandstones (desertic episode); perilacustrine sandstones (lacustrine transgression); and green pelite and diatomite (true lacustrine environment; Vignaud et al. 2002; Schuster et al. 2006). Sahelanthropus tchadensis and its associated vertebrate remains have been uncovered from the perilacustrine sandstones (Anthracotheriid Unit). Sedimentological data are in agreement with this mosaic of environments, indicating a vegetated perilacustrine belt between lake and desert (Vignaud et al. 2002). The Okavango Delta in central Kalahari (Botswana) appears to be a good modern analogue in presenting similar habitat diversity (mosaic of lacustrine and riparian waters, swamps, patches of forest, wooded savannah, grassland and desertic areas). Although the precise habitat of the TM 266 hominid among this mosaic of landscapes available is still uncertain, it was probably a wooded one (Brunet et al. 2005). Other significant hominid discoveries associated with wooded environments in Middle Awash, Ethiopia (Ardipithecus ramidus and Ar. kadabba) and Lukeino, Kenya (Or. tugenensis) also rule out the role played by an open environment or savannah in favouring the acquisition of bipedal posture in the course of hominid evolution. Thus, sedimentological and faunal data rather suggest wooded environments for Ar. ramidus (White et al. 1994; Woldegabriel et al. 1994) and Ar. kadabba (Woldegabriel et al. 2001; Haile-Selassie & Woldegabriel 2009). In 2001 those authors noted: ‘It therefore seems increasingly likely that early hominids did not frequent open habitats until after 4.4 Myr. Before that, they may have been confined to woodland and forest habitats’ (p. 177). Moreover, according to the recent description of a partial skeleton of Ar. ramidus (White et al. 1994, 2009a,b) from Aramis, Ethiopia at 4.4 Ma, it appears that this hominid may be the same new evolutionary grade as are the three late Miocene taxa. It was a climbing biped, both terrestrial and arboreal, with an opposable grasping big toe (without arched feet and walking flat-footed), living in a woodland landscape (Lovejoy 2009; Lovejoy et al. 2009a,b,c,d; Suwa et al. 2009a,b; White et al. 2009a,b). A wooded habitat (open woodland with denser stands of trees in the vicinity) has been also suggested for the Kenyan Or. tugenensis (Pickford et al. 2002).

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chadian hominids and Darwin’s prediction This is of fundamental importance since the three late Miocene taxa, Ar. kadabba, Or. tugenensis and S. tchadensis, were all probably habitual bipeds. All these Late Miocene hominids demonstrate that the savannah hypothesis is now falsified.

5. NEW PARADIGMS . . . FOR A NEW EARLY HOMINID STORY During the last 150 years, most of the models for hominid evolution have been overturned by successive discoveries. This fact obviously highlights the importance of fieldwork, as our understanding of our evolutionary story has, at most, a life expectancy that usually does not go beyond new findings. Twenty years ago, available fossil hominid remains led us to consider eastern African savannah as the cradle of mankind. Now, it appears that the earliest members of our family have favoured wooded environments, and were not restricted to eastern or southern Africa but were rather living in a wider geographical region, including at least central and eastern Africa. In the last decade, the number of recognized hominid taxa and the length of our geological roots, from 3.6 Ma in the 1970s to 7 Ma today, have doubled. These new hominids, while extending the geographical and temporal limits of our family, are Late Miocene ones with new associations of anatomical characters representing a new evolutionary grade. In Chad, the radiometrical dating of S. tchadensis indicates that the divergence between chimpanzee and human lineages occurred before 7 Ma, which is earlier than generally (Kumar & Hedges 1998; Pilbeam 2002) or more recently thought by the molecular phylogenists (Patterson et al. 2006). Besides, from a palaeobiogeographical point of view, published results derived from fieldwork show that central Africa was, at least between 3 and 7 Ma, a crossroad region marked by sporadic faunal exchanges with northern and eastern Africa (Brunet et al. 1995, 1996, 1997, 1998, 2000, 2002a,b, 2004; Brunet & White 2001; Geraads et al. 2001; Vignaud et al. 2002; Boisserie et al. 2003, 2005; Likius et al. 2003; Mackaye et al. 2005; Peigne´ et al. 2005; Lihoreau et al. 2006). Better identification of the migratory patterns and the faunal exchanges between northern, central, eastern and southern Africa during the Mio-Pliocene is a key element that is indispensable for a new understanding of the origin and dispersal of the first members of the human clade and therefore its evolutionary history. We need more data from these geographical areas and notably from north-eastern Africa (e.g. Libya, Egypt and Sudan). Finally, for a better understanding of the early human story palaeontologists and palaeoanthropologists need more data, and thus will have to conduct more and more geological and palaeontological field surveys. We especially thank the Chadian authorities (Ministe`re de l’Education Nationale de l’Enseignement Supe´rieur et de la Recherche, Universite´ de N’Djamena/Departement de Paleontologie, Center National d’Appui a` la RechercheCNAR); the Ministere Franc¸ais de l’Enseignement Phil. Trans. R. Soc. B (2010)

M. Brunet

3319

supe´rieur et de la Recherche: Universite´ de Poitiers; Agence Nationale de la Recherche—Projet ANR 05-BLAN-0235; Center National de la Recherche Scientifique (CNRS: De´partement INEE, and ECLIPSE); the Ministe`re des Affaires Etrange`res (DCSUR, Paris and Projet FSP 2005-54 de la Coope´ration FrancoTchadienne, Ambassade de France a` N’Djamena); the Re´gion Poitou-Charentes; the NSF programme RHOI (USA) and the Arme´e Franc¸aise (Mission d’Assistance Militaire and dispositif Epervier). We thank all the members of the Mission Pale´oanthropologique FrancoTchadienne, including all our friends and colleagues who participated in acquisition of the field data; G. Florent and C. Noe¨l for their administrative guidance; and X. Valentin for his technical support. A lot of thanks go to our colleagues A. Walker and E.-G. Emonet for the review and editing of our manuscript. All the drawings are due to the talent of S. Riffaut.

ENDNOTE 1

M.P.F.T.: Mission Pale´oanthropologique Franco-Tchadienne, an international scientific collaboration between Colle`ge de France, University of Poitiers, University of N’Djamena and CNAR (N’Djamena) including now more than 60 researchers from 10 countries.

REFERENCES Boisserie, J.-R., Brunet, M., Likius, A. & Vignaud, P. 2003 Hippopotamids from the Djurab Pliocene faunas, Chad, Central Africa. J. Afr. Earth Sci. 36, 15–27. (doi:10. 1016/S0899-5362(03)00021-6) Boisserie, J.-R., Likius, A., Vignaud, P. & Brunet, M. 2005 A new late Miocene hippopotamid from Toros-Menalla, Chad. J. Vert. Paleontol. 25, 665 –673. (doi:10.1671/ 0272-4634(2005)025[0665:ANLMHF]2.0.CO;2) Brunet, M. 2006 D’Abel a` Toumaı¨, Nomade Chercheur d’Os. Paris, France: Editions Odile Jacob. Brunet, M. 2009a Origine et Histoire des Hominide´s . . . Nouveaux paradigms. Paris, France: Lec¸on inaugurale du Colle`ge de France Editions Fayard. Brunet, M. 2009b Origine et e´volution des hominide´s: Toumaı¨, une confirmation e´clatante de la pre´diction de Darwin. C.R. Palevol 8, 311 –319. (doi:10.1016/j.crpv. 2008.09.007) Brunet, M. & White, T. D. 2001 Deux nouvelles espe`ces de Suini (Mammalia, Suidae) du continent African (Ethiopie; Tchad). C. R. Acad. Sci. Paris 332, 51–57. Brunet, M., Beauvillain, A., Coppens, Y., Heintz, E., Moutaye, A. H. E. & Pilbeam, D. 1995 The first australopithecine 2500 kilometres west of the Rift Valley (Chad). Nature 378, 273 –274. (doi:10.1038/378273a0) Brunet, M., Beauvillain, A., Coppens, Y., Heintz, E., Moutaye, A. H. E. & Pilbeam, D. 1996 Australopithecus bahrelghazali, une nouvelle espe`ce d’hominide´ ancien de la re´gion de Koro Toro (Tchad). C. R. Acad. Sci. Paris 322, 907–913. Brunet, M. et al. 1997 Tchad: un nouveau site a` Hominide´s Plioce`ne. C. R. Acad. Sci. Paris 324, 341 –345. Brunet, M. et al. 1998 Tchad: de´couverte d’une faune de mammife`res du Plioce`ne infe´rieur. C. R. Acad. Sci. Paris 326, 153–158. Brunet, M. et al. 2000 Chad: discovery of a vertebrate fauna close to the Mio-Pliocene boundary. J. Vert. Paleontol. 20, 205– 209. (doi:10.1671/0272-4634(2000) 020[0205:CDOAVF]2.0.CO;2) Brunet, M. et al. 2002a A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418, 145 –151. (doi:10.1038/nature00879)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3320

M. Brunet

Chadian hominids and Darwin’s prediction

Brunet, M. et al. 2002b Reply to Wolpoff M. H., Senut B., Pickford M., Hawks J. 2002 Sahelanthropus or ‘Sahelpithecus’? Nature 419, 582. (doi:10.1038/419582a) Brunet, M. et al. 2004 ‘Toumaı¨’, Mioce`ne supe´rieur du Tchad, le nouveau doyen du rameau humain. C. R. Palevol Paris 3, 275 –283. Brunet, M., Guy, F., Pilbeam, D., Lieberman, D. E., Likius, A., Mackaye, H. T., Ponce de Leon, M., Zollikofer, P. E. & Vignaud, P. 2005 New material of the earliest hominid from the Upper Miocene of Chad. Nature 434, 752–755. (doi:10.1038/nature03392) Coppens, Y. 1983 Les plus anciens fossiles d’Hominide´s. In Recent advances in the evolution of Primates, pp. 1–9. Vatican City: Pontificiae Academiae Scientiarum Scripta Varia. Dart, R. 1925 Australopithecus africanus, the man-ape of South Africa. Nature 115, 195 –199. (doi:10.1038/ 115195a0) Darwin, C. h. 1859 On the origin of species by means of natural selection. London, UK: John Murray (Reprinted, Everyman edition 1928. New York: Dutton). Darwin, C. h. 1871 The descent of man and selection in relation to sex. Princeton, NJ: Princeton University Press (Reprinted 1981). Fuhlrott, C. J. 1859 Menschliche Ueberreste aus einer Felsengrotte des Du¨sselthals. Ein Beitrag zur Frage u¨ber die Existenz fossiler Menschen. Verhanlungen des naturhistorischen Vereins der preussischen Rheinlande und Westphalens 16, 131 –153. Fuhlrott, C. J. 1865 Der fossile Mensch aus dem Neanderthal und sein Verha¨ltniß zum Alter des Menschengeschlechts. Duisburg, Germany: Kessinger Publishing (78 S 2Abb. Published 2010.) Galik, K., Senut, B., Pickford, M., Gommery, D., Treil, J., Kuperavage, A. J. & Eckhardt, R. B. 2004 External and internal morphology of the BAR 1002–00 Orrorin tugenensis femur. Science 305, 1450–1453. (doi:10.1126/ science.1098807) Geraads, D., Brunet, M., Mackaye, H. T. & Vignaud, P. 2001 Fossil Bovidae (Mammalia) from the Koro Toro Australopithecine sites, Chad. J. Vert. Paleontol. 21, 335 –346. (doi:10.1671/0272-4634(2001)021[0335: PBMFTK]2.0.CO;2) Guy, F., Lieberman, D. E., Pilbeam, D., Ponce de Leon, M., Likius, A., Mackaye, H. T., Vignaud, P., Zollikofer, C. & Brunet, M. 2005 Morphological affinities of the Sahelanthropus tchadensis (Late Miocene Hominid, Chad) cranium. Proc. Natl Acad. Sci. USA 102, 18 836 –18 841. (doi:10.1073/pnas.0509564102) Haile-Selassie, Y. 2001 Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412, 178 –181. (doi:10. 1038/35084063) Haile-Selassie, Y. & Woldegabriel, G. 2009 Ardipithecus kadabba: late Miocene evidence from the Middle Awash. Ethiopia: University of California Press. Haile-Selassie, Y., Suwa, G. & White, T. 2004 Late Miocene hominids from the Middle Awash, Ethiopia, and early hominid dental evolution. Science 303, 1503–1505. (doi:10.1126/science.1092978) Kumar, S. & Hedges, S. B. 1998 A molecular timescale for vertebrate evolution. Nature 392, 917 –919. (doi:10.1038/ 31927) Lebatard, A. E. et al. 2008 Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali Mio-Pliocene early hominids from Chad. Proc. Natl Acad. Sci. USA 105, 3226–3231. (doi:10.1073/pnas. 0708015105) Lihoreau, F., Boisserie, J. R., Viriot, L., Coppens, Y., Likius, A., Mackaye, H. T., Tafforeau, P., Vignaud, P. & Brunet, M. 2006 Anthracothere dental anatomy reveals a late Phil. Trans. R. Soc. B (2010)

Miocene Chado-Libyan bioprovince. Proc. Natl Acad. Sci. USA 103, 8763– 8767. (doi:10.1073/pnas. 0603126103) Likius, A., Brunet, M., Geraads, D. & Vignaud, P. 2003 Le plus vieux Camelidae (Mammalia, Artiodactyla) d’Afrique: limite Mio-Plioce`ne, Tchad. Bull. Soc. Ge´olologique France 174, 187 –193. (doi:10.2113/ 174.2.187) Lovejoy, C. O. 2009 Reexamining human origins in light of Ardipithecus ramidus. Science 326, 74e1–74e8. (doi:10. 1126/science.1175834) Lovejoy, C. O., Simpson, S. W., White, T. D., Asfaw, B. & Suwa, G. 2009a Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326, 70e1–70e8. (doi:10.1126/science. 1175827) Lovejoy, C. O., Suwa, G., Spurlock, L., Asfaw, B. & White, T. D. 2009b The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science 326, 71e1–71e6. (doi:10.1126/science.1175831) Lovejoy, C. O., Latimer, B., Suwa, G., Asfaw, B. & White, T. D. 2009c Combining prehension and propulsion: the foot of Ardipithecus ramidus. Science 326, 72e1–72e8. (doi:10.1126/science.1175832) Lovejoy, C. O., Suwa, G., Simpson, S. W., Matternes, J. H. & White, T. D. 2009d The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science 326, 100–106. (doi:10.1126/science. 1175833) Mackaye, H. T., Brunet, M. & Tassy, P. 2005 Selenetherium kolleensis nov. gen. nov. sp. un nouveau Proboscidea (Mammalia) dans le Plioce`ne tchadien. Ge´obios Lyon 38, 765 –777. (doi:10.1016/j.geobios.2003.09.010) Ohman, J., Lovejoy, C. O. & White, T. D. 2005 Questions about Orrorin femur. Science 307, 845. (doi:10.1126/ science.307.5711.845b) Patterson, N., Richter, D. J., Gnerre, S., Lander1, E. S. & Reich, D. 2006 Genetic evidence for complex speciation of humans and chimpanzees. Nature 441, 1103 –1108. (doi:10.1038/nature04789) Peigne´, S., de Bonis, L., Likius, A., Mackaye, H. T., Vignaud, P. & Brunet, M. 2005 New machairodontine (Carnivora, Felidae) from the Late Miocene hominid locality of Toros-Menalla, Chad. C. R. Palevol Paris 4, 243 –253. (doi:10.1016/j.crpv.2004.10.002) Pickford, M. 2005 Orientation of the foramen magnum in Late Miocene to extant African apes and hominids. Anthropol. Brno XLIII, 191 –198. Pickford, M., Senut, B., Gommery, D. & Treil, J. 2002 Bipedalism in Orrorin tugenensis revealed by its femora. C. R. Palevol Paris 1, 191 –203. (doi:10.1016/S16310683(02)00028-3) Pilbeam, D. 2002 Perspectives on the Miocene Hominoidea. In The primate fossil record (ed. W. Hartwig), pp. 303–310. Cambridge, UK: Cambridge University Press. Schuster, M., Duringer, P., Ghienne, J. F., Vignaud, P., Mackaye, H. T., Likius, A. & Brunet, M. 2006 The age of the Sahara desert. Science 311, 821. (doi:10.1126/ science.1120161) Senut, B., Pickford, M., Gommery, D., Mein, P. & Cheboi, K. 2001 First hominid from the Miocene (Lukeino formation, Kenya). C. R. Acad. Sci. Paris 332, 137–144. Suwa, G., Asfaw, B., Kono, R. T., Kubo, D., Lovejoy, C. O. & White, T. D. 2009a The Ardipithecus ramidus skull and its implications for hominid origins. Science 326, 68e1–68e7. (doi:10.1126/science.1175825) Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, C. O. & White, T. D. 2009b Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 94–99. (doi:10.1126/science.1175824)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Chadian hominids and Darwin’s prediction Vignaud, P. et al. 2002 Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418, 152–155. (doi:10.1038/nature00880) White, T. D. 2006 Early hominid femora: the inside story. C. R. Palevol Paris 5, 99–108. (doi:10.1016/j.crpv.2005. 09.006) White, T. D., Suwa, G. & Asfaw, B. 1994 Australopithecus ramidus, a new species of Early hominid from Aramis, Ethiopia. Nature 371, 306– 312. (doi:10.1038/ 371306a0) White, T. D., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, C. O., Suwa, G. & WoldeGabriel, G. 2009a Ardipithecus ramidus and the paleobiology of early hominids. Science 326, 65–86. (doi:10.1126/science.1175802) White, T. D. et al. 2009b Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 87– 93. (doi:10.1126/science.1175822) Woldegabriel, G., White, T. D., Suwa, G., Renne, P., Heinzelin, J., de Hurt, W. K. & Heiken, G. 1994

Phil. Trans. R. Soc. B (2010)

M. Brunet

3321

Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371, 330– 333. (doi:10.1038/371330a0) Woldegabriel, G., Haile-Selassie, Y., Rennek, P. R., Hart, W. K., Ambrose, S. H., Asfaw, B., Heiken, G. & White, T. 2001 Geology and palaeontology of the Late Miocene Middle Awash valley, Afar rift, Ethiopia. Nature 412, 175 – 178. (doi:10.1038/35084058) Wolpoff, M. H., Senut, B., Pickford, M. & Hawks, J. 2002 Sahelanthropus or ‘Sahelpithecus’? Nature 419, 581 –582. (doi:10.1038/419581a) Wolpoff, M. H., Hawks, J., Senut, B., Pickford, M. & Ahern, J. 2006 An ape or the ape: is the Toumaı¨ cranium TM 266 a hominid? PaleoAnthropology 2006, 36–50. Zollikofer, C., Ponce De Leon, M., Lieberman, D. E., Guy, F., Pilbeam, D., Likius, A., Mackaye, H. T., Vignaud, P. & Brunet, M. 2005 Virtual cranial reconstruction of Sahelanthropus tchadensis. Nature 434, 755–759. (doi:10. 1038/nature03397)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3323–3331 doi:10.1098/rstb.2010.0064

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia) Yohannes Haile-Selassie* Department of Physical Anthropology, The Cleveland Museum of Natural History, 1 Wade Oval Drive, Cleveland, OH 44106, USA The earliest evidence of Australopithecus goes back to ca 4.2 Ma with the first recorded appearance of Australopithecus ‘anamensis’ at Kanapoi, Kenya. Australopithecus afarensis is well documented between 3.6 and 3.0 Ma mainly from deposits at Laetoli (Tanzania) and Hadar (Ethiopia). The phylogenetic relationship of these two ‘species’ is hypothesized as ancestor– descendant. However, the lack of fossil evidence from the time between 3.6 and 3.9 Ma has been one of its weakest points. Recent fieldwork in the Woranso-Mille study area in the Afar region of Ethiopia has yielded fossil hominids dated between 3.6 and 3.8 Ma. These new fossils play a significant role in testing the proposed relationship between Au. anamensis and Au. afarensis. The Woranso-Mille hominids (3.6 – 3.8 Ma) show a mosaic of primitive, predominantly Au. anamensis-like, and some derived (Au. afarensis-like) dentognathic features. Furthermore, they show that, as currently known, there are no discrete and functionally significant anatomical differences between Au. anamensis and Au. afarensis. Based on the currently available evidence, it appears that there is no compelling evidence to falsify the hypothesis of ‘chronospecies pair’ or ancestor–descendant relationship between Au. anamensis and Au. afarensis. Most importantly, however, the temporally and morphologically intermediate Woranso-Mille hominids indicate that the species names Au. afarensis and Au. anamensis do not refer to two real species, but rather to earlier and later representatives of a single phyletically evolving lineage. However, if retaining these two names is necessary for communication purposes, the Woranso-Mille hominids are best referred to as Au. anamensis based on new dentognathic evidence. Keywords: Australopithecus afarensis; Australopithecus ‘anamensis’; phylogeny; Woranso-Mille; Ethiopia

1. INTRODUCTION The genus Australopithecus was named in the first quarter of the twentieth century (Dart 1925) and includes at least seven species from South Africa, Tanzania, Kenya, Ethiopia, and Chad (Dart 1925; Broom 1938; Leakey 1959; Arambourg & Coppens 1968; Johanson et al. 1978; Brunet et al. 1995; Asfaw et al. 1999). Some workers assign three of these species (Australopithecus boisei, Australopithecus aethiopicus and Australopithecus robustus) to a different genus, Paranthropus (Broom 1938), based largely on morphological specializations related to trophic parameters (Clarke 1977; Grine 1986, 1988; Wood & Ellis 1986; Wood & Chamberlain 1987; Turner & Wood 1993). Some palaeontologists have even moved the type species of the genus, Australopithecus africanus into Paranthropus (e.g. Cela-Conde & Altaba 2002; see also Cela-Conde & Ayala 2007), leaving Australopithecus with only three species. Whether Australopithecus is a paraphyletic (Strait et al. 1997) or monophyletic (Tobias 1967) genus, most researchers

* [email protected] One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

agree that one of its species gave rise to the genus Homo, possibly Australopithecus garhi from the Middle Awash region of Ethiopia (Asfaw et al. 1999; but see Strait & Grine 2004). It was only 30 years ago that Australopithecus afarensis was recognized as the ‘oldest indisputable evidence of the family Hominidae’ at 3.6 Ma ( Johanson et al. 1978; see Kimbel & Delezene 2009 for detailed review). However, at the end of the twentieth and beginning of the twenty-first centuries, a number of new hominid taxa were recovered, some of which are twice as old (the family Hominidae is here defined following Haile-Selassie 2001 and Haile-Selassie et al. 2004). During the 1990s, the discovery of Ardipithecus ramidus (1994, Ethiopia, 4.4 Ma; White et al. 1994, 1995; Semaw et al. 2005) was followed by Australopithecus ‘anamensis’ (1995, Kenya, 3.9 – 4.2 Ma; Leakey et al. 1995, 1998; Ward et al. 1999, 2001). More recent fieldwork in Ethiopia, Kenya and Chad have pushed the record further into the Late Miocene with the discovery of Ardipithecus kadabba (HaileSelassie 2001; Haile-Selassie et al. 2004, 2009), Orrorin tugenensis (Senut et al. 2001; Pickford et al. 2002) and Sahelanthropus tchadensis (Chad, 6–7 Ma; Brunet et al. 2002, 2005). The phylogenetic relationships among these earlier hominids remain a point of

3323

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3324

Y. Haile-Selassie

Hominids from Woranso-Mille, Ethiopia

contention (see Haile-Selassie et al. 2004, 2009, for details), and Pliocene hominid fossils are poorly sampled from the 3.6–3.9 and 4.4–5.2 Ma time intervals. The hominid-bearing Woranso-Mille palaeontological study area (WORMIL) has been explored since its discovery in 2004 (Haile-Selassie et al. 2007). The fossiliferous deposits in the north and northwestern parts of the study area sample the period between 3.4 and 3.8 Ma (Deino et al. 2010), a time frame poorly known in the hominid fossil record (Kimbel et al. 2006). These ages were determined using 40Ar/39Ar radiometric dating method (Deino et al. 2010). The study area has thus far yielded about 90 fossil hominid specimens, mostly from the time period between 3.6 and 3.8 Ma. Additional hominid specimens were collected from slightly younger (3.4 –3.6 Ma) deposits. Most of these specimens represent isolated teeth and partial jaws, although they also include a 3.58 Ma partial skeleton of Au. afarensis (Haile-Selassie et al. 2010a) and additional fragmentary postcranial remains. Moreover, a total of 4300 fossil specimens of diverse vertebrate taxa have been collected thus far, representing more than 25 mammalian genera and a number of new species. Here, a brief summary of early Australopithecus to which the WORMIL hominids belong is presented, followed by a brief description of the new hominids and their phylogenetic relationships. Finally, a discussion is presented on the evolutionary tempo and mode of early Australopithecus and the proposed ancestor – descendant relationship between Au. anamensis and Au. afarensis in light of the new fossil evidence from Woranso-Mille.

2. EARLY AUSTRALOPITHECUS The origin of the genus Australopithecus remained elusive until new discoveries from the Early Pliocene in eastern Africa began to shed some light (White et al. 2006). Based on the currently available fossil evidence, Au. anamensis is the earliest species of the genus. It is documented from deposits in Kenya and Ethiopia, dated between 4.2 and 3.9 Ma (Leakey et al. 1995, 1998; Ward et al. 2001; White et al. 2006). The integrity and amount of variation in Au. afarensis have been rigorously debated since its naming in the 1970s (Johanson et al. 1978, 1982; Johanson & White 1979; White et al. 1981, 1993, 2000; Kimbel et al. 1985, 2004; White 1985; Kimbel & White 1988; Lockwood et al. 2000; Reno et al. 2003, 2005; Plavkan et al. 2005, among others). Some argued that the species hypodigm pooled from two asynchronous and geographically disparate areas, Laetoli (Tanzania; Leakey 1987; Leakey et al. 1987) and Hadar (Ethiopia), represents more than one species (Leakey & Walker 1980; Olson 1981, 1985; Senut & Tardieu 1985; Zihlman 1985). However, the discovery of more specimens at Hadar since the early 1990s and detailed analyses of the pooled hypodigm have demonstrated that the amount of variation in Au. afarensis does not significantly exceed what is observed in a single species of extant taxa (Kimbel et al. 1985, 2004; Kimbel & White 1988; Lockwood et al. 2000; White et al. 2000). Phil. Trans. R. Soc. B (2010)

Further analysis of Au. afarensis mandibles and teeth also indicated that there was a directional trend toward an increase in mandibular size through time, but not in the size of the teeth, contributing to the larger range of variation seen in the species (Lockwood et al. 2000; see also Kimbel et al. 2004). The postcranial anatomy of Au. afarensis is inferred to indicate obligate bipedality (for example, Lovejoy 1975, 1978; White 1980a,b; Latimer 1983, 1991; Latimer & Lovejoy 1989; Kramer 1999), although some argued that it was partly arboreal (for example, Stern & Susman 1981, 1983, 1991; Jungers & Stern 1983; Stern 2000). The Laetoli footprints, however, yield incontrovertible evidence that Au. afarensis was fully bipedal (for example, White & Suwa 1987). 3. THE WORANSO-MILLE FOSSIL HOMINIDS A total of 55 hominid dentognathic (mostly isolated teeth) and fragmentary postcranial elements have been recovered from the Am-Ado (AMA), Aralee Issie (ARI), Mesgid Dora (MSD) and Makah Mera (MKM) collection areas of the WORMIL study area (figure 1). Their age has been chronometrically constrained to between 3.57 and 3.82 Ma (Deino et al. 2009). The associated faunal assemblage is dominated largely by cercopithecids, tragelaphines and aepycerotines, among others, indicating a more closed habitat with riverine gallery forest and abundant water. (a) Mandibles Two mandibular fragments were recovered from the MSD collection area. MSD-VP-5/16 is a well-preserved left mandible with M1 – 2, anteriorly broken at the I2 level. It was found during the 2006 field season from Mesgid Dora locality 5. Posteriorly, the preserved corpus extends as far as slightly posterior to the M3 level. The preserved corpus base is intact. The entire ascending ramus is missing. MSD-VP-5/ 50 is a left mandible with P3 – M3 found during the 2009 field season from Mesgid Dora locality 5. This specimen is anteriorly broken lateral to the midline. Posteriorly, part of the ascending ramus is preserved although some parts of its base below the ascending ramus are missing (figure 2). MSD-VP-5/16 probably belongs to a female individual largely owing to its small corpus size that is comparable to A.L. 128-23 (White & Johanson 1982). However, the molars (M1 – 2) in MSD-VP-5/ 16 are larger relative to the corpus dimensions. Australopithecus afarensis-like mandibular features of MSD-VP-5/16 include corpus robusticity (corpus breadth at mid-M1/corpus height at mid-M1 100) of 62.5, the presence of a lateral corpus hollow, and a more vertical mandibular symphysis, as judged from the preserved part of the anterior corpus (Haile-Selassie et al. 2010b). The mandible’s greatest anterior breadth, however, is at the canine level, more like Au. anamensis (Leakey et al. 1995; Ward et al. 1999; see Haile-Selassie et al. 2010b for details). The anterior corpus of MSD-VP-5/50 is morphologically more similar to Au. anamensis mandibles

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Y. Haile-Selassie

Hominids from Woranso-Mille, Ethiopia

3325

(a) 40°28¢0≤E

40°30¢0≤E

AMA 11°32¢0≤N

11°32¢0≤N

ARI MSD

M

MKM

illl

er

ive r

11°30¢0≤N

11°30¢0≤N

KSD

1.0

0.5

2 km

40°28¢0≤E

(b)

30

(i) Aralee Issie (ARI)

KT

fossils reworked tuff tuff

(iii) Korsi Dora (KSD)

(ii) Waki-Mille confluence (WMC) Mesgid Dora (MSD) Makah Mera (MKM)

basalt

ARI-08-5 P5

MLT?

10

30

KT WM-KSD-1&3 (mean 3.570 ± 0.014)

KT

WM-ut-1 (3.72 ± 0.03)

20

MKM-08-13

MDT

0m

MDT MKM

10

40°30¢0≤E

20

WT WM-MD-5 (3.77 ± 0.04)MDT BRT (WM07/W-1)

WT MLT BRT? MLT

MSD

10

WM-W-2 (3.76 ± 0.02)

0m

P6 P4 P2 P1

?P7 ?P8 0m

skeleton

conglomerate sandstone & pebbles, with T is tuffaceous siltstone & sandstone siltstone & claystone brown silty claystone sandstone

0m

WM-W-1 (3.82 ± 0.18)

rhyzoliths planar lamination in tuff trough-cross stratification in tuff carbonate nodules horizontal stratification desiccation cracks ripple cross-stratification tuffaceous fossiliferous reverse magnetic polarity normal magnetic polarity indeterminate magnetic polarity

bedded siltstone & sandstone laminated mudstone & sandstone

WMC

40°32¢0≤E

fault

bioturbated siltstone

Figure 1. (a) Satellite imagery showing the location of hominid collection areas in the Woranso-Mille palaeontological site. (b) Stratigraphic sections showing the provenance and age of fossiliferous horizons.

than to those of Au. afarensis (figure 3). The corpus of MSD-VP-5/50 is very deep and transversely narrow at the M1 and other molar levels. Its breadth at M1 (20.7 mm) is within the range seen in Au. afarensis (Kimbel et al. 2004) and Au. anamensis (Ward et al. 2001), whereas its height at the same position (44.6 mm) and its robusticity index (46.6) are slightly outside the range documented for both groups. Australopithecus anamensis mandibles have a mean robusticity index (53.6, n ¼ 3; Ward et al. 2001) slightly lower than that of Au. afarensis (57.5, n ¼ 19; Kimbel et al. 2004). A.L. 277-1 approaches MSDVP-5/50 in terms of its robusticity index (48.4; Kimbel et al. 2004) although the latter is absolutely deeper and wider. The inferomedial sweep of the corpus contour at the C – P4 level seen in MSD-VP-5/50 is comparable to Au. anamensis mandibles (figure 3). This lateral corpus profile has been described as uniquely characteristic of Au. anamensis mandibles such as Phil. Trans. R. Soc. B (2010)

KNM-KP 29281, KNM-KP 29287, KNM-KP 31713, and KNM-ER 20432 from Kanapoi and Allia Bay (Ward et al. 2001; Kimbel et al. 2006). Australopithecus afarensis mandibles are different in having an almost vertical contour descending as far as the corpus base. However, LH 4 is an exception to this general characteristic of most Au. afarensis mandibles, showing a slight inferomedial sweep at the C – P3 level (Kimbel et al. 2006). The ascending ramus root of MSD-VP-5/50 is positioned more posteriorly (mid-M2) with most of the M3 buccal face visible laterally. However, the canine does not appear to be aligned in the longitudinal axis of the postcanine tooth row, although it is seen in the other, much smaller mandible (MSD-VP-5/16). In Au. afarensis mandibles, the ascending ramus root is usually at M1. The overall morphology of MSD-VP-5/50, particularly the anterior lateral corpus profile, is intermediate between Kanapoi mandibles and LH 4 and serves, together with KNM-ER 20432, as a

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3326

Y. Haile-Selassie

Hominids from Woranso-Mille, Ethiopia (a)

(b)

Figure 2. Occlusal, medial and lateral views of mandibular specimens from Woranso-Mille dated at 3.7–3.8 Ma. (a) MSD-VP5/16, left mandible with M1 – 2. (b) MSD-VP-5/50, left mandible with P3 –M3. Note the size variation between the two mandibles and the deep corpus in (b). Scale bar, 5 cm.

(a)

(b)

(c)

lateral

(d)

medial

(e)

(f) sup. tr. torus

Figure 3. Cross sections of Au. anamensis and Au. afarensis mandibular corpora at distal P3. (a) KNM-KP 29281; (b) KNMER 20432; (c) MSD-VP-5/50; (d) A.L. 400-1a (right side reversed); (e) A.L. 277-1 and (f) A.L. 417-1a. Modified from Kimbel et al. (2006). Cross-section of MSD-VP-5/50 was acquired following the methods described by Kimbel et al. (2006). Scale bar, 2 cm.

good transition from Kanapoi to Laetoli/Hadar lateral mandibular corpus profiles (figure 3). These WORMIL mandibles show a mosaic of features shared with both Au. anamensis and Au. afarensis. Some of Phil. Trans. R. Soc. B (2010)

the mandibular features shared with Au. anamensis are the maximum anterior symphyseal breadth being at the canine (for example, MSD-VP-5/16; Ward et al. 1999) and the more posterior position of the ascending ramus

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Hominids from Woranso-Mille, Ethiopia (a)

(c)

Y. Haile-Selassie

3327

(b)

KNM-KP 34725

RdC

ARI-VP-1/190

LdC 0

RdC cm

A.L. 333-35

RdC 4

Figure 4. Dental remains from Woranso-Mille. (a) Occlusal (top row) and mesial (bottom row) views of ARI-VP-3/80g (LM2), ARI-VP-1/90 (LM3), ARI-VP-3/80d (LM2) and ARI-VP-1/462 (LM1). These molars show the lingual slope on upper and buccal slope on lower molars like Au. anamensis. (b) MSD-VP-5/50, ARI-VP-3/80a and ARI-VP-2/95, P3s from the Woranso-Mille showing variation in P3 occlusal crown morphology. (c) Comparison of lower deciduous canine root length relative to crown height. KNM-KP 34 725 (Au. anamensis), ARI-VP-1/190 (Woranso-Mille) and A.L. 333-35 (Au. afarensis). Like Au. anamensis, the Woranso-Mille specimen has longer root relative to the crown height compared with Au. afarensis. Image of the Au. anamensis specimen was obtained from Carol Ward and A.L. 333-35 was made from cast.

root (MSD-VP-5/50, see figure 2; Haile-Selassie et al. 2010b), which is also shared with the earlier Ar. ramidus (Suwa et al. 2009; White et al. 2009). The mandibular features shared with Au. afarensis include the presence of an incipient lateral corpus hollow (for example, MSD-VP-5/16), usually described as characteristic of this species. Judged from the preserved parts of MSDVP-5/16, the mandibular symphysis does not show the more posteroinferiorly retreating condition seen in Au. anamensis (Ward et al. 2001; Kimbel et al. 2006). However, MSD-VP-5/50 shows a more receding symphysis as seen from the transverse cross-section at the P3 level. (b) Dentition In terms of the dentition, the upper and lower molars have occlusally tapering lingual and buccal faces, respectively, a trait documented in Au. anamensis (Ward et al. 2001). As in Au. anamensis, the upper molars, particularly M2 – 3, taper distally (figure 4a). The deciduous lower canine (ARI-VP-1/190) is similar in its crown morphology to Au. afarensis specimens such as A.L. 333-35, LH 2, and DIK-1-1 from Hadar, Laetoli and Dikika, respectively (White 1977, 1980a,b; Johanson et al. 1982; Alemseged et al. 2006). However, ARI-VP-1/190 has a relatively much longer root and less lingual relief as seen in Au. anamensis (figure 4c). The known P3s from WORMIL show both Au. afarensis-like (ARI-VP-2/95) and Au. anamensis-like (ARI-VP-3/80, MSD-VP-5/50) occlusal morphology and document variation in the morphology of the P3 (figure 4b). The P3 occlusal morphology of MSD-VP5/50 is more similar to KNM-ER 20 432 from Allia Bay than to KNM-KP 27 286 from Kanapoi in its mesiodistally elongated crown and asymmetry, clearly defined mesial marginal ridge, and larger posterior fovea. The lingual cusp is also hardly developed. Enamel thickness, as measured on naturally fractured WORMIL teeth, is also within the range seen for both hypodigms. The postcranial elements are not as informative owing to their fragmentary nature. The dentognathic morphological observations, Phil. Trans. R. Soc. B (2010)

however, indicate that the WORMIL specimens are morphologically intermediate between Au. anamensis and Au. afarensis. 4. PHYLOGENETIC RELATIONSHIPS Ardipithecus ramidus from the Middle Awash and Gona study areas in Ethiopia, dated between 4.3 and 4.6 Ma (WoldeGabriel et al. 1994; Semaw et al. 2005), is considered to be the possible ancestor of Au. anamensis although other possibilities cannot be ruled out (White et al. 2006, 2009). Recent studies on a larger sample of Ar. ramidus material, including a partial skeleton, from the Middle Awash show that Ar. ramidus and Au. anamensis occupied different ‘adaptive plateaus’ (White et al. 2009). Although further investigation is imperative to understand the full implication of these adaptive differences, the ancestor–descendant relationship between these two species remains one of the alternatives given the currently available fossil evidence. The temporal distribution and apparent, but limited, morphological differences between the hypodigms currently divided into Au. afarensis and Au. anamensis justified the retention of both species names as a chronospecies pair (Leakey et al. 1995, 1998; Ward et al. 2001; Kimbel et al. 2006; White et al. 2006). However, the discovery of the WORMIL specimens dated at 3.7 – 3.8 Ma minimizes the differences between the inferred chronospecies pair and suggests that it represents a single lineage and should probably be referred to by a single species name in order to avoid taxonomic confusion. Australopithecus anamensis is interpreted to have been an obligate biped (Leakey et al. 1995, 1998; Ward et al. 2001), unlike Ar. ramidus, which was a facultative biped with substantial arboreal adaptation (Lovejoy et al. 2009). Australopithecus anamensis shares a number of derived dental characters and locomotor adaptations with Au. afarensis, and both are grouped in the same ‘adaptive plateau’ (White et al. 2009). The presence of temporal and spatial discontinuity in their fossil record, rather than observed morphological

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3328

Y. Haile-Selassie

Hominids from Woranso-Mille, Ethiopia

differences, was probably one of the apparent reasons to distinguish them at the species level. The discovery of the WORMIL hominids not only fills some part of the spatial and temporal discontinuity, but also reduces the inferred anatomical differences between the two populations. The phylogenetic relationship between the two timesuccessive ‘species’ of Au. anamensis (3.9–4.2 Ma) and Au. afarensis (3.0–3.6 Ma) has been addressed in detail using various analytical methods (Leakey et al. 1995, 1998; Ward et al. 1999, 2001; White 2002; Kimbel et al. 2006; White et al. 2006). Australopithecus anamensis is suggested to have rapidly evolved from its putative ancestor Ar. ramidus (White et al. 2006). However, this remains to be more rigorously tested, particularly in light of the new revelations about Ar. ramidus (e.g. Lovejoy et al. 2009; Suwa et al. 2009; White et al. 2009). Australopithecus anamensis and Au. afarensis are considered by most workers as a chronospecies pair sampling a single phyletically evolving lineage, although other alternatives have also been entertained (Kimbel et al. 2006; White et al. 2006). Most analytical methods have, thus far, failed to falsify the proposed ancestor– descendant relationship, or unequivocally recognize them as two distinct lineages. The Woranso-Mille hominids dated at 3.6–3.8 Ma are morphometrically intermediate between Au. afarensis and Au. anamensis. They represent the best fossil hominid sample that clearly bridges the temporal and morphological gaps between Au. afarensis and Au. anamensis, lending strong support to the suggestion that they represent a chronospecies pair (White et al. 2009). Therefore, every available line of evidence suggests that Au. anamensis represents an earlier deme of Au. afarensis. Their separation at a species level was clearly an artefact of the lack of adequate fossils from the time between Allia Bay (3.9 Ma) and Laetoli (3.6 Ma) than the presence of discrete and functionally significant anatomical characters distinguishing the two groups. Cladistic analysis on four site-samples of Au. afarensis and Au. anamensis (Hadar, Laetoli, Allia Bay and Kanapoi) demonstrated that the Au. anamensis– Au. afarensis lineage is paraphyletic because the younger Au. afarensis sample from Hadar appears to be the sister taxon of Au. africanus (Kimbel et al. 2006, p. 145). Moreover, even Au. afarensis is paraphyletic since the Laetoli sample shares some dentognathic features exclusively with Au. anamensis. The WoransoMille specimens, regardless to which group they are assigned, further demonstrate the paraphyly of not only the entire Au. afarensis– Au. anamensis lineage, but also that of Au. anamensis. Kimbel et al. (2006, p. 146) suggested that the two most preferred solutions for the taxonomic conundrum related to Au. afarensis and Au. anamensis are the ‘recognition of a single evolutionary species or the maintenance of the status quo . . .’. The evidence from Woranso-Mille strongly supports the former as the most parsimonious solution and Au. africanus as the sister taxon of this species. Haile-Selassie et al. (2010b) avoided specific assignment of the Woranso-Mille specimens to either group. Based on the dentognathic description and comparison, however, they showed that the Woranso-Mille hominids shared more dental characters with Au. Phil. Trans. R. Soc. B (2010)

anamensis than with Au. afarensis. New discoveries from the 2009 field season support this observation by yielding critical information on the anterior mandibular morphology of the Woranso-Mille hominids. The transverse profile of MSD-VP-5/50 at posterior P3 shows that the lateral mandibular corpus shape is more like those from Allia Bay and Kanapoi than like those of Au. afarensis (figure 3) shown by Kimbel et al. (2006). If the Woranso-Mille hominids dated between 3.7 and 3.8 Ma had to be assigned to one of these two arbitrary groups, they could be put into the earlier Au. anamensis with some confidence. The temporal range of Au. anamensis would then be extended to between 3.7 and 4.2 Ma. It should also be noted that Au. anamensis from Asa Issie is bracketed between 3.77 and 4.2 Ma (White et al. 2006). Although this does not result in any changes in terms of how these two groups are related to each other, it would mean that specimens such as the Belohdeli frontal (BEL-VP-1/1; Asfaw 1987), the hominid specimens from Fejej (Fleagle et al. 1991; Kappleman et al. 1996; Grine et al. 2006a,b), and teeth and femur fragment from Galili (Haile-Selassie & Asfaw 2000; Macchiarelli et al. 2004; Viola et al. 2008) should be recognized as Au. anamensis. However, this assignment would simply be based on their geological age although it gives great valence to the idea of Au. anamensis–Au. afarensis being a chronospecies pair.

5. DISCUSSION The 3.7 – 3.8 Ma WORMIL hominid specimens share a number of dental characters with both Au. afarensis and Au. anamensis. They are temporally and morphologically intermediate between the two groups and suggest that Au. anamensis and Au. afarensis do not warrant an evolutionarily meaningful distinction at the species level. The Woranso-Mille hominids clearly connect Au. anamensis and Au. afarensis regardless of which end of the continuum they belong to, and suggest that the recognition of two different species names for two temporally and morphologically continuous populations of a single phyletically evolving species is confusing and unwarranted. Following the currently available classification, the dental and mandibular morphological similarities of the WORMIL specimens (dated at 3.7 – 3.8 Ma) with Au. anamensis outweigh their similarity with Au. afarensis sensu stricto (i.e. specimens from Hadar and Laetoli). If the two names have to be retained, mainly for communication purposes as some researchers suggest, the available but limited evidence supports assignment of the WORMIL hominids to Au. anamensis, extending the temporal range of the latter group to 3.7 Ma. There is considerable size range in the relatively small WORMIL upper (n ¼ 9) and lower (n ¼ 19) molar samples although they fall within the range of both Au. anamensis and Au. afarensis. However, they also represent some of the largest molars in the entire Au. anamensis/Au. afarensis sample, particularly the M3s (for example, ARI-VP-1/90, ARI-VP-1/215). Lockwood et al. (2000) observed a statistically significant temporal trend towards an increase in M3 crown size (mainly by mesiodistal elongation) in Au. afarensis,

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Hominids from Woranso-Mille, Ethiopia although they noted that outliers (Lockwood et al. 2000) and small sample sizes (White 1985) from specific time periods could bias this observation. At the same time, an increase in M3 crown area might have been the general trend in the Au. anamensis–Au. afarensis lineage, as seen in the shift from molars with sloping buccal (lowers) and lingual (uppers) faces in Au. anamensis to molars with more vertical lingual and buccal faces in Au. afarensis, which would have resulted in an increase in overall crown occlusal surface. This increase in occlusal area would have resulted in larger chewing surface, which could be linked to an increase in trophic capability in using a wide variety of resources (Teaford & Ungar 2000; Grine et al. 2006a,b), ranging from soft fruits and leaves to harder and brittle fallback foods (Ungar 2004; Grine et al. 2006b). Although Au. afarensis was probably better fitted (largely owing to its larger molars and thicker enamel, among others) for a variety of food items including fallback resources, dental microwear analyses on a limited number of teeth fails to show differences in the dietary preferences of Au. afarensis and Au. anamensis (Grine et al. 2006a,b). However, this remains to be tested with a larger sample of Au. anamensis.

6. CONCLUSION Palaeontological fieldwork at a newly discovered fossiliferous area in the central Afar region of Ethiopia has yielded new hominid fossil remains dated between 3.4 and 3.8 Ma. The temporal placement of these fossils renders them crucial to test some of the outstanding human evolutionary hypotheses such as the phylogentic relationships between Ar. ramidus and Au. anamensis, and the issue of ancestor – descendant relationship between Au. anamensis and Au. afarensis. The 3.7 – 3.8 Ma hominid specimens from the Woranso-Mille clearly show that they are morphologically intermediate between Au. anamensis and Au. afarensis and their dental measurements overlap with both groups, lending support to the hypothesis of Au. anamensis/Au. afarensis being a chronospecies pair representing a single lineage. Regardless of what part of this ‘pair’ the Woranso-Mille hominids are assigned to, however, they document the best example of the presence of transitional populations in a single phyletically evolving hominid lineage. Slightly younger fossil hominids (3.0–3.6 Ma) not described here promise to shed some light on current debates related to early middle Pliocene hominid diversity. The Woranso-Mille palaeontological site has opened a new window into the deep human past and promises to yield more fossils relevant to answering crucial questions in human evolutionary studies, including the presence or absence of early hominid diversity during the middle Pliocene. I thank the Authority for Research and Conservation of Cultural Heritage and the National Museum of Ethiopia of the Ministry of Culture and Tourism for field and laboratory permissions and facilities, the Afar Regional Government, its local administrative units, and the Afar people of Mille District, for facilitating and directly participating in my research endeavours. I thank all of the field participants who helped find the fossils and many Phil. Trans. R. Soc. B (2010)

Y. Haile-Selassie

3329

others for discussion and access to their unpublished data. I thank Stephanie Melillo for assistance with figures and Liz Russell for photography. Finally, discussions with Bill Kimbel, Denise Su, Gen Suwa, Carol Ward and Tim White significantly improved the content of this manuscript. The WORMIL project was financially supported by National Science Foundation (NSF; grant nos 0234320, 0542037), The Leakey Foundation, Wenner-Gren Foundation, and National Geographic Society.

REFERENCES Alemseged, Z., Spoor, F., Kimbel, W. H., Bobe, R., Geraads, D., Reed, D. & Wynn, J. G. 2006 A juvenile early hominin from Dikika, Ethiopia. Nature 443, 296–301. (doi:10.1038/nature05047) Arambourg, C. & Coppens, Y. 1968 Decouverte d’un Australopithecien nouveau dans les gisements de l’Omo (Ethiopie). S. Afr. J. Sci. 64, 58–59. Asfaw, B. 1987 The Belohdelie frontal—new evidence of early hominid cranial morphology from the Afar of Ethiopia. J. Hum. Evol. 16, 611–624. (doi:10.1016/ 0047-2484(87)90016-9) Asfaw, B., White, T., Lovejoy, O., Latimer, B., Simpson, S. & Suwa, G. 1999 Australopithecus garhi: a new species of early hominid from Ethiopia. Science 284, 629–635. (doi:10. 1126/science.284.5414.629) Broom, R. 1938 The Pleistocene anthropoid apes of South Africa. Nature 142, 377 –379. (doi:10.1038/142377a0) Brunet, M., Beauvillain, A., Coppens, Y., Heintz, E., Moutaye, A. H. E. & Pilbeam, D. 1995 The first Australopithecine 2,500 kilometers west of the Rift Valley (Chad). Nature 378, 273 –275. (doi:10.1038/378273a0) Brunet, M. et al. 2002 A new hominid from the upper Miocene of Chad, central Africa. Nature 418, 145 –151. (doi:10.1038/nature00879) Brunet, M. et al. 2005 New material of the earliest hominid from the upper Miocene of Chad. Nature 434, 752 –755. (doi:10.1038/nature03392) Cela-Conde, C. & Altaba, C. 2002 Multiplying genera versus moving species: a new taxonomic proposal for the family. S. Afr. J. Sci. 98, 229– 232. Cela-Conde, C. & Ayala, F. 2007 Human evolution: trails from the past. Oxford, UK: Oxford University Press. Clarke, R. J. 1977 The cranium of the Swartkrans hominid SK 847 and its relevance to human origins. PhD dissertation, University of the Witwatersrand, Johannesburg. Dart, R. 1925 Australopithecus africanus: the man-ape of South Africa. Nature 115, 195–199. (doi:10.1038/115195a0) Deino, A., Scott, G. R., Saylor, B., Alene, M., Angelini, J. & Haile-Selassie, Y. 2010 40Ar/39Ar dating of WoransoMille: a new hominid-bearing Pliocene site in the west-central Afar Rift, Ethiopia. J. Hum. Evol. 58, 111–126. (doi:10.1016/j.jhevol.2009.11.001) Fleagle, J. G., Rasmussen, D. T., Yirga, S., Bown, T. M. & Grine, F. E. 1991 New hominid fossils from Fejej, Southern Ethiopia. J. Hum. Evol. 21, 145–152. (doi:10. 1016/0047-2484(91)90005-G) Grine, F. E. 1986 Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J. Hum. Evol. 15, 783–882. (doi:10.1016/S0047-2484(86)80010-0) Grine, F. E. 1988 New craniodental fossils of Paranthropus from the Swartkrans Formation and their significance in ‘robust’ australopithecine evolution. Evolutionary history of the ‘robust’ Australopithecines (ed. F. E. Grine), pp. 223–243. New York, NY: Aldine de Gruyter. Grine, F. E., Ungar, P. S. & Teaford, M. F. 2006a Was the early Pliocene hominin ‘Australopithecus’ anamensis a hard object feeder? S. Afr. J. Sci. 102, 301 –310.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3330

Y. Haile-Selassie

Hominids from Woranso-Mille, Ethiopia

Grine, F. E., Ungar, P. S., Teaford, M. F. & El-Zaatari, S. 2006b Molar microwear in Praeanthropus afarensis: evidence for dietary stasis through time and under diverse paleoecological conditions. J. Hum. Evol. 51, 297 –319. (doi:10.1016/j.jhevol.2006.04.004) Haile-Selassie, Y. 2001 Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412, 178 –181. (doi:10. 1038/35084063) Haile-Selassie, Y. & Asfaw, B. 2000 A newly discovered early Pliocene hominid bearing paleontological site in the Mulu Basin, Ethiopia. Am. J. Phys. Anthropol. 111, 170. Haile-Selassie, Y., Suwa, G. & White, T. D. 2004 Late Miocene teeth from Middle Awash. Ethiopia, and early hominid dental evolution. Science 303, 1503–1505. (doi:10.1126/science.1092978) Haile-Selassie, Y., Deino, A., Saylor, B., Umer, M. & Latimer, B. 2007 Preliminary geology and paleontology of new hominid-bearing Pliocene localities in the central Afar region of Ethiopia. Anthropol. Sci. 115, 215 –222. (doi:10.1537/ase.070426) Haile-Selassie, Y., Suwa, G. & White, T. D. 2009 Chapter 7: Hominidae. In Ardipithecus kadabba. Evidence from the Late Miocene of Africa (eds Y. Haile-Selassie & G. WoldeGabriel), pp. 159 –236. Berkeley, CA: University of California Press. Haile-Selassie, Y., Latimer, B., Alene, M.., Deino, A. L., Gibert, L., Melillo, S. M., Saylor, B. Z., Scott, G. R. & Lovejoy, O. C. 2010a An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia. Proc. Natl Acad. Sci. USA 107, 12 121– 12 126. (doi: 10.1073/ pnas.1004527107) Haile-Selassie, Y., Saylor, B., Deino, A., Alene, M. & Latimer, B. 2010b New hominid fossils from WoransoMille (central Afar, Ethiopia) and taxonomy of early Australopithecus. Am. J. Phys. Anthropol. 141, 406 –417. (doi:10.1002/ajpa.21159) Johanson, D. C. & White, T. D. 1979 A systematic assessment of early African hominids. Science 203, 321 –330. (doi:10.1126/science.104384) Johanson, D. C., White, T. D. & Coppens, Y. 1978 A new species of the genus Australopithecus (Primates: Hominidae) from the Pliocene of eastern Africa. Kirtlandia 28, 1–14. Johanson, D. C., White, T. D. & Coppens, Y. 1982 Dental remains from the Hadar Formation. Ethiopia: 1974– 1977 collections. Am. J. Phys. Anthropol. 57, 545 –603. (doi:10.1002/ajpa.1330570406) Jungers, W. L. & Stern, J. T. 1983 Body proportions, skeletal allometry and locomotion in the Hadar hominids: a reply to Wolpoff. J. Hum. Evol. 12, 673 –684. (doi:10.1016/ S0047-2484(83)80007-4) Kappleman, J., Swisher III, C. C., Fleagle, J. G., Yirga, S., Bown, T. M. & Feseha, M. 1996 Age of Australopithecus afarensis from Fejej, Ethiopia. J. Hum. Evol. 30, 139 – 146. (doi:10.1006/jhev.1996.0010) Kimbel, W. H. & Delezene, L. K. 2009 ‘Lucy’ Redux: a review of research on Australopithecus afarensis. Am. J. Phys. Anthropol. 52, 2–48. Kimbel, W. H. & White, T. D. 1988 Variation, sexual dimorphism and the taxonomy of Australopithecus. In Evolutionary history of the ‘robust’ Australopithecines (ed. F. E. Grine), pp. 175–192. New York, NY: Aldine de Gruyter. Kimbel, W. H., White, T. D. & Johanson, D. C. 1985 Craniodental morphology of the hominids from Hadar and Laetoli: evidence of ‘Paranthropus’ and ‘Homo’ in the mid-Pliocene of eastern Africa? In Ancestors: the hard evidence (ed. E. Delson), pp. 120–137. New York, NY: Alan R. Liss. Kimbel, W. H., Rak, Y. & Johanson, D. C. 2004 The skull of Australopithecus afarensis. New York, NY: Oxford University Press. Phil. Trans. R. Soc. B (2010)

Kimbel, W. H., Lockwood, C. A., Ward, C. V., Leakey, M. G., Rak, Y. & Johanson, D. C. 2006 Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. J. Hum. Evol. 51, 134–152. (doi:10.1016/j.jhevol.2006.02.003) Kramer, P. A. 1999 Modeling the locomotor energetics of extinct hominids. J. Exp. Biol. 202, 2807– 2818. Latimer, B. 1983 The anterior foot skeleton of Australopithecus afarensis. Am. J. Phys. Anthropol. 60, 217. Latimer, B. 1991 Locomotor adaptations in Australopithecus afarensis: the issue of arboreality. In Origine(s) de la bipe´die chez les Hominide´s (eds B. Senut & Y. Coppens), pp. 169 –176. Paris, France: CNRS. Latimer, B. & Lovejoy, C. O. 1989 The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality. Am. J. Phys. Anthropol. 78, 369– 386. (doi:10. 1002/ajpa.1330780306) Leakey, L. S. B. 1959 A new fossil skull from Olduvai. Nature 184, 491–493. (doi:10.1038/184491a0) Leakey, M. D. 1987 The Laetoli hominid remains. In Laetoli: a Pliocene site in Northern Tanzania (eds M. D. Leakey & J. M. Harris), pp. 108–109. Oxford, UK: Clarendon Press. Leakey, R. E. F. & Walker, A. C. 1980 Status of Australopithecus afarensis. Science 207, 1103–1103. (doi:10.1126/ science.207.4435.1103) Leakey, M. D., Hay, R. L., Curtis, G. H., Drake, R. E., Jakes, M. K. & White, T. D. 1976 Fossil hominids form the Laetolil Beds. Nature 262, 460–466. (doi:10.1038/ 262460a0) Leakey, M. G., Feibel, C. S., McDougall, I. & Walker, A. 1995 New four-million-year-old hominid species from Kanapoi and Allia Bay, Kenya. Nature 376, 565–571. (doi:10.1038/376565a0) Leakey, M. G., Feibel, C. S., McDougall, I., Ward, C. & Walker, A. 1998 New specimens and confirmation of an early age for Australopithecus anamensis. Nature 393, 62– 66. (doi:10.1038/29972) Lockwood, C. A., Kimbel, W. H. & Johanson, D. C. 2000 Temporal trends and metric variation in the mandibles and teeth of Australopithecus afarensis. J. Hum. Evol. 39, 23–55. (doi:10.1006/jhev.2000.0401) Lovejoy, C. O. 1975 Biomechanical perspectives on the lower limb of early hominids. In Primate functional morphology and evolution (ed. R. H. Tuttle), pp. 291 –306. Paris, France: Mouton. Lovejoy, C. O. 1978 A biomechanical review of the locomotor diversity of early hominids. In Early hominids of Africa (ed. C. Jolly), pp. 403–429. New York, NY: St. Martin’s Press. Lovejoy, C. O., Latimer, B., Suwa, G., Asfaw, B. & White, T. D. 2009 Combining prehension and propulsion: the foot of Ardipithecus ramidus. Science 326, 72e1– 72e8. Macchiarelli, R. et al. 2004 Early pliocene hominid tooth from Galili, Somali Region, Ethiopia. Coll. Anthropol. 28, 65–76. Olson, T. R. 1981 Basicranial morphology of the extant hominoids and Pliocene hominids: the new material from the Hadar Formation, Ethiopia and its significance in early human evolution and taxonomy. In Aspects of human evolution (ed. C. B. Stringer), pp. 99–128. London, UK: Taylor and Francis. Olson, T. R. 1985 Cranial morphology and systematics of the Hadar Formation hominids and ‘Australopithecus’ africanus. In Ancestors: the hard evidence (ed. E. Delson), pp. 102 –119. New York, NY: Alan R. Liss. Pickford, M., Senut, B., Gommery, D. & Treild, J. 2002 Bipedalism in Orrorin tugenensis revealed by its femora. C. R. Palevol. 1, 1 –13. (doi:10.1016/S1631-0683(02) 00011-8)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Hominids from Woranso-Mille, Ethiopia Plavkan, J. M., Lockwood, C. A., Kimbel, W. H., Lague, M. R. & Harmon, E. H. 2005 Sexual dimorphism in Australopithecus afarensis revisited: how strong is the case for a human-like patter of dimorphism? J. Hum. Evol. 48, 313– 320. (doi:10.1016/j.jhevol.2004.09.006) Reno, P. L., Meindl, R. S., McCollum, M. A. & Lovejoy, C. O. 2003 Sexual dimorphism in Australopithecus afarensis was similar to that of modern humans. Proc. Natl Acad. Sci. USA 100, 9404–9410. (doi:10.1073/pnas.1133 180100) Reno, P. L., Meindl, R. S., McCollum, M. A. & Lovejoy, C. O. 2005 The case is unchanged and remains robust: Australopithecus afarensis exhibits only moderate dimorphism. A reply to Plavkan et al. (2005). J. Hum. Evol. 49, 279 –288. (doi:10.1016/j.jhevol.2005.04.008) Semaw, S., Simpson, S. W., Quade, J., Renne, P. R., Butler, R. F., McIntosh, W. C., Levin, N., Dominguez-Rodrigo, M. & Rogers, M. 2005 Early Pliocene hominids from Gona. Nature 433, 301 –305. (doi:10.1038/nature03177) Senut, B. & Tardieu, C. 1985 Functional aspects of Plio-Pleistocene hominid limb bones: implications for taxonomy and phylogeny. In Ancestors: the hard evidence (ed. E. Delson), pp. 193–201. New York, NY: Alan R. Liss. Senut, B., Pickford, M., Gommery, D., Mein, P., Cheboi, K. & Coppens, Y. 2001 First hominid from the Miocene (Lukeino Formation, Kenya). C. R. Acad. Sci. IIA332, 137–144. Stern, J. T. 2000 Climbing to the top: a personal memoir of Australopithecus afarensis. Evol. Anthropol. 9, 113– 133. (doi:10.1002/1520-6505(2000)9:3,113::AID-EVA N2.3.0.CO;2-W) Stern, J. T. & Susman, R. L. 1981 Electromyography of the gluteal muscles in Hylobates, Pongo, and Pan: implications for the evolution of hominid bipedality. Am. J. Phys. Anthropol. 55, 153–166. (doi:10.1002/ajpa.1330550203) Stern, J. T. & Susman, R. L. 1983 The locomotor anatomy of Australopithecus afarensis. Am. J. Phys. Anthropol. 60, 279 –317. (doi:10.1002/ajpa.1330600302) Stern, J. T. & Susman, R. L. 1991 ‘Total morphological pattern’ versus the ‘magic trait:’ conflicting approaches to the study of early hominid bipedalism. In Origine(s) de la bipe´die chez les Hominide´s (eds B. Senut & Y. Coppens), pp. 99– 112. Paris, France: CNRS. Strait, D. S. & Grine, F. E. 2004 Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J. Hum. Evol. 47, 399–452. (doi:10.1016/j.jhevol.2004.08.008) Strait, D. S., Grine, F. E. & Moniz, M. A. 1997 A reappraisal of early hominid phylogeny. J. Hum. Evol. 32, 17–82. (doi:10.1006/jhev.1996.0097) Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, C. O. & White, T. D. 2009 Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 94– 99. Teaford, M. F. & Ungar, P. S. 2000 Diet and the evolution of the earliest human ancestors. Proc. Natl Acad. Sci. USA 95, 13 506–13 511. (doi:10.1073/pnas.260368897) Tobias, P. V. 1967 The cranium and maxillary dentition of Australopithecus (Zinjanthropus) boisei. Olduvai Gorge, Vol. 2. Cambridge, UK: Cambridge University Press. Turner, A. & Wood, B. A. 1993 Comparative palaeontological context for the evolution of the early hominid masticatory system. J. Hum. Evol. 24, 301–318. (doi:10.1006/jhev.1993.1023) Ungar, P. 2004 Dental topography and diets of Australopithecus afarensis and early Homo. J. Hum. Evol. 46, 605–622. (doi:10.1016/j.jhevol.2004.03.004) Viola, R., Kullmer, O., Sandrock, O., Hujer, W. & Seidler, H. 2008 An early australopithecine femur from Galili, Ethiopia. J. Vert. Paleo. 28(Suppl. 3), 156A– 157A. Phil. Trans. R. Soc. B (2010)

Y. Haile-Selassie

3331

Ward, C. V., Leakey, M. G. & Walker, A. 1999 The new hominid species Australopithecus anamensis. Evol. Anthropol. 7, 197 –205. (doi:10.1002/(SICI)1520-6505(1999) 7:6,197::AID-EVAN4.3.0.CO;2-T) Ward, C. V., Leakey, M. G. & Walker, A. 2001 Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J. Hum. Evol. 41, 255 –368. (doi:10.1006/jhev. 2001.0507) White, T. D. 1977 New fossil hominids from Laetolil, Tanzania. Am. J. Phys. Anthropol. 46, 197–230. (doi:10.1002/ ajpa.1330460203) White, T. D. 1980a Evolutionary implications of Pliocene hominid footprints. Science 208, 175–176. (doi:10.1126/ science.208.4440.175) White, T. D. 1980b Additional fossil hominids from Laetoli, Tanzania: 1976–1979 specimens. Am. J. Phys. Anthropol. 53, 487 –504. (doi:10.1002/ajpa.1330530405) White, T. D. 1985 The hominids of Hadar and Laetoli: an element-by-element comparison of the dental samples. In Ancestors: the hard evidence (ed. E. Delson), pp. 138– 152. New York, NY: Alan R. Liss. White, T. D. 2002 Earliest hominids. In The primate fossil record (ed. W. Hartwig), pp. 407–417. Cambridge, UK: Cambridge University Press. White, T. D. & Johanson, D. C. 1982 Pliocene hominid mandibles from the Hadar Formation. Ethiopia: 1974–1977 collections. Am. J. Phys. Anthropol. 57, 501–544. (doi:10.1002/ajpa.1330570405) White, T. D. & Suwa, G. 1987 Hominid footprints at Laetoli: facts and interpretations. Am. J. Phys. Anthropol. 72, 485 –514. (doi:10.1002/ajpa.1330720409) White, T. D., Johanson, D. C. & Kimbel, W. H. 1981 Australopithecus africanus: its phyletic position reconsidered. S. Afr. J. Sci. 77, 445– 470. White, T. D., Suwa, G., Hart, W. K., Walter, R. C., WoldeGabriel, G., de Heinzelin, J., Clark, J. D., Asfaw, B. & Vrba, E. 1993 New discoveries of Australopithecus at Maka in Ethiopia. Nature 366, 261–265. (doi:10.1038/366261a0) White, T. D., Suwa, G. & Asfaw, B. 1994 Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371, 306 –312. (doi:10.1038/371306a0) White, T. D., Suwa, G. & Asfaw, B. 1995 Corrigendum. Nature 375, 88. (doi:10.1038/375088a0) White, T. D., Suwa, G., Simpson, S. W. & Asfaw, B. 2000 Jaws and teeth of Australopithecus afarensis from Maka, Middle Awash, Ethiopia. Am. J. Phys. Anthropol. 111, 45–68. (doi:10.1002/(SICI)1096-8644(200001)111: 1,45::AID-AJPA4.3.0.CO;2-I) White, T. D. et al. 2006 Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883– 889. (doi:10.1038/ nature04629) White, T. D., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, O. C., Suwa, G. & WoldeGabriel, G. 2009 Ardipithecus ramidus and the paleobiology of early hominids. Science 326, 75–86. (doi:10.1126/science.1175802) WoldeGabriel, G., White, T. D., Suwa, G., Renne, P. R., de Heinzelin, J., Hart, W. K. & Heiken, G. 1994 Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371, 330 –333. (doi:10.1038/ 371330a0) Wood, B. A. & Chamberlain, A. 1987 The nature and affinities of the ‘robust’ australopithecines: a review. J. Hum. Evol. 16, 625 –641. (doi:10.1016/00472484(87)90017-0) Wood, B. A. & Ellis, M. 1986 Evidence for dietary specialization in the ‘robust’ australopithecines. Anthropos 23, 101–124. Zihlman, A. 1985 Australopithecus afarensis: two sexes or two species? In Hominid evolution, past, present, and future (ed. P. V. Tobias), pp. 213– 220. New York, NY: Alan R. Liss.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3333–3344 doi:10.1098/rstb.2010.0039

Anterior dental evolution in the Australopithecus anamensis –afarensis lineage Carol V. Ward1, *, J. Michael Plavcan2 and Fredrick K. Manthi3,4 1

Department of Pathology and Anatomical Sciences, University of Missouri, M263 Medical Sciences Building, Columbia, MO 65212, USA 2 Department of Anthropology, University of Arkansas, 330 Old Main, Fayetteville, AR 72701, USA 3 Department of Earth Sciences, National Museums of Kenya, P.O. Box 40658, Nairobi, Kenya 4 Turkana Basin Institute, Stony Brook University, Stony Brook, NY 11794, USA Australopithecus anamensis is the earliest known species of the Australopithecus – human clade and is the likely ancestor of Australopithecus afarensis. Investigating possible selective pressures underlying these changes is key to understanding the patterns of selection shaping the origins and early evolution of the Australopithecus – human clade. During the course of the Au. anamensis – afarensis lineage, significant changes appear to occur particularly in the anterior dentition, but also in jaw structure and molar form, suggesting selection for altered diet and/or food processing. Specifically, canine tooth crown height does not change, but maxillary canines and P3s become shorter mesiodistally, canine tooth crowns become more symmetrical in profile and P3s less unicuspid. Canine roots diminish in size and dimorphism, especially relative to the size of the postcanine teeth. Molar crowns become higher. Tooth rows become more divergent and symphyseal form changes. Dietary change involving anterior dental use is also suggested by less intense anterior tooth wear in Au. afarensis. These dental changes signal selection for altered dietary behaviour and explain some differences in craniofacial form between these taxa. These data identify Au. anamensis not just as a more primitive version of Au. afarensis, but as a dynamic member of an evolving lineage leading to Au. afarensis, and raise intriguing questions about what other evolutionary changes occurred during the early evolution of the Australopithecus – human clade, and what characterized the origins of the group. Keywords: Australopithecus anamensis; Australopithecus afarensis; dental evolution

1. INTRODUCTION Fossil evidence documenting the first 4 Myr of hominin evolution has grown substantially over the past two decades. While several early taxa have been identified (Ardipithecus, Sahelanthropus and Orrorin), much of our understanding of what the earliest members of the Australopithecus –human clade were like still comes from the best-known species of Australopithecus, Australopithecus afarensis. However, Au. afarensis only appears as early as 3.6 Ma and is not well represented in the fossil record until 3.4 – 3 Ma (review in Kimbel et al. 2006, see also White et al. 2000). The new fossils from Woranso-Mille, Ethiopia (Haile-Selassie et al. 2010), are 3.7 – 3.8 Ma and probably part of this lineage as well. Australopithecus anamensis is the earliest known member in this clade, appearing by 4.17 Ma in Kenya and Ethiopia, and is the likely ancestor of Au. afarensis. Unfortunately, Au. anamensis is relatively poorly represented in the fossil record, so our understanding about this first 400 000 to about 800 000 years of the evolution of the Australopithecus – human

* Author for correspondence ([email protected]). One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

clade is only sketchy at present. Even so, emerging evidence from what few fossils are known is beginning to hint that Au. anamensis was a species in transition and may offer important insights into the origins of a number of key hominin traits. A previous detailed investigation of morphological changes through time in the successive site samples of Au. anamensis and Au. afarensis (Kimbel et al. 2006) documented a series of apomorphies that progressively appear throughout these samples, involving primarily the dentition, but also some aspects of maxillary and mandibular form. The pattern of the appearance of these traits strongly supports the hypotheses of anagenetic evolution of Au. anamensis to Au. afarensis. One of the most important apomorphies of the Australopithecus – human clade is habitual terrestrial bipedality with loss of significant climbing abilities. Unfortunately, little is known about the postcranial skeleton of Au. anamensis. Australopithecus anamensis is only known from a femoral shaft, along with some unpublished vertebral fragments, partial metatarsal, eroded distal pedal phalanx and manual phalanx, all from Asa Issie (White et al. 2006), a distal humerus, capitate, partial manual phalanx and partial tibia from Kanapoi (Patterson & Howells 1967;

3333

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3334

C. V. Ward et al.

Dental evolution in Australopithecus

Leakey et al. 1995, 1998), and a nearly complete radius from Allia Bay (Patterson & Howells 1967; Heinrich et al. 1993; Leakey et al. 1995, 1998). The tibial diaphysis is oriented orthogonally to the talocrural joint, as is that of all later hominins, indicating a knee placed directly over the ankle during the single-limb support phase of terrestrial bipedal gait (Ward et al. 1999b). However, more cannot be said at the present time about the details or extent of its adaptation to terrestrial bipedality. In almost all other major features, the known Au. anamensis postcranial elements resemble those attributed to Au. afarensis. The exception may be in the capitate, which appears to have separate dorsal and plantar articular facets for MC2 like in extant African apes, and unlike Australopithecus, Homo, Ardipithecus, Proconsul (Beard et al. 1986; Lovejoy et al. 2009) or the unknown 3.5 Ma hominin from South Turkwel, Kenya (Leakey et al. 1998; Ward et al. 1999a). This small feature may indicate some differences in locomotor or manipulative function, but until more fossils are recovered our ability to infer postcranial variation among species is highly limited, and little more than can be said about whether the same pattern of locomotor or manipulative ability seen in Au. afarensis also characterized Au. anamensis. Even less is known about its cranial anatomy. Only a temporal bone and some maxillary fragments are known. Australopithecus anamensis appears to have a smaller external auditory porus than later hominins, and a potentially more obtuse angle of the tympanic plate along with a weakly developed articular eminence (Leakey et al. 1995; Ward et al. 2001). However, little can be said of the functional or evolutionary significance of this morphology without more cranial fossils. In contrast to the skeleton and skull, there are several aspects of the jaws and teeth that are preserved for both Au. anamensis and Au. afarensis, enabling significant comparisons to be made in these elements. Previous research has noted evolutionary changes in relative canine size, canine and premolar morphology, mandibular and maxillary contours and incisor dimensions (Leakey et al. 1995; Ward et al. 2001; Kimbel et al. 2006; White et al. 2006). However, the relative paucity of fossils attributable to Au. anamensis obscures detailed understanding of the quality, quantity and integration of many features that impact hypotheses about the evolution of adaptations in this lineage. Overall, while the Kanapoi and Allia Bay fossils are distinguishable from those at Laetoli and Hadar, Au. anamensis is generally considered to be just an early member of the Au. afarensis lineage, with a few isolated morphological plesiomorphies. However, there is general consensus that Au. afarensis demonstrates evidence of a greater emphasis on the ability to masticate tougher or more abrasive food items, possibly associated with shifts in habitat or resource exploitation (Teaford & Ungar 2000; Ward et al. 2001; White et al. 2006) and/or broadening potential ecological niches. New fossil evidence provides even more evidence for shifting adaptations throughout this lineage. The purpose of this paper is to review and summarize the morphology of the jaws and teeth of Phil. Trans. R. Soc. B (2010)

Au. anamensis and Au. afarensis based on previously published fossils, integrate data from some newly discovered specimens from Kanapoi (Manthi et al. in preparation) which provide new insights and consider the suite of differences seen between these taxa in an adaptive and evolutionary context. We note that most change occurs in the anterior portion of the face and jaws, with the most dramatic alterations occurring at or near the canine–premolar complex, but that patterns of change within teeth in proportions and shape often are uncorrelated. We propose that these changes signal possible dietary change and/or altered use of the anterior dentition in food processing in the early evolution of the Australopithecus–human clade, in conjunction with shifts in masticatory adaptations.

2. CANINE TOOTH SIZE, DIMORPHISM AND THE CANINE/P3 COMPLEX The evolution of the canine teeth and mandibular honing premolar in hominins has received a great deal of attention ever since Darwin (1871). Canine tooth size reduction is one of the few defining features of the hominin clade (Wolpoff 1980; Greenfield 1992; Haile-Selassie 2001, 2004; White et al. 2006, 2009; Suwa et al. 2009) and is recognized as a signal of important behavioural and adaptive changes (Plavcan & Van Schaik 1997). For example, recent discussion of Ardipithecus ramidus places great emphasis on the importance of the canine/premolar complex for inferring changes in behaviour and diet—an assessment with a long tradition in anthropology (e.g. Darwin 1871; Brace 1971; Leutenegger & Kelly 1977; Wolpoff 1978, 1979, 1980; Lovejoy 1981, 2009). At this point, two major features in hominin canine evolution are widely accepted. First, male canine teeth reduced in size relative to a likely ape ancestral condition, with a concomitant reduction of canine sexual dimorphism, early in the hominin lineage (Brace 1963; Jungers 1978; Wolpoff 1980; Greenfield 1992; Suwa et al. 2009). Second, by Au. afarensis, the canine honing complex is reduced or lost (Greenfield 1992; Haile-Selassie 2001, 2004; Kimbel et al. 2006; White et al. 2006). It is widely assumed that the loss of the hone is associated with selection for use of the tooth in diet, probably in food acquisition. The most explicit functional statement is that the mandibular canine changes to a more diamond-shaped profile so that the mesial crest can occlude with the lateral maxillary incisor (Greenfield 1992; Haile-Selassie 2004). This observation is used to support the hypothesis that canine reduction and changes in morphology are a consequence of selection for incorporation of the tooth into a functional incisal battery (Greenfield 1992). While it may seem that canine crown reduction is a necessary precursor to alterations in canine form for other, presumably dietary, functions, an alternative hypothesis has been proposed. It is possible that canine tooth crown shape change is integrally linked to selection for the use of the canine in food processing and so would have occurred concomitantly with size reduction, not after it (Greenfield 1992). Such reduction could be linked in two ways—first would

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Dental evolution in Australopithecus be a general selective pressure for the use of canines in food processing that results in crown size reduction following relaxation of selection for the use of the tooth as a weapon. Second would be that selection for canine crown reduction would only be linked with changes in tooth form associated with dietary use of the tooth following an initial canine crown reduction and loss of dimorphism through a separate, unspecified mechanism. In other words, one model posits that canine tooth size in all primates, including hominins, reflects a balance between conflicting selection pressures for large canines as weapons and small canines for food acquisition (Greenfield 1992), and the other posits that selection for dietary functions only occurred after canine dimorphism was lost, with a secondary crown reduction associated with the development of occlusal features that transform the canine into a tool for food processing and/or acquisition. The large sample of Ar. ramidus fossils from 4.4 Ma strongly suggests that substantial reduction in male canine crown size and loss of significant dimorphism probably occurred near the origin of hominins and may not be apomorphic for the Australopithecus– human clade (White et al. 1994, 1995; Suwa et al. 2009). Indeed, Au. anamensis canine crowns appear to be approximately the same overall size as those of Ar. ramidus. Comparisons of associated dentitions demonstrate Au. anamensis had slightly larger basal dimensions of its canines relative to postcanine tooth size than did Au. afarensis (Ward et al. 2001). Overall, individual tooth sizes do not differ between the species, with the exception of the maxillary canine mesiodistal dimension and some dimensions of P3 and P4. The few preserved canine crowns in Au. anamensis appear no more variable, or presumably dimorphic, than those of Au. afarensis so there appears to be no evidence of evolution of dimorphism during this time period, either. However, a single large Au. anamensis mandibular canine alveolus (KNM-KP 29287; Ward et al. 2001), and to some extent a canine root with heavily worn crown from Fejej, Ethiopia (FJ-4-SB-1a; Fleagle et al. 1991), suggested potentially greater canine crown size sexual dimorphism early in this lineage than previously appreciated, with the implication that canine dimorphism decreased at some point in the Au. anamensis – afarensis lineage. If so, this would be evidence of social and/or dietary evolution. Three new associated dentitions from Kanapoi have clarified details of canine size and proportions of Au. anamensis (Manthi et al. in preparation), provided new data on canine proportions and morphology, and suggested that Au. anamensis is a key taxon for understanding the adaptive significance of changes in canine form. KNM-KP 47951 has the largest mandibular root of any known hominin (figure 1). Comparison of mandibular root size in Au. anamensis with those Au. afarensis, extant great apes and Homo reveals that root size variation in Au. anamensis was very strong, most like Pongo in magnitude (figure 1, table 1), implying strong dimorphism. This stands in stark contrast to Au. afarensis, which shows much less variation in root dimensions, and is intermediate to extant Homo and Pan in mean size. Unlike the roots, mandibular Phil. Trans. R. Soc. B (2010)

C. V. Ward et al.

3335

canine crowns are similar in all dimensions in Au. anamensis and Au. afarensis, and both have slightly larger and more dimorphic crowns than do modern humans, as also reported for Ar. ramidus (Suwa et al. 2009) but less so than in extant apes. Therefore, not only was there a clear dissociation between crown size and root size in Au. anamensis, such that size and dimorphism in the crowns were lost while size and dimorphism in the roots were retained, but the loss of root size dimorphism occurred sometime during the evolution of Au. anamensis into Au. afarensis. Interestingly, not only does KNM-KP 47951 demonstrate that the large alveolus of KNM-KP 29287 did not imply unusual crown size dimorphism, it also demonstrates that the canine root of KNM-KP 29287 would not have been unusually large, and may in fact have been a small male. It would not, however, have supported a larger crown than those preserved for Au. anamensis (Plavcan et al. 2009). Even with the new data, no dimensions of the mandibular canine crowns (length, breadth or height) differ between species (figure 1, table 2). However, there are dimensional differences in the maxillary canines (see also Ward et al. 2001; White et al. 2006) (figure 2, table 2). Australopithecus anamensis and Au. afarensis are equivalent in maxillary canine crown height and buccolingual breadth, but Au. anamensis maxillary canines are mesiodistally longer than are those of Au. afarensis (figure 3a, tables 2 and 3). Proportionately, Au. anamensis canines are almost exactly intermediate in basal crown shape (measured as mesiodistal length relative to buccolingual breadth) between extant great apes and Au. afarensis (figure 3a). Furthermore, Au. afarensis canine basal shape proportions are identical to those of extant Homo, after accounting for their size difference. The apparent progressive decrease in relative canine size from Au. ramidus to Au. afarensis, through Au. anamensis (White et al. 2006), tracks mesiodistal length only, but not overall size of the tooth. The change in canine basal proportions reflects change in canine – P3 function. It has long been noted that the Au. afarensis canine/premolar complex loses its ‘honing’ function, in the sense that the distal edge of the maxillary canine no longer exclusively wears against the labial surface of the mandibular P3 as in other primates (Wolpoff 1979; Greenfield 1992; Haile-Selassie 2004). Metrically, it is only the maxillary canine and mandibular premolar—the honing teeth—that change basal shape (figure 3b) to become less elongate in outline. Mandibular canines and maxillary P3s do not. This implies no overall selection to reduce the teeth, but only selection to alter contact between the honing pair. So, while there may have been a loss of honing with early hominins (HaileSelassie 2001, 2004; Brunet et al. 2002), canine – P3 occlusal relationships continue to evolve. In addition to basal outlines, the canines and P3 change other aspects of their crown shape significantly from Au. anamensis to Au. afarensis, strongly suggesting that selection favoured an altered function of these teeth. Both mandibular and maxillary canines become more symmetrical in lingual profile. Maxillary canines have higher shoulders and shorter mesial crests, and mandibular canines have lower mesial

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

C. V. Ward et al.

Dental evolution in Australopithecus

(a) 35

0

(b) 50 45 40 35 30 25 20 15 10 5 0

(c) 25

(d ) 25

20

20

25

root length (mm)

10

root MD (mm)

crown MD (mm)

5

15 10

15 10

0

0

(e) 18

( f ) 18

16

16 root BL (mm)

5

14 12 10 8

14 12 10 8

4

4

2

2

0

0

.g G

G

P.

or

6

o py rilla gm P. tro aeu s gl od H yte .s s Au api . a ens Au fare . a ns na is m es is

6

.g

crown BL (mm)

5

ill gm a tro aeu s gl o H dyte .s s Au apie ns .a f Au aren .a s na is m es is

15

P.

20

py

crown height (mm)

30

P.

3336

Figure 1. Dental dimensions for mandibular canine crowns and roots for extant great apes, humans, Au. anamensis and Au. afarensis. Arrows indicate new specimen KNM-KP 47951. Data in table 1. (a) Crown height, (b) root length, (c) crown mesiodistal, (d) root mesiodistal, (e) crown buccolingual and ( f ) root buccolingual.

shoulders and a less narrow, blade-like outline (figure 3c). Lower premolars develop a larger metaconid, and the protoconid shifts buccally. Marginal ridges become proportionately more distinctive, and the anterior fovea opens in a more occlusal direction (Leakey et al. 1995, 1998; Ward et al. 2001; HaileSelassie 2004; Suwa et al. 2009; White et al. 2006). These shape changes increase transverse contact area between maxillary and mandibular teeth, most logically owing to increased use of the canine in food acquisition or preparation, and perhaps the premolar in mastication as well. The fossils demonstrate that canine shape changed significantly along with a shift in canine – P3 occlusal relationships in the Au. anamensis – afarensis lineage, while canine size remained approximately the same. It is also notable that Au. afarensis canine crowns show the same basal proportions as in Homo Phil. Trans. R. Soc. B (2010)

(figure 3a), demonstrating that the major proportional changes in canine dimensions in hominin evolution happened between 3.9 and 3.4 Ma. The dissociation between crown size and shape changes demonstrates that selection impacting crown shape was independent of that causing crown height reduction. This in turn bears on hypotheses that purport to explain the adaptive significance of canine crown size reduction in hominins (Brace 1963; Bailit & Friedlaender 1966; Wolpoff 1969, 1980; Calcagno & Gibson 1988). Crown height was reduced prior to the appearance of Au. anamensis, if Ar. ramidus indeed reflects the ancestral hominin condition (Suwa et al. 2009), and certainly by the origins of the Australopithecus – human clade. Data now suggest that crown height did not reduce in order to provide room for expanding postcanine dentitions (Jungers 1978), because basal dimensions and root size did

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Dental evolution in Australopithecus

C. V. Ward et al.

3337

Table 1. Descriptive statistics for mandibular canine dimensions of extant combined-sex and fossil samples. All data are in millimetres. Data for Gorilla, Pongo, Pan troglodytes and Homo were collected for this project. Data for Pan pansicus were taken from Plavcan (1990) and do not include values for root dimensions. Height, crown height; BL, buccolingual; MD, mesiodistal; RBL, root buccolingual; RMD, root mesiodistal; RL, root length. height

BL

MD

RBL

RMD

RL

Gorilla gorilla n min. max. mean standard deviation CV

50 12.65 31.25 20.89 5.47 26.2

50 9.18 16.26 12.44 2.32 18.6

50 11.53 21.66 15.55 2.82 18.1

50 8.65 16.03 11.89 2.41 20.3

50 11.12 21.4 15.17 3.03 20.0

50 22.02 45.27 33.18 4.13 12.4

Pongo pygmaeus n min. max. mean standard deviation CV

16 13.58 26.82 19.52 4.18 21.4

17 7.97 14.53 10.49 2.51 23.9

17 11.08 17.8 13.83 2.13 15.4

17 7.4 14.17 10.12 2.48 24.5

17 10.2 17.52 13.39 2.31 17.25

16 20.35 41.04 27.56 6.09 22.1

Pan troglodytes n min. max. mean standard deviation CV

30 12.51 25.5 17.63 3.52 20.0

30 7.98 15.22 10.93 1.77 16.2

30 10.1 17.17 12.8 1.92 15.0

30 7.6 14.92 10.43 1.76 16.9

30 8.19 16.9 12.18 2.26 18.6

30 19.99 38.0 28.59 5.03 17.6

Pan paniscus n min. max. mean standard deviation CV

29 9.5 16.13 12.27 2.02 16.5

30 5.88 9.13 7.13 0.88 12.3

30 7.88 11.88 9.66 1.16 12.0

—

—

—

Homo sapiens n min. max. mean standard deviation CV

36 7.67 12.65 9.99 1.23 12.3

36 5.45 7.9 6.72 0.64 9.5

36 5.94 9.13 7.67 0.71 9.3

36 3.7 6.58 5.36 0.61 11.4

36 5.82 8.99 7.49 0.68 9.1

36 10.94 20.2 15.96 2.18 13.6

Australopithecus afarensis n min. max. mean standard deviation CV

6 10.9 17 13.12 2.22 16.9

10 6.9 10.6 8.48 1.25 14.7

11 9.3 13.9 10.88 1.38 12.7

9 6.4 9.5 7.82 1.08 13.8

9 8.8 13.1 10.54 1.31 12.4

3 20.91 24.29 22.77 1.72 7.5

Australopithecus anamensis n min. max. mean standard deviation CV

3 10 15.71 13.27 2.94 22.2

7 6.6 10.40 8.81 1.32 15.0

7 9 13.90 11.04 1.66 15.0

9 5.9 10.3 7.99 1.43 17.9

8 8.2 13.81 10.44 1.72 16.5

3 20.2 31.79 26.86 5.99 22.3

not reduce concomitantly with crowns. Crown height also did not reduce in order to enhance an incisal or biting function (Szalay 1975; Wolpoff 1980; Greenfield 1992) because shape change in the crown did not accompany crown height reduction. Following a loss of function of the canine teeth as weapons (for behavioural reasons, or following masticatory changes precluding the use of projecting Phil. Trans. R. Soc. B (2010)

canines), male canine size—especially crown height— reduced to the size of those of female extant apes, as has occurred in other primates (Plavcan et al. 1995). However, canine shape becomes altered simultaneously with mandibular lateral incisor breadth (Ward et al. 2001) and premolar form only with the appearance of Au. afarensis in the absence of further crown height reduction.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3338

C. V. Ward et al.

Dental evolution in Australopithecus Table 2. Probabilities from t-tests for significant differences between Au. anamensis and Au. afarensis canine crown areas and linear dimensions using ln-transformed data. Numbers are for two-tailed probabilities. Area is calculated as the length times the breadth of the crown dimensions. Abbreviations as in table 1; mand, mandibular; max, maxillary.

(a) 45

crown height (mm)

40 35 30 25 20 15

max mand

10

area

MD

BL

RMD

RBL

height

0.546 0.482

0.007 0.208

0.226 0.98

0.009 0.831

0.625 0.843

0.211 0.971

5 0

any event, it is now clear that crowns and roots did not change shape and size as part of a unimodal selection pressure that drove the canines to the modern human form. Rather, the patterns of morphological change suggest to us that the selective pressure shaping canine form during the evolution of Au. anamensis and early Au. afarensis was distinct from that of the earliest hominins, and of later Homo. This function almost certainly related to food acquisition or processing, but in a manner distinctive to early Australopithecus.

(b) 25

crown MD (mm)

20 15 10 5 0 (c) 25

crown BL (mm)

20 15 10 5

G .g P. ori py lla gm P. a tro eus gl od H ytes .s ap ie A. ns af ar A. ensi s an am es is

0

Figure 2. Dental dimensions for maxillary canine crowns for extant great apes, humans, Au. anamensis and Au. afarensis. Data in table 3. (a) Crown height, (b) crown mesiodistal, and (c) crown buccolingual.

It could be possible that smaller canine roots in Au. afarensis could be related to decreased loading of the canines in puncturing or crushing (Spencer 2003), but microwear studies in Au. afarensis imply that, in fact, use of the canine for these activities probably was greater in Au. afarensis than in apes (Ryan & Johanson 1989). Comparisons with Au. anamensis microwear will be necessary to explore this possibility further. To date, the fossil record is insufficient to evaluate whether these events in canine and premolar evolution were indeed simultaneous, but they are so within the current resolution available in the fossil record. In Phil. Trans. R. Soc. B (2010)

3. MANDIBULAR AND MAXILLARY MORPHOLOGY Other morphologies distinguishing Au. anamensis and Au. afarensis also are related to the change in canine tooth size, and in morphology of the canine/premolar complex. In particular, canine tooth root size affects the occlusal outline of the anterolateral corner of the mandible. The mandible of Au. anamensis is distinct from that of Au. afarensis in having an inflated alveolar profile along the roots, so that the canines are set anteriorly to the postcanine tooth rows (figure 4) (Ward et al. 2001). In the male mandible, the effect of a large root is particularly notable. In contrast, in Au. afarensis, the broadest region across the anterior mandible is found adjacent to P3, and the canines are set medial to the premolars. There also is less variation in this contour among mandibles, presumably related to less canine root size dimorphism than in Au. anamensis. Certainly, canine size is correlated with mandibular form in primates (Plavcan & Daegling 2006). Another factor influencing the relatively broad anterior portion of the mandible in Au. anamensis is that the lower lateral incisors are relatively broader than in Au. afarensis (Ward et al. 2001). Both canine root breadths and incisor breadth would affect anterior mandibular size and shape. The maxilla of Au. anamensis, and early Au. afarensis from Laetoli (Garusi 1; Puech 1986; Puech et al. 1986), appears to have narrowly spaced, relatively straight maxillary tooth rows, also seen in the Woranso-Mille sample (Haile-Selassie et al. 2010). They also have rounded margins of the lateral nasal aperture. Both of these features are plausibly related to reduction in canine tooth root size. Canine root length may not be related to maxillary shape (Cobb & Willis 2008; Plavcan et al. 2009), but root basal area would certainly affect maxillary breadth in this region and thus the supporting bone. Thus, the selective force that shaped canine root size reduction is plausibly linked to pressures that

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Dental evolution in Australopithecus

C. V. Ward et al.

3339

(c) ln (crown mesiodistal length) (mm)

(a) 3.3 Au. anamensis 2.9

2.5

2.1

1.7 1.7

1.9

2.1

2.3

2.5

2.7

3.1

2.9

ln (crown buccolingual breadth) (mm) Au. afarensis

crown mesiodistal/buccolingual

(b) 1.6 1.4 1.2 1.0 0.8 p < 0.05

0.6

mandibular canine P3

p < 0.05 maxillary canine P3

Figure 3. Illustrations of canine shape differences between Au. anamensis and Au. afarensis. (a) Scatterplot of ln-transformed maxillary canine mesiodistal length compared with buccolingual breadth. Open squares: Gorilla gorilla, Pan paniscus, P. troglodytes, Pongo pygmaeus; open triangles: Homo sapiens; grey diamonds: Au. afarensis; black circles: Au. anamensis. Australopithecus anamensis retains relatively long canines mesiodistally and are most similar in proportions to extant apes. Australopithecus afarensis canines are similar buccolingually but are mesiodistally shorter than those of Au. anamensis. Humans have the same proportions as seen in Au. afarensis, but are smaller overall. (b) Basal proportion differences are seen only in the maxillary canine and mandibular premolar, the teeth that hone, but not mandibular canine or maxillary premolar, illustrating that observed shape changes are associated with a further reduction in honing and a shift in occlusal relationships in this complex. (c) Morphologic differences in canines and P3. Australopithecus anamensis has a lower mesial crown shoulder and longer mesial crest in the maxillary canine, a narrower, more blade-like mandibular crown with pronounced distal tubercle and a more unicuspid P3 with centrally placed paraconid compared with Au. afarensis. Data in tables 1 and 3. Scale bar, 1 cm.

altered mandibular and possibly maxillary geometry. Teaford & Ungar (2000) noted that mandibular corpus robusticity is intermediate in Au. anamensis between that of great apes and later hominins, suggesting an increase in adaptation to resist heavier masticatory stresses with Au. afarensis. That Au. afarensis was adapted to greater masticatory stresses is also suggested by the increased height of its molar crowns (Leakey et al. 1995; Ward et al. 1999b, 2001). Australopithecus afarensis mandibles also tend to have more posteriorly divergent tooth rows than does Au. anamensis, whose tooth rows are narrower and more parallel, more like those of extant apes (Ward et al. 2001). Narrow tooth rows increase symphyseal stresses owing to wishboning and torsion of the mandible during mastication Phil. Trans. R. Soc. B (2010)

(Hylander 1984, 1985; Ravosa 2000). Australopithecus anamensis had a correspondingly large postincisive planum and strongly developed mandibular tori, probably related to this overall geometry. A wider geometry in Au. afarensis would reduce forces from wishboning owing to pull of the external masticatory muscles and bone (Hylander 1985). More divergent tooth rows also decrease symphyseal torsional stresses. It is notable, therefore, that despite altered mandibular geometry, symphyseal robusticity still tends to be relatively greater in Au. afarensis than Au. anamensis. Given the effects of mandibular geometry on symphyseal stresses, it may be that selection for more divergent tooth rows influenced the reduction of lateral incisor breadth and canine root size in order to reduce

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3340

C. V. Ward et al.

Dental evolution in Australopithecus

Table 3. Descriptive statistics for maxillary canine crown dimensions of extant combined-sex and fossil samples. Abbreviations as in table 1.

Gorilla gorilla n min. max. mean standard deviation CV

height

BL

MD

50 12.14 41.56 22.08 7.44 33.7

50 10.26 22.12 13.88 2.78 20.0

50 12.54 23.23 17.17 3.24 18.9

Pongo pygmaeus n min. max. mean standard deviation CV

18 12.74 30.45 20.15 6.15 30.5

18 8.09 15.43 11.80 2.19 18.6

18 11.11 18.56 14.76 2.72 18.4

Pan troglodytes n min. max. mean standard deviation CV

30 11.86 27.27 18.05 4.03 22.3

30 8.09 14.25 10.56 1.79 17.0

30 9.63 19.31 12.82 2.31 18.0

Pan paniscus n min. max. mean standard deviation CV

24 8.63 20.38 13.40 3.48 26.0

30 6.13 11.13 8.01 1.44 18.0

30 8.63 14.38 10.54 1.56 14.8

Homo sapiens n min. max. mean standard deviation CV

50 6.48 12.26 9.28 1.23 13.3

50 6.56 9.82 8.24 0.71 8.6

50 5.96 8.49 7.45 0.57 7.7

Australopithecus afarensis n min. max. mean standard deviation CV

8 9.2 15.4 12.35 2.18 17.7

8 9.3 12.5 10.7 1.00 9.3

8 8.9 11.6 9.81 0.84 8.6

Australopithecus anamensis n min. max. mean standard deviation CV

3 12 16 14.4 2.12 14.7

7 8.8 11.2 10.20 0.75 7.4

8 9.91 12.4 11.10 0.82 7.4

the breadth of the anterior mandible in Au. afarensis. This may have co-occurred with widening of the posterior part of the mandible, too. In order to maintain appropriate occlusal relationships, this could also have led to concomitant reduction in maxillary canine root dimensions, and corresponding reduction in maxillary inflation along the canine juga and lateral nasal aperture. Phil. Trans. R. Soc. B (2010)

Thus, the mandibular morphology of Au. afarensis implies selection for the ability to process harderto-chew foods, possibly opening up new niches. However, it is not only the masticatory system that has changed; reduction in lateral incisor breadth and reshaping of the canine crowns and the canine – premolar complex also suggest that selection for altered function of the anterior dentition in food processing occurred in the transition from Au. anamensis to Au. afarensis.

4. TOOTH WEAR One feature not previously appreciated from published fossils is that for those specimens showing substantial tooth wear, there appears to be differentially heavy anterior tooth wear in Au. anamensis compared with Au. afarensis. Quantitative comparisons of gross wear patterns are difficult owing to the fragmentary preservation of the dentitions, but qualitative comparisons can be made. Overall, Au. anamensis appear to have higher frequencies of heavier tooth wear than seen in Au. afarensis. Three out of four known Au. anamensis maxillae that preserve molars and anterior teeth all have heavy anterior wear relative to that of the molars (figure 5). KNM-KP 29283 has dentine exposure crossing both lingual cusps of M1 and M2. Its incisors and canines preserve only a narrow band of enamel labially, but were wearing onto the roots lingually. The new specimen, KNM-KP 47952 (Manthi et al. in preparation), also has unusually high anterior tooth wear, with only 1–2 mm of enamel remaining along the lingual surfaces of its incisors and canines. In apparent contrast, dentine is only exposed on M2 as a tiny pit on the paracone. Even if this molar is not associated, which it almost certainly is, there is an unusually heavy amount of anterior wear. Another Kanapoi fossil, KNM-KP 30498, has M2 preserved, but on M1 has a small area of dentine exposed only on the paracone. Its I1 is worn all the way up to the basal tubercle, probably about halfway through the original length of the tooth. The canine of this same specimen is worn almost up to its mesial or distal tubercles. In fact, no unworn incisors are known from Au. anamensis at all, except those of young individuals whose teeth are either not yet or barely in occlusion, and/or who exhibit little or no molar wear. The only relatively unworn maxilla with canine is ASI-VP-2/344 from Aramis, which has no dentine exposure on M2 but still exhibits apical wear on its canine (White et al. 2006). This specimen appears comparable in wear to teeth in the Au. afarensis maxilla AL 200-1. In contrast, no comparably heavy differential wear is found in the associated maxillary dentitions of Au. afarensis at Hadar or Laetoli, and none is as heavily worn as any of the three Kanapoi specimens. The M2s of AL 444 (Kimbel et al. 2004) are more worn than those of KNM-KP 47952, but less than those of KNM-KP 29283, but most of the incisor and canine crowns are intact in AL 444. AL 199-1 and AL 200-1 have less wear on their molars than any Au. anamensis maxilla, and while they have some wear on the incisors and canines, it is not heavy. The

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Dental evolution in Australopithecus

C. V. Ward et al.

3341

Figure 4. Top row photos: occlusal views of all three Kanapoi mandibles, from left to right KNM-KP 29281, KNM-KP 29287, KNM-KP 31713. Bottom row line drawings: several mandibles of Au. afarensis, from left to right: LH 4, AL 123-23, AL 333w-60, AL 266-1, AL 400-1a, AL 277-1 and AL 198-1. Arrows denote anterolateral inflection of occlusal outline. Note the canine roots set medial to that of P3 in the Au. afarensis, and in contrast that the canines are set anterior to the P3 in the Au. anamensis fossils so that the anterolateral corner of the occlusal profile is formed by the canine juga in this earlier species. Scalar bar, 0–4 cm.

KNM-KP 30498

KNM-KP 47952

KNM-KP 29283

Figure 5. Lingual views (top) of anterior teeth of KNM-KP 30498 and KNM-KP 47952 and occlusal views (bottom) of these anterior teeth and their associated molars. KNM-KP 29283 shown in medial (top) and occlusal (bottom) views for comparison. KNM-KP 30498 preserves I1, C, P3, M1 and M3 crowns, relevant teeth reversed to show all as if they were from the left side. KNM-KP 47952 preserves I1, I2, C and M2. All three specimens show relatively heavy anterior wear relative to molar wear. See text for discussion. Scalar bar, 0–4 cm. Phil. Trans. R. Soc. B (2010)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3342

C. V. Ward et al.

Dental evolution in Australopithecus

most worn published Au. afarensis incisor is AL 19817a (Johanson et al. 1982) which is comparable to that of KNM-KP 30498. Unfortunately it is not associated with any postcanine teeth, so further comparison cannot be made. Mandibular tooth wear is not directly comparable to maxillary wear, but even in sufficiently preserved mandibular dentitions, anterior tooth wear is at least as great or greater on the teeth relative to the molars in Au. anamensis when compared with Au. afarensis. The Au. afarensis mandible with the most heavily worn molars, AL 198-1, has dentine exposed across the occlusal face of M1 and buccal cusps of M2, but still has most of its canine crown preserved. It is only slightly less worn anteriorly than the Au. anamensis type mandible KNM-KP 29281. The most heavily worn mandibular dentition of all is the Au. anamensis specimen FJ-4-SB-1a from Fejej, Ethiopia (Fleagle et al. 1991), which has a similar level of molar wear to AL 198-1, yet it has dentine exposure over almost the entire P3 cusp and the associated canine is almost completely worn to the root, preserving only a narrow band of enamel. In summary, no anterior teeth are known from Hadar in which the entire crown is missing, yet many specimens attributed to Au. anamensis are very heavily worn. All individuals with sufficiently heavy molar wear to expose dentine on M2 have very heavily worn anterior teeth in Au. anamensis, whereas this is not the case for Au. afarensis. Only expanding sample sizes will provide an adequate test of how typical this distinction is, but current fossils are suggestive. There could be three possible explanations for this, which are not mutually exclusive, and all hint at selection for altered involvement of the anterior dentition. The first possibility is that the anterior permanent dentition erupts earlier relative to the molars in Au. anamensis than Au. afarensis, and that there was a shift to delay eruption of the incisors and canines in Au. afarensis relative to molar development. The second would be ingesting or biting foods with higher levels of tannins, which might increase intraoral friction and cause higher tooth wear (Prinz & Lucas 2000). The third possibility is that there is a difference between these samples in patterns of food processing involving the anterior dentition in which the teeth are suffering greater mechanical abrasion (Teaford & Ungar 2000). Under any of these scenarios, anterior tooth use or dietary properties probably would have differed between Au. afarensis and Au. anamensis. We suggest that the chemical hypothesis does not provide the most satisfactory explanation because relative anterior wear appears to decrease in concert with shape changes in incisor breadth, canine length and crown shape, as well as premolar proportions and crown morphology. The combination of changes in both wear gradient and dental morphology hints at a mechanical factor. Detailed study of anterior tooth microwear and dental growth patterns are needed to help test the various hypotheses of altered tooth wear between these species. Regardless, no matter what the explanation, the pattern suggests a shift in diet or anterior tooth use of some sort. Phil. Trans. R. Soc. B (2010)

5. SUMMARY AND CONCLUSIONS The discovery of new fossils, even though representing only a small portion of the anatomy of Au. anamensis, dictates a more careful, circumspect view of the role of this taxon in hominin evolution, and thereby the pattern of the origin of the adaptive suite of behaviours and characters shaping the early evolution of the Australopithecus –human clade. Australopithecus anamensis documents a morphology in the anterior face and dentition that is clearly transitional between a more primitive hominin form, and that seen in Au. afarensis. Given that the fossil record consists of mainly teeth and jaws, it should come as no surprise that the evidence suggests that any adaptive shift from Au. anamensis – afarensis lineage was related to diet. The data from the new Kanapoi fossils, in combination with previously published data, demonstrate that adaptively significant differences exist between Au. anamensis and Au. afarensis. These morphologies are not isolated, but seem to reflect an adaptive shift to a diet involving heavier mastication and at the same time altered use of the anterior dentition in food processing. Taken together, the greatest known differences between Au. anamensis and Au. afarensis are associated with evolutionary changes within the canine/P3 complex, and with adaptations for coping with increasing masticatory loads on the postcanine dentition. It has long been supposed that reduction in canine crown height accompanied selection for an increased ability to masticate tougher or harder foods, as well as with origins of habitual terrestrial bipedality. Ardipithecus ramidus demonstrates that crown height reduction is not linked to increased ability to masticate tougher or harder foods (White et al. 1994; Suwa et al. 2009), and Au. anamensis demonstrates that shape change altering occlusal relationships between the canine and premolar, and reduction in canine crowns and roots were dissociated. Even though the canine/P3 complex changed form in the Au. anamensis/Au. afarensis lineage, canine crown size itself remained stable, while the dentition and mandible showed progressive changes that suggest adaptation to heavy loads. The dissociation between changes in root and crown size is distinctive in the evolution in Au. anamensis – afarensis. Given that Ardipithecus also has large roots relative to its crowns (Suwa et al. 2009), the Au. anamensis condition appears primitive for hominins. A reduction in root size is achieved with the appearance of Au. afarensis, a species in which the premolars are more molariform, lower lateral incisors less broad and maxillary canine crowns are mesiodistally shorter with concomitant shorter mesial crests, mandibular canines less blade-like and more symmetrical in profile. Tooth rows are less parallel and anterolateral mandibular and maxillary contours less inflated, probably related to the presence of smaller canine roots. An association between root size reduction and a shift to a more functionally advantageous jaw morphology is worth investigating. Furthermore, the new Kanapoi fossils highlight the nature of Au. anamensis as a truly transitional species between a more primitive condition to what is seen in Au. afarensis, and to some extent later hominins.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Dental evolution in Australopithecus Australopithecus anamensis was not just a primitive version of Au. afarensis, it was the species at the root of the Australopithecus – human clade in which some key aspects of Australopithecus morphology were developing (see also Haile-Selassie et al. 2010). At the same time, not all of the characteristics seen in Au. afarensis were present at the origin of the Australopithecus – human clade, so not all distinguish members of this clade from its sister taxa. Whether apparent dietary evolution co-occurred with shifts in locomotor or manipulative adaptations, body size, dimorphism, cranial morphology or brain size during the early evolution of the Australopithecus– human clade can only be elucidated with more fossils from the time of first occurrence of Australopithecus (4.17 Ma) and Au. afarensis from Hadar (3.4–3.0 Ma). We hypothesize that Au. anamensis is best viewed as not simply a primitive precursor to Au. afarensis, but rather part of a dynamic morphological transition from a primitive, ape-like morphology to the unique set of morphological adaptations and behaviours that characterized the australopithecine bauplan and the early evolution of the Australopithecus–human clade. We thank the National Museums of Kenya, Emma Mbua, Robert Moru, the Royal Museum of Central Africa, Cleveland Museum of Natural History and United States National Museum for access to specimens. We thank Chris Dean, Bill Kimbel, Meave Leakey, Faydre Paulus, Matt Ravosa, Peter Ungar and Bernard Wood for assistance, advice and helpful discussions. We thank Alan Walker and Chris Stringer for generously inviting us to participate in this symposium. We thank the Wenner Gren Foundation, Leakey Foundation, Turkana Basin Institute and National Science Foundation for support in various aspects of this project.

REFERENCES Bailit, H. & Friedlaender, J. 1966 Tooth size reduction: a hominid trend. Am. Anthropol. 68, 665 –672. (doi:10. 1525/aa.1966.68.3.02a00030) Beard, K. C., Teaford, M. F. & Walker, A. 1986 New wrist bones of Proconsul africanus and P. nyanzae from Rusinga Island, Kenya. Folia Primatol. 47, 97–118. (doi:10.1159/ 000156268) Brace, C. 1963 Structural reduction in evolution. Am. Nat. 97, 39–49. (doi:10.1086/282252) Brace, C. L. 1971 Sexual dimorphism in human evolution. Nature 228, 31–49. Brunet, M. et al. 2002 A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418, 145–151. (doi:10.1038/nature00879) Calcagno, J. & Gibson, K. 1988 Human dental reduction: natural selection or probable mutation effect? Am. J. Phys. Anthropol. 77, 505–517. (doi:10.1002/ajpa.1330770411) Cobb, S. & Willis, A. 2008 Is premaxilla morphology determined by the spatial requirements of the developing incisor dentition? Am. J. Phys. Anthropol. 135, 79– 80. Darwin, C. 1871 The descent of man and selection in relation to sex. London, UK: John Murray. Fleagle, J. G., Rasmussen, D. T., Yirga, S., Bown, T. M. & Grine, F. E. 1991 New hominid fossils from Fejej, Southern Ethiopia. J. Hum. Evol. 21, 145 –152. (doi:10. 1016/0047-2484(91)90005-G) Greenfield, L. O. 1992 Origin of the human canine: a new solution to an old enigma. Yrbk Phys. Anthropol. 35, 153 –185. (doi:10.1002/ajpa.1330350607) Phil. Trans. R. Soc. B (2010)

C. V. Ward et al.

3343

Haile-Selassie, Y. 2001 Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412, 187–191. (doi:10. 1038/35084063) Haile-Selassie, Y. 2004 Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303, 1503–1505. (doi:10.1126/science.1092978) Haile-Selassie, Y. 2010 Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia). Phil. Trans. R. Soc. B 365, 3323–3331. (doi:10.1098/rstb.2010.0064) Haile-Selassie, Y., Saylor, B. Z., Deino, A., Alene, M. & Latimer, B. M. 2010 New hominid fossils from Woranso-Mille (Central Afar, Ethiopia) and taxonomy of early Australopithecus. Am. J. Phys. Anthropol. 141, 406–417. (doi:10.1002/ajpa.21159) Heinrich, R. E., Rose, M. D., Leakey, R. E. & Walker, A. C. 1993 Hominid radius from the middle Pliocene of Lake Turkana, Kenya. Am. J. Phys. Anthropol. 92, 139– 148. (doi:10.1002/ajpa.1330920203) Hylander, W. L. 1984 Stress and strain in the mandibular symphysis of primates: a test of competing hypotheses. Am. J. Phys. Anthropol. 64, 1 –46. (doi:10.1002/ajpa. 1330640102) Hylander, W. L. 1985 Mandibular function and biomechanical stress and scaling. Am. Zool. 25, 315 –330. (doi:10. 1093/icb/25.2.315) Johanson, D., White, T. & Coppens, Y. 1982 Dental remains from the Hadar Formation, Ethiopia: 1974–1977 collections. Am. J. Phys. Anthropol. 57, 545 –604. (doi:10.1002/ajpa.1330570406) Jungers, W. 1978 On canine reduction in early hominids. Curr. Anthropol. 51, 155 –156. Kimbel, W. H., Rak, Y. & Johanson, D. 2004 The skull of Australopithecus afarensis. New York, NY: Oxford University Press. Kimbel, W., Lockwood, C., Ward, C. V., Leakey, M., Rak, Y. & Johanson, D. 2006 Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. J. Hum. Evol. 51, 134–152. (doi:10.1016/j.jhevol. 2006.02.003) Leakey, M. G., Feibel, C. S., McDougall, I. & Walker, A. 1995 New four-million-year-old hominid species from Kanapoi and Alia Bay, Kenya. Nature 376, 565 –571. (doi:10.1038/376565a0) Leakey, M. G., Feibel, C. S., MacDougall, I., Ward, C. V. & Walker, A. 1998 New specimens and confirmation of an early age for Australopithecus anamensis. Nature 363, 62–66. Leutenegger, W. & Kelly, J. T. 1977 Relationship of sexual dimorphism in canine size and body size to social, behavioral, and ecological correlates in anthropoid primates. Primates 18, 117 –136. (doi:10.1007/BF02382954) Lovejoy, C. O. 1981 The origin of man. Science 211, 341–350. (doi:10.1126/science.211.4480.341) Lovejoy, C. 2009 Reexamining human origins in light of Ardipithecus ramidus. Science 326, 74e1–74e8. (doi:10. 1126/science.1175834) Lovejoy, C., Simpson, S., White, T., Asfaw, B. & Suwa, G. 2009 Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive. Science 326, 70e1–70e8. (doi:10.1126/science.1175827) Manthi, F., Plavcan, J. & Ward, C. V. In preparation. New fossils attributed to Australopithecus anamensis from Kanapoi, Kenya. Patterson, B. & Howells, W. W. 1967 Hominid humeral fragment from early Pleistocene of Northwestern Kenya. Science 156, 64–66. (doi:10.1126/science.156. 3771.64) Plavcan, J. M. 1990 Sexual dimorphism in the dentition of extant anthropoid primates. PhD dissertation, Duke University. University Microfilms: Ann Arbor, MI.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3344

C. V. Ward et al.

Dental evolution in Australopithecus

Plavcan, J. & Daegling, D. 2006 Interspecific and intraspecific relationships between tooth size and jaw size in primates. J. Hum. Evol. 51, 171– 184. (doi:10.1016/j. jhevol.2006.02.005) Plavcan, J. M. & Van Schaik, C. P. 1997 Intrasexual competition and body weight dimorphism in anthropoid primates. Am. J. Phys. Anthropol. 103, 37–68. (doi:10.1002/(SICI)10968644(199705)103:1,37::AID-AJPA4.3.0.CO;2-A) Plavcan, J. M., Van Schaik, C. & Kappeler, P. 1995 Competition, coalitions and canine size in primates. J. Hum. Evol. 28, 245 –276. (doi:10.1006/jhev.1995.1019) Plavcan, J. M., Ward, C. V. & Paulus, F. 2009 Estimating canine tooth crown height in early Australopithecus. J. Hum. Evol. 57, 2–10. (doi:10.1016/j.jhevol.2009.04. 005) Prinz, J. & Lucas, P. 2000 Saliva tannin interactions. J. Oral Rehabil. 27, 991 –994. (doi:10.1046/j.1365-2842.2000. 00578.x) Puech, F. 1986 Australopithecus afarensis Garusi 1, diversite´ et spe´cialisation des premiers Hominide´s d’apre`s les caracte`res maxillo-dentaires. C. R. Acad. Sci., Paris 303, 1819–1823. Puech, P. F., Cianfarani, F. & Roth, H. 1986 Reconstruction of the maxillary dental arcade of Garusi Hominid 1. J. Hum. Evol. 15, 325 –332. (doi:10.1016/S00472484(86)80015-X) Ravosa, M. J. 2000 Size and scaling in the mandible of living and extinct apes. Folia Primatol. 71, 305–322. (doi:10. 1159/000021754) Ryan, A. & Johanson, D. 1989 Anterior dental microwear in Australopithecus afarensis: comparisons with human and nonhuman primates. J. Hum. Evol. 18, 235 –268. (doi:10.1016/0047-2484(89)90051-1) Spencer, M. A. 2003 Tooth-root form and function in platyrrhine seed-eaters. Am. J. Phys. Anthropol. 122, 325 –335. (doi:10.1002/ajpa.10288) Suwa, G., Kono, R., Simpson, S., Asfaw, B., Lovejoy, C. & White, T. 2009 Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 94–99. (doi:10.1126/science.1175824) Szalay, F. S. 1975 Hunting-scavenging protohominids: a model for hominid origins. Man 10, 420– 429. (doi:10. 2307/2799811)

Phil. Trans. R. Soc. B (2010)

Teaford, M. F. & Ungar, P. S. 2000 Diet and the evolution of the earliest human ancestors. Proc. Natl Acad. Sci. USA 97, 13 506–13 511. (doi:10.1073/pnas.260368897) Ward, C. V., Leakey, M. G., Brown, B., Brown, F., Harris, J. & Walker, A. 1999a South Turkwel: a new Pliocene hominid site in Kenya. J. Hum. Evol. 36, 69–95. (doi:10.1006/jhev. 1998.0262) Ward, C. V., Walker, A. & Leakey, M. G. 1999b The new hominid species Australopithecus anamensis. Evol. Anthropol. 7, 197–205. (doi:10.1002/(SICI)15206505(1999)7:6,197::AID-EVAN4.3.0.CO;2-T) Ward, C. V., Leakey, M. & Walker, A. 2001 Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J. Hum. Evol. 41, 255– 368. (doi:10.1006/jhev. 2001.0507) White, T. D., Suwa, G. & Asfaw, B. 1994 Australopithecus ramidis, a new species of early hominid from Aramis, Ethiopia. Nature 371, 306– 312. (doi:10.1038/371306a0) White, T. D., Suwa, G. & Asfaw, B. 1995 Corrigendum. Nature 375, 88. White, T., Suwa, G., Simpson, S. & Asfaw, B. 2000 Jaws and teeth of Australopithecus afarensis from Maka, Middle Awash, Ethiopia. Am. J. Phys. Anthropol. 111, 45–68. (doi:10.1002/(SICI)1096-8644(200001)111: 1,45::AID-AJPA4.3.0.CO;2-I) White, T. et al. 2006 Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883 –889. (doi:10.1038/ nature04629) White, T., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, C., Suwa, G. & WoldeGabriel, G. 2009 Ardipithecus ramidus and the paleobiology of early hominids. Science 326, 75–86. (doi:10.1126/science.1175802) Wolpoff, M. 1969 The effect of mutations under conditions of reduced selection. Soc. Biol. 16, 11– 23. Wolpoff, M. H. 1978 Some aspects of canine size in the australopithecines. J. Hum. Evol. 7, 115–126. (doi:10. 1016/S0047-2484(78)80003-7) Wolpoff, M. H. 1979 Anterior dental cutting in the Laetolil hominids and the evolution of the bicuspid P3. Am. J. Phys. Anthropol. 51, 233– 234. (doi:10.1002/ajpa. 1330510210) Wolpoff, M. 1980 Paleoanthropology. New York, NY: Knopf.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3345–3354 doi:10.1098/rstb.2010.0033

Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis Peter S. Ungar1,*, Robert S. Scott2, Frederick E. Grine3 and Mark F. Teaford4 1

Department of Anthropology, University of Arkansas, Old Main 330, Fayetteville, AR 72701, USA 2 Department of Anthropology, Rutgers University, New Brunswick, NJ, USA 3 Departments of Anthropology and Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA 4 Center for Functional Anatomy and Evolution, Johns Hopkins University, Baltimore, MD, USA Many researchers have suggested that Australopithecus anamensis and Australopithecus afarensis were among the earliest hominins to have diets that included hard, brittle items. Here we examine dental microwear textures of these hominins for evidence of this. The molars of three Au. anamensis and 19 Au. afarensis specimens examined preserve unobscured antemortem microwear. Microwear textures of these individuals closely resemble those of Paranthropus boisei, having lower complexity values than Australopithecus africanus and especially Paranthropus robustus. The microwear texture complexity values for Au. anamensis and Au. afarensis are similar to those of the grass-eating Theropithecus gelada and folivorous Alouatta palliata and Trachypithecus cristatus. This implies that these Au. anamensis and Au. afarensis individuals did not have diets dominated by hard, brittle foods shortly before their deaths. On the other hand, microwear texture anisotropy values for these taxa are lower on average than those of Theropithecus, Alouatta or Trachypithecus. This suggests that the fossil taxa did not have diets dominated by tough foods either, or if they did that directions of tooth – tooth movement were less constrained than in higher cusped and sharper crested extant primate grass eaters and folivores. Keywords: Australopithecus; molar; diet; microwear textures

1. INTRODUCTION Researchers have recognized for more than three decades that patterns of microscopic use wear on teeth hold the potential to provide information about the diets of early hominins (e.g. Grine 1977, 1981, 1986; Puech 1979; Ryan 1980; Walker 1981; Ungar et al. 2006). Many studies of hominin dental microwear have been published over the past thirty years, including feature-based quantitative analyses of molar occlusal surface microwear in Australopithecus afarensis 1 and Australopithecus anamensis (Grine et al. 2006a,b). Data presented here extend this work by comparing the microwear textures of these species with those of other early hominins and recent primate taxa with known diets. Results indicate that sampled Au. anamensis and Au. afarensis individuals tend to have relatively simple microwear surface textures varying in degree of anisotropy. This pattern is comparable to that previously reported for Paranthropus boisei (Ungar et al. 2008), but differs from that of Au. africanus, and especially of Paranthropus robustus (Scott et al. 2005; see also Grine 1986).

* Author for correspondence ([email protected]). One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

(a) Background Australopithecus anamensis and Au. afarensis have traditionally been argued to be the earliest hominins to show an adaptive shift from diets dominated by soft, sugary forest fruits to hard and brittle or abrasive foods (Ward et al. 1999; Teaford & Ungar 2000; White et al. 2000; Wood & Richmond 2000; Walker 2002; Macho et al. 2005). Australopithecus afarensis, for example, has long been noted to have thickly enamelled, large and flat crowned cheek teeth and robustly constructed crania and mandibles, at least when compared with our nearest living relatives, the chimpanzees (e.g. McHenry 1984; Hylander 1988; White et al. 2000). This enhanced craniodental toolkit has led workers to suggest that ‘nuts, seeds, and hard fruit may have been an important component to the diet of this species’ (Wood & Richmond 2000). These hominins have also been thought to have had dietary adaptations intermediate between those of frugivorous forest apes and later hominins. White et al. (2000), for example, considered them to have taken the ‘initial functional steps that would eventually culminate in the far more derived, specialized masticatory apparatus of later hominid species’ such as Au. africanus and especially Par. boisei and Par. robustus. As White et al. (1981) noted, while Au. africanus showed several craniodental features foreshadowing the functional specializations seen in

3345

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3346

P. S. Ungar et al.

Pliocene hominin microwear textures

Paranthropus, Au. afarensis retained at least some more primitive traits, such as relatively larger front teeth and less swollen and inflated cusps on their postcanines. Picq (1990) further suggested that the height and thickness of the Au. afarensis mandibular corpus, and robusticity of the symphysis, were intermediate between those of chimpanzees on the one hand and those of Au. africanus and especially Paranthropus species on the other. He argued the same for the height of the ramus and size of the mandibular condyle. Picq (1990) used these lines of evidence to build a scenario in which Au. afarensis was still dependent on the fruits of the forest, but seasonally sought sustenance in more open settings with ‘tougher foods containing abrasive structures’ and ‘nuts protected by skins or a hard shell’. Ungar & Teaford (2001) called this a ‘mixed forest–savanna resource adaptation’. Ungar (2004) further noted that the degree of differences in occlusal slope and relief between Au. afarensis and chimpanzees are as expected for differences in ‘fallback’ foods, suggesting that the early hominins may have preferred soft, sugar-rich fruits, but had the ability to make more effective use of hard, brittle resources as seasonal availabilities required. Following its initial description, Au. anamensis quickly took on the role of ‘intermediate form’ in terms of dietary adaptation between the earlier Ardipithecus and Au. afarensis. Like Au. afarensis, Au. anamensis had thicker post-canine tooth enamel and larger average cheek teeth than Ardipithecus, again suggesting a dietary shift towards harder foods or more abrasive ones (Ward et al. 1999; Teaford & Ungar 2000; Wood & Richmond 2000; Walker 2002; Suwa et al. 2009). Still, in comparison with Au. afarensis, Au. anamensis molars were ‘not very high-crowned’ (Walker 2002), and the larger values for enamel thickness in Au. anamensis when compared with Ar. ramidus may reflect, at least in part, increased tooth size in the former (Suwa et al. 2009, supporting online material). Further, Au. anamensis lacked changes in the geometry of the mandible and maxilla seen in Au. afarensis, Au. africanus and especially Paranthropus (Ward et al. 1999), such as greater mandibular corpus robusticity, which might buttress the jaw against higher peak force magnitudes or repetitive loading in mastication (Teaford & Ungar 2000). These differences led Teaford & Ungar (2000) to speculate that hard and perhaps abrasive foods may have become even more important components of the diet of Au. afarensis. Walker (2002) suggested that changes from Au. anamensis to Au. afarensis were carried to extremes in Au. africanus and especially Paranthropus. The microwear evidence paints a somewhat more complex picture. One might predict heavy pitting associated with hard-object consumption in Au. anamensis and Au. afarensis and an increase in pitting from the earlier to the later species. Contrary to expectation though, both show fairly fine features and microwear surfaces dominated by striations rather than pits (Grine et al. 2006a,b; Suwa et al. 2009, supporting online material). This pattern is more similar to that seen in the tough food folivore Gorilla gorilla beringei than in hard-object feeders, Phil. Trans. R. Soc. B (2010)

such as the grey-cheeked mangabey Lophocebus albigena and the brown capuchin, Cebus apella. Further, the microwear pattern for these hominins is remarkably homogeneous between specimens across both time and paleoecological context. Grine et al. (2006a,b) suggest that these results highlight the difference between ‘faculty’ and ‘biological role’ (Bock & von Wahlert 1965) or dietary potential and what an animal eats on a day-to-day basis. As a result, Grine et al. (2006a,b) suggested that the shift in diet-related adaptive morphology in Au. anamensis and Au. afarensis may relate more to occasional but critical fallback food exploitation than to preferred resources. We might predict, if Au. africanus and especially Par. boisei and Par. robustus show further craniodental specializations for the consumption of hard, brittle foods, that samples of these species should have more individuals showing high levels of microwear pitting or surface complexity with fewer fine, parallel striations and with texture anisotropy, compared with Au. afarensis and especially Au. anamensis. Here we present the first microwear texture analysis of Au. afarensis and Au. anamensis for comparison with Au. africanus, Par. boisei and Par. robustus. Microwear texture analysis has proved to provide a threedimensional characterization of microwear surfaces free from the need to identify and measure individual features (e.g. Ungar et al. 2003, 2007a,b, 2008; Scott et al. 2005, 2006, 2009a; El-Zaatari 2008; Krueger et al. 2008; Ungar & Scott 2009; Krueger & Ungar in press). While microwear texture analysis and conventional feature-based analyses to date have yielded similar results for other hominins (compare Grine (1986) with Scott et al. (2005) and Ungar et al. (2006) with Ungar & Scott (2009)), texture analyses are particularly well suited for between-studies comparisons, because data collected are free from observer measurement error. Further, microwear texture results for Au. africanus, Par. robustus and Par. boisei are available in the literature for comparison (Scott et al. 2005; Ungar et al. 2008). Indeed, only texture data are available for Par. boisei. Microwear texture analysis studies indicate that hard-object feeding extant primates (and other mammals) tend to have higher average levels of texture complexity and lower levels of anisotropy on their molar occlusal surfaces than seen in tough food eaters (see Ungar et al. 2007b for a review). Here we test the hypothesis that interpretations of craniodental functional morphology described above are reflected in microwear texture patterns. If so, Au. afarensis and especially Au. anamensis specimens should show less surface complexity and more anisotropy than those of Au. africanus, and especially Par. boisei and Par. robustus.

2. MATERIAL AND METHODS Dental microwear texture data are presented here for the molar teeth of Au. anamensis from Kanapoi and Allia Bay in Kenya and Au. afarensis from the Laetolil Beds in Tanzania and the Hadar Formation in Ethiopia. Specimens included in this study are the same as

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Pliocene hominin microwear textures

P. S. Ungar et al.

3347

Table 1. Microwear texture analysis data for Au. anamensis and Au. afarensis. specimen Au. anamensis KNM-ER 35236 KNM-KP 29287 KNM-KP 34725 Au. afarensis AL 128-23 AL 145-35 AL 188-1 AL 200-1b AL 225-8 AL 288-1i AL 333-74 AL 333w-12 AL 333w-1a AL 333w-57 AL 333w-59 AL 333w-60 AL 366-1 AL 400-1a AL 486-1 AL 487-1c LH4 LH 15 LH 22

Asfc

epLsar1.8

Smc

HAsfc9

HAsfc81

0.97466 0.80791 1.30999

0.00307 0.00299 0.00244

0.15015 0.20908 0.50835

0.58516 0.34424 0.38439

0.71286 0.58869 0.83670

0.64728 0.87280 0.53380 0.70342 1.06196 0.68804 0.53915 1.16543 0.71150 0.69913 0.19077 0.77945 0.85189 0.72866 0.97104 0.46932 0.54767 1.07480 0.82274

0.00122 0.00337 0.00390 0.00572 0.00594 0.00184 0.00602 0.00374 0.00553 0.00382 0.00285 0.00515 0.00090 0.00223 0.00139 0.00236 0.00163 0.00419 0.00319

0.70776 0.26841 0.34143 0.21016 0.26836 1.20858 0.50798 0.27184 0.59957 0.34153 0.94135 0.41635 0.59981 0.41634 0.15015 0.26690 2.40210 0.20835 0.59962

0.30052 0.45188 0.29913 0.40769 0.61132 0.34728 0.24058 0.45849 0.32997 0.26405 0.34335 0.31759 0.35013 0.26509 0.38916 0.36286 0.27204 0.72182 0.25273

0.37230 0.56429 0.33684 0.57363 0.99634 0.49713 0.33415 0.50411 0.37838 0.31046 0.38715 0.36561 0.42788 0.38790 0.44262 0.39707 0.29177 0.87299 0.31400

those employed in feature-based SEM microwear analyses reported by Grine et al. (2006a,b). All permanent molars available to us were first examined to determine the suitability for microwear analysis. Those that preserved wear facets were cleaned with cotton swabs soaked in alcohol or acetone to remove adherent dirt or preservatives. Moulds of occlusal surfaces were then made using President Jet Regular Body vinyl dental impression material (Colte`ne-Whaledent Corp.), and casts were produced from these molds using Epotek 301 epoxy and hardener (Epoxy Technologies Inc.). Replicas were examined by light microscopy and SEM as necessary to determine the suitability for microwear analysis following the criteria described by Teaford (1988). Most specimens had occlusal surfaces obscured by taphonomic damage and so had to be excluded from this study. In the end, the molars of only three of the Au. anamensis specimens and 19 Au. afarensis individuals available to us were found to preserve unobscured antemortem occlusal surface microwear. A list of all specimens considered can be found in Grine et al. (2006a,b) and those included in this study are presented in table 1. All specimens included in this study were analysed using a Sensofar Plm white-light confocal profiler (Solarius, Inc.) with an integrated vertical scanning interferometer. Three-dimensional point clouds were collected for ‘phase II’ facets (the buccal occlusal surfaces of lower molars and the lingual occlusal surface of uppers) using a 100 long working distance objective. The point clouds sampled elevations at intervals of 0.18 mm along the x- and y-axes, with a vertical resolution of 0.005 mm. Data were obtained for four adjacent fields on facets 9 or 10n, for a combined Phil. Trans. R. Soc. B (2010)

work envelope of 276 mm 204 mm. The featurebased study of these specimens reported in Grine et al. (2006a,b) used a pixel resolution of 0.25 mm and combined sample area of 0.04 mm2. Resulting point clouds were analysed using TOOTHFrax and SFRAX scale-sensitive fractal analysis (SSFA) software (Surfract Corp.). SSFA as applied to microwear research is described in detail elsewhere (e.g. Scott et al. 2006). The basic premise is that surface texture varies with scale of observation, and that this variation can be used to characterize functionally relevant aspects of microwear. SSFA texture variables included in this study are area-scale fractal complexity (Asfc), anisotropy (epLsar), scale of maximum complexity (Smc) and heterogeneity of complexity (HAsfc). Values for individual specimens are reported as medians of the four fields sampled for each specimen. Area-scale fractal complexity is a measure of change in roughness with scale. The faster a measured surface area increases with resolution, the more complex the surface. Anisotropy is characterized as variation in lengths of transect lines measured at a given scale (we use 1.8 mm) with orientations sampled at 58 intervals across a surface. An anisotropic surface will have shorter transects in the direction of the surface pattern than perpendicular to it (e.g. a transect that cross-cuts parallel scratches must trace the peaks and valleys of each individual feature). Thus, a heavily pitted surface typically has high Asfc and low epLsar values, whereas one dominated by homogeneous, parallel striations has low Asfc and high epLsar values. Other variables used to characterize microwear surface texture include Smc, the scale range over which Asfc is calculated, and HAsfc, variation of Asfc across a surface (in this

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3348

P. S. Ungar et al.

Pliocene hominin microwear textures

Table 2. Summary statistics for early hominins.

n Asfc mean s.d. epLsar mean s.d. Smc mean s.d. HAsfc9 mean s.d. HAsfc81 mean s.d.

Au. anamensis

Au. afarensis

Au. africanus

Par. boisei

Par. robustus

3

19

10

7

9

1.031 0.256

0.740 0.236

1.522 0.387

0.625 0.268

3.543 1.449

0.003 0.000

0.003 0.002

0.004 0.002

0.003 0.002

0.002 0.001

0.289 0.192

0.565 0.521

1.834 4.256

0.516 0.269

0.216 0.053

0.438 0.129

0.368 0.124

0.617 0.259

0.460 0.136

1.054 0.564

0.713 0.124

0.461 0.187

1.004 0.367

0.621 0.232

2.101 1.026

case, each field of view was divided into a 3 3 grid ¼ HAsfc9, and a 9 9 grid ¼ HAsfc81). High Smc values should correspond to more complex coarse features. High HAsfc values are observed for surfaces that vary in complexity across a facet. Statistical analyses focused on comparisons of microwear textures of Au. afarensis with those of Au. africanus and Par. robustus from South Africa as reported in Scott et al. (2005) and with Par. boisei from eastern Africa as reported by Ungar et al. (2008). Australopithecus anamensis data could not be compared statistically with those of the other hominins given an available sample of only three specimens, although newly recovered specimens (e.g. Haile-Selassie, this volume) hold the potential for larger microwear datasets in the future. First, differences in central tendencies between taxa were assessed using a MANOVA performed on ranked data (Conover & Iman 1981) for all variables (Asfc, epLsar, Smc, HAsfc9 and HAsfc81). Individual ANOVAs and multiple comparisons tests were used to determine the sources of significant variation. Both Tukey’s honestly significant difference (HSD) and Fisher’s least significant difference (LSD) tests were used to balance risks of type I and type II errors (Cook & Farewell 1996). Values of p , 0.05 for Tukey’s HSD tests may be assigned significance with some confidence, whereas values of p , 0.05 on Fisher’s LSD but not Tukey’s LSD tests are considered suggestive but of marginal significance. Degree of variance in microwear textures within taxa may be as important for distinguishing species as differences in central tendencies, especially given differences in foraging and feeding strategies between primates. With this in mind, raw data for each variable were transformed for Levene’s test following the procedure described by Plavcan & Cope (2001) to compare distribution variances between taxa. A MANOVA was used to assess the variation in variance between taxa, and as with the comparisons of central tendencies, ANOVAs and multiple comparisons tests were used to determine the sources of significant variation as needed. Complexity and anisotropy results for Au. anamensis and Au. afarensis were also compared with those for a Phil. Trans. R. Soc. B (2010)

series of extant primates with known differences in feeding behaviors to put the microwear texture analysis results for these hominins in the context of modern primate diets. The baseline series includes: (i) the mantled howler, Alouatta palliata and the silvered leaf monkey, Trachypithecus cristatus, C. apella and L. albigena from the dataset reported by Scott et al. (2005); (ii) G. gorilla beringei, G. g. gorilla, Pan troglodytes and the orangutan Pongo pygmaeus from Ungar et al. (2007b); and (iii) the yellow baboon Papio cynocephalus and the gelada baboon Theropithecus gelada from Scott et al. (2009b). The mantled howler and silvered leaf monkey are typically characterized as folivores, whereas the brown capuchin and greycheeked mangabey are considered to be hard-object fallback feeders. Among the great apes, chimpanzees are the most frugivorous, and gorillas, especially the G. g. beringei sample considered here (the Fossey collection at the US National Museum of Natural History), are the most folivorous (see references in Ungar et al. 2007b). Orangutans are intermediate in their diets. Finally, geladas are specialized grass eaters, whereas yellow baboons have a more catholic diet including fruits, leaves and animal prey (see Post 1982; Norton et al. 1987; Dunbar 1988; Altmann 1998; Pochron 2000; Bentley-Condit 2009). 3. RESULTS Results for Au. anamensis and Au. afarensis are presented in tables 1–4 and are illustrated in figures 1 and 2. (a) Comparisons with other fossil hominins The early hominins are well-separated from one another by microwear texture complexity. First, the specimens from South Africa have higher Asfc values on average than those from eastern Africa, regardless of the species considered. Within the eastern African sample, Au. anamensis may have slightly higher complexity on average than Au. afarensis or Par. boisei, but larger samples of Au. anamensis are really needed to evaluate this (only one Au. anamensis specimen is outside the range of Au. afarensis or Par. boisei). No significant variation in

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Pliocene hominin microwear textures

P. S. Ungar et al.

3349

Table 3. Analyses of hominin microwear texture data (central tendencies). All data rank transformed to mitigate violation of assumptions inherent to parametric statistics (Conover & Iman 1981). *p , 0.05 for Fisher’s LSD test, **p , 0.05 for both Tukey’s HSD and Fisher’s LSD tests (shown in italic). value multivariate test results Wilks’s l Pillai trace Hotelling–Lawley trace

d.f.

F

539 539 539

p-value

0.037 0.963 26.382

205.783 205.783 205.783

0.000 0.000 0.000

ANOVA test results F d.f. p-value

Asfc 32.397 443 0.000

epLsar 2.735 443 0.041

Smc 4.056 443 0.007

HAsfc9 12.096 443 0.000

HAsfc81 23.204 443 0.000

paired comparisons Au. afarensis Au. africanus Au. afarensis Au. anamensis Au. afarensis Par. boisei Au. afarensis Par. robustus Au. africanus Au. anamensis Au. africanus Par. boisei Au. africanus Par. robustus Au. anamensis Par. boisei Au. anamensis Par. robustus Par. boisei Par. robustus

Asfc 219.279** 29.579* 4.564 227.357** 9.700 23.843** 28.078* 14.143* 217.778** 231.921**

epLsar 26.037 1.596 2.977 13.263* 7.633 9.014 19.300** 1.381 11.667 10.286

Smc 21.084 12.649 22.613 16.705** 13.733 21.529 17.789** 215.262 4.056 19.317**

HAsfc9 215.421** 26.421 28.421 227.088** 9.000 7.000 211.667* 22.000 220.667** 218.667**

HAsfc81 219.616** 212.982* 28.887* 229.982** 6.633 10.729* 210.367* 4.095 217.000** 221.095**

Table 4. Analyses of hominin microwear texture data (variance). Microwear data transformed for Levene’s test (X 0 ¼ jX— mean (X)j) following Plavcan & Cope (2001). *p , 0.05 for Fisher’s LSD test, **p , 0.05 for both Tukey’s HSD and Fisher’s LSD tests (shown in italic).

multivariate test results Wilks’s l Pillai trace Hotelling–Lawley trace ANOVA test results F d.f. p-value paired comparisons Au. afarensis Au. africanus Au. afarensis Au. anamensis Au. afarensis Par. boisei Au. afarensis Par. robustus Au. africanus Au. anamensis Au. africanus Par. bosei Au. africanus Par. robustus Au. anamensis Par. boisei Au. anamensis Par. robustus Par. boisei Par. robustus

value

F

d.f.

p-value

0.127 1.254 4.174 Asfc 24.38 443 0.000 Asfc 20.140 20.009 20.035 21.078** 0.131 0.105 20.938** 20.026 21.069** 21.043**

5.627 3.837 7.827 epLsar 3.828 443 0.010 epLsar 0.000 0.001* 0.000 0.001** 0.001 0.000 0.001* 20.001* 0.000 0.001**

20 130 20 168 20 150 Smc 3.822 443 0.010 Smc 22.087** 0.181 0.090 0.282 2.268* 2.177* 2.368** 20.091 0.101 0.191

0.000 0.000 0.000 HAsfc9 4.476 443 0.004 HAsfc9 20.118 20.010 20.023 20.305** 0.107 0.095 20.187* 20.012 20.294* 20.282**

complexity is noted between Au. afarensis and Par. boisei. Within the South African sample, Par. robustus has more complex microwear surfaces on average than Au. africanus. The Par. robustus sample also shows significantly greater variation in its complexity values than do any of the other taxa. All other taxa have similar levels of within-species variation in complexity. The species do not differ as much in anisotropy as they do in complexity, though Par. robustus has both a lower average epLsar and less variability in this variable than either Au. africanus or Au. afarensis. The Par. robustus sample also has a lower average scale of maximum complexity than Au. afarensis, Au. africanus Phil. Trans. R. Soc. B (2010)

HAsfc81 10.296 443 0.000 HAsfc81 20.157 0.048 20.072 20.68** 0.205 0.084 20.523** 20.120 20.728** 20.608**

or Par. boisei, though no other significant differences in Smc central tendencies are noted. In addition, Au. africanus has significantly greater variation in Smc values than Au. afarensis, Par. robustus and (marginally) both Au. anamensis and Par. boisei. It should be noted though that the high Au. africanus variance is driven by a single outlier with an extremely high Smc value. The Par. robustus sample also has higher average HAsfc values than Au. anamensis, Au. afarensis, Par. boisei or (at least marginally) Au. africanus. In addition, Au. africanus has higher HAsfc values than Au. afarensis. Further, Par. boisei has marginally lower HAsfc values than Au. africanus, but marginally higher

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3350

P. S. Ungar et al.

Pliocene hominin microwear textures

(a)

(b)

Figure 1. Photosimulations of molar microwear surfaces of (a) Au. anamensis and (b) Au. afarensis generated from point cloud data collected using the white-light confocal profiler. Each image represents a surface 208 mm 280 mm.

heterogeneity (at least for HAsfc81) than Au. afarensis. Finally, Par. robustus has more variation in its HAsfc values than Au. anamensis, Au. afarensis, Au. africanus and Par. boisei. In summary, Au. afarensis microwear textures are most similar to those of Par. boisei, with the only difference being a marginally higher average value for one of the heterogeneity measures. Australopithecus afarensis also has lower complexity on average and less heterogeneity than Au. africanus, as well as less variation in scale of maximum complexity (though the latter result is driven largely by a single outlier). Australopithecus afarensis differs most markedly from Par. robustus. Australopithecus afarensis has lower complexity and heterogeneity of complexity, higher scale of maximum complexity, and marginally higher anisotropy. The degree of variation in anisotropy values is also greater for Au. afarensis, though the variation in complexity and heterogeneity are greater in Par. robustus. In fact, Par. robustus is very much the ‘outlier’ compared with the other taxa in most cases. This hominin tends towards a greater spread in and larger average values for complexity, scale of maximum complexity and heterogeneity of complexity, though less spread in, and lower values for anisotropy. Results for Au. anamensis are more difficult to have confidence in, given its sample size, though these do separate clearly from Par. robustus. There are some additional ‘hints’ suggested by the data if the patterns hold with larger samples. Australopithecus anamensis has marginally higher average complexity and lower variation Phil. Trans. R. Soc. B (2010)

in anisotropy than either Au. afarensis or Par. boisei, as well as marginally higher heterogeneity than Au. afarensis. These results will be of limited interpretability until larger samples are available for study. (b) Comparisons with extant primates Microwear complexity and anisotropy results for Au. anamensis and Au. afarensis are illustrated alongside data for living primates in figure 3. These hominins are on the low end for both Asfc and epLsar, both in their means and in their variations, when considered in light of the extant primate baseline. The distributions and central tendencies of complexity values for these hominins are most comparable to those reported for A. palliata, T. gelada and T. cristatus. They lack the degrees of dispersion in Asfc seen in the other primates, especially C. apella, P. cynocephalus and L. albigena. In contrast, the anisotropy values for the hominins are most different from those for A. palliata, T. gelada and T. cristatus and are more similar to those of the other primates, especially P. troglodytes and P. cynocephalus. 4. DISCUSSION (a) Microwear and the diets of Au. anamensis and Au. afarensis Dental microwear texture analysis results suggest that neither the Au. anamensis nor the Au. afarensis individuals included in this study had diets dominated by hard, brittle foods in the days, weeks or perhaps even months prior to their deaths. While these species have been suggested to show an adaptive shift from diets dominated by soft forest fruits to hard, brittle foods (e.g. Ward et al. 1999; Teaford & Ungar 2000; White et al. 2000; Wood & Richmond 2000; Walker 2002), none of the specimens examined exhibit the high microwear surface texture complexity expected of a hard-object feeder. The distribution of Asfc values more closely resembles those of the grasseating T. gelada and the folivores A. palliata and T. cristatus than hard-object feeding L. albigena or C. apella. The anisotropy results for Au. anamensis and Au. afarensis are, on the other hand, most different from those of A. palliata, T. cristatus and T. gelada among the baseline series. These three extant primates have higher average anisotropy values than the early hominins. High anisotropy is often taken as a proxy for tough food consumption and repetitive chew cycles with opposing teeth moving past one another along constrained paths. At first glance, this might suggest that Au. anamensis and Au. afarensis specimens sampled also avoided tough foods in the period prior to death, although the combination of low anisotropy and low complexity averages in Au. anamensis and Au. afarensis is unusual for primates. Most extant primate samples published to date have either high anisotropy averages combined with low complexity values, associated with the consumption of tough foods, or low anisotropy combined with high complexity averages consistent with a hard-brittle item diet. We propose that Au. anamensis and Au. afarensis may have indeed consumed tough foods, but that their

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Pliocene hominin microwear textures

P. S. Ungar et al.

3351

anisotropy (epLsar1.8)

(a) 0.008 0.007 0.006 0.005 0.004 0.003 0.002 0.001 1

0

heterogeneity (HAsfc81)

(b)

2

3 complexity (Asfc)

4

5

6

4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0

2

4

6

8

10

12

14

16

scale of maximal complexity (Smc) Figure 2. Plots of (a) anisotropy versus complexity and (b) heterogeneity of complexity versus scale of maximum complexity (below) for early hominin individuals considered by taxon. Open triangle, Au. afarensis; filled triangle, Au. africanus; open circle, Par. boisei; filled circle, Par. robustus; diamond, Au. anamensis.

0.01 0.005 0

A. palliata

G. g. gorilla

0.01 0.005 0

T. gelada

G. gorilla beringei

0.01 0.005 0

T. cristatus

P. troglodytes

0.01 0.005 0

Au. afarensis

L. albigena

Au. anamensis

P. cynocephalus

P. pygmaeus

C. apella

0.01 0.005 0 0.01 0.005 0

5

10

15

20

0

5

10

15

20

Figure 3. Plots of anisotropy versus complexity for various extant primates, compared with data for Au. anamensis and Au. afarensis.

anisotropy values are low because their dentognathic morphology did not limit occlusal movements to the degree presumed for primates with steeper occlusal surfaces, such as A. palliata, T. cristatus and T. gelada. The flatter teeth of early hominins offer fewer constraints to masticatory movements during food fracture and may therefore allow ‘grinding’ action (sensu Simpson 1933; Phil. Trans. R. Soc. B (2010)

Kay & Hiiemae 1974), wherein food items are milled between opposing surfaces. The combination of flat teeth and tough foods would be expected to result in a combination of low complexity and low anisotropy. Still, the relationship between microwear feature anisotropy and occlusal topographic relief remains to be investigated fully.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3352

P. S. Ungar et al.

Pliocene hominin microwear textures

(b) Comparisons with other early hominins Studies of craniodental functional morphology have suggested to several researchers a tendency towards increasing specialization for hard objects from Au. anamensis to Au. afarensis, Au. africanus and finally Par. robustus and Par. boisei (see White et al. 1981, 2000; Ward et al. 1999; Teaford & Ungar 2000; Wood & Richmond 2000; Walker 2002). Australopithecus africanus evinces a higher average Asfc than Au. afarensis, and Par. robustus has an even higher average Asfc value. The same is true for heterogeneity and variation in the scale of maximum complexity (though the latter result appears to be driven by a single outlier). These findings are all consistent with an increasing component of hard, brittle items in the diet of Au. africanus compared with Au. afarensis and Par. robustus compared with Au. africanus. On the other hand, the distribution of Asfc values for Par. boisei is very similar to that of Au. afarensis. Further, while the sample for Au. anamensis is too small for a reasonable comparison with other taxa, its mean Asfc value and heterogeneity are, if anything, slightly higher than that of Au. afarensis. Thus, if high texture complexity is considered to be a proxy for the consumption of hard, brittle items, there is no evidence for an increase in the role of such foods in the diet from Au. anamensis to Au. afarensis to Par. boisei. Ungar et al. (2008) remarked on the apparent discordance between microwear in Par. boisei and biomechanical models for this species based on craniodental functional morphology. They proposed that Par. boisei may represent a hominin example of Liem’s Paradox, wherein craniodental specializations developed as an adaptation to processing less preferred, mechanically challenging foods, even though the microwear suggests that these hominins rarely consumed such foods. This does not, however, explain either the microwear differences between Par. boisei and Par. robustus (given similarities in their gnathodental adaptations) or the similarities between Par. boisei, Au. anamensis and Au. afarensis (given differences in their gnathodental adaptations). The story becomes even more complicated when we consider these taxa in their presumed phylogenetic contexts, especially the purported anagenetic lineage leading from Au. anamensis to Au. afarensis, Par. aethopicus and finally Par. boisei (Kimbel et al. 2006; Rak et al. 2007). Many workers have suggested an ancestor – descendant relationship between Au. anamensis and Au. afarensis (Ward et al. 1999, 2001; White et al. 2000, 2006; Walker 2002). Such relationships are consistent with numerical cladistic studies (Strait et al. 1997; Strait & Grine 2004) and with changes in dentognathic characters among temporally successive samples from Kanapoi, Allia Bay, Laetoli and Hadar (Kimbel et al. 2006). Studies of cranial morphology have suggested that the pattern of intracranial venous sinus drainage is shared between Au. afarensis and Paranthropus species for the exclusion of Au. africanus and Homo (Falk & Conroy 1983; Kimbel 1984; Falk 1988), and additional fossils have reinforced this similarity (Kimbel et al. 2004; de Ruiter et al. 2006). Kimbel et al. (2004) have, moreover, identified an additional Phil. Trans. R. Soc. B (2010)

six cranial characters that Au. afarensis shares with one or more species of Paranthropus, although they regarded them, like the pattern of intracranial venous drainage, as being homoplastic. Most recently, similarities in ramal morphology between Au. afarensis and Par. robustus mandibles have been observed by Rak et al. (2007), who interpreted them as synapomorphies, suggesting that Au. afarensis and Par. robustus are united in a single clade and that this possibly includes Par. aethiopicus and Par. boisei, although no fossils attributable to the latter two species preserve the relevant anatomy. The evidence suggesting an ancestor – descendant relationship between Au. afarensis and Paranthropus, and particularly that for an Au. afarensis – Par. aethiopicus – Par. boisei lineage in eastern Africa, is not wholly inconsistent with their hypothesized cladistic relationships (Strait et al. 1997; Kimbel et al. 2004; Strait & Grine 2004). Similarities in microwear texture results for Au. anamensis, Au. afarensis and Par. boisei may make sense if these taxa comprise an anagenetic lineage and all shared food-type preferences. One possible scenario might be increasing craniodental specializations through the lineage for repetitive loading given consumption of tough foods in the face of morphological constraints imposed by relatively flat cheek teeth. This would be consistent with a C4 isotope signature in Par. boisei (van der Merwe et al. 2008) and the consumption of tough grasses or sedges, assuming that the specimens examined thus far are representative. Carbon stable isotope studies of Au. anamensis, Au. afarensis and additional Par. boisei specimens would provide a valuable test of this hypothesis. On the other hand, if Par. boisei and Par. robustus form a clade excluding Au. africanus, the two early hominins from South Africa probably independently increased their consumption of hard, brittle foods as evidenced by increased pit percentages in both hominins. In any case, the microwear texture patterns of the eastern African early hominins are more similar to one another than to those of the South African early hominins, independent of whether one is considering Australopithecus or Paranthropus. So in the end, what can be said of the microwear of Au. anamensis and Au. afarensis? We may reasonably infer that specimens examined for this study did not have a diet dominated by hard and brittle foods, at least shortly before death. Picq (1990) proposed that Au. afarensis often consumed soft foods that were not fracture resistant, but had craniomandibular adaptations for seasonal consumption of hard, brittle foods. Grine et al. (2006a,b) further suggested that traditional microwear results for both Au. anamensis and Au. afarensis are best explained by food preferences for less mechanically challenging foods, though as Ungar (2004) noted, their occlusal morphology would have allowed the consumption of hard, brittle items in times of dietary stress when favored foods were unavailable. The microwear texture analysis data presented here cannot be used to falsify the notion of rare hard-object feeding, but it also provides no evidence for it. Whether or not the craniodental specializations seen in Au. anamensis and Au. afarensis are adaptations for the occasional consumption of

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Pliocene hominin microwear textures hard, brittle foods, however, their microwear texture patterns are consistent with the regular consumption of softer and or tougher items. We are grateful to curators at the National Museums of Ethiopia, Kenya and Tanzania for permission to examine and make moulds of specimens in their care and thank Alejandro Pere´z-Pere´z for his assistance with preparing these replicas. Kristin Krueger helped with the preparation of figure 1. This study was funded by the US National Science Foundation.

ENDNOTE 1

One of us (F.E.G.) prefers the nomen Praeanthropus afarensis, as use of the generic name Australopithecus for Au. anamensis and Au. afarensis probably violates the criterion of monophyly (Grine & Strait 2000). Because of the lack of consensus among the authors on the taxonomy of these hominins, we employ here the more commonly used nomenclature.

REFERENCES Altmann, S. A. 1998 Foraging for survival: yearling baboons in Africa. Chicago, IL: University of Chicago Press. Bentley-Condit, V. K. 2009 Food choices and habitat use by the Tana River yellow baboons (Pap. cynocephalus): a preliminary report on five years of data. Am. J. Primatol. 71, 432 –436. (doi:10.1002/ajp.20670) Bock, W. J. & von Wahlert, G. 1965 The role of ecological factors in the origin of higher levels of organization. Syst. Zool. 14, 272–300. (doi:10.2307/2411681) Conover, W. J. & Iman, R. L. 1981 Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 35, 124– 129. (doi:10.2307/2683975) Cook, R. J. & Farewell, V. T. 1996 Multiplicity considerations in the design and analysis of clinical trials. J. R. Stat. Soc. 159, 93–110. de Ruiter, D. J., Steininger, C. M. & Berger, L. R. 2006 A cranial base of Australopithecus robustus from the hanging remnant of Swartkrans, South Africa. Am. J. Phys. Anthropol. 130, 435 –444. (doi:10.1002/ajpa.20386) Dunbar, R. I. M. 1988 Primate social systems. Ithaca, NY: Cornell University Press. El-Zaatari, S. 2008 Occlusal microwear texture analysis and the diets of historical/prehistoric hunter-gatherers. Int. J. Osteoarchaeol 20, 67– 87. (doi:10.1002/oa.1027) Falk, D. 1988 Enlarged occipital/marginal sinuses and emissary foramina: their significance in hominid evolution. In Evolutionary history of the ‘robust’ australopithecines (ed. F. E. Grine), pp. 85–96. New York, NY: Aldine de Gruyter. Falk, D. & Conroy, G. C. 1983 The cranial venous sinus system in Australopithecus afarensis. Nature 306, 779– 781. (doi:10.1038/306779a0) Grine, F. E. 1977 Analysis of early hominid deciduous molar wear by scanning electron microscopy: a preliminary report. Proc. Electr. Microscop. Soc. S. Afr. 7, 157 –158. Grine, F. E. 1981 Trophic differences between ‘gracile’ and ‘robust’ australopithecines: a scanning electron microscope analysis of occlusal events. S. Afr. J. Sci. 77, 203 –230. Grine, F. E. 1986 Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J. Hum. Evol. 15, 783– 822. (doi:10.1016/S0047-2484(86)80010-0) Grine, F. E. & Strait, D. S. 2000 The phylogenetic relationships of recently described early hominid species. Am. J. Phys. Anthropol. (Suppl. 30), 167. Grine, F. E., Ungar, P. S. & Teaford, M. F. 2006a Was the Early Piocene hominin ‘Australopithecus’ anamensis a hard object feeder? S. Afr. J. Sci. 102, 301 –310. Phil. Trans. R. Soc. B (2010)

P. S. Ungar et al.

3353

Grine, F. E., Ungar, P. S., Teaford, M. F. & El-Zaatari, S. 2006b Molar microwear in Praeanthropus afarensis: evidence for dietary stasis through time and under diverse paleoecological conditions. J. Hum. Evol. 51, 297 –319. (doi:10.1016/j.jhevol.2006.04.004) Hylander, W. L. 1988 Implications of in vivo experiments for interpreting the functional significance of ‘robust’ australopithecine jaws. In Evolutionary history of the ‘robust’ australopithecines (ed. F. E. Grine), pp. 55–83. New York, NY: Aldine de Gruyter. Kay, R. F. & Hiiemae, K. M. 1974 Jaw movement and tooth use in recent and fossil primates. Am. J. Phys. Anthropol. 40, 227 –256. (doi:10.1002/ajpa.1330400210) Kimbel, W. H. 1984 Variation in the pattern of cranial venous sinuses and hominid phylogeny. Am. J. Phys. Anthropol. 63, 243 –263. (doi:10.1002/ajpa. 1330630302) Kimbel, W. H., Rak, Y. & Johanson, D. C. 2004 The skull of Australopithecus afarensis. New York, NY: Oxford University Press. Kimbel, W. H., Lockwood, C. A., Ward, C. V., Leakey, M. G., Rak, Y. & Johanson, D. C. 2006 Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. J. hum. Evol. 51, 134 –152. (doi:10.1016/j.jhevol.2006.02.003) Krueger, K. L. & Ungar, P. S. In press. Incisor microwear textures of five bioarcheological groups. Int. J. Osteoarcheol. (doi:10:1002/oz.1093) Krueger, K. L., Scott, J. R. & Ungar, P. S. 2008 Technical note: dental microwear textures of ‘Phase I’ and ‘Phase II’ facets. Am. J. Phys. Anthropol. 137, 485–490. (doi:10. 1002/ajpa.20928) Macho, G. A., Shimizu, D., Jiang, Y. & Spears, L. R. 2005 Australopithecus anamensis: a finite element approach to studying the functional adaptations of extinct hominins. Anat. Rec. 283A, 310–318. (doi:10.1002/ar.a.20175) McHenry, H. M. 1984 Relative cheek tooth size in Australopithecus. Am. J. Phys. Anthropol. 64, 297– 306. (doi:10.1002/ajpa.1330640312) Norton, G. W., Rhine, R. J., Wynn, G. W. & Wynn, R. D. 1987 Baboon diet: a five-year study of stability and variability in the plant feeding and habitat of the yellow baboons (Pap. cynocephalus) of Mikumi National Park, Tanzania. Fol. Primatol. 48, 78–120. (doi:10.1159/ 000156287) Picq, P. 1990 The diet of Australopithecus afarensis: an attempted reconstruction. C. R. Acad. Sci. Ser. II 311, 725–730. Plavcan, J. M. & Cope, D. A. 2001 Metric variation and species recognition in the fossil record. Evol. Anthropol. 10, 204 –222. (doi:10.1002/evan.20001) Pochron, S. T. 2000 The core dry-season diet of yellow baboons (Papio hamadryas cynocephalus) in Ruaha National Park, Tanzania. Fol. Primatol. 71, 346 –349. (doi:10.1159/000021758) Post, D. G. 1982 Feeding behavior of yellow baboons (Papio cyncocephalus) in the Amboseli National Park, Kenya. Int. J. Primatol. 3, 403 –430. (doi:10.1007/ BF02693741) Puech, P. F. 1979 Diet of early man: evidence from abrasion of teeth and tools. Curr. Anthropol. 20, 590 –592. (doi:10. 1086/202335) Rak, Y., Ginzburg, A. & Geffen, E. 2007 Gorilla-like anatomy on Australopithecus afarensis mandibles suggests Au. afarensis link to robust australopiths. Proc. Natl Acad. Sci. USA 104, 6568–6572. (doi:10.1073/pnas. 0606454104) Ryan, A. S. 1980 Anterior dental microwear in hominid evolution: comparisons with human and nonhuman primates. PhD dissertation, University of Michigan.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3354

P. S. Ungar et al.

Pliocene hominin microwear textures

Scott, R. S., Ungar, P. S., Bergstrom, T. S., Brown, C. A., Grine, F. E., Teaford, M. F. & Walker, A. 2005 Dental microwear texture analysis reflects diets of living primates and fossil hominins. Nature 436, 693–695. (doi:10.1038/ nature03822) Scott, R. S., Ungar, P. S., Bergstrom, T. S., Brown, C. A., Childs, B. E., Teaford, M. F. & Walker, A. 2006 Dental microwear texture analysis: technical considerations. J. Hum. Evol. 51, 339–349. (doi:10.1016/j.jhevol.2006. 04.006) Scott, J. S., Godfrey, L. R., Jungers, W. L., Scott, R. S., Simons, E. L., Teaford, M. F., Ungar, P. S. & Walker, A. 2009a Dental microwear texture anlaysis of megaladapids and archaeolemurids. J. Hum. Evol. 56, 405 –416. (doi:10.1016/j.jhevol.2008.11.003) Scott, R. S., Teaford, M. F. & Ungar, P. S. 2009b Dietary diversity and dental microwear variability in Theropithecus gelada and Pap. cynocephalus. Am. J. Phys. Anthropol. (Suppl. 48), 234. Simpson, G. G. 1933 Paleobiology of Jurassic mammals. Paleobiology 5, 27–158. Strait, D. S. & Grine, F. E. 2004 Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J. Hum. Evol. 47, 399 –452. (doi:10.1016/j.jhevol.2004.08.008) Strait, D. S., Grine, F. E. & Moniz, M. A. 1997 A reappraisal of early hominid phylogeny. J. Hum. Evol. 32, 17– 82. (doi:10.1006/jhev.1996.0097) Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, C. O. & White, T. D. 2009 Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 94– 99. (doi:10.1126/science.1175824) Teaford, M. F. 1988 Scanning electron microscope diagnosis of wear patterns versus artifacts on fossil teeth. Scan. Microsc. 2, 1167– 1175. Teaford, M. F. & Ungar, P. S. 2000 Diet and the evolution of the earliest human ancestors. Proc. Natl. Acad. Sci. USA 97, 13 506 –13 511. (doi:10.1073/pnas. 260368897) Ungar, P. S. 2004 Dental topography and diets of Australopithecus afarensis and early Homo. J. Hum. Evol. 46, 605 –622. (doi:10.1016/j.jhevol.2004.03.004) Ungar, P. S. & Scott, R. S. 2009 Dental evidence for diets of Early Homo. In The first humans: origins of the genus Homo (eds F. E. Grine, R. E. Leakey & J. G. Fleagle), pp. 121 – 134. New York, NY: Springer-Verlag. Ungar, P. S. & Teaford, M. F. 2001 The dietary split between apes and the earliest human ancestors. In Humanity from African naissance to coming millennia (ed. P. V. Tobias et al.), pp. 337 –354. Florence, Italy: Firenza University Press. Ungar, P. S., Brown, C. A., Bergstrom, T. S. & Walker, A. 2003 Quantification of dental microwear by tandem

Phil. Trans. R. Soc. B (2010)

scanning confocal microscopy and scale-sensitive fractal analyses. Scanning 25, 185 –193. (doi:10.1002/sca. 4950250405) Ungar, P. S., Grine, F. E., Teaford, M. F. & El Zaatari, S. 2006 Dental microwear and diets of African early Homo. J. Hum. Evol. 50, 78–95. (doi:10.1016/j.jhevol.2005.08. 007) Ungar, P. S., Merceron, G. & Scott, R. S. 2007a Dental microwear texture analysis of Varswater bovids and Early Pliocene paleoenvironments of Langebaanweg, Western Cape Province, South Africa. J. Mammal. Evol. 14, 163–181. (doi:10.1007/s10914007-9050-x) Ungar, P. S., Scott, R. S., Scott, J. R. & Teaford, M. F. 2007b Dental microwear analysis: historical perspectives and new approaches. In Dental anthropology (eds J. D. Irish & G. C. Nelson), pp. 389–425. Cambridge, UK: Cambridge University Press. Ungar, P. S., Grine, F. E. & Teaford, M. F. 2008 Dental microwear indicates that Paranthropus boisei was not a hard-object feeder. PLoS ONE 3, 1– 6. van der Merwe, N. J., Masao, F. T. & Bamford, M. K. 2008 Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. S. Afr. J. Sci. 104, 153–155. Walker, A. 1981 Diet and teeth. Dietary hypotheses and human evolution. Phil. Trans. R. Soc. Lond. B 292, 57–64. (doi:10.1098/rstb.1981.0013) Walker, A. 2002 New perspectives on the hominids of the Turkana Basin, Kenya. Evol. Anthropol. 11(Suppl. 1), 38–41. Ward, C. V., Leakey, M. G. & Walker, A. C. 1999 The new hominid species, Australopithecus anamensis. Evol. Anthropol. 7, 197 –205. (doi:10.1002/(SICI)1520-6505(1999) 7:6,197::AID-EVAN4.3.0.CO;2-T) Ward, C. V., Leakey, M. G. & Walker, A. 2001 Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J. Hum. Evol. 41, 255– 368. (doi:10.1006/jhev. 2001.0507) White, T. D., Johanson, D. C. & Kimbel, W. H. 1981 Australopithecus africanus: its phyletic position reconsidered. S. Afr. J. Sci. 77, 445– 470. White, T. D., Suwa, G., Simpson, S. & Asfaw, B. 2000 Jaws and teeth of Australopithecus afarensis from Maka, Middle Awash, Ethiopia. Am. J. Phys. Anthropol. 111, 45–68. (doi:10.1002/(SICI)1096-8644(200001)111:1,45::AID -AJPA4.3.0.CO;2-I) White, T. D. et al. 2006 Asa Issie, aramis and the origin of Australopithecus. Nature 440, 883 –889. (doi:10.1038/ nature04629) Wood, B. & Richmond, B. G. 2000 Human evolution: taxonomy and paleobiology. J. Anat. 197, 19– 60. (doi:10. 1046/j.1469-7580.2000.19710019.x)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3355–3363 doi:10.1098/rstb.2010.0086

An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar to modern humans Philip L. Reno1,*, Melanie A. McCollum3,4, Richard S. Meindl2,3 and C. Owen Lovejoy2,3,* 1

Department of Developmental Biology, Stanford University School of Medicine, 279 Campus Drive, Beckman 300, Stanford, CA 94305-5329, USA 2 Department of Anthropology, and 3School of Biomedical Sciences, Kent State University, Lowry Hall Room 226, Kent, OH 44242-0001, USA 4 Department of Cell Biology, University of Virginia, Charlottesville, VA 22902, USA

In a previous study, we introduced the template method as a means of enlarging the Australopithecus afarensis postcranial sample to more accurately estimate its skeletal dimorphism. Results indicated dimorphism to be largely comparable to that of Homo sapiens. Some have since argued that our results were biased by artificial homogeneity in our Au. afarensis sample. Here we report the results from inclusion of 12 additional, newly reported, specimens. The results are consistent with those of our original study and with the hypothesis that early hominid demographic success derived from a reproductive strategy involving male provisioning of pair-bonded females. Keywords: A.L. 333; taphonomy; monogamy; skeletal dimorphism; modelling

1. INTRODUCTION Accurately inferring early hominid sexual dimorphism is an important element in interpreting their paleobiology. We previously concluded that skeletal size dimorphism in Australopithecus afarensis was significantly lower than that of gorillas and could not be statistically distinguished from that of modern humans (Reno et al. 2003, 2005). These findings, which contrast with previous assessments (Zihlman & Tobias 1985; McHenry 1991; Lockwood et al. 1996), were achieved through the use of the ‘template method’. This method relied on the A.L. 288-1 partial skeleton (‘Lucy’), as a source of simple ratios between femoral head diameter (FHD) and other skeletal dimensions. These ratios were then used to obtain estimates of FHD for skeletal dimensions that were also measurable in A.L. 288-1. Postcranial variation within the (thus maximized) Au. afarensis sample from the Middle Awash region of Ethiopia (‘Combined Afar’, CA) and that within the temporally and geographically constricted Au. afarensis sample from Afar Locality 333 were then compared with bootstrapped samples of modern humans, chimpanzees and gorillas. This method was specifically designed to overcome problems inherent in calculating sexual dimorphism from a small number of specimens whose sexes must be judged a priori on the basis of size (e.g. Zihlman & Tobias 1985; McHenry 1991).

* Authors for correspondence ([email protected]; olovejoy@aol. com). One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

Any given assemblage of Au. afarensis fossils was formed by a combination of random sampling and various taphonomic processes. The effect of these processes on sample variation can be modelled by bootstrapping from taxa of known dimorphism. Humans (Homo sapiens), chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla) represent the three genera most closely related to early hominids and essentially encompass the entire range of primate skeletal sexual dimorphism. Because the sex of any Au. afarensis element is essentially unknown, sampling with regard to sex of extant taxa is allowed to vary freely. That is, the sex ratio in each iteration is allowed to vary by simple probability (i.e. the binomial expansion). In sufficiently small samples, this can occasionally result in samples composed of only one sex. In order to simulate the Au. afarensis assemblages as precisely as possible (and limit the variation introduced by sampling different anatomical locations), bootstrapped samples of living hominoids were required to exactly match the anatomical compositions of the A.L. 333 and the CA samples (e.g. the number of proximal tibias included in each bootstrapped sample was required to exactly match the number of proximal tibias represented in the Au. afarensis sample being simulated). For each iteration, each postcranial metric was converted to a FHD based on ratios calculated from a template specimen that was also randomly chosen to serve as the equivalent of A.L. 288-1. A.L. 333 probably represents a simultaneous death assemblage (White & Johanson 1989; Behrensmeyer et al. 2003). In our previous analysis (Reno et al. 2003), two separate simulations of A.L. 333 were generated. In one, each of 22 postcranial

3355

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3356

P. L. Reno et al.

Au. afarensis skeletal dimorphism

metrics preserved at the site was randomly drawn from our complete samples of extant taxa (N 50). This exactly modelled A.L. 333 in being composed of as many as 22 separate individuals. However, it is unlikely that each A.L. 333 specimen in fact represents one of 22 different individuals. Based on mandibular dentitions, the minimum number of individuals (MNI) at the site is nine (White & Johanson 1989). Therefore, in a second simulation, we randomly selected nine individuals to serve as the source of all 22 metrics. This ensures that many individuals are multiply represented in the sample of metrics. Our procedures assume only that each ‘death’ assemblage (fossil sample or extant simulation) was a random sample of its parent population—the biological species from which each was derived (i.e. Au. afarensis, H. sapiens, P. troglodytes and G. gorilla). These samples have been challenged as not being representative of the Au. afarensis size distribution (Plavcan et al. 2005; Scott & Stroik 2006). The rationale has been that because ‘Lucy-sized’ individuals are absent from the A.L. 333 assemblage, it must over-sample large, presumably male, adult individuals. If true, then our lower estimates of skeletal dimorphism in A.L. 333 may have been flawed by biased sampling during the accumulation, fossilization and/ or recovery of the assemblage. This argument is now subject to a simple test. Additional postcranial elements of Au. afarensis have now been reported for both A.L. 333 and other Middle Awash localities (Kimbel et al. 2004; Drapeau et al. 2005; Harmon 2006). Inclusion of these additional 12 specimens raises our postcranial sample to 41 and more than doubles the number of individuals represented from non-A.L. 333 localities. This expanded sample provides an opportunity to more accurately assess size dimorphism in Au. afarensis and determine whether smaller Lucysized individuals were disproportionately lacking from A.L. 333.

2. MATERIAL AND METHODS In addition to the 29 fossil specimens in our original study (Reno et al. 2003), we have now added four specimens from A.L. 333 and eight from other Middle Awash localities (Kimbel et al. 2004; Drapeau et al. 2005; Harmon 2006; table 1). Metrics from these specimens (some as yet undescribed), as well as their homologues from the A.L. 288-1 partial skeleton, were provided by William Kimbel. Details of the template method and our bootstrapping procedures are described in Reno et al. (2003, 2005). Since those publications, we have observed that the template method yields extreme FHD estimates in rare cases where a small or large skeletal metric is paired with a template specimen with an unusual metric to FHD ratio (all within the bounds of natural variation). While such pairings are infrequent, they nevertheless have the potential to confound results by artificially inflating dimorphism statistics in extant samples. As a means of correcting bias from such cases, we now systematically discard estimated FHDs that are more than 10 mm above or below the Phil. Trans. R. Soc. B (2010)

observed range of the extant taxon being sampled. However, this correction is potentially quite conservative as the relative size range of many metrics is actually greater than that of FHD (see below). The three bootstrap simulations reported here were performed separately to model the following enlarged Au. afarensis samples: (i) 26 specimens from the A.L. 333; (ii) 15 non-333 specimens from other Hadar localities and Maka; and (iii) 41 specimens in the CA sample. The 15 specimens in the non-333 sample must represent 15 separate individuals. Therefore, 15 metrics were each randomly drawn from the entire chimpanzee, human or gorilla samples. In contrast, it is unlikely that 26 different individuals contributed to the A.L. 333 sample. Therefore, for each iteration, a separate random subsample of nine chimpanzee, human or gorilla individuals (based upon an MNI from mandiblar dentitions (White & Johanson 1989)) served as the pool from which 26 metrics were then drawn. For the CA simulations, a ‘hybrid’ was created for each iteration in which 26 metrics representing A.L. 333 were sampled from nine randomly selected individuals. These were combined with an additional 15 drawn from the entire sample to represent non-333 individuals. Plavcan et al. (2005) argued that only five to eight individuals contributed to the A.L. 333 postcranial sample, and it is certainly hypothetically possible that some of the (at least) nine known adult individuals did not contribute to the postcranial sample. However, our simulations already permit sampling of fewer than nine individuals because not all nine individuals selected for each iteration are necessarily randomly sourced for the 26 metrics used to simulate A.L. 333. Therefore, it was unnecessary to perform additional simulations from isolated comparative samples artificially restricted to less than nine potential contributors. Both the coefficient of variation (CV) and the binomial dimorphism index (BDI) were calculated in each simulation. The CV was calculated using the small sample correction (Sokal & Rohlf 1995). The BDI was defined specifically for the calculation of sexual dimorphism in samples of unknown sex. It rests upon three assumptions: (i) both sexes are present in each sample; (ii) every specimen has an equal probability of being male or female, but (iii) when any two specimens are potentially of a different sex, the larger is always male. Using this algorithm, a sample of n yields a total of n 2 1 possible sex allocations and therefore n 2 1 skeletal dimorphism estimates. The BDI is then the weighted average of the n 2 1 dimorphism values based on the probability of each sex allocation occurring under the binomial expansion. Note that in light of the assumption that males are always larger than females, the BDI tends to overestimate dimorphism in minimally dimorphic species. Two estimates of dimorphism (actual DM: male mean/female mean based on known sex) were calculated for each extant sample drawn. The first used estimated FHD dimensions estimated for each specimen by the template method (template sexual dimorphism: TSD) to measure dimorphism, and the second used the original FHDs for each randomly

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Au. afarensis skeletal dimorphism

P. L. Reno et al.

3357

Table 1. Australopithecus afarensis sample used for simulations.

metric

specimen(s)

estimated FHD

estimated GMEAN

FHD/GMEAN ratio

HHD: max. diameter of humeral head OLCB: ML width of humerus measured tangent to the superior margin of the olecranon fossa

A.L. 333-107a A.L. 137-48A A.L. 137-50b A.L. 223-23b A.L. 322-1 A.L. 333-29 A.L. 333w-31 Mak VP 1/3 A.L. 333w-22 A.L. 444-14b A.L. 333x-14c A.L. 333x-15c A.L. 333x-5 A.L. 333w-36 A.L. 438-1ab A.L. 152-2b A.L. 288-1ap A.L. 333-3 A.L. 827b A.L. 211-1 A.L. 333-95c Mak VP 1/1 A.L. 333-117 A.L. 333-123b A.L. 333-142b A.L. 333-4 A.L. 333w-56 A.L. 333-140b A.L. 129-1b A.L. 333x-26 A.L. 333-42 A.L. 330-6b A.L. 333-6 A.L. 333-7 A.L. 333-96 A.L. 545-3b A.L. 333-9A A.L. 333-9B A.L. 333w-37 A.L. 333-85 A.L. 333-147b

39.4 32.6 38.3 35.3 27.9 33.2 34.3 37.8 39.5 37.2 44.3 44.5 37.1 29.8 40.9 33.1 28.6 40.9 38.1 36.4d 35.3d 34.4d 38.7 33.0 30.1 35.2 33.6 30.2 27.9 38.5 36.7 37.4 37.2 42.9 38.4 31.9 42.8 38.9 37.8 40.6 36.0

32.6 27.0 31.6 29.2 23.1 27.4 28.4 31.3 32.7 30.4 36.6 36.8 30.6 24.6 33.8 27.4 23.6 33.8 31.5 30.1 29.1 28.4 32.0 27.2 24.8 29.1 27.8 24.9 23.0 31.8 30.3 30.9 30.8 35.5 31.7 26.1 35.4 32.1 31.3 33.5 29.8

1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.22 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.21 1.22 1.21 1.21 1.21 1.21 1.21

CAPD: max. diameter of capitulum RHD: max. diameter of the radial head ULB: ML width of ulna immediately distal to radial facet FHD: max. diameter of femoral head

TRCD: max. femoral shaft diameter immediately below lesser trochanter FNKH: femoral neck height normal to long axis at midpoint GSTB: AP femoral width immediately above gastrocnemius tubercles CNDC: ML distance between centers of medial and lateral tibial condyles PRXTB: max. ML tibial bicondylar breadth DSTTB: AP articular length at ML mid-point of articular surface of distal tibia

FIBD: max. ML diameter of distal fibula

TAL: max. AP length of talus a

Because of slight eccentricity in this specimen the average of the mediolateral (ML) and anteroposterior (AP) diameters was used instead. Specimens new to this analysis. These specimens lack epiphyseal fusion and are not strictly adults. They were included because they constitute three of the largest fossils in the sample and their omission would further decrease fossil dimorphism estimates. d These values are based on a slightly different metric than the one used in the previous analysis (AP subtrochanteric diameter reported by Lovejoy et al. (1982)) and therefore differ from those reported in Reno et al. (2003). The new metric corresponds more closely with that taken from the comparative samples and better reflects the relative size of these specimens (i.e. 333-3 is clearly larger than any of these three specimens). b c

selected individual (direct sexual dimorphism: DSD) to determine it. Comparison of TSD and DSD assesses the effect of using a template specimen to estimate dimorphism. Because calculation of dimorphism statistics (BDI and CV) for Au. afarensis requires use of a template specimen (A.L. 288-1), these can be assessed only by comparison with TSD produced by the simulations.

3. RESULTS Table 1 lists each Au. afarensis specimen used in the current analysis, the metric from which its FHD was Phil. Trans. R. Soc. B (2010)

calculated using the template (A.L. 288-1) and the resulting estimated FHD. Also included in table 1 are estimated geometric means (GMEAN) of all included metrics that could also be calculated by the template method in addition to the FHD. These are included to illustrate that the results of the template method do not depend on the choice of FHD to measure sample dimorphism. Note that ratios between estimated FHD and estimated GMEAN are always identical. Thus, any measure of sample variation (i.e. CV or BDI) will be identical and any scalar metric from the template will produce the same result. Therefore, any species-specific allometric

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3358

P. L. Reno et al.

Au. afarensis skeletal dimorphism

estimated femoral head diameter (mm)

50

45

40

35

30

25

20 A.L. 333

non-333

Figure 1. Estimated FHD for individual Au. afarensis specimens included in this analysis. Circles, original specimens; triangles, specimens new to this analysis.

relationships with FHD have no effect on the outcome of the procedure. Estimated FHDs for each of the original 29 specimens of Reno et al. (2003) plus the 12 additional specimens included in the present analysis are shown in figure 1. As it demonstrates, the new specimens increase representation of small individuals at A.L. 333 but not to the extreme range represented by the smallest individuals of the non-333 sample. On the other hand, the new specimens expand the upper size range of the non-333 sample (although not to the extent observed in A.L. 333) and appreciably increase the representation of intermediate-sized individuals in the non-333 sample such that there is no longer any potential demarcation between large and small specimens in the combined CA sample. These novel specimens provide little reason to conclude that A.L. 333 under-represents small Lucysized individuals. To the contrary, given the large number of intermediate-sized specimens, it is quite possible that such extremely small individuals may actually be over-represented in the non-333 sample. Table 2 presents samples sizes, CVs, actual DM and the BDI for each metric. Dimorphism in humans is intermediate between non-dimorphic chimpanzees and highly dimorphic gorillas for nearly all characters (only the chimpanzee capitulum (CAPD) BDI and CV are slightly greater than humans). However, within each taxon, the extent to which skeletal metrics differ between the sexes varies extensively. Significantly, variation in FHD in all three hominoid taxa is low in comparison to that observed for most other skeletal metrics (thus, FHD will have a smaller relative range). Given these findings, the template method can be expected to overestimate the means and dispersions of direct dimorphism values. Although the BDIs correlated well with the actual dimorphism observed for each metric, they tended Phil. Trans. R. Soc. B (2010)

to overestimate size dimorphism in the minimally dimorphic species (compare values in chimpanzees and gorillas; table 2). As noted above, this is an expected finding because males are always assumed to be larger than females. Frequency histograms of dimorphism values generated by simulating the A.L. 333, CA and non-333 samples are provided in figure 2. As expected, human dimorphism values were found to be intermediate between those of chimpanzees and gorillas. Also as expected (see discussion above), templatederived size dimorphism statistics tended to overestimate direct dimorphism values (table 3). For each iteration, a Pearson correlation coefficient was computed between the resulting template-derived estimated FHDs and the directly measured FHDs. The means and standard deviations of these correlation coefficients for all simulations are presented in table 4. The strength of the correlation between template and direct values varied among species as a direct consequence of their relative dimorphism. As expected, in non-dimorphic chimpanzees, the error in estimating FHD was relatively high compared with the size range of the species. In contrast, in highly dimorphic gorillas, it was relatively low. The patterns of correlation observed between template FHD and direct FHD in the extant taxa verify that the template method satisfactorily reflects actual dimorphism levels in these samples. As in our original analysis, BDI and CV calculated for Au. afarensis were most similar to those of humans (figure 2). This was true not only of the A.L. 333 and CA samples, but also for the non-333 sample. Table 5 presents exact counts of the number of iterations that fell above or below the Au. afarensis value in each simulation. As these data demonstrate, dimorphism within the expanded A.L. 333 sample increased from a BDI of 1.167 in our previous analysis to a value of 1.195 here, which places Au. afarensis dimorphism in the middle of the distribution of human values. However, because of its small sample size (modelled as representing nine individuals), it is statistically indistinguishable from any of the three hominoids. Unlike the results for A.L. 333, dimorphism within the expanded CA sample decreased from a BDI of 1.222 in our original study to 1.209 here, a value that is significantly different from that of both the extremely dimorphic gorillas and the minimally dimorphic chimpanzees. The slightly higher dimorphism value of 1.213 calculated for the non-333 sample also differed significantly from that of gorillas using a directional test (which is appropriate considering gorillas set the upper range of primate dimorphism). Because of its reliance on estimated rather than actual FHDs, the template method contributes an additional source of error to estimates of dimorphism. In order to ensure that this error is not a function of the size of the template specimen—a potential concern given the unusually small size of A.L. 288-1—we compared dimorphism values generated by different sized templates. Template size has no systematic effect (figure 3), and therefore our results are not biased by the small size of A.L. 288-1.

Phil. Trans. R. Soc. B (2010)

HHD

23 25 6.64 1.066 1.115 0.049

25 25 8.92 1.170 1.169 20.001

24 25 14.92 1.325 1.305 20.020

species

chimpanzees male (n) female (n) CV actual DM BDI difference

humans male (n) female (n) CV actual DM BDI difference

gorillas male (n) female (n) CV actual DM BDI difference

25 25 18.09 1.390 1.378 20.012

25 25 11.08 1.176 1.202 0.026

23 25 9.42 1.073 1.163 0.090

OLCB

25 25 15.02 1.300 1.297 20.003

25 25 9.17 1.124 1.161 0.037

23 25 9.49 1.090 1.165 0.075

CAPD

24 25 14.60 1.296 1.290 20.006

25 25 8.87 1.151 1.160 0.009

22 25 6.65 1.038 1.113 0.075

RHD

25 25 16.74 1.324 1.324 0.000

25 25 13.07 1.203 1.237 0.034

23 25 9.03 1.059 1.155 0.096

ULB

25 25 12.66 1.258 1.252 20.006

25 25 8.81 1.157 1.161 0.004

23 25 6.48 1.049 1.114 0.065

FHD

25 25 12.66 1.225 1.242 20.003

25 25 9.64 1.142 1.165 0.023

23 25 7.80 1.054 1.133 0.079

TRCD

25 25 14.00 1.258 1.268 0.010

25 25 11.00 1.178 1.199 0.021

23 25 7.27 1.032 1.123 0.091

FNEKH

25 25 14.98 1.297 1.299 0.002

25 25 8.67 1.100 1.151 0.051

23 25 7.31 1.029 1.126 0.097

GSTB

25 25 14.23 1.275 1.284 0.009

25 25 10.17 1.173 1.186 0.013

23 25 7.40 1.036 1.127 0.091

CNDC

25 25 13.62 1.279 1.271 20.008

25 25 7.73 1.134 1.140 0.006

23 25 5.98 1.041 1.103 0.062

PRXTB

25 25 13.80 1.257 1.259 0.002

25 25 12.07 1.183 1.214 0.031

23 25 8.20 1.003 1.147 0.144

DSTTB

23 25 16.06 1.330 1.325 20.005

25 25 9.67 1.116 1.166 0.050

22 25 6.72 1.052 1.110 0.058

FIBD

21 22 10.98 1.208 1.208 0.000

25 25 8.02 1.135 1.141 0.006

19 24 6.23 1.029 1.106 0.077

TALUS

Table 2. Sample sizes and dimorphism statistics for individual metrics measured directly from chimpanzee, human and gorilla specimens. Metrics are explained in table 1.

19 22 13.29 1.279 1.264 20.015

25 25 8.02 1.151 1.153 0.002

18 24 5.32 1.043 1.093 0.050

GMEAN

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Au. afarensis skeletal dimorphism P. L. Reno et al. 3359

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3360

P. L. Reno et al.

Au. afarensis skeletal dimorphism

A.L. 333

(a) 300

1.195

250 200 150 100 50 0

11.23

Combined Afar

(b) 300

1.209 250 200 150 100 50 0 1.05 1.10 1.15 1.20 1.25 1.30 1.35 1.40 1.45 1.50 1.55 1.60

11.89

non-333

(c) 300

1.213 250 200 150 100 50 0 1.05 1.10 1.15 1.20 1.25 1.30 1.35 1.40 1.45 1.50 1.55 1.60

12.03

4

6

BDI

8

10 12 14 16 18 20 22 24 26 28 CV

Figure 2. Frequency histograms of dimorphism values generated by simulating the (a) A.L. 333, (b) Combined Afar and (c) non-333 assemblages using chimpanzee (white bars), human (grey bars) and gorilla (black bars) comparative samples (1000 iterations each). The vertical line in each plot indicates dimorphism for the Au. afarensis sample. Table 3. Summary statistics from each of the extant hominoid simulations. chimpanzee TSD A.L. 333 simulation: 1000 iterations actual DM mean 1.045 s.d. 0.050 BDI mean 1.155 s.d. 0.029 CV mean 9.29 s.d. 1.59

human DSD

9.52 1.33

non-A.L. 333: 1000 iterations actual DM mean 1.057 s.d. 0.053 BDI mean 1.161 s.d. 0.037 CV mean 9.67 s.d. 2.00 Phil. Trans. R. Soc. B (2010)

DSD

TSD

DSD

1.053 0.046

1.152 0.052

1.160 0.040

1.290 0.060

1.258 0.046

1.102 0.027

1.198 0.037

1.140 0.036

1.272 0.053

1.206 0.051

6.05 1.31

Combined Afar simulation: 1000 iterations actual DM mean 1.049 1.051 s.d. 0.036 0.030 BDI mean 1.162 1.108 s.d. 0.025 0.014 CV mean s.d.

TSD

gorilla

6.24 0.82

11.50 1.90

8.21 1.74

14.94 2.26

11.78 2.07

1.155 0.038

1.159 0.026

1.297 0.041

1.258 0.029

1.203 0.031

1.150 0.025

1.292 0.037

1.227 0.032

11.55 1.54

8.50 1.16

15.49 1.54

12.21 1.18

1.050 0.033

1.162 0.054

1.156 0.029

1.305 0.061

1.258 0.032

1.107 0.019

1.194 0.042

1.148 0.025

1.294 0.052

1.223 0.033

6.43 0.94

11.36 2.18

8.67 1.29

16.14 2.31

12.54 1.39

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Au. afarensis skeletal dimorphism Table 4. Means and standard deviations of the correlations between actual and estimated FHD computed for each of the 1000 iterations. chimpanzee A.L. 333 mean 0.453 s.d. 0.179 Combined Afar mean 0.498 s.d. 0.132 non-333 mean 0.565 s.d. 0.190

human

gorilla

0.620 0.145

0.819 0.087

0.642 0.102

0.831 0.056

0.675 0.147

0.832 0.091

4. DISCUSSION The present study is based on dimorphism estimates generated from 41 fossils representing a minimum of 20 separate individuals. While we look forward to the potential of adding more fossils when available, it is likely that the sample is now reaching a ‘critical mass’ such that additional specimens are unlikely to appreciably change the dimorphism estimates. Results confirm our previous conclusions that dimorphism is only minimal to moderate in Au. afarensis. Skeletal variation in the CA sample differs significantly from those of gorillas and chimpanzees but cannot be statistically distinguished from that of modern humans (table 5). Significantly, the dimorphism values calculated for the non-333 sample demonstrate that the results obtained for the combined sample are not biased in any way by the composition of A.L. 333, a finding that renders moot all criticisms of our original study which relied on this argument (i.e. Plavcan et al. 2005; Scott & Stroik 2006). Incorporation of four additional individuals of small to intermediate body size did indeed increase the dimorphism in the A.L. 333 sample, just sufficient to prevent statistical significance in its difference from gorillas (table 5). However, as is confirmed by both the lower dimorphism values actually calculated for this sample (figure 2), and the nearly equivalent ranges of variation observed between the A.L. 333 and non-333 samples (figure 1), this finding reflects A.L. 333’s small sample size (n ¼ 9), as sample size has a profound impact on adequately inferring dimorphism (Koscinski & Pietraszewski 2004). Indeed, the A.L. 333 locality, which represents one of the most complete and taphonomically unbiased hominid sites ever found, still probably provides the most accurate sample of Au. afarensis dimorphism. It should also be noted, in addition, that an upper limit to dimorphism within this species is set by combining specimens from geographically and temporally distinct sites (i.e. the total CA sample), as this practice must enhance the variance beyond that typical of local demes. The inclusion of new specimens also reinforces the fact that, while A.L. 333 preserves a number of large specimens, and multiple small individuals have been recovered from non-333 localities, the majority of Au. afarensis specimens are intermediately sized (figure 1). It is thus also noteworthy that the CA Phil. Trans. R. Soc. B (2010)

P. L. Reno et al.

3361

sample, which includes both large and small size extremes, can reject both low chimpanzee and high gorilla-like dimorphism. This also stresses the need to maximize sample size to include the numerous intermediate sized specimens, as this tends to ensure that more complete yet extreme-sized individuals (i.e. A.L. 288-1, A.L. 128/129 and A.L. 333-3) do not unduly influence dimorphism estimates (e.g. Gordon et al. 2008). It is clear that our method of assessing skeletal dimorphism within the A.L. 333 assemblage is appropriate regardless of any sex bias due to sampling error (e.g. as argued by Plavcan et al. (2005) and Scott & Stroik (2006)). Moreover, the presence of small juvenile specimens preserved at A.L. 333 suggests that no systematic size sorting occurred during the formation of the assemblage. As noted above, because the sex of each postcranial element in the Au. afarensis sample is unknown, the numbers of males and females included within the bootstrapped samples were allowed to vary freely. Therefore, the bootstrapped simulations produced all possibilities with respect to sex composition. Indeed, some of our simulations generated samples containing only one sex. That Au. afarensis displayed only moderate size dimorphism is consistent with the minimal size dimorphism observed in Ardipithecus ramidus (Suwa et al. 2009; White et al. 2009). Indeed, given the absence of appreciable skeletal size dimorphism in both Pan and Ardipithecus, there is now strong evidence that the last common ancestor of chimpanzees, bonobos and humans also displayed minimal skeletal dimorphism and that it probably increased in hominids subsequent to 4.4 Ma. Recently, Lawler (2009) established that ecological factors (e.g. substrate preference or feeding niche) often produce dimorphism ratios that differ substantially from those predicted by simple sexual selection theory (e.g. the ‘tournament sex’ of Devore & Lovejoy (1985)). Lovejoy (1981, 1993, 2009) has argued that a provisioning model favours the selection of large males by females because greater body mass increases both mobility and predator resistance in males. Also, selection of small females by males reduces that female’s fat/protein requirements and thereby lowers competition with the male’s offspring for nutrient-rich foods. In addition, the obviously minimal intermale aggression in Ar. ramidus, as now established by the multiple trait shifts in its sectorial canine complex (including those of size, crown form, eruption time and upper/lower canine differences (Suwa et al. 2009; White et al. 2009)), makes it even more unlikely that extreme dimorphism would evolve so rapidly in Au. afarensis via direct male – male competition for mates. Instead, moderate dimorphism appears to be an ecologically driven feature in the hominid lineage that probably continued into later taxa (i.e. Au. africanus (Harmon 2009)), and although most probably the result of sexual selection, it was probably not driven by direct male – male agonistic competition for mates, but rather by ecologically driven male and female choice. Indeed, it would seem that there are now two competing explanations for the increase in skeletal dimorphism from 4.4 Ma (Ar. ramidus, White et al. 2009) to 3.2 Ma

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3362

P. L. Reno et al.

Au. afarensis skeletal dimorphism

Table 5. Simulations of Au. afarensis dimorphism from three different fossil assemblages. These are exact counts of values that fall less than or greater than the Au. afarensis value. Each count can be transformed into a proportion by dividing by 1000. chimpanzee

less than

greater than

1.195 11.23

905 878

95 122

484 447

516 553

74 51

926 949

1.209 11.89

960 954

40 46

607 597

393 403

8 7

992 993

1.213 12.03

916 870

84 130

698 627

302 373

50 35

950 965

1.5 chimpanzee 1.4 1.3 1.2 1.1 1.0 1.5 human 1.4 1.3 1.2 1.1 1.0 1.5 gorilla 1.4 1.3 1.2 1.1 1.0 template specimen by increasing FHD

CV

greater than

30 25 chimpanzee 20 15 10 5 0

CV

less than

BDI

greater than

BDI

less than

BDI

Combined Afar BDI CV non-333 BDI CV

gorilla

30 25 human 20 15 10 5 0

CV

A.L. 333 BDI CV

human

fossil assemblage dimorphism

30 gorilla 25 20 15 10 5 0 template specimen by increasing FHD

Figure 3. Box and whisker plots showing range of sample dimorphism values generated for each template specimen. Template specimens are arrayed by increasing FHD. Boxes indicate interquartile range, whiskers 95% interval; circles are outliers.

(A.L. 333, Kimbel et al. 1994): (i) an increase in male – male agonism for mate selection or (ii) the enhancement of male resistance to predation in response to occupation of novel environments by the more ecologically expansive Australopithecus radiation, including the invasion of new predator-rich environments such as lake margins, savannas and veldts. Given that the former of these two choices would likely depress sub-adult survivorship and increase parenting load on females, when coupled with the now clear adaptive radiation of Australopithecus that followed Ar. ramidus, the latter of these two seems far more likely.

5. CONCLUSIONS The template method is a robust technique for estimating size variance in early hominids and is the only method currently available with which sample Phil. Trans. R. Soc. B (2010)

sizes sufficient for statistical reliability are likely to be generated from rare early hominid fossils. It should be noted, moreover, that this method is fully applicable to other species of fossil hominoids, so long as a partial skeleton and a sufficiently large series of unassociated fossils with homologous anatomical sites are available (e.g. Proconsul (Walker & Teaford 1989; Ward et al. 1993), Ar. ramidus (White et al. 2009) and Au. africanus (Clarke 1999)). For South African Australopithecus, however, special consideration of taphonomic variables will have to be made, since cave assemblages are probably the result of carnivore kills (Brain 1981). Because no specific size-sorting mechanism has been identified for A.L. 333, this site remains an appropriate venue for examination of skeletal dimorphism in Au. afarensis. We thank Yohannes Haile-Selassie of the Cleveland Museum of Natural History for access to primate skeletons and to Lyman Jellema for technical assistance. William Kimbel

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Au. afarensis skeletal dimorphism kindly provided metrics to unpublished fossil specimens. We also thank Alan Walker and Chris Stringer for organizing the discussion meeting and the staff of the Royal Society for ensuring its success.

REFERENCES Behrensmeyer, A. K., Harmon, E. H. & Kimbel, W. H. 2003 Environmental context and taphonomy of the A.L. 333 Locality, Hadar, Ethiopia. Abstracts of the Paleoanthropology Society. See http://www.paleoanthro. org/abst2003.htm. Brain, C. K. 1981 The hunters or the hunted. Chicago, IL: University of Chicago Press. Clarke, R. J. 1999 Discovery of complete arm and hand of the 3.3 million-year-old Australopithecus skeleton from Sterkfontein. S. Afr. J. Sci. 95, 477 –480. Devore, I. & Lovejoy, C. O. 1985 The natural superiority of women. In The physical and mental health of aged women (eds M. R. Haug, A. B. Ford & M. Sheafor), pp. 27– 38. New York, NY: Springer. Drapeau, M. S., Ward, C. V., Kimbel, W. H., Johanson, D. C. & Rak, Y. 2005 Associated cranial and forelimb remains attributed to Australopithecus afarensis from Hadar, Ethiopia. J. Hum. Evol. 48, 593– 642. (doi:10. 1016/j.jhevol.2005.02.005) Gordon, A. D., Green, D. J. & Richmond, B. G. 2008 Strong postcranial size dimorphism in Australopithecus afarensis: results from two new resampling methods for multivariate data sets with missing data. Am. J. Phys. Anthropol. 135, 311 –328. (doi:10.1002/ajpa.20745) Harmon, E. H. 2006 Size and shape variation in Australopithecus afarensis proximal femora. J. Hum. Evol. 51, 217– 227. (doi:10.1016/j.jhevol.2006.01.009) Harmon, E. 2009 Size and shape variation in the proximal femur of Australopithecus africanus. J. Hum. Evol. 56, 551 –559. (doi:10.1016/j.jhevol.2009.01.002) Kimbel, W. H., Johanson, D. C. & Rak, Y. 1994 The first skull and other new discoveries of Australopithecus afarensis at Hadar, Ethiopia. Nature 368, 449–451. (doi:10.1038/368449a0) Kimbel, W. H., Rak, Y. & Johanson, D. C. 2004 The skull of Australopithecus afarensis. New York, NY: Oxford University Press. Koscinski, K. & Pietraszewski, S. 2004 Methods to estimate sexual dimorphism from unsexed samples: a test with computer-generated samples. Anthropol. Rev. 67, 33– 55. Lawler, R. R. 2009 Monomorphism, male– male competition, and mechanisms of sexual dimorphism. J. Hum. Evol. 57, 321–325. (doi:10.1016/j.jhevol.2009.07.001) Lockwood, C. A., Richmond, B. G., Jungers, W. L. & Kimbel, W. H. 1996 Randomization procedures and sexual dimorphism in Australopithecus afarensis. J. Hum. Evol. 31, 537–548. (doi:10.1006/jhev.1996.0078) Lovejoy, C. O. 1981 The origin of man. Science 211, 341 –350. (doi:10.1126/science.211.4480.341) Lovejoy, C. O. 1993 Modeling human origins: are we sexy because we’re smart, or smart because we’re sexy?

Phil. Trans. R. Soc. B (2010)

P. L. Reno et al.

3363

In The origin and evolution of humans and humanness (ed. D. T. Rasmussen), pp. 1 –28. Boston, MA: Jones and Bartless Publisher. Lovejoy, C. O. 2009 Reexamining human origins in light of Ardipithecus ramidus. Science 326, 74e1–74e8. (doi:10. 1126/science.1175834) Lovejoy, C. O., Johanson, D. C. & Coppens, Y. 1982 Hominid lower-limb bones recovered from the Hadar formation—1974 –1977 collections. Am. J. Phys. Anthropol. 57, 679– 700. (doi:10.1002/ajpa.1330570411) McHenry, H. M. 1991 Sexual dimorphism in Australopithecus afarensis. J. Hum. Evol. 20, 21–32. (doi:10.1016/00472484(91)90043-U) Plavcan, J. M., Lockwood, C. A., Kimbel, W. H., Lague, M. R. & Harmon, E. H. 2005 Sexual dimorphism in Australopithecus afarensis revisited: how strong is the case for a human-like pattern of dimorphism? J. Hum. Evol. 48, 313 –320. (doi:10.1016/j.jhevol.2004. 09.006) Reno, P. L., Meindl, R. S., McCollum, M. A. & Lovejoy, C. O. 2003 Sexual dimorphism in Australopithecus afarensis was similar to that of modern humans. Proc. Natl Acad. Sci. USA 100, 9404–9409. (doi:10.1073/ pnas.1133180100) Reno, P. L., Meindl, R. S., McCollum, M. A. & Lovejoy, C. O. 2005 The case is unchanged and remains robust: Australopithecus afarensis exhibits only moderate skeletal dimorphism. A reply to Plavcan et al. (2005). J. Hum. Evol. 49, 279 –288. (doi:10.1016/j.jhevol.2005. 04.008) Scott, J. E. & Stroik, L. K. 2006 Bootstrap tests of significance and the case for humanlike skeletal-size dimorphism in Australopithecus afarensis. J. Hum. Evol. 51, 422 –428. (doi:10.1016/j.jhevol.2006.06.001) Sokal, R. R. & Rohlf, F. J. 1995 Biometry. New York, NY: W. H. Freeman and Co. Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, C. O. & White, T. D. 2009 Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 94–99. (doi:10.1126/science.1175824) Walker, A. & Teaford, M. 1989 The hunt for Proconsul. Sci. Am. 260, 76–82. (doi:10.1038/scientificamerican0189-76) Ward, C. V., Walker, A., Teaford, M. F. & Odhiambo, I. 1993 Partial skeleton of Proconsul nyanzae from Mfangano Island, Kenya. Am. J. Phys. Anthropol. 90, 77–111. (doi:10.1002/ajpa.1330900106) White, T. D. & Johanson, D. C. 1989 The hominid composition of Afar Locality 333: some preliminary observations. In Hominidae, pp. 97–101. Milan, Italy: Jaka Book. White, T. D., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, C. O., Suwa, G. & WoldeGabriel, G. 2009 Ardipithecus ramidus and the paleobiology of early hominids. Science 326, 75–86. (doi:10.1126/science. 1175802) Zihlman, A. L. & Tobias, P. V. 1985 Australopithecus afarensis: two sexes or two species? In Hominid evolution: past, present and future, pp. 213 –220. New York, NY: Alan R. Liss, Inc.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3365–3376 doi:10.1098/rstb.2010.0070

The cranial base of Australopithecus afarensis: new insights from the female skull William H. Kimbel1,* and Yoel Rak2 1

Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA 2 Department of Anatomy, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

Cranial base morphology differs among hominoids in ways that are usually attributed to some combination of an enlarged brain, retracted face and upright locomotion in humans. The human foramen magnum is anteriorly inclined and, with the occipital condyles, is forwardly located on a broad, short and flexed basicranium; the petrous elements are coronally rotated; the glenoid region is topographically complex; the nuchal lines are low; and the nuchal plane is horizontal. Australopithecus afarensis (3.7 – 3.0 Ma) is the earliest known species of the australopith grade in which the adult cranial base can be assessed comprehensively. This region of the adult skull was known from fragments in the 1970s, but renewed fieldwork beginning in the 1990s at the Hadar site, Ethiopia (3.4 – 3.0 Ma), recovered two nearly complete crania and major portions of a third, each associated with a mandible. These new specimens confirm that in small-brained, bipedal Australopithecus the foramen magnum and occipital condyles were anteriorly sited, as in humans, but without the foramen’s forward inclination. In the large male A.L. 444-2 this is associated with a short basal axis, a bilateral expansion of the base, and an inferiorly rotated, flexed occipital squama—all derived characters shared by later australopiths and humans. However, in A.L. 822-1 (a female) a more primitive morphology is present: although the foramen and condyles reside anteriorly on a short base, the nuchal lines are very high, the nuchal plane is very steep, and the base is as relatively narrow centrally. A.L. 822-1 illuminates fragmentary specimens in the 1970s Hadar collection that hint at aspects of this primitive suite, suggesting that it is a common pattern in the A. afarensis hypodigm. We explore the implications of these specimens for sexual dimorphism and evolutionary scenarios of functional integration in the hominin cranial base. Keywords: Australopithecus; cranial base; bipedality

1. INTRODUCTION As the critical intersection of the locomotor, neural and masticatory systems, the cranial base is a frequently consulted source for insight into the evolution of the human head in phylogenetic and functional–adaptive contexts. A great deal of experimental and comparative research on extant primates has been conducted to elucidate the relative influence of each of these systems on cranial base form (e.g. Lieberman et al. 2000), but the fossil record—especially its earlier segments—is less often studied because of small samples, poor preservation, and/or inaccessible endocranial spaces. Yet, the ultimate test of hypotheses regarding the conjunction of structural innovations and their purported functions in an adaptive context is the relative timing of their first appearances in taxa potentially ancestral (or at least sister) to the extant taxa targeted by most of this research. Therefore, it is important to glean as much information as possible from the available fossil remains.

* Author for correspondence ([email protected]). One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

The 3.7 – 3.0 Myr old hominin species Australopithecus afarensis is usually considered to be the plesiomorphic (‘primitive’, African apelike) sister taxon to subsequent australopiths and the genus Homo (e.g. Kimbel et al. 2004; Strait & Grine 2004). Relative to these successor taxa, the skull and dentition of A. afarensis is characterized by numerous primitive features, many of which are part of, or at least influenced by, the masticatory system (see Kimbel & Delezene 2009, for a recent review). The cranial base was spottily represented in the initial (1970s) hypodigm of the species; a single partial calvaria of an adult male individual from A.L. 333 (ca 3.2 Ma) was the principal source of information until the first complete adult skull of the species was recovered in 1992 (A.L. 444-2, a large adult male, ca 3 Ma). These specimens showed that, in contrast to the primitive morphology of the temporal bone (e.g. low-relief mandibular fossa, tubular tympanic element, highly inflated squama, asterionic notch sutural pattern, etc.), the calvaria is derived in its anteriorly positioned foramen magnum and occipital condyles on a short, broad cranial base—features shared with modern humans. The female calvaria of A. afarensis was until recently known only from fragments of the calotte, and while

3365

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3366

W. H. Kimbel & Y. Rak

A. afarensis cranial base

these hinted at several morphological differences from the larger (male) skulls, particularly in aspects of occipital squama form, interpreting this morphology in the context of the entire skull was not possible. Fieldwork in the 2000s rectified this with the recovery of a nearly complete skull of a small, probably female individual, A.L. 822-1. This specimen adds information on variation in A. afarensis cranial base form, casts previously known fragmentary remains of small (female) individuals of this species in a new light,

Figure 1. The reconstructed A.L. 822-1 skull, oblique view. Approximately 45% natural size.

(a)

and reveals an apparently unique (in the extant African hominoid context) pattern of sexual dimorphism in the australopith cranial base. Our more comprehensive description of the A.L. 822-1 skull is in preparation, but here we focus on the cranial base of this specimen and its substantive role in illuminating these issues. 2. THE A.L. 822-1 SKULL The skull A.L. 822-1 was found by the late Dato Adan, an Afar member of the Hadar Research Project, during the 2000 field season. It was recovered from the surface of sediments of the Hadar Formation’s KH-1 sub-member and is estimated to be approximately 3.1 Ma (C. Campisano 2009, personal communication). It is the third adult individual from Hadar to preserve both the mandible and cranium (A.L. 444-2, KH-2 sub-member, ca 3 Ma and A.L. 417-1, SH-3 sub-member, ca 3.3 Ma, are the other two). The specimen was recovered in approximately 200 fragments, which have been cleaned, reconstructed and reassembled to constitute most of an adult skull with almost all of the dentition (figure 1). The reconstruction of the original specimen reveals remnant distortion, owing to both warping and crushing, in (i) the failure of the palatal and calvarial midlines to align, (ii) the temporal bones’ placement on different coronal planes, and (iii) some bilateral compression of both palatal and mandibular arches (figure 2). We describe in detail this deformation and the steps taken to correct it in our comprehensive comparative study currently in preparation. The data and analyses presented here are based on our final restoration using casts of the original fossil. The A.L. 822-1 skull presents numerous characteristics diagnostic of A. afarensis (see Johanson et al. 1978; White et al. 1981, 1993, 2000; Rak 1983;

(b)

Figure 2. Pattern of distortion in the A.L. 822-1 reconstruction. (a) Basal view. Note the asymmetric positions of the temporal bones, resulting from deformation of the (anatomical) left side. (b) Superior view. Note the offset of the face in relation to the calvarial midline. Red line denotes anatomical midline. Phil. Trans. R. Soc. B (2010)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

A. afarensis cranial base A.L. 822-1

22.5

10.5

0

25.0 27.5 30.0 32.5 mm mandibular condyle ML breadth (n = 6)

11.0

11.5 12.0 12.5 13.0 13.5 mandibular M1 breadth (n = 18)

14 mm

25

W. H. Kimbel & Y. Rak 50

75

3367

100

27.5 30.0 32.5 35.0 37.5 40.0 42.5 mm mandible corpus depth @ M1 (n = 20)

9.0

9.5 10.0 10.5 11.0 11.5 12.0 12.5 mm maxillary canine breadth (n = 12)

Figure 3. Box-plot metrical profile of A.L. 822-1. Data for A.L. 822-1 shown in Hadar A. afarensis sample distribution. Bold vertical line indicates value for A.L. 822-1; rectangle defines the 25th and 75th quartiles; diamond defines the mean and 95% CI; short vertical line within rectangle defines the median.

Figure 5. Hadar cranium A.L. 444-2. Note the low position of the compound temporal/nuchal crest (arrow), which approximates the biasterion line, a phylogenetically derived condition of other mature males of A. afarensis. Approximately 50% natural size. Figure 4. Lateral view of A.L. 822-1 ‘final’ restoration (cast), showing the superiorly extended position of the nuchal lines as expressed by W. E. Le Gros Clark’s nuchal area height index: maximum height of nuchal lines (upper horizontal line) above Frankfurt Horizontal (lower horizontal line) as a percentage of maximum cranial vault height above FH (vertical line).

Kimbel et al. 1984, 1994, 2004; Kimbel & Delezene 2009). These include: — strongly prognathic, biconvex maxillary subnasal surface, — narrow midface (nasal aperture and interorbital block), — mild sagittal convexity of the low frontal squama, — medial to lateral supraorbital thickness gradient, — posteriorly convergent temporal lines, — steeply inclined nuchal plane, — low upper scale (la-i) and long lower scale (i-o) of occipital squama, Phil. Trans. R. Soc. B (2010)

— sharply angled articular surface of the occipital condyle, — flattened, horizontally oriented tympanic elements, — hollowed lateral surface of the mandibular corpus (beneath the premolars) with high ramal root and narrow extramolar sulcus, — marked topographic step down from mesial P3 to the distal-P3 to M3 occlusal platform. The A.L. 822-1 skull is most probably that of a female. Its overall cranial dimensions are small, closely approximating those of the very small though incomplete Hadar adult calvaria A.L. 162-128 (Kimbel et al. 1982). The mastoid process is much smaller than the mastoids of male crania such as A.L. 333-45, A.L. 333-84 and A.L. 444-2. Consistent with its small external dimensions, our preliminary estimate of endocranial volume (using mustard seed) is 385 cc, which is similar to that estimated for A.L. 162-28 (375 – 400 cc) and smaller than the estimates

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3368

W. H. Kimbel & Y. Rak

A. afarensis cranial base

Table 1. Nuchal area height index in hominoids. Negative value indicates nuchal area height is below Frankfurt Horizontal. Comparative data from Kimbel et al. (2004).

taxon/specimen Australopithecus afarensis A.L. 444-2 A.L. 333-45 (recon.) A.L. 822-1 Australopithecus africanus Sts. 5 Australopithecus boisei OH 5 KNM-ER 406 KNM-ER 13 750 KNM-ER 732 Australopithecus aethiopicus KNM-WT 17 000 Homo sapiens (n ¼ 10) Pan troglodytes male (n ¼ 10) Pan troglodytes female (n ¼ 10) Gorilla gorilla male (n ¼ 10) Gorilla gorilla female (n ¼ 10)

nuchal area height index (%)

13 12 23 10 11 7 23 12 14 22 51 47 108 67

for clearly male crania A.L. 333-45 (ca 485 cc) and A.L. 444-2 (ca 550 cc; Holloway & Yuan 2004). As shown in figure 3, the condyle of the A.L. 822-1 mandible is the second smallest in mediolateral diameter among six Hadar condyles, and its maxillary canine breadth falls near the top of the smallest quartile in the Hadar sample distribution (n ¼ 12). Other aspects of A.L. 822-1 cranial morphology consistent with female status are discussed below. 3. THE CRANIAL BASE OF A.L. 822-1 (a) Nuchal area height and morphology of the occipital bone In the 1940s W. E. Le Gros Clark argued that the small, horizontally oriented nuchal plane of the occipital bone of South African australopith crania was compatible only with a humanlike poise of the head on the cervical vertebral column (Le Gros Clark 1947, p. 309; 1950, p. 241 – 243). He devised the ‘nuchal area height index’ to express the much smaller degree to which the insertion area of the neck muscles extended superiorly (relative to the Frankfurt horizontal (FH) baseline) as a percentage of maximum calvarial height in fossil and living hominins as compared with the great apes. In the African great apes the height of the nuchal area constitutes (on average) approximately 50 per cent of the calvarial height in both male and female chimpanzees and 67 per cent in female gorillas (in male gorillas the index is more than 100 per cent because the superior extension of the enormous compound temporal/nuchal crest actually surpasses maximum vault height). Among the australopiths, in contrast, the percentage averages only about 10 per cent (with a total range of 23% to þ14%, n ¼ 10), which is much closer to what is observed in modern humans (average ¼ 22%, i.e. nuchal plane height is slightly below the FH; see table 1). Phil. Trans. R. Soc. B (2010)

Two large (presumptive male) A. afarensis crania have nuchal area height index values slightly higher than the australopith average of 10 per cent (A.L. 333-45, in which FH is based on the ‘composite reconstruction’ of Kimbel et al. 1984, 13%; A.L. 444-2, 12%). For A.L 822-1, however, the value is ca 23 per cent, about 9 per cent higher than for any other measurable, undistorted australopith cranium and about midway between chimpanzee and human means (figure 4). The relatively high index value is consistent with the visibly steep nuchal plane in A.L. 822-1, which faces posteroinferiorly at ca 678 to the FH. (The usual way of expressing nuchal plane steepness is the inclination of the inion – opisthion chord relative to FH; for A.L. 822-1, this angle is 428. However, when the foramen magnum is anteriorly located—as it is in all australopiths (see below)—the inion – opisthion chord angle can understate the steepness of the more lateral surfaces on which the mass of the nuchal muscles insert.) The superiorly extensive, steeply angled nuchal plane of A.L. 822-1 illuminates the morphology of other less complete A. afarensis crania. In A. afarensis partial calvariae A.L. 162-28 and KNM-ER 2602, the nuchal plane is steep and the superior nuchal lines highly arched; the transition between nuchal and occipital planes across the superior nuchal lines is smooth and convex; and the nuchal plane consists of bilateral, posterolaterally directed plates that merge at a median topographic peak (Kimbel et al. 1984, 2004; Kimbel 1988). While neither fossil can be oriented precisely on FH, their anatomical similarity to A.L. 822-1 is remarkable. Both specimens are small presumptive females that bear compound temporal/nuchal crests; although A.L. 822-1 does not, the temporal lines sweep laterally towards the asteria within a few millimetres of the highly arched superior nuchal lines. Except for the relatively low nuchal area height index value, the overall morphological pattern of these female specimens is extremely primitive. Figure 5 depicts the large, male A. afarensis cranium A.L. 444-2 in posterior view. Asterion in hominins usually lies close to the FH and the low position of the superior nuchal line relative to the biasterion line is indicated in the figure. We draw attention to the distinction between Hadar crania that have high nuchal lines and steep nuchal planes (A.L. 822-1, A.L. 16228 and A.L. 439-1; the A.L. 288-1a, ‘Lucy’, occipital, too incomplete to orient with precision, bears these same hallmarks), and those in which the nuchal lines are lower (closer to the biasterion line) and the nuchal plane much more horizontal (A.L. 333-45, A.L. 444-2), as in most later hominins. With one exception, this difference divides the sample by size, which we take to indicate sex, with males showing the more derived morphology. The exception is A.L. 439-1, a very large male occipital (comparable in size to that of A.L. 444-2). Although this specimen bears massive compound temporal/nuchal (T/N) crests that extend on each side from the middle of the nuchal line laterally to asterion, it is not fully mature judging from the open lambdoidal suture. The same morphology is replicated in yet another even more

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

A. afarensis cranial base fragmentary Hadar occipital, A.L. 444-1 (from the same locality as the complete, old adult A.L. 444-2 skull); this specimen, which consists of two nonarticulating squamous fragments that span the boundary between nuchal and occipital planes on opposite sides, is from a large, thick-vaulted cranium and bears a weak compound T/N crest. The relatively feeble expression of the compound crest, together with the completely patent and ‘puffy’ lambdodial sutural surface, argues for a younger subadult growth stage of this apparently male individual compared with A.L. 439-1. As in A.L. 439-1, however, the nuchal plane is very steep, facing more posteriorly than inferiorly, even making allowance for errors in orientation of the fragments. These two relatively young, large male individuals present a significant contrast with older adult males as represented by A.L. 333-45 and A.L. 444-2. The expanded sample of Hadar skulls permits the identification of a cross-sectional ontogenetic transformation of male occipital morphology (from young to old, A.L. 444-1!439-1!333-45!444-2). This transformation entails increasing horizontality of the nuchal plane, which results in greater flexion of the occipital squama on the sagittal plane; increasing topographic flattening of the nuchal plane; lowering of the nuchal crest, and related to these shifts, an alteration of the compound T/N crest from a posterosuperior extension of the nuchal plane to an inferior projection of the occipital plane (see Kimbel et al. 2004, for comparative observations and data). We do not, based on presently available evidence, see the same transformation in female individuals of A. afarensis. All four specimens from which relevant information can be extracted are mature (A.L. 162-28, A.L. 822-1 and KNM-ER 2602, probably A.L. 288-1a) and these clearly demonstrate the symplesiomorphic pattern associated with young males of the species. This similarity partly explains (along with an expansive posterior temporalis) why compound T/N crests are so common in the smaller crania of this species (Kimbel et al. 2004).

(b) Position and orientation of the foramen magnum The margins of the foramen magnum in A.L. 822-1 are preserved on two fragments: one extends from the basioccipital posterolaterally to include the right occipital condyle and adjacent jugular process; the other is a strip of nuchal plane bearing a short (14 mm) segment of the margin just anterolateral to opisthion (although this fragment does not connect to the main portion of the occipital squama, external morphology constrains its placement to within a few mm). Between these two pieces we can estimate the size and position of the foramen within a narrow error range (+2 mm). In A. afarensis, as in all australopith species, the foramen magnum, and with it the occipital condyles, resides in an anterior position on the cranial base. Typically, this is assessed through indices expressing the anteroposterior position of basion (ba) or opisthion (o) in relation to cranial length. We use Weidenreich’s (1943) index relating the position of opisthion to the Phil. Trans. R. Soc. B (2010)

W. H. Kimbel & Y. Rak

3369

Table 2. Position and orientation of foramen magnum. Index calculated as the projected length opisthion– opisthocranion/projected length glabella –opisthocranion. Negative value for foramen orientation indicates anteroinferior orientation.

taxon/specimen Australopithecus afarensis A.L. 444-2 A.L. 333-45 (recon.) A.L. 822-1 Australopithecus africanus Sts. 5 Australopithecus boisei OH 5 KNM-ER 406 KNM-ER 13 750 Australopithecus aethiopicus KNM-WT 17 000 Homo sapiens (n ¼ 10) Pan troglodytes male (n ¼ 10) Pan troglodytes female (n ¼ 10) Gorilla gorilla male (n ¼ 10) Gorilla gorilla female (n ¼ 10)

FM position FM index (%) orientation (8)

24 19 23

16 — 14

19

20

24 18 20

7 13 —

21 31 12 14 7 13

— 28 18 20 27 30

horizontal projected length of the calvaria (g – op).1 In our sample of African great apes, the mean index value ranges between 7 per cent (male gorillas, with their massive compound crests) and 14 per cent (female chimpanzees). In humans the more anterior position of opisthion is conveyed by the much higher mean index value in our sample of 31 per cent (range ¼ 28 – 34%). Individual australopith values vary between 18 and 24 per cent, with the two A. afarensis specimens (A.L. 444-2 ¼ 24%, A.L. 822-1 ¼ 23%) falling at the high end of this range (table 2). Weidenreich’s reported values for Asian Homo erectus crania yields an average of about 26 per cent (range ¼ 24 – 28%). The importance of these data on foramen magnum position among fossil hominins is that neither hypothesized postural/locomotor differences (i.e. between the australopiths and H. erectus) nor absolute brain-size differences (with H. erectus having endocranial volumes 1.5 to 2.0 times larger than australopith values) has a large impact on the position of the foramen on the cranial base. Rather, the major difference is between the quadrupedal apes and the bipedal hominins. However, a different division applies to the data on foramen magnum orientation (ba– o line relative to FH). In humans the foramen is forwardly inclined (i.e. the plane of the foramen faces anteroinferiorly) whereas in the great apes it is posteriorly inclined (posteroinferior orientation). In A. afarensis the reconstructed angle of the ba-o line is ca 148 in A.L. 822-1 and ca 168 in A.L. 444-2, values that lie within the range for other australopith crania. The australopith range (table 2) is well below the range for our sample of modern humans (the mean value for which is ca 288; again, the foramen faces anteroinferiorly) but overlaps the low end of the range for

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3370

W. H. Kimbel & Y. Rak

A. afarensis cranial base

Table 3. Measures of basi-occipital length.

taxon/specimen Australopithecus afarensis A.L. 444-2 A.L. 822-1 A.L. 417-1 Australopithecus africanus Sts. 5 MLD 37/38 Stw 187 Australopithecus boisei OH 5 KNM-ER 406 KNM-ER 407 Australopithecus aethiopicus KNM-WT 17 000 Homo sapiens (n ¼ 10) Pan troglodytes male (n ¼ 10) Pan troglodytes female (n ¼ 10) Gorilla gorilla male (n ¼ 10) Gorilla gorilla female (n ¼ 10)

msp

basi-occip. length (mm)

basi-occip. lg/biorbital br * 100

20 22 19

21 23 24

25 21 17

29 — —

20 25 21

20 24 —

25 21 28 26 37 29

27 22 29 28 33 30

be

bt bz gorilla F chimpanzee M AL 822-1 AL 444-2 Sts 5 KNM-ER 406 KNM-WT 17 000

Figure 6. Schematic of relative cranial base breadth in hominoids. Dashed vertical lines represent the biorbital breadth of A.L. 822-1, to which all specimens are size-adjusted. MSP, midsagittal plane; be, terminus of bi-entoglenoid breadth; bt, terminus of bi-articular tubercle breadth; bz, terminus of bizygomatic breadth. Heavy red line defines the breadth of the articular eminence. Note in A.L. 822-1, chimpanzees (males, n ¼ 10) and gorillas (females, n ¼ 10) the close approximation of the entoglenoid processes, expressing a narrow central cranial base.

Table 4. Cranial base breadth in hominoids.

taxon/specimen Australopithecus afarensis A.L. 444-2 A.L. 333-45 (recon.) A.L. 822-1 Australopithecus africanus Sts. 5 MLD 37/38 Australopithecus boisei OH 5 KNM-ER 406 KNM-ER 13 750 KNM-ER 23 000 KNM-ER 407 Australopithecus aethiopicus KNM-WT 17 000 Homo sapiens (n ¼ 10) Pan troglodytes male (n ¼ 10) Pan troglodytes female (n ¼ 10) Gorilla gorilla male (n ¼ 10) Gorilla gorilla female (n ¼ 10)

bi-entoglenoid br (mm)

bi-entogl. br/ biorbital br * 100

80 78 57

84 89 62

65 62

76 —

89 85 86 80 65

84 89 80 — —

80 74 61

85 77 67

59

65

72

63

64

64

chimpanzees (mean ¼ ca 198; gorilla means are about 50% higher; see Kimbel et al. 2004, for details). Thus, in contrast to the data on foramen magnum position, which align A. afarensis and other australopiths with modern humans, the data on orientation of the foramen situate the australopiths in an intermediate Phil. Trans. R. Soc. B (2010)

position between modern apes and humans, but closer to the former (chimpanzees, specifically). Whereas the anterior shift of basion and opisthion accounts for the forward location of the foramen magnum in australopiths and modern humans, the relative vertical positions of these landmarks (beneath the FH, for example) explain the differences in orientation of the foramen (Kimbel et al. 2004). Because the vertical position of basion is similar in apes and humans, differences in foramen orientation reduce to differences in the vertical position of opisthion. In humans, uniquely, opisthion sits much further below FH than basion (the foramen opens anteroinferiorly), which can be explained as a consequence of overall expansion and rotation of the occipital squama with encephalization (e.g. Weidenreich 1941; Biegert 1957). In the small-brained A. afarensis, although the foramen magnum is far forward on the base, opisthion is elevated relative to basion and so the plane of the foramen inclines posteriorly, more similar to what is observed in the apes. Occipital morphology in A. afarensis is consistent with these signs of affinity from the foramen magnum. As discussed above, the orientation of the nuchal plane, the height of the nuchal muscles’ insertion area, and the degree of sagittal flexion of the occipital squama range from symplesiomorphic (apelike) to more derived, but taken as a package convey an intermediate position on the hominoid occipital bone morphocline. At the derived end of the morphocline occipitals approach a quasi-human form in their relatively horizontal nuchal plane, low nuchal area height index and strongly flexed squama, but they do not show the strongly rotated squama that in modern humans confines the maximum height of the nuchal area below the FH (on average) and drops opisthion

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

A. afarensis cranial base 90

W. H. Kimbel & Y. Rak

3371

Z OH 5 ER 13 750

85

80

Z ER 406

ER 23 000, WT 17 000 333-45

X 444-2

bientoglenoid breadth

75

70

+

ER 407

65

Sts 5 MLD 37/38 60

X 58-22 X 822-1

55

50

25

30

35 40 internal palate breadth at M2

45

50

Figure 7. Bivariate plot of palate breadth and cranial base (bi-entoglenoid) breadth in hominoids. Light brown data points, male gorilla; dark brown, female gorilla; light blue, male chimpanzee; X, Australopithecus afarensis; þ, A. africanus; Z, A. boisei.

very far below basion, introducing a negative angle to the foramen’s orientation. It bears noting that the position of the foramen magnum, which is relatively anterior in A. afarensis and close to the condition in modern humans, is not linked to this impressive range of variation in occipital bone morphology.

(c) Length and breadth of the cranial base Along with the anterior position of the foramen magnum, the shortened external length of the cranial base is a derived feature in A.L. 822-1 shared with modern humans. This can be judged from the length of the basi-occipital fragment associated with this fossil (22 mm) as well as that attributed to another Hadar specimen, A.L. 417-1 (19 mm), which essentially match the mean for modern humans both absolutely and relative to biorbital breadth (table 3). A shortened external base can be inferred for specimens of A. afarensis in which the basi-occipital is missing, such as the large (male) crania A.L. 333-45 and A.L. 444-2, from the anteroposterior distance between the carotid foramen and foramen ovale (which roughly approximates basi-occipital length) or the length of the petrous elements (which frame the basi-occipital area), both of which are shorter than in gorillas and chimpanzees. Phil. Trans. R. Soc. B (2010)

Most other early hominins share the shortened external anterior cranial base with A. afarensis (table 3). Dean & Wood (1982), however, showed that the A. africanus base is unusual in its somewhat elongated anteroposterior dimensions compared with other australopiths and early Homo. Specimen Sts 5 indeed has absolutely and relatively long basi-occipital and petrous elements compared with other hominins (table 1), but it is the only A. africanus cranium in which these dimensions can be judged relative to a non-calvarial size standard (such as biorbital breadth or palatal length). In absolute terms the basi-occipital of MLD 37/38 and Stw 187 are as short as those of A. afarensis, so it is unclear whether Sts 5 is typical of A. africanus. Relative to body size and skull size the modern human cranial base is short, but also wide, whereas the great apes exhibit the opposite proportions.2 Tobias (1967) noted that the mandibular fossa is equally wide (mediolaterally) in gorillas and OH 5 (the type specimen of Australopithecus boisei), but only in the latter does the fossa project laterally far beyond the calvarial wall to anchor the temporal root of the flaring zygomatic arch. In gorillas, he found, the mandibular fossae, in spite of their great breadth, are actually closer together on the cranial base and so do not project nearly as far from the calvarial wall. This difference is depicted graphically in figure 6,

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3372

W. H. Kimbel & Y. Rak

A. afarensis cranial base

Table 5. Palate dimensions in fossil hominins. Palate depth is the midline height of the palatine process of the maxilla above the inner alveolar margin at M2. Palate breadth is the width across the internal alveolar crests at mid-M2. Palate length is the direct distance between orale and staphylion (reconstructed in some specimens). Relative palatal breadth (Palatal Index) is calculated as palate breadth/palate length * 100.

taxon/specimen

palate depth

Australopithecus afarensis A.L. 58-22 — A.L. 199-1 11.0 A.L. 200-1a 8.5 A.L. 417-1d 14.0 A.L. 427-1 11.0 A.L. 442-1 — A.L. 444-2 12.0 A.L. 486-1 11.2 A.L. 822-1 14.0 Australopithecus africanus Sts. 5 18.0 Sts. 53 — Stw. 73 14.5 Australopithecus robustus SK 12 12.8 SK 46 12.2 SK 48 15.5 SK 79 13.5 SKW 11 15.0 Australopithecus boisei KNM-ER 405 22.0 KNM-ER 406 20.0 OH 5 21.0 KNM-CH 1 —

palate breadth

palate length

palatal index

27.0 32.0 33.5 28.5 32.0 25.0 41.0 33.0 31.0

— 54.0 65.0 58.0 — — 75.0 — 63.0

— 59.3 51.5 49.1 — — 54.7 — 49.2

35.7 32.0 30.0

65.3 54.0 58.0

54.7 59.3 51.7

32.0 35.0 — — 34.6

— — — — 60.0

— — — — 57.7

38.0 37.4 38.2 40.8

75.0 70.0 79.1 72.0

50.7 53.4 48.3 56.7

where it can be seen that many other australopiths resemble the morphology Tobias (1967) described for OH 5. A notable exception is A.L. 822-1, which, in relative terms (note that all specimens in the figure are scaled to the biorbital breadth of this Hadar cranium), has a very narrow cranial base. As measured across the entoglenoid processes (the reconstructed positions of which are validated by the bicondylar breadth of the specimen’s mandible), the cranial base of A.L. 822-1 is as narrow as average for our sample of female gorillas, and narrower than in any other of the figured australopith specimens, including Sts 5 and the A.L. 444-2 cranium of A. afarensis, in which the mandibular fossae are spread far apart on the base. Another Hadar specimen, A.L. 58-22, appears similar to A.L. 822-1 in its narrow cranial base. This specimen is a craniofacial fragment with part of the right posterior maxilla, sphenoid and temporal bone; the vomer establishes the midline (Kimbel et al. 1982). As with A.L. 822-1, the bi-entoglenoid distance (60 mm) is small compared with the larger Hadar crania, by at least 20 mm (table 4). This absolute difference may reflect sexual dimorphism in cranial base dimensions in A. afarensis, as both of these Hadar specimens also have abbreviated mandibular fossa Phil. Trans. R. Soc. B (2010)

breadths compared with clearly male crania (A.L. 333-45, A.L. 444-2). Biorbital breadth is not available for A.L. 58-22, but another way to assess the relative width of the central cranial base is by a simple index expressing the bi-entoglenoid distance as a percentage of the bi-articular tubercle distance. When this is done, it can be seen that in spite of small fossa breadths (which would increase the index), the bientoglenoid distance is relatively small in these two specimens (ca 48%), compared with the larger Hadar crania (ca 55%) and other early hominins, including A. africanus (ca 54%, n ¼ 2).

(d) The cranial base and palate shape In their diagnosis of A. afarensis, Johanson et al. (1978, p. 6) listed as a distinguishing feature of the adult cranium ‘palate shallow, especially anteriorly; dental arcade long, narrow and straight-sided’. Subsequent discovery and analysis have confirmed this symplesiomorphic feature set of the A. afarensis palate (Kimbel et al. 2004). However, two specimens found since 1990 extend the range of variation in this species’ palatal form. In both A.L. 417-1 and A.L. 822-1 the palate is both very narrow and very deep: internal palate depth (both 14 mm at M2) is the greatest among seven measureable Hadar specimens, while relative palate breadth (internal breadth at M2/length 100 ¼ ca 49%) is the lowest among five Hadar specimens and, indeed, among 11 of 12 australopith specimens in our sample overall (table 5). The very narrow palate of the smaller Hadar crania is potentially related to the narrow cranial base in these A. afarensis individuals. Recall that the base (measured between the entoglenoid processes) of A.L. 822-1 is as relatively narrow as in gorillas. Cranial base width cannot be measured for A.L. 417-1, but in A.L. 58-22, which (as described in the previous section) has a cranial base width approximately as small as that of A.L. 822-1, estimated palate breadth (ca 27 mm, at M2) is the second smallest in the A. afarensis sample (palate length for A.L. 58-22 cannot be estimated). The relationship between the narrowness of the palate and the narrowness of the cranial base would appear to hold, albeit on limited available evidence. This relationship is explored further in the context of African great ape comparative data in figure 7. Among the apes there is a strong correlation (r 2 ¼ 0.52, p , 0.0001) between absolute values of palate breadth and bi-entoglenoid breadth, which appears largely to be a function of strong size-dimorphism in gorillas (figure 7). Using size-standardized variables (with biorbital breadth as the standard), the correlation is much weaker (because male gorillas no longer stand out; r 2 ¼ 0.14, p , 0.017). However, in both cases the smaller A. afarensis individuals are the most apelike of the small fossil hominin sample in their combination of narrow palates and narrow cranial bases, with A. boisei and even A. africanus specimens highly divergent (indeed, humanlike, though humans were not included in our analysis) in their broader cranial bases. Of considerable interest is the position of A.L. 444-2, the large male A. afarensis skull. Compared

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

A. afarensis cranial base with the smaller specimens, it has a much broader cranial base for its palate breadth than predicted by either great ape regression, which hints at an unusual—but perhaps not exceptional—pattern of sexual dimorphism in A. afarensis. Note that there are no small A. boisei specimens in the sample for which both palate and cranial base breadths can be measured (only OH 5 and KNM-ER 406 preserve both dimensions). However, the bi-entoglenoid breadth of KNM-ER 407, considered by consensus a female A. boisei calvaria, is less than 10 mm wider than that of the two A. afarensis females (see y-axis in figure 7), and if we grant this individual a palate breadth somewhere between, say, those of A.L. 822-1 and Sts 5 (ca 31 – 36 mm), then the presumptive female-to-male trend in the cranial base versus palate breadth relationship for A. boisei would be very similar to that of A. afarensis. That is, compared with extant African apes (and other anthropoid species; M. Spencer 2010, personal communication), males have a much wider cranial base for their palate width than females (see also the suggestive position of other large A. boisei and A. aethiopicus specimens on the y-axis of figure 7). (Unfortunately, the fossil record does not permit us to extract any more information from the size-standardized data.) This suggests a unique pattern of cranial sexual dimorphism among australopith species.

4. DISCUSSION The A.L. 822-1 skull focuses attention on several aspects of adult cranial base morphology that were not previously well understood for A. afarensis. First, this Hadar specimen presents a particularly primitive basicranial profile. Its relatively narrow cranial base, high nuchal lines, and correspondingly steep nuchal plane are more similar to African great ape conditions compared with other australopiths so far known. While other more fragmentary A. afarensis specimens hint at relatively generalized occipital form, A.L. 822-1 places this morphology within the context of the entire skull for the first time. Second, A.L. 822-1 points to a pattern of cranial sexual dimorphism neither recognized previously among the australopiths nor encountered among extant hominoids. The apelike cranial base proportions and nuchal area form are already presented in derived conditions in larger A. afarensis specimens usually considered to be males (A.L. 333-45, A.L. 444-2). In these crania the basicranium is wider (absolutely and size-standardized) and the position of the nuchal lines approximates FH, with a horizontal nuchal plane, differences that raise the question of whether species-level taxonomic distinction between the two morphs is warranted. Two further points argue otherwise. First, the combination of high nuchal lines and a steep nuchal plane in two large, immature occipital specimens (A.L. 439-1, A.L. 444-1) suggests that this dimorphism in the Hadar cranial sample has an ontogenetic basis, with young males ‘passing through’ the final adult form of the smaller females to reach mature male (and more derived) morphology. Second, the adult cranial Phil. Trans. R. Soc. B (2010)

W. H. Kimbel & Y. Rak

3373

sample of A. boisei hints at the same pattern of cranial base breadth dimorphism, while the occipital of the L338y-6 calotte (Shungura Formation, Member E), interpreted by Rak & Howell (1978) as a immature male of this species, has a very steep nuchal plane, as is also observed in the young Hadar males. These observations convince us that the variation in Hadar occipital and cranial base form, though phylogenetically informative, is intraspecific. A similar case has previously been made for the polymorphic lower third premolar in A. afarensis (Kimbel et al. 2004, 2006). Finally, the expanded cranial sample of A. afarensis highlights the strongly mosaic nature of basicranial evolution in the hominin clade. Evolutionary changes in the cranial base and occipital squama that are thought to unite early hominins with modern humans (and which, for example, have raised suspicions of pervasive homoplasy in the crania of robust australopiths and Homo), were still not completed by the time of A. afarensis, ca 3.5 – 3.0 Ma. Thus, although an anteriorly located foramen magnum and a short basioccipital segment are shared with extant humans, the narrow cranial base, posteriorly inclined foramen magnum, high nuchal lines and concomitantly steep nuchal plane, are apelike characteristics that are inferred to have been commonly, though not universally, expressed in this taxon. Upright posture and a large brain are the most commonly invoked influences on the cranial base morphology of modern humans (see Lieberman et al. 2000, for a review). According to Le Gros Clark (1947), Robinson (1958) and Olson (1981), among others, the descent of the nuchal musculature and the rotation of the nuchal plane to a horizontal position beneath the brain case mirrors the adoption of upright posture and bipedal locomotion in the hominin clade. Biegert (1957; also Weidenreich 1941), in contrast, argued that the architectural remodelling of the hominin posterior calvaria was a by-product of cerebral expansion, which introduced a strongly flexed basicranial axis and a ‘rolling up’ of the braincase that impelled the foramen magnum and occipital condyles forward. After casting doubt on the oft-proposed correlation among foramen magnum orientation, occipital condyle position and mode of locomotion in primates, Biegert (1963) pointed to the horizontal nuchal plane and anterior foramen magnum of A. africanus (Sts 5) as evidence of an initial phase of encephalization in hominin evolution. Robinson (1958), citing the case of the ‘short-faced squirrel monkey’ (Saimiri ), noted that the orientation of the nuchal plane (steep) and the position of the occipital condyles and foramen magnum on the cranial base (anterior) are not necessarily related, which recalls the situation in A. afarensis. The review by Lieberman et al. (2000) concluded that the orientation of the foramen magnum (as distinct from its anteroposterior position) is unrelated to the posture of the head on the vertebral column but, with cranial base flexion, is primarily a reflection of brain size relative to cranial base length. The skulls of A. afarensis bear on these issues. This species is demonstrably an upright biped with a mean

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3374

W. H. Kimbel & Y. Rak

A. afarensis cranial base

endocranial volume (ca 450 cc) slightly larger than that of Pan troglodytes, to which, among the living hominoid taxa, it is probably closest in body size. The marked variation in the height of the nuchal muscle insertions and angulation of the nuchal plane in A. afarensis would seem to negate a major role for upright locomotion in dictating morphological variation in this region of the hominin skull. One caveat is that we do not have a good idea about how the head was held on the cervical vertebral column in Australopithecus; while the anterior position of the occipital condyles suggests a head posture more similar to that of modern humans than apes, the slightly posterior orientation of the foramen magnum, the strongly angled atlanto-occipital articular surfaces (on A.L. 333-45, A.L. 822-1, and the A.L. 333-83 first cervical vertebra), and the long, straight and robust spine of the lower cervical vertebra (C6, A.L. 333-106), may be signs of a mechanical environment dissimilar to that of the modern human craniovertebral interface. We do not know the extent of cervical lordosis in these early hominins, but it would not surprise us to find a less lordotic cervical column in A. afarensis than in modern humans. Obviously, whether measured absolutely or relative to estimated body mass, brain size in A. afarensis is much closer to that of apes than modern humans. This indicates that the humanlike anterior position of the foramen magnum is largely, if not entirely, unrelated to overall brain size. Perhaps, though, relative neocortical (cerebral) expansion is responsible for the forward migration of the foramen. In this context, the (by now) clear evidence of a relatively posterior position of the lunate sulcus on earliest australopith brain endocasts (Holloway et al. 2004) can be seen as a sign of relative cerebral expansion, which, posteriorly, is manifested as a bulging of the occipital poles over the cerebellar lobes, and, perhaps, a forward ‘rotation’ of the cranial base (similar to what Biegert 1963 hypothesized). In the A. afarensis brain endocast the absolute and relative size of the cerebellar lobes (and especially their anteroposterior length) is much smaller than in African great apes, in which the cerebral and cerebellar lobes protrude subequally (Holloway & Yuan 2004). However, it is unclear to what extent the form of the braincase beneath the tentorium cerebelli would be affected morphogenetically by enlargement of the cerebrum posteriorly; this is an area in need of further research. The ape-sized brain of A. afarensis rests on a base with a much shorter basi-occipital segment than in any great ape. As shown by Lieberman et al. (2000; see also Spoor 1997; McCarthy 2001), brain size relative to cranial base length explains a fairly large amount (but not all) of the observed variation in cranial base angle across a wide spectrum of anthropoid primates. We do not know the exact length of the anterior cranial base (sella turcica to foramen caecum) in A. afarensis, but evidence from fragmentary specimens (i.e. A.L. 58-22, A.L. 417-1) and the demonstrably short segment between basion and the rear of the palate indicate a total cranial base length less than an ape of comparable brain size. (The index of relative encephalization 1, which expresses Phil. Trans. R. Soc. B (2010)

the cube root of endocranial volume as a percentage of cranial base length [ba-sella þ sella-fc], is roughly 0.94 in A.L. 822-1, which is smaller than values for fossil and extant Homo but in the zone of overlap for the small sample of australopiths and extant apes measured from CT scans by Spoor 1997.) Similarly, we can only estimate the (internal) flexion of the cranial base in A. afarensis, using the preserved morphology of A.L. 822-1 (which includes a marked superior deflection of the external basioccipital surface at basion) with support from the other more fragmentary specimens mentioned above; for A.L. 822-1 the angle (ba-se/se-fc; CBA1 of Lieberman et al. 2000) is approximately 1428 (+58), which is some 15– 208 more flexion than great ape species’ means and close to the modern human mean. This Hadar skull has a more highly flexed cranial base than extant African apes of similar relative brain size (details in preparation; see also Spoor 1997; Lieberman et al. 2000, for comparative data). Although the influence of body posture on primate cranial base form has been discounted by recent research (see Lieberman et al. 2000), we see the anterior position of the foramen magnum and occipital condyles as the major cranial base distinction between Australopithecus and Homo, on one hand, and the great apes on the other. The fact that this distinction maps onto primary locomotor differences speaks to upright posture in hominins as an important factor in the positional shifts of these cranial base structures. In our view (see also Spoor 1997; Kirk & Russo 2010), the adoption of upright posture (though not necessarily striding bipedal locomotion per se) in hominins led to a forward migration of the foramen magnum/occipital condyles and a shortened cranial base.3 The combination of a small, ape-sized brain on a relatively short base introduced the flexion of the basicranial axis. Thus, despite their small brains, the anterior position of the foramen magnum (basion) in Australopithecus was associated with the relatively short, flexed cranial base typical of modern humans by ca 3 Ma (figure 8). Subsequent changes in the orientation of the foramen magnum (anteroinferior-facing) in the Homo clade are probably linked to an increase in endocranial volume and the consequent descent of opisthion beneath the braincase, as discussed above (see Kimbel et al. 2004 for details). The introduction of the cervical vertebral lordosis may also play a role in this change, but the fossil record is currently mute on the timing of the initial appearance of this innovation. If we consider the potential link between cranial base configuration and facial orientation (e.g. Ross & Ravosa 1993; Lieberman et al. 2000), the short, flexed base may account for the relatively vertical midfacial segment in A. afarensis, which creates an overall less prognathic facial profile than in chimpanzees and gorillas (Kimbel et al. 2004: fig. 3.24, where midfacial prognathism is measured as the angle between a line connecting nasion or sellion to nasospinale and the FH). In the great apes pronounced midfacial prognathism—a dorsal deflection of the nasionnasospinale segment in relation to a weakly flexed cranial base—results in an airorynch facial configuration. The contrasting klinorynch condition is a

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

A. afarensis cranial base

na fc

se 157°

O ba

ns pr gorilla

na fc

se 142° O

ns ba pr

A.L. 822-1

fc na

se 137°

ns

ba O H. sapiens

pr

Figure 8. Midsagittal craniograms of A.L. 822-1, female gorilla, and modern human, showing cranial base and midfacial angles. A.L. 822-1 anterior cranial base (sella-foramen caecum) reconstructed with additional information from A.L. 417-1 and A.L. 58-22. See text for discussion.

hallmark of the human facial skeleton already manifested, at least incipiently, in A. afarensis (figure 8). The prognathic maxilla, with its strongly inclined nasoalveolar clivus, would not be expected to be impacted as directly by cranial base form, and this remains the most apelike aspect of the A. afarensis face.

5. CONCLUSIONS The A.L. 822-1 specimen, providing the first view of the complete small, presumptively female skull of Phil. Trans. R. Soc. B (2010)

W. H. Kimbel & Y. Rak

3375

A. afarensis, reveals a particularly generalized pattern of morphology in occipital squama and cranial base. With superiorly extended nuchal lines, a concomitantly steep nuchal plane, and a narrow cranial base, this skull is notably more apelike than other australopith crania, including those of larger, clearly male, individuals of this species, which share derived states of these characters with subsequent australopith species and Homo. It throws into sharp relief the morphology of previously known fragmentary cranial specimens from the Hadar site, demonstrating that the generalized pattern is probably common in small (female) individuals of this species. Qualitative data on a cross-sectional cranial growth series contained within the Hadar sample suggest that some of the variation in A. afarensis is indeed intraspecific because young adult males resemble mature females more than they do older males in their generalized occipital form. Although the inference is limited by the few data available, these observations suggest for A. afarensis a pattern of cranial sexual dimorphism unknown among extant hominoids, with adult males characterized by relatively wider cranial bases and more horizontal nuchal muscle origin surfaces than females. At least for the cranial base width, this dimorphism may apply to A. boisei as well; no other australopith taxon currently permits comparison. Morphological variation in the cranial base of A. afarensis is consistent with a mosaic pattern of evolutionary change in this region of the skull. Early australopiths were upright bipeds with small brains. The anterior position of the foramen magnum and occipital condyles on a short (though not necessarily broad), flexed cranial base—a derived character complex linked plausibly to upright posture—is unrelated to substantial variation in the morphology of the nuchal region of the calvaria, which is often thought to mirror postural differences. In species potentially descendant from A. afarensis the nuchal region became more uniformly humanlike in form and orientation, the functional basis for which remains poorly understood. A derived, relatively upright midfacial profile, which likewise ties A. afarensis to later australopiths and Homo, may be related to these cranial base modifications and thus, indirectly, to upright posture itself. We thank the Authority for Research and Conservation of Cultural Heritage and the National Museum of Ethiopia, Ethiopian Ministry of Culture and Tourism, and the Afar Regional State government for permission to conduct the field (Hadar) and laboratory (Addis Ababa) research. We are grateful to the (US) National Science Foundation for grants supporting the field and lab work. Thanks are due Dr Mark Spencer for discussion and Mr Lucas Delezene for help with collecting the comparative data.

ENDNOTES 1

Weidenreich chose opisthion rather than basion for this purpose probably because none of the Homo erectus crania he described preserves the anterior margin of the foramen magnum. 2 Here, cranial base length is taken as the combined length of the segments basion to sella turcica to foramen cecum. Width of the base is measured between the summits of the entoglenoid processes. 3 As noted by Schultz (1955), in ontogenetic context the hominin foramen magnum does not migrate anteriorly; from the relatively

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3376

W. H. Kimbel & Y. Rak

A. afarensis cranial base

anterior position common to all juvenile hominoids, the foramen fails to shift posteriorly with growth of the cranium, as it does in all great apes.

REFERENCES Biegert, J. 1957 Der Formwandel des Primaten-Scha¨dels und seine Beziehungen zur ontogenetischen Entwicklung und den phylogenetischen Specialization der Kopforgane. Morph. Jb. 98, 77–199. Biegert, J. 1963 The evaluation of characters of the skull, hands and feet for primate taxonomy. In Classification and human evolution (ed. S. L. Washburn), pp. 116–145. Chicago, IL: Aldine de Gruyter. Dean, M. C. & Wood, B. A. 1982 Basicranial anatomy of Plio-Pleistocene hominids from East and South Africa. Am. J. Phys. Anthropol. 59, 157–174. (doi:10.1002/ajpa. 1330590206) Holloway, R. L. & Yuan, M. S. 2004 Endocranial morphology of A.L. 444-2. In The skull of Australopithecus afarensis (eds W. H. Kimbel, Y. Rak & D. C. Johanson), pp. 123 –135. Oxford, UK: Oxford University Press. Holloway, R. L., Clarke, R. J. & Tobias, P. V. 2004 Posterior lunate sulcus in Australopithecus africanus: Was Dart right? C. R. Palevol. 3, 287–293. (doi:10.1016/j.crpv. 2003.09.030) Johanson, D. C., White, T. D. & Coppens, Y. 1978 A new species of the genus Australopithecus (Primates: Hominidae) from the Pliocene of eastern Africa. Kirtlandia 28, 1 –14. Kimbel, W. H. 1988 Identification of a partial cranium of Australopithecus afarensis from the Koobi Fora Formation, Kenya. J. Hum. Evol. 17, 647 –656. (doi:10.1016/00472484(88)90022-X) Kimbel, W. H. & Delezene, L. K. 2009 ‘Lucy’ redux: a review of research on Australopithecus afarensis. Yrbk. Phys. Anthropol. 52, 2–48. (doi:10.1002/ajpa.21183) Kimbel, W. H., Johanson, D. C. & Coppens, Y. 1982 Pliocene hominid cranial remains from the Hadar Formation, Ethiopia. Am. J. Phys. Anthropol. 57, 453 – 499. (doi:10.1002/ajpa.1330570404) Kimbel, W. H., White, T. D. & Johanson, D. C. 1984 Cranial morphology of Australopithecus afarensis: a comparative study based on a composite reconstruction of the adult skull. Am. J. Phys. Anthropol. 64, 337 –388. (doi:10. 1002/ajpa.1330640403) Kimbel, W. H., Johanson, D. C. & Rak, Y. 1994 The first skull and other new discoveries of Australopithecus afarensis at Hadar, Ethiopia. Nature 368, 449 –451. (doi:10.1038/368449a0) Kimbel, W. H., Rak, Y. & Johanson, D. C. 2004 The skull of Australopithecus afarensis. Oxford, UK: Oxford University Press. Kimbel, W. H., Lockwood, C. A., Ward, C. V., Leakey, M. G., Rak, Y. & Johanson, D. C. 2006 Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. J. Hum. Evol. 51, 134–152. (doi:10.1016/j.jhevol.2006.02.003) Kirk, E. G. & Russo, G. A. 2010 Forward shift of the foramen magnum in humans and other bipedal mammals. Am. J. Phys. Anthropol. Suppl. 50, 142 –143. (doi:10. 1002/ajpa.21273)

Phil. Trans. R. Soc. B (2010)

Le Gros Clark, W. E. 1947 Observations on the anatomy of the fossil Australopithecinae. J. Anat. 81, 300 –333. Le Gros Clark, W. E. 1950 New palaeontological evidence bearing on the evolution of the Hominoidea. Quart. J. Zool. Soc. 105, 225 –264. Lieberman, D. E., Ross, C. F. & Ravosa, M. J. 2000 The primate cranial base: ontogeny, function and integration. Yrbk. Phys. Anthropol. 42, 117 –169. McCarthy, R. C. 2001 Anthropoid cranial base architecture and scaling relationships. J. Hum. Evol. 40, 41–66. (doi:10.1006/jhev.2000.0446) Olson, T. R. 1981 Basicranial morphology of the extant hominoids and Pliocene hominids: the new material from the Hadar Formation, Ethiopia and its significance in early human evolution and taxonomy. In Aspects of human evolution. (ed. C. B. Stringer), pp. 99–128. London, UK: Taylor and Francis. Rak, Y. 1983 The australopithecine face. New York, NY: Academic Press. Rak, Y. & Howell, F. C. 1978 Cranium of a juvenile Australopithecus boisei from the Lower Omo Basin, Ethiopia. Am. J. Phys. Anthropol. 48, 345–366. (doi:10. 1002/ajpa.1330480311) Robinson, J. T. 1958 Cranial cresting patterns and their significance in the Hominoidea. Am. J. Phys. Anthropol. 16, 397–428. (doi:10.1002/ajpa.1330160403) Ross, C. F. & Ravosa, M. J. 1993 Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. Am. J. Phys. Anthropol. 91, 305 –324. (doi:10.1002/ajpa. 1330910306) Schultz, A. H. 1955 The position of the occipital condyles and of the face relative to the skull base in primates. Am. J. Phys. Anthropol. 13, 97–120. (doi:10.1002/ajpa. 1330130108) Spoor, C. F. 1997 Basicranial architecture and relative brain size of Sts 5 (Australopithecus africanus) and other Plio-Pleistocene hominids. S. Afr. J. Sci. 93, 182 –186. Strait, D. S. & Grine, F. E. 2004 Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J. Hum. Evol. 47, 399–452. (doi:10.1016/j.jhevol.2004.08.008) Tobias, P. V. 1967 The Cranium and Maxillary Dentition of Australopithecus (Zinjanthropus) boisei. In Olduvai Gorge, vol. 2. London, UK: Cambridge University Press. Weidenreich, F. 1941 The brain and its roˆle in the phylogenetic transformation of the human skull. Trans. Am. Phil. Soc. 31, 320 –442. (doi:10.2307/1005610) Weidenreich, F. 1943 The skull of Sinanthropus pekinensis. Palaenotol. Sin. New Ser. D10, l– 484. White, T. D., Johanson, D. C. & Kimbel, W. H. 1981 Australopithecus africanus: its phyletic position reconsidered. S. Afr. J. Sci. 77, 445–470. White, T. D., Suwa, G., Hart, W. K., Walter, R. C., WoldeGabriel, G., de Heinzelin, J., Clark, J. D., Asfaw, B. & Vrba, E. 1993 New discoveries of Australopithecus at Maka in Ethiopia. Nature 366, 261 –265. (doi:10. 1038/366261a0) White, T. D., Suwa, G., Simpson, S. & Asfaw, B. 2000 Jaws and teeth of Australopithecus afarensis from Maka, Middle Awash, Ethiopia. Am. J. Phys. Anthropol. 111, 45–68. (doi:10.1002/(SICI)1096-8644(200001)111: 1,45::AID-AJPA4.3.0.CO;2-I)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3377–3388 doi:10.1098/rstb.2010.0042

Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000 Fred Spoor1,2,*, Meave G. Leakey3,4 and Louise N. Leakey3,5 1

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany 2 Department of Cell and Developmental Biology, University College London, UK 3 Koobi Fora Research Project, Nairobi, Kenya 4 Department of Anatomical Sciences, and 5 Department of Anthropology, Stony Brook University, New York, USA

The 3.5-Myr-old hominin cranium KNM-WT 40000 from Lomekwi, west of Lake Turkana, has been assigned to a new hominin genus and species, Kenyanthropus platyops, on the basis of a unique combination of derived facial and primitive neurocranial features. Central to the diagnosis of K. platyops is the morphology of the maxilla, characterized by a flat and relatively orthognathic subnasal region, anteriorly placed zygomatic processes and small molars. To study this morphology in more detail, we compare the maxillae of African Plio-Pleistocene hominin fossils and samples of modern humans, chimpanzees and gorillas, using conventional and geometric morphometric methods. Computed tomography scans and detailed preparation of the KNM-WT 40000 maxilla enable comprehensive assessment of post-mortem changes, so that landmark data characterizing the morphology can be corrected for distortion. Based on a substantially larger comparative sample than previously available, the results of statistical analyses show that KNM-WT 40000 is indeed significantly different from and falls outside the known range of variation of species of Australopithecus and Paranthropus, contemporary Australopithecus afarensis in particular. These results support the attribution of KNM-WT 40000 to a separate species and the notion that hominin taxonomic diversity in Africa extends back well into the Middle Pliocene. Keywords: human evolution; Pliocene; Africa; Kenyanthropus platyops; maxilla; geometric morphometrics

1. INTRODUCTION Whether or not the Pliocene hominin fossil record from Hadar (Ethiopia) and Laetoli (Tanzania) represents more than one species was the subject of ongoing debate in the 1980s (see Boaz 1988 for a review). Recovery of additional fossils and studies of intraspecific variation and temporal trends have subsequently resulted in a broad consensus supporting the interpretation of a single, sexually dimorphic species, Australopithecus afarensis (Lockwood et al. 1996, 2000; Kimbel et al. 2004; Kimbel & Delezene 2009). However, fossils found at two other sites have reopened the debate of species diversity in the African Middle Pliocene. A partial mandible and upper premolar, discovered in 1994 in the Koro-Toro area of Chad and approximately 3.5 Myr old, have been assigned to a new species, Australopithecus bahrelghazali (Brunet et al. 1995, 1996). This attribution has been questioned as the limited morphology preserved by

* Author for correspondence ([email protected]). Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rstb.2010.0042 or via http://rstb.royalsocietypublishing.org. One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

these fossils is considered to be within the range of variation of A. afarensis (White et al. 2000; Ward et al. 2001; Kimbel 2007; Wood & Lonergan 2008). However, a detailed analysis of symphyseal shape of both the type specimen and a previously unpublished second mandible supports a separate specific status (Guy et al. 2008). A second site providing possible evidence for species diversity is Lomekwi, west of Lake Turkana (Kenya). Fieldwork in the early 1980s and late 1990s resulted in hominin discoveries dated between 3.5 and 3.2 Ma, including a well-preserved temporal bone, 2 partial maxillae, 3 partial mandibles, 44 isolated teeth and a largely complete although distorted cranium, KNM-WT 40000 (Brown et al. 2001; Leakey et al. 2001). Several of these specimens were found to show a morphology markedly different from that of contemporary A. afarensis (Leakey et al. 2001). Accordingly, the cranium and one fragmentary maxilla were assigned to a new genus and species, Kenyanthropus platyops, based on a unique combination of derived facial and primitive neurocranial features (Leakey et al. 2001). A number of recent studies and reviews have cautiously considered K. platyops as a valid taxon (Strait & Grine 2004; Kimbel 2007; Cobb 2008; Nevell & Wood 2008;

3377

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3378

F. Spoor et al.

The maxilla of KNM-WT 40000

Wood & Lonergan 2008). On the other hand, White (2003) questioned the taxon’s validity, and the notion of Pliocene hominin diversity. In his view it cannot be excluded that KNM-WT 40000 is an early Kenyan variant of A. afarensis, given the distortion of the specimen and the known cranial variation in early hominin species and among modern apes and humans. Central to the diagnosis of K. platyops is the morphology of the maxilla, characterized by a flat and relatively orthognathic subnasal region, an anteriorly placed zygomatic process and small molars. In the present study, this morphology, as shown by KNM-WT 40000, is investigated in more detail. We made quantitative comparisons, using geometric morphometric and univariate methods, with Plio-Pleistocene hominin fossils from Ethiopia, Kenya, Tanzania and South Africa and with samples of modern humans, gorillas and chimpanzees. Such analyses are obviously affected by the post-mortem distortion of KNM-WT 40000, the reason the initial description provided limited metric comparisons only (Leakey et al. 2001). The impact of the preservation of the maxilla was therefore evaluated in detail using new evidence based on additional preparation of the specimen and computed tomography (CT). The information thus obtained was used to adjust landmarks representing the key morphological features. In statistical analyses the morphology of the specimen is considered both in its preserved form and corrected for distortion. Using a substantially larger comparative sample than available to Leakey et al. (2001), the present study aims to assess two specific hypotheses. 1. KNM-WT 40000 does not differ significantly from A. afarensis with respect to the morphological features of the maxilla included in the differential diagnosis of K. platyops (Leakey et al. 2001). Rejection of this null hypothesis would provide evidence for species diversity in eastern Africa at around 3.5 Ma. 2. KNM-WT 40000 does not differ significantly from species of Australopithecus and Paranthropus with respect to the morphological features of the maxilla included in the differential diagnosis of K. platyops (Leakey et al. 2001). Rejection of this null hypothesis would support the attribution of KNM-WT 40000 to a separate species.

2. MATERIAL AND METHODS In geometric morphometric shape analyses the KNMWT 40000 maxilla was compared with all available hominin specimens attributed to Australopithecus and Paranthropus that preserve the morphology concerned. These are: Australopithecus anamensis (KNM-KP 29283), A. afarensis (A.L. 199-1, A.L. 200-1, A.L. 417-1, A.L. 427-1, A.L. 444-2 and A.L. 486-1), Australopithecus africanus (MLD 9, Sts 52, Sts 71 and Stw 498), Australopithecus garhi (BOU-VP-12/130), Paranthropus aethiopicus (KNM-WT 17000), Paranthropus boisei (OH 5) and Paranthropus robustus (SK 11, SK 12, SK 13, SK 46, SK 48, SK 83 and SKW 11). All are adults, with the exception of Phil. Trans. R. Soc. B (2010)

A.L. 486-1, Sts 52, OH 5, SK 13 and SKW 11, which are subadults (third molars not in occlusion). The intraspecific variation in maxillary shape among the fossils was examined by making comparisons with samples of modern humans and African great apes. The modern human sample consists of 55 specimens (sex mostly unknown), representing indigenous populations from all six widely inhabited continents, housed at the Natural History Museum (London) and at the Department of Cell and Developmental Biology at University College London. The African ape samples (all non-captive) include 50 specimens of the eastern lowland gorilla (Gorilla gorilla gorilla; 26 males, 24 females) and 61 specimens of chimpanzee (Pan troglodytes, all subspecies represented; 28 males, 33 females) from the collections of the Powell Cotton Museum (Birchington), the Royal College of Surgeons (London), the Natural History Museum (London) and the Department of Cell and Developmental Biology at University College London. Specimens are adult and lack signs of substantial pathology, of the alveolar process of the maxilla in particular. CT was used to examine internal morphology and record surface landmarks of some of the fossil specimens. KNM-WT 40000 was scanned with a Siemens AR.SP medical scanner at the Diagnostic Center, Nairobi (Kenya). Scans in sequential mode were made in the transverse plane, parallel to the postcanine alveolar margin, using a slice thickness and increment of 1.0 mm. Images were reconstructed with a SP90 kernel, extended CT-scale and a 0.17 mm pixel size. The tooth roots were segmented by Kornelius Kupczik and the first author. New CT data with improved spatial resolution (isotropic voxel size 0.069 mm) were obtained more recently with the portable BIR ACTIS 225/300 high-resolution industrial CT scanner of the Department of Human Evolution at the Max Planck Institute for Evolutionary Anthropology (Leipzig, Germany), at the time installed at the National Museums of Kenya in Nairobi. Other CT data of hominin fossils used here are from the digital archives of the National Museums of Kenya, and the Department of Anthropology, University of Vienna. Visualization of the CT datasets was done using AMIRA 4.1.2 (Mercury Computer Systems). A set of maxillary landmarks was selected using three criteria: (i) they should quantify the features used in the differential diagnosis of K. platyops; (ii) it should be possible to take these landmarks from the KNM-WT 40000 maxilla and correct them for distortion of the specimen; and (iii) the number of fossil specimens used in the comparative sample should be as large as possible. Optimizing all three criteria resulted in the selection of five two-dimensional landmarks, taken from the specimens projected in lateral view: nasospinale (ns), prosthion (pr), the buccal alveolar margin between the canine and third premolar (pc), the buccal alveolar margin between the second and third molar (m23) and the antero-inferior takeoff of the zygomatic process (azp), a point most anterior, inferior and medial on the root of the process (figure 1). These landmarks quantify the orientation of

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

The maxilla of KNM-WT 40000 (a) ns

azp

pr

pc

m23

(b)

Figure 1. CT-based parallel-projected 3D reconstructions comparing the maxillae in lateral view of (a) A.L. 200-1 (reversed right side of cast, Australopithecus afarensis) and (b) KNM-WT 40000 (left side of original, Kenyanthropus platyops). The five landmarks are shown, together with the connecting wire frame used in figure 3 (see text for the abbreviations of the landmarks). The broken surface of the zygomatic process of KNM-WT 40000 facing laterally is not visualized to emphasize the outline compared with the equivalent morphology in A.L. 200-1. Scale bar, 10 mm.

the subnasal clivus in the midsagittal plane (ns-pr), the anterior zygomatic process position along the postcanine tooth row (azp relative to pc-m23) and the degree of anterior projection and transverse flatness of the subnasal clivus (pr – pc or sagittally projected length of the canine and incisor alveolar margin). The five landmarks were mostly recorded from digital images of the specimens in exact lateral view and taken with a focal distance of 1 – 2 m to minimize parallax artefacts. Nasospinale and prosthion may not be visible in this view and are indicated by markers (see Spoor et al. 2005 for details of this method). The landmarks of KNM-WT 40000, A.L. 444-2, Sts 52a, Sts 71, KNM-WT 17000 and OH 5 were taken from CT datasets, using AMIRA 4.1.2 (Mercury Computer Systems) to obtain parallel-projected three dimensional surface reconstructions in a lateral view and sagittal sections to locate nasospinale and prosthion. The left side of the extant specimens was used, the mean of both sides of A.L. 200-1 and OH 5 and the best preserved side of the other fossils (left for KNM-WT 40000). All landmark coordinates were recorded with IMAGEJ 1.42d (National Institutes of Health, USA). To examine the impact of the distortion of KNMWT 40000 on the landmark positions, additional surface preparation was done of the anterior and lateral aspects of the left maxilla. Small remnants of the matrix on the bone surface were removed and cracks fully exposed. Bone edges on either side of the crack could thus be matched, identifying possible Phil. Trans. R. Soc. B (2010)

F. Spoor et al.

3379

shifts along the crack. Moreover, the width of the cracks along specific trajectories linking the five landmarks (figure 2a,d ) were measured to the nearest tenth of a millimetre with digital callipers, making sure that the distance was taken between matching edges. The midsagittal surface area above prosthion is not well preserved, and the expansion of the subnasal clivus in the sagittal plane was examined more laterally along a line from the I2/C interalveolar septum to the left lower corner of the nasal aperture (figure 2a). The crack widths were used to calculate the percentage of surface expansion between the five landmarks, and the x and y coordinates were adjusted accordingly. Both preparation and measurements were done under a binocular microscope, using acetone to temporarily enhance the difference between bone and matrix. Generalized procrustes analyses of the landmark coordinates and principal component analyses (PCAs) of the output were performed with MORPHOLOGIKA 2.5 (O’Higgins & Jones 1998). With this software, the maxillary shape variation associated with each principal component (PC) can be explored visually by morphing a wireframe of the five landmarks according to the position on a bivariate plot of two PCs. F-tests and t-tests of the individual PC scores, with sequential Bonferroni correction for multiplicity (Rice 1989), were done using PAST 1.93 (Hammer et al. 2001) and MS EXCEL 2003. One-tailed distributions were used in the t-tests when the hypotheses and the species diagnosis of K. platyops specifically state the nature of a possible difference (e.g. KNM-WT 40000 is subnasally less prognathic than A. afarensis). Consequently, two-tailed distributions were used only for the comparison of PCs related to zygomatic process position in KNM-WT 40000 and P. robustus, where there is no prior prediction of the nature of the difference. KNM-WT 40000 was also compared with species individually by combining all PCs obtained in separate analyses of KNM-WT 40000 and each species. The Mahalanobis’ distance of KNM-WT 40000 from the centroid of the species sample is compared with the distances from that centroid of the specimens in the sample (software written by Paul O’Higgins, Hull York Medical School, UK). All statistical analyses were done separately for KNM-WT 40000 in its preserved form and corrected for distortion. A drawback of the landmark-based approach is that it limits the number of specimens that can be included. That is because each must preserve the full area covered by the landmarks, whereas less complete specimens may be informative regarding individual diagnostic aspects of the K. platyops maxilla. When interpreting the main shape analysis, two maxillary features were therefore considered individually as well, to assess consistency among a larger number of fossils than those preserving all five landmark locations. The subnasal clivus angle marks the orientation in the sagittal plane of the segment nasospinale to prosthion relative to the postcanine alveolar margin, up to the M2/M3 septum. It was measured using IMAGEJ from digital images or CT-based visualizations of a specimen in a lateral

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3380

F. Spoor et al.

The maxilla of KNM-WT 40000

(a)

(b) P3

ns M2

pr

(c)

(e)

M

B

(d) 6% 18% 20% 18% 16%

Figure 2. Distortion of KNM-WT 40000. (a) Anterior view, giving the midline (black line) to indicate the midface skewing, left nasospinale (ns), prosthion (pr) and the trajectory used to calculate the height expansion of the subnasal area (white line). (b) CT-based 3D reconstruction of the maxilla in superior view, showing the tooth roots inside the translucent bone. (c) A high-resolution sagittal CT image through the buccal roots of the left P3 to M2 (orientation indicated by the black line in (b)). The thin black lines mark a longer crack through the premolar roots. (d) Lateral view of the left maxilla, showing the pattern of matrix-filled cracks highlighted by wetting with acetone. The five landmarks are shown as in figure 1. The trajectories along which crack widths were measured are given by lines with associated percentages of expansion (black line refers to the subnasal trajectory shown in (a)). (e) The right M2 crown (M, mesial; B, buccal), with black lines marking the endpoint of cracks highlighted with acetone. The white lines indicate the match at the mesial end of the widest crack. The dark area on the mesiolingual corner is a strong shadow of the enamel more distally, rather than damage to the dentine. Scale bars, (a,b) 30 mm, (c,d ) 10 mm and (e) 3 mm.

view, where feasible estimating the postcanine alveolar margin orientation if the exact position of landmarks pc or m23 is not preserved. Furthermore, the anterior position of the zygomatic root is considered relative to the dental row, following Lockwood & Tobias (1999, table 7). These features were recorded by the authors from the original specimens, with additional observations regarding zygomatic root position in A. afarensis provided by William H. Kimbel (Arizona Sate University, USA). Finally, the crown size of the right M2 was assessed on the basis of conventional mesiodistal and buccolingual measurements, defined in two different ways Phil. Trans. R. Soc. B (2010)

(Tobias 1967; White 1977). Full preparation of the M2 crown had been done at the time of the first announcement (Leakey et al. 2001), and measurements of cracks affecting the length and width had been taken at the time. Comparative data of M2 size in Plio-Pleistocene hominins were taken from the literature, combined with our own measurements.

3. PRESERVATION OF THE MAXILLA The facial parts of KNM-WT 40000 show postmortem distortion in the form of lateral skewing of the nasal area and a network of matrix-filled surface

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

The maxilla of KNM-WT 40000 (a)

SKW11*

F. Spoor et al.

3381

0.15 Stw498

0.10

SK13*

Sts71

WT17k

KP29283

0.05

BOUVP12/130 MLD9 Sts52*

OH5*

PC1

–0.1

SK83

0.1

WT40k

SK12

–0.05 SK11

AL486-1* AL200-1

AL427-1

SK46 AL199-1

–0.10

AL417-1 AL444-2

PC2

0.06

(b)

WT40k

AL199-1 Stw498 SK12

SK13*

0.02

AL200-1 SKW11*

AL427-1 PC4

SK11 OH5*

AL417-1

–0.075

0.05

Sts71 KP29283 SK83

MLD9

Sts52*

AL444-2 BOUVP12/130 WT17k

AL486-1*

SK46

–0.04 PC5 0.3

(c) A. africanus

0.2

H. sapiens P. troglodytes WT40k PC1

–0.6

–0.2

G. gorilla

P. robustus –0.2

A. afarensis –0.3 PC2

Figure 3. Bivariate plots of PCs. (a) PC2 against PC1 and (b) PC5 against PC4 of the fossils samples. (c) PC2 against PC1 of the combined fossil and extant samples. KNM-WT 40000 (black dot) is corrected for distortion. The prefix KNM- of the Kenyan specimens is omitted, and an asterisk indicates subadults. Convex hulls are given for A. afarensis (solid line), A. africanus (dash-dot line) and P. robustus (dashed line), as well as in (c), the 95% confidence ellipses of these taxa and the extant species (solid line). The grey-shaded wire frames in (a,b) are defined in figure 1 and indicate the maxillary shapes represented at the extremes of the PC axes. See the main text for the percentage of variance represented by each PC. Phil. Trans. R. Soc. B (2010)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3382

F. Spoor et al.

The maxilla of KNM-WT 40000

cracks associated with clay-induced expansion mainly affecting the alveolar and zygomatic processes (Leakey et al. 2001; figure 2a,d ). Before assessing the degree of expansion in the landmarked part of the maxilla, it is worth considering whether this area shows any evidence of substantial post-mortem shape changes as well. A good indicator of structural integrity of the alveolar process is the internal preservation of the tooth roots. Those present, of the left I1 to M2 and the right C to M3, are visualized in a CT-based three dimensional reconstruction of the maxilla in superior view (figure 2b). The roots are well preserved, without distinct misalignments or distortion, and the dental arcade is symmetrical in shape. The only exception is the largely exposed right canine root which is in the correct position at the alveolar margin, but the apex is tilted anteriorly. A more detailed view of the internal preservation of the left maxilla is provided by a high-resolution sagittal CT image through the buccal roots of the left P3 to M2 (figure 2c). Several fine cracks through the roots can be seen, and the mesiobuccal root canal of the M2 is expanded, but this is not accompanied by substantial displacement of the root parts on opposite sides of the cracks. The mesiodistal distance between the P4, M1 and M2 is increased by matrix expansion, particularly of the alveolar space around the roots. However, this is less so between the P3 and P4. Overall, the internal CT evidence suggests a pattern of expansion without substantial shape changes due to skewing or other directional deformation. The well-preserved state of the premolar root area is of particular importance as it indicates that the overlying anterior zygomatic process position is unlikely to have been altered by the distortion. This is further confirmed by the absence of major shifts of surface bone fragments between the premolar alveolar margin and the anterior zygomatic root. The percentages of bone expansion along the measured trajectories vary from 16 per cent along the postcanine alveolar margin to 20 per cent transversely over the canine jugum (figure 2d). The one exception is the area superior to the canine alveolus where the expansion in transverse direction is only 6 per cent. The right M2 crown is shown in figure 2e. The widest crack runs from the mesial interstitial facet to the distolingual corner, a second shorter one from the central area of the main break to the lingual crown margin and a third thin one from the central area to the distal interstitial facet. Enamel and occlusal dentine edges of the breaks provide good clues regarding the match of the four parts they delineate. A refit of the crown would require the two lingual parts to be moved buccally, the triangular distolingual part to be moved mesially and the mesiolingual part to be moved slightly distally. Closing the cracks would result in an estimated 1.2 mm reduction of the buccolingual width of the crown. The mesiodistal length along the crown axis (White 1977) is not affected by the cracks, and has only been corrected for an estimated 0.5 mm of mesial interstitial wear. However, the maximum length (Tobias 1967) requires correction for the 0.7 mm distal displacement of the triangular distolingual part. The buccolingual width is not Phil. Trans. R. Soc. B (2010)

affected by occlusal wear as it has not reached the level of maximum bulging of the buccal and lingual surfaces. The recently acquired high-resolution CT scans will provide the opportunity to prepare a full three dimensional virtual reconstruction of the right M2 crown.

4. MORPHOMETRIC COMPARISONS The PCA of the hominin fossil sample described here uses the corrected landmark configuration of KNMWT 40000 (table 1). The first six PCs account for 99.9 per cent of the variation. Although PC3 – PC6 contribute less than 10 per cent each, these were still assessed because KNM-WT 40000 could specifically differ from the other fossils in morphology that is less variable among the Australopithecus and Paranthropus specimens which dominate the sample. PC1, PC2, PC4 and PC5 were found to provide evidence in relation to the hypotheses examined here, and these are shown in bivariate plots (figure 3), with wireframes marking the shapes represented at either end of each axis. PC3 and PC6 will be briefly described as well. PC1 (eigenvalue 0.0263; 72% of variance) represents the variation in anteroposterior position of the anterior zygomatic process (landmark azp) and the relative length and transverse flatness of the subnasal clivus (ns– pr and pr – pc, respectively). PC1 separates Australopithecus species, with a more posteriorly positioned zygomatic and a shorter and transversely curved (projecting) subnasal clivus, from Paranthropus species, with a more anteriorly positioned zygomatic and a longer and transversely flat subnasal clivus (figure 3a). Addressing hypothesis 1, the PC1 score of KNM-WT 40000 differs significantly from that of A. afarensis (table 1), reflecting its more anteriorly placed zygomatic and a subnasal clivus that is transversely flat. When compared with multiple species (hypothesis 2), the difference between KNM-WT 40000 and A. afarensis is statistically significant, as is the difference from A. africanus. The PC1 scores suggest that KNM-WT 40000 is intermediate between Australopithecus and Paranthropus with respect to this particular morphology. However, the difference from P. robustus is not statistically significant, with the subadult SKW 11 having a score close to KNM-WT 40000. PC2 (eigenvalue 0.0054; 15% of variance) represents both the inferosuperior and anteroposterior position of the zygomatic process and the length of subnasal clivus. This PC separates A. afarensis, with a more inferoposteriorly positioned zygomatic and longer subnasal clivus, from A. africanus, with a more anterosuperiorly positioned zygomatic and shorter clivus (figure 3a). KNM-WT 40000 and A. garhi are intermediate, A. anamensis falls with A. africanus, and Paranthropus specimens show the full range of PC2-related morphological variation. KNM-WT 40000 is not significantly different from A. afarensis (hypothesis 1) or from other hominin species more in general (hypothesis 2). PC3 (eigenvalue 0.0029; 8% of variance) purely represents the inferosuperior height of landmark azp, the anterior zygomatic root position, above the postcanine alveolar margin. KNM-WT 40000 does not differ

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

The maxilla of KNM-WT 40000

F. Spoor et al.

3383

Table 1. PCs of the maxillary shape analysis. The landmarks of KNM-WT 40000 are corrected for distortion. The sample size (n), mean, minimum, maximum and standard deviation (s.d.) are given, and the comparisons of KNM-WT 40000 by t-test list the probability ( p; one-tailed, except þtwo-tailed) and the significance (multiple comparisons after sequential Bonferroni correction). n.s., not significant; *p , 0.05; **p , 0.01.

KNM-WT 40000

PC1

PC2

PC4

PC5

20.068

20.003

0.049

0.065

A. anamensis

n¼1

0.167

0.064

20.045

20.009

A. afarensis

n mean min. max. s.d.

6 0.1285 0.053 0.198 0.0623

6 20.0742 20.129 20.001 0.0498

6 20.0012 20.024 0.018 0.0136

6 0.0014 20.030 0.038 0.0262

A. garhi

n¼1

0.178

0.029

20.011

20.027

A. africanus

n mean min. max. s.d.

4 0.1065 0.064 0.152 0.0401

4 0.0558 0.025 0.092 0.0316

4 0.0076 20.046 0.043 0.0382

4 20.0004 20.015 0.030 0.0208

P. aethiopicus

n¼1

20.152

0.068

20.010

20.040

P. robustus

n mean min. max. s.d.

6 20.1879 20.259 20.070 0.0654

6 0.0073 20.070 0.142 0.0855

6 20.0040 20.087 0.048 0.0488

6 0.0014 20.024 0.019 0.0169

P. boisei

n¼1

20.194

0.020

0.018

20.005

0.016 *

0.120 n.s.

0.010 **

0.037 *

0.016 * 0.015 * 0.151þ n.s.

0.120 n.s. 0.098 n.s. 0.919þ n.s.

0.010 * 0.204 n.s. 0.182 n.s.

0.037 * 0.034 n.s. 0.009 *

comparison with A. afarensis p sign. comparison with Australopithecus and Paranthropus A. afarensis p sign. A. africanus p sign. P. robustus p sign.

significantly from A. afarensis, A. africanus or P. robustus, and this morphology does not relate to the hypotheses. PC4 (eigenvalue 0.0011; 3% of variance) represents the subnasal clivus orientation associated with variations in the midline area only, as shown by the angle of ns– pr to the entire alveolar margin (pr – pc – m23; figure 3b). KNM-WT 40000 has the highest score in the sample and is significantly less prognathic than A. afarensis (table 1). When compared with multiple species, this difference from A. afarensis is statistically significant as well, but differences from A. africanus and P. robustus are not. PC5 (eigenvalue 0.0006; 2% of variance) represents the subnasal clivus orientation associated with variations of the entire subnasal area. The midline clivus (ns– pr) and the canine – incisor alveolar margin (pr – pc) jointly vary in orientation relative to the postcanine alveolar margin (pc – m23; figure 3b). KNM-WT 40000 is by far the most orthognathic in the sample, and the difference from A. afarensis is statistically significant (table 1, figure 3b). When compared with multiple species, KNM-WT 40000 is significantly different from A. afarensis and P. robustus. Phil. Trans. R. Soc. B (2010)

PC4 and PC5 jointly contribute to an overall pattern of differences in subnasal prognathism in the fossil sample (figure 3b). KNM-WT 40000 is the most orthognathic, whereas the P. aethiopicus specimen KNM-WT 17000, the A. garhi type BOU-VP-12/130 and the A. anamensis specimen KNM-KP 29283 are the most prognathic. The other species of Australopithecus and Paranthropus do not differ notably. PC6 (eigenvalue 0.0003; 1% of variance) represents the angle and length proportions between the alveolar margins of the anterior (canine – incisor) and postcanine teeth. There is no separation between taxa, and KNM-WT 40000 does not differ significantly from A. afarensis, A. africanus and P. robustus. Using the landmark configuration of KNM-WT 40000 as preserved rather than corrected for distortion results in PC scores that are only marginally different from those reported in table 1. Significance levels of the t-tests are the same as for the corrected landmarks, except for multiple species comparisons of PC5 with A. afarensis and A africanus (electronic supplementary material, S1). When excluding the five subadult specimens from the fossil samples, KNM-WT 40000 differs significantly from A. afarensis for PC1, 4 and 5, as

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3384

F. Spoor et al.

The maxilla of KNM-WT 40000

Table 2. Mahalanobis’ distance test comparing KNM-WT 40000 using all PCs combined. D 2, squared Mahalanobis’ distance of KNM-WT 40000 from centroid of species sample; SDU, standard deviation unit of Mahalanobis’ distances within the sample; d.f., degrees of freedom; p, probability that KNM-WT 40000 belongs to the species. For sample sizes less than six, the probability is not calculated (n/a) because estimates of the variance are insufficiently reliable. D2

SDU

d.f.

KNM-WT 40000 (corrected) A. afarensis 21.065 4.589 6 A. africanus 37.084 6.089 4 P. robustus 13.284 3.644 6 KNM-WT 40000 (as preserved) A. afarensis 18.909 4.348 6 A. africanus 36.609 6.050 4 P. robustus 13.738 3.706 6 KNM-WT 40000 (corrected), adults only A. afarensis 33.088 5.752 5 A. africanus 28.397 5.328 3 P. robustus 20.390 4.515 4

p-value

,0.0025 n/a ,0.05 ,0.005 n/a ,0.05 n/a n/a n/a

before, but for PC2 as well (electronic supplementary material, S2). When compared with multiple species, KNM-WT 40000 differs significantly from A. afarensis for PC4 and from P. robustus for PC1. Results of Mahalanobis’ distance tests comparing KNM-WT 40000 with A. afarensis, A. africanus and P. robustus individually, and using all PCs combined, are given in table 2. Differences from A. afarensis and P. robustus are statistically significant, whereas the A. africanus sample is too small for a probability to be calculated. A PCA of the fossil hominins combined with modern humans, chimpanzees and gorillas shows how the main aspects of variation of the fossil samples, as reflected by PC1 and PC2 (48% and 19% of the variance), compare with those shown by larger samples of extant species. A bivariate plot of PC2 against PC1 shows that the areas of observed variation (convex hulls) of A. afarensis and P. robustus are not substantially different from those of the extant species, whereas A. africanus, with fewer specimens in the sample, appears somewhat less variable (figure 3c). With samples sizes of 50 or more, 95% confidence ellipses of the extant species have a close fit with the observed variation, but for the small fossil samples the ellipses are large. Importantly, F-tests indicate that the standard deviations of PC1 and PC2 obtained for the fossil taxa are not significantly different from those of the extant species (table 3). The M2 crown size of KNM-WT 40000 falls below the currently known range of variation of all hominin species included in the comparisons (table 4). Its mesiodistal length is the same as the minimum known for A. anamensis, but the particular specimen has a larger buccolingual width than KNM-WT 40000 (KNM-ER 30200: 13.2 as opposed to 12.4). Statistically, both the mesiodistal length and buccolingual width are significantly smaller in KNM-WT Phil. Trans. R. Soc. B (2010)

Table 3. Interspecific comparisons of the standard deviations of PC1 and PC2 obtained in the maxillary shape analysis, giving F and probability ( p) values. The differences are not statistically significant after sequential Bonferroni correction. PC1

A. afarensis –H. sapiens A. afarensis –P. troglodytes A. afarensis –G. gorilla A. africanus –H. sapiens A. africanus –P. troglodytes A. africanus –G. gorilla P. robustus–H. sapiens P. robustus–P. troglodytes P. robustus–G. gorilla

PC2

F

p-value

F

p-value

1.010 1.083 1.371 1.570 1.435 1.134 1.023 1.119 1.416

0.865 0.758 0.503 0.811 0.885 0.914 0.827 0.720 0.470

1.441 1.192 1.368 2.233 2.698 2.351 2.954 2.445 2.805

0.450 0.648 0.505 0.560 0.451 0.529 0.040 0.088 0.053

40000 than in A. afarensis (table 4). When compared with multiple species of Australopithecus and Paranthropus, its mesiodistal length is only significantly smaller than in P. boisei, but its buccolingual width is smaller than in all species other than A. anamensis.

5. DISCUSSION The taxonomic diagnosis of K. platyops and initial description of its type specimen KNM-WT 40000 were mainly based on qualitative comparisons (Leakey et al. 2001). Here we analyse the maxilla of KNM-WT 40000 quantitatively and test the specific hypotheses that the specimen is not different from the contemporary taxon A. afarensis and, more broadly, that it is not different from species of Australopithecus and Paranthropus. Based on the analyses of maxillary shape and M2 crown size, both hypotheses can be rejected. These findings thus support the notion that there was hominin species diversity in the Middle Pleistocene and corroborate the validity of K. platyops as a separate species. It is worth pointing out that the observed differences are substantial, given that statistical significance is obtained for small samples, with Bonferroni corrections when comparing KNM-WT 40000 with multiple species. Moreover, comparisons of the A. afarensis, A. africanus and P. robustus samples used here with larger samples of modern humans, chimpanzees and gorillas indicate that these fossils show representative levels of intraspecific morphological variation. Hence, the observed differences from KNM-WT 40000 are unlikely to be an artefact of under-sampled variation in the three fossil species. The observation by Leakey et al. (2001) that the M2 crown size of KNM-WT 40000 is smaller than the known range of variation shown by species of Australopithecus and Paranthropus is upheld here based on the largest sample currently available. The difference is most distinct for the buccolingual width. This is the more reliable measure in KNM-WT 40000 as it is not affected by interstitial or occlusal wear, and the crack expanding the width is well defined and can be corrected for with confidence.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

The maxilla of KNM-WT 40000

F. Spoor et al.

3385

Table 4. Mesiodistal (MD) length and buccolingual (BL) width of the M 2, and the subnasal clivus (ns-pr) angle to the postcanine alveolar margin. The sample size (n), mean, minimum, maximum and standard deviation (s.d.) are given. Comparisons by t-test of KNM-WT 40000 with hominin species list the probability ( p, one-tailed) and significance (n.s., not significant; multiple comparisons with sequential Bonferroni correction). MD1 and BL1 defined after White (1977), MD2 and BL2 after Tobias (1967). The subnasal clivus angle was measured among adult and subadult specimens (M 2 in full occlusion) listed in the electronic supplementary material, S3. *p , 0.05; **p , 0.01; ***p , 0.001. M 2 size

KNM-WT 40000

MD1

MD2

BL1

BL2

source

subnasal angle

11.4

11.9

12.4

12.8

Leakey et al. (2001), this study

47

A. anamensis

n mean min. max. s.d.

8 — 12.88 11.4 14.3 1.04

8 — 14.50 12.9 16.7 1.19

Ward et al. (2001), White et al. (2000)

1 27

A. afarensis

n mean min. max. s.d.

12 — 13.00 12.1 14.1 0.60

13 — 14.80 13.4 15.8 0.60

Kimbel & Delezene (2009)

6 34.6 29 39 3.5

A garhi

n¼1

14.4

—

17.7

—

Asfaw et al. (1999)

27

A. africanus

n — mean min. max. s.d.

24 14.12 12.6 16.6 1.09

—

28 Moggi-Cecchi et al. (2006), J. Moggi-Cecchi 15.95 (2006, personal communication), this study 13.5 17.9 1.23

9 34.2 30 37 1.9

P. aethiopicus

n¼1

—

—

—

31

P. robustus

n — mean min. max. s.d.

24 14.00 11.6 15.7 0.99

—

24 J. Moggi-Cecchi (2006, personal communication), 15.73 this study 14.0 16.9 0.94

8 36.8 32 39 4.1

P. boisei

n — mean min. max. s.d.

6 15.84 14.7 17.2 1.03

—

6 Tobias (1967), Leakey & Walker (1988), Wood 18.18 (1991), this study 16.6 21.0 1.55

2 35.9 33 39

—

comparison with A. afarensis p 0.013 sign. *

0.001 **

comparison with Australopithecus A. anamensis p 0.111 sign. n.s. A. afarensis p 0.013 sign. n.s. A. africanus p sign. P. robustus p sign. P. boisei p sign.

and Paranthropus 0.073 n.s. 0.001 ** 0.029 0.010 n.s. * 0.024 0.003 n.s. * 0.008 0.012 * *

The geometric morphometric shape analysis of the maxilla shows that zygomatic process position together with subnasal clivus length and transverse flatness account for most of the variance in the hominin fossil sample (PC1 and PC2 combined, 86%, figure 3a). PC1 associates a more anteriorly positioned zygomatic process with a transversely flatter and longer subnasal clivus, along a gradient of genera: Paranthropus, Kenyanthropus (i.e. KNM-WT 40000) Phil. Trans. R. Soc. B (2010)

0.011 *

0.011 * 0.000 *** 0.024 *

and Australopithecus. In contrast, PC2 associates a more anteriorly positioned zygomatic process with a shorter subnasal clivus and separates A. afarensis from A. africanus only. There is no evidence of intraspecific differences within Paranthropus regarding PC1 and PC2, as KNM-WT 17000 and OH 5 fall in the middle of the range of P. robustus. Apart from zygomatic root position and transverse subnasal flatness, subnasal prognathism is a third

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3386

F. Spoor et al.

The maxilla of KNM-WT 40000

Table 5. Anterior position of the zygomatic process along the dental row. Accession codes CH, ER, KP and WT lack the prefix KNM-. P3

P3/P4

KP 29283 A.L. 442-1

A. anamensis A. afarensis

A. garhi A. africanus

Sts 52a

SK 13a SK 47a SK 821

WT 40000 WT 38350 WT 17000 TM 1517 SK 48 SK 52a SK 79 SK 83 SKW 11a

KGA 10-525 CH 1Ba ER 732 WT 17400a

KGA 10-525 ER 405 ER 406 OH 5

K. platyops P. aethiopicus P. robustus

P. boisei

a

P4

MLD 6 MLD 45 Sts 17 Sts 52a Sts 53 Sts 71 Stw 252a,b Stw 391 Stw 505

P4/M1

M1

A.L. 58-22 A.L. 200-1a A.L. 333-1 A.L. 427-1 A.L. 444-2 A.L. 486-1a A.L. 651-1 BOU-VP-12/130 MLD 9 TM 1511 TM 1512 TM 1514 Sts 63 Sts 3009 Stw 13 Stw 183a,b Stw 498

A.L. 199-1 A.L. 333-2 A.L. 413-1 A.L. 417-1d A.L. 822-1

Sts 5

DNH 7 SK 11 SK 12 SK 29 SK 46 SK 79 SKW 12

Immature specimen. Listed as A. africanus, but affinities uncertain (Lockwood & Tobias 2002).

b

prominent aspect of maxillary shape characterizing KNM-WT 40000. It is also expressed by two separate patterns of variation (PC4 and PC5; figure 3b), which differ depending on whether the clivus orientation varies in the midline only (PC4), or involves the entire subnasal area, from canine jugum to canine jugum bilaterally (PC5). As most specimens in the sample (P. robustus, P. boisei, A. afarensis and A. africanus) tend to show similar levels of prognathism, this morphology does account for only 5 per cent of the variance in the total sample. However, it does single out the orthognathic morphology of KNM-WT 40000 and to a lesser extent the more prognathic shape in A. anamensis, A. garhi and P. aethiopicus. This pattern illustrates that in interspecific comparisons the higher PCs associated with small amounts of overall variance can provide highly relevant information regarding individual specimens, because the distribution of the variance depends on the sample composition. In all, the analyses confirm the occurrence of three different facial patterns among the early hominins considered here. Australopithecus is characterized by a prognathic, transversely curved subnasal area combined with posteriorly positioned zygomatics (figure 1a), Paranthropus by a prognathic, transversely Phil. Trans. R. Soc. B (2010)

flat subnasal area with anteriorly positioned zygomatics and Kenyanthropus by a more orthognatic, transversely flat subnasal area with anteriorly positioned zygomatics (figure 1b). Two of the facial features, the degree of midline subnasal prognathism and the position of the zygomatic process, can be quantified individually in a larger number of early hominin specimens than could be included in the geometric morphometric analyses. It can thus be assessed whether the evidence from larger samples is consistent with the landmark-based results. The subnasal angle, which combines the shape variation associated with PC4 and PC5, is larger in KNM-WT 40000 (478) than in any of the Australopithecus and Paranthropus specimens that could be measured (27– 398; table 4, electronic supplementary material, S3). Those differences that can be tested, from A. afarensis, A. africanus and P. robustus, are statistically significant. The anterior zygomatic root positions of early hominins, associated with PC1 and PC2, are summarized in table 5. The position in KNM-WT 40000 at the level of the P3/P4 interalveolar septum is commonly found in Paranthropus as well. On the other hand, it falls outside the range of variation of Australopithecus, with the

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

The maxilla of KNM-WT 40000 exception of the left side of the subadult specimen Sts 52. Importantly, in A. afarensis, the position is always more posterior, in one instance at the distal half of P4, and more commonly at the P4/M1 septum or M1. Hence, these univariate observations do fully confirm the characterization of K. platyops as subnasally orthognathic combined with anteriorly positioned zygomatics. The A. afarensis specimen most similar in geological age to KNM-WT 40000 is the Garusi 1 maxilla (Laetoli approx. 3.6 Ma). It is too fragmentary to be included in the PCA, or even to allow the quantification of subnasal clivus orientation or zygomatic process position. However, it is possible to make some inferences about its morphology that are relevant here. There is no evidence of the zygomatic root in the premolar area, and the anterior position must thus have been at P4/M1 or more posteriorly. Subnasally, Garusi 1 is very prognathic, has rounded nasal margins around the canine alveoli and lacks a clear nasal sill. In the latter characters, it differs from the A. afarensis Hadar sample and is more similar to A. anamensis (Kimbel et al. 2006; Kimbel 2007), and in all these aspects, Garusi 1 contrasts strongly with KNM-WT 40000. KNM-WT 40000 is poorly preserved, and Leakey et al. (2001) reported on the specimen by extracting meaningful information from selected areas after carefully mapping the post-mortem distortion. Bone expansion associated with clay-filled cracks is frequently encountered among fossils found in the Turkana Basin and has been routinely recognized as a phenomenon affecting a specimen’s morphology (e.g. the descriptions in Wood 1991). Naming it expanding matrix distortion, White (2003) states to have ‘formalized’ this taphonomic process, defining five stages. He assigned KNM-WT 40000 to stage 4, but as no definition of these stages has been published, it is not possible to evaluate this classification. It is worth pointing out that some areas of the cranium, such as parts of the left temporal bone, show very little distortion, whereas others, such as the cranial vault, are highly affected. Thus, characterizing the specimen by a single stage has little value. The analyses presented here show that the distortion has had little impact on the characters of maxillary shape relevant to the diagnosis of K. platyops. The preservation of the tooth roots and the integrity of the dental arcade indicate that distinct directional shape changes, such as skewing or compression, did not occur in the lower part of the left maxilla. Expansion cracks did cause a size increase of about 18 per cent, but this occurred mostly at a similar rate across the area, thus having little effect on shape. In all, there is no indication that the position of the zygomatic root or the subnasal clivus shape were modified substantially, particularly in a way that would mimic normal morphological differences between species. The only striking contrast in expansion rate was found between the area above (6%) and over the left canine jugum (20%). This difference is consistent with the CT-based observation that internal expansion is strongest in the alveolar space around the roots, a phenomenon that is understandable as it becomes readily filled with clay, unlike trabecular bone not open to the outside. Moreover, positioned at the Phil. Trans. R. Soc. B (2010)

F. Spoor et al.

3387

corner of the dental arcade, the canine alveolus has more thin overlying bone than other teeth, making the jugum particularly vulnerable to cracking. Apart from the zygomatic process position, subnasal clivus morphology and a small upper molar size Leakey et al. (2001) also lists similarly sized I1 and I2 roots and upper premolars that are threerooted as features characterizing the maxilla of K. platyops. These have not been considered here, but warrant further study. The unusual incisor root proportions (figure 2b) and their spatial relationship to the transversely flat, orthognathic subnasal area is of particular interest, and using high-resolution CT this can now be examined in more detail. The partial maxilla KNM-WT 38350 shares with KNM-WT 40000 the anterior zygomatic root position, three-rooted premolars and a small molar size and was therefore designated as the paratype of K. platyops (Leakey et al. 2001). However, it is too fragmentary a specimen to enable a full comparison with the unique facial morphology of KNM-WT 40000. The partial mandible KT12/H1, the holotype of the broadly contemporary species A. bahrelghazali, is characterized by a sagittally and transversely flat anterior corpus, said to reflect a more orthognathic face (Brunet et al. 1996). If correct, this would increase the likelihood that KNM-WT 40000 and KT12/H1 are conspecific. However, the association between subnasal and symphyseal shapes is not well understood (Spoor et al. 2005), and how K. platyops relates to A. bahrelghazali remains unclear. Thus, although there is good evidence, presented here and elsewhere (Leakey et al. 2001; Guy et al. 2008), of hominin species diversity in the Middle Pliocene of Africa, additional fossils will be required to reveal the full nature and interrelationships of the lineages present at that time. We thank Alan Walker and Chris Stringer for inviting us to contribute this work and the National Museums of Kenya, the National Museum of Ethiopia, the Transvaal Museum (South Africa), Department of Anatomy, Witwatersrand University (South Africa), the Institute of Human Origins (USA) and the museums listed in §2 for access to specimens in their care. We are grateful to Berhane Asfaw, Michel Brunet, Ron Clarke, Nick Conard, Chris Dean, Heidi Fouri, Philipp Gunz, John Harrison, Jean Jacques Hublin, Louise Humphrey, Paula Jenkins, Don Johanson, Andre Keyser, Bill Kimbel, Rob Kruszynski, Kornelius Kupczik, the late Charlie Lockwood, Emma Mbua, Jacopo Moggi-Cecchi, Sam Muteti, Paul O’Higgins, Matt Skinner, Gen Suwa, Heiko Temming, Brian Villmoare, Tim White and Andreas Winzer for help with various aspects of this study. Financial support was provided by the Leakey Foundation, the National Geographic Society and the Max Planck Society.

REFERENCES Asfaw, B., White, T., Lovejoy, O., Latimer, B., Simpson, S. & Suwa, G. 1999 Australopithecus garhi: a new species of early hominid from Ethiopia. Science 284, 629–635. (doi:10. 1126/science.284.5414.629) Boaz, N. T. 1988 Status of Australopithecus afarensis. Yrbk. Phys. Anthropol. 31, 85–113. (doi:10.1002/ajpa. 1330310506)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3388

F. Spoor et al.

The maxilla of KNM-WT 40000

Brown, B., Brown, F. & Walker, A. 2001 A. New hominids from the Lake Turkana Basin, Kenya. J. Hum. Evol. 41, 29–44. (doi:10.1006/jhev.2001.0476) Brunet, M., Beauvillain, A., Coppens, Y., Heintz, E., Moutaye, A. H. E. & Pilbeam, D. 1995 The first australopithecine 2 500 kilometres west of the Rift Valley (Chad). Nature 378, 273–274. (doi:10.1038/ 378273a0) Brunet, M., Beauvillain, A., Coppens, Y., Heintz, E., Moutaye, A. H. E. & Pilbeam, D. 1996 Australopithecus bahrelghazali, une nouvelle espe`ce d’hominide´ ancien de la re´gion de Koro Toro (Tchad). C. R. Acad. Sci. Paris 322, 907 –913. Cobb, S. 2008 The facial skeleton of the chimpanzee – human last common ancestor. J. Anat. 212, 469 –485. (doi:10.1111/j.1469-7580.2008.00866.x) Guy, F., Mackaye, H. T., Likius, A., Vignaud, P., Schmittbuhl, M. & Brunet, M. 2008 Symphyseal shape variation in extant and fossil hominoids, and the symphysis of Australopithecus bahrelghazali. J. Hum. Evol. 55, 37–47. (doi:10.1016/j.jhevol.2007.12.003) Hammer, Ø., Harper, D. A. T. & Ryan, P. D. 2001 PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9. Kimbel, W. K. 2007 The species and diversity of australopiths. In Handbook of Paleoanthropology, vol. III (eds W. Henke, T. Hardt & I. Tattersall), pp. 1539– 1573. Berlin, Germany: Springer. Kimbel, W. H. & Delezene, L. K. 2009 ‘Lucy’ redux: a review of research on Australopithecus afarensis. Yrbk. Phys. Anthropol. 52, 2–48. (doi:10.1002/ajpa.21183) Kimbel, W. H., Rak, Y. & Johanson, D. C. 2004 The skull of Australopithecus afarensis. New York, NY: Oxford University Press. Kimbel, W. H., Lockwood, C. A., Ward, C. V., Leakey, M. G., Rak, Y. & Johanson, D. C. 2006 Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the early hominin fossil record. J. Hum. Evol. 51, 134 –152. (doi:10.1016/j.jhevol.2006.02.003) Leakey, R. E. F. & Walker, A. 1988 New Australopithecus boisei specimens from East and West Lake Turkana, Kenya. Am. J. Phys. Anthropol. 76, 1 –24. (doi:10.1002/ ajpa.1330760102) Leakey, M. G., Spoor, F., Brown, F. H., Gathogo, P. N., Kiarie, C., Leakey, L. N. & McDougall, I. 2001 New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature 410, 433– 440. (doi:10. 1038/35068500) Lockwood, C. A. & Tobias, P. V. 1999 A large male hominin cranium from Sterkfontein, South Africa, and the status of Australopithecus africanus. J. Hum. Evol. 36, 637 –685. (doi:10.1006/jhev.1999.0299) Lockwood, C. A. & Tobias, P. V. 2002 Morphology and affinities of new hominin cranial remains from Member 4 of the Sterkfontein Formation, Gauteng Province, South

Phil. Trans. R. Soc. B (2010)

Africa. J. Hum. Evol. 42, 389–450. (doi:10.1006/jhev. 2001.0532) Lockwood, C. A., Richmond, B. G., Jungers, W. L. & Kimbel, W. H. 1996 Randomization procedures and sexual dimorphism in Australopithecus afarensis. J. Hum. Evol. 31, 537–548. (doi:10.1006/jhev.1996.0078) Lockwood, C. A., Kimbel, W. H. & Johanson, D. C. 2000 Temporal trends and metric variation in the mandibles and dentition of Australopithecus afarensis. J. Hum. Evol. 39, 23–55. (doi:10.1006/jhev.2000.0401) Moggi-Cecchi, J., Grine, F. E. & Tobias, P. V. 2006 Early hominid dental remains from Members 4 and 5 of the Sterkfontein Formation (1966 –1996 excavations): catalogue, individual associations, morphological descriptions and initial metrical analysis. J. Hum. Evol. 50, 239–328. (doi:10.1016/j.jhevol.2005.08.012) Nevell, L. & Wood, B. 2008 Cranial base evolution within the hominin clade. J. Anat. 212, 455 –468. (doi:10. 1111/j.1469-7580.2008.00875.x) O’Higgins, P. & Jones, N. 1998 Facial growth in Cercocebus torquatus: an application of three dimensional geometric morphometric techniques to the study of morphological variation. J. Anat. 193, 251–272. (doi:10.1046/j.14697580.1998.19320251.x) Rice, W. R. 1989 Analyzing tables of statistical tests. Evolution 43, 223– 225. (doi:10.2307/2409177) Spoor, F., Leakey, M. G. & Leakey, L. N. 2005 Correlation of cranial and mandibular prognathism in extant and fossil hominids. Trans. R. Soc. S. Afr. 60, 85–89. Strait, D. S. & Grine, F. E. 2004 Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J. Hum. Evol. 47, 399–452. (doi:10.1016/j.jhevol.2004.08.008) Tobias, P. V. 1967 The cranium and maxillary dentition of Australopithecus (Zinjanthropus) boisei. Olduvai Gorge, vol. 2. Cambridge, UK: Cambridge University Press. Ward, C. V., Leakey, M. G. & Walker, A. 2001 Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J. Hum. Evol. 41, 255– 368. (doi:10.1006/jhev. 2001.0507) White, T. D. 1977 New fossil hominids from Laetolil, Tanzania. Am. J. Phys. Anthropol. 46, 197–230. (doi:10. 1002/ajpa.1330460203) White, T. D. 2003 Early hominids—diversity or distortion? Science 299, 1994–1997. (doi:10.1126/science.1078294) White, T. D., Suwa, G., Simpson, S. & Asfaw, B. 2000 Jaws and teeth of Australopithecus afarensis from Maka, Middle Awash, Ethiopia. Am. J. Phys. Anthropol. 111, 45–68. (doi:10.1002/(SICI)1096-8644(200001)111: 1,45::AID-AJPA4.3.0.CO;2-I) Wood, B. 1991 Koobi Fora research project. Vol. 4: hominid cranial remains. Oxford, UK: Clarendon Press. Wood, B. & Lonergan, N. 2008 The hominin fossil record: taxa, grades and clades. J. Anat. 212, 354–376. (doi:10. 1111/j.1469-7580.2008.00871.x)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3389–3396 doi:10.1098/rstb.2010.0059

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene Julia A. Lee-Thorp1,*, Matt Sponheimer2, Benjamin H. Passey3, Darryl J. de Ruiter4 and Thure E. Cerling5 1

Research Laboratory for Archaeology, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK Department of Anthropology, University of Colorado at Boulder, 233 UCB, Boulder, CO 80309, USA 3 Department of Earth and Planetary Sciences, Johns Hopkins University, Baltimore, MD 21218, USA 4 Department of Anthropology, Texas A&M University, College Station, TX 77843, USA 5 Department of Geology and Geophysics, University of Utah, Salt Lake City, UT 84112, USA

2

Accumulating isotopic evidence from fossil hominin tooth enamel has provided unexpected insights into early hominin dietary ecology. Among the South African australopiths, these data demonstrate significant contributions to the diet of carbon originally fixed by C4 photosynthesis, consisting of C4 tropical/savannah grasses and certain sedges, and/or animals eating C4 foods. Moreover, high-resolution analysis of tooth enamel reveals strong intra-tooth variability in many cases, suggesting seasonal-scale dietary shifts. This pattern is quite unlike that seen in any great apes, even ‘savannah’ chimpanzees. The overall proportions of C4 input persisted for well over a million years, even while environments shifted from relatively closed (ca 3 Ma) to open conditions after ca 1.8 Ma. Data from East Africa suggest a more extreme scenario, where results for Paranthropus boisei indicate a diet dominated (approx. 80%) by C4 plants, in spite of indications from their powerful ‘nutcracker’ morphology for diets of hard objects. We argue that such evidence for engagement with C4 food resources may mark a fundamental transition in the evolution of hominin lineages, and that the pattern had antecedents prior to the emergence of Australopithecus africanus. Since new isotopic evidence from Aramis suggests that it was not present in Ardipithecus ramidus at 4.4 Ma, we suggest that the origins lie in the period between 3 and 4 Myr ago. Keywords: carbon isotopes; enamel; C4 resources; australopiths

1. INTRODUCTION Diet is a fundamental feature of a species’ biology, strongly influencing basic body size and morphology, life-history strategies for survival of the young in particular, social organization and the manner of its adaptations to its environment. Consequently, the nature of ancestral diets remains one of the most active topics of research in human evolution. Many years after Dart first puzzled over how the newly discovered ‘man-like apes’ (in reference to the Taung child and its kind) had survived in Taung’s xeric, open, Kalahari environment, so alien to all the other forest-loving great apes (Dart 1925, 1926), we are still actively debating these issues today (e.g. White et al. 2009a). Dart could not have comprehended, at that time, the full scale of environmental shifts that occurred in Africa in the past several millions years, or indeed the depth of time encompassed. But he made some surprisingly prescient suggestions, including the likely expansion of the conventional frugivorous and

* Author for correspondence ([email protected]). One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

folivorous hominid diet to include roots, bulbs and animal foods such as insects, scorpions, lizards, bird’s eggs and the young of small antelope (Dart 1926). Effectively, it was a pre-statement of the ‘Dietary Breadth’ hypothesis. These debates have continued apace, but although our understanding of the nature of environments and preferred habitats has advanced substantially, the fossil record has grown and more sophisticated methods have been applied to study morphology and the biomechanics of food processing, our comprehension of the important dietary shifts that must have occurred during the early emergence of hominins in the Pliocene is still uncertain. Such challenges have encouraged the development of new methods for examining dietary ecology. In an earlier Royal Society meeting on human evolution almost 30 years ago, Alan Walker set out a series of what he considered to be the more promising emerging avenues in early hominin dietary research (Walker 1981). Among other candidates, Walker suggested the inspection of tooth microwear, and carbon isotope and trace element analysis of fossil bones (Walker 1981, p. 58). It was evident at the 2009 meeting that the first two methods have undergone considerable development and progress since that time, in opening new

3389

This journal is q 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3390

J. A. Lee-Thorp et al.

Isotopes and hominin diets

windows on hominin dietary ecology. Walker’s predictions followed closely on a flurry of pioneering studies in the late 1970s that began to explore the systematics of these three approaches. In the case of stable isotopes, studies demonstrated the direct relationship between carbon isotopes in the diet and in animal tissues (DeNiro & Epstein 1978a), others that these distinctions held for wild grazers and browsers (DeNiro & Epstein 1978b; Vogel 1978) and finally that it provided a new approach for addressing an archaeological question about the introduction of maize agriculture (van der Merwe & Vogel 1978). Other studies hinted that these methods might be extended to fossils at greater time depth if based on the mineral rather than the organic phase of bone (e.g. Ericson et al. 1981; Sullivan & Krueger 1981). At that stage, almost all chemical studies were based on bone collagen or bone mineral (a biological apatite), but the latter is an extremely unstable structure, which is vulnerable to diagenesis. It was not until the potential of the more crystalline, stable enamel phase was explored and demonstrated (Lee-Thorp & van der Merwe 1987) that the full potential of the method to older fossils could be realized. Following earlier work (Parker & Toots 1980; Elias et al. 1982), the potential of trace elements, especially strontium to calcium ratios (Sr/ Ca), as trophic indicators in fossil foodwebs was explored extensively (Sillen 1988, 1992), but these efforts have largely stalled. This may be a reflection of the former strong focus on fossil bone, with its attendant problems of diagenesis. A single, broader enamel-based study in the South African hominin sites was unable to replicate the trophic patterns seen earlier for Paranthropus robustus (Sponheimer & Lee-Thorp 2006); instead, it was suggested that Sr/Ca and Ba/Ca, in combination, may be more informative about plant resources. That suggestion awaits further exploration, and trace elemental analysis will not be discussed further here. Our main purposes in this paper are to review the evidence for the shift to incorporate C4 resources in early hominin diets, to present new data for temporal variability in C4 consumption in the earlier South African australopith, Australopithecus africanus, which is comparable to that of P. robustus (Sponheimer et al. 2006b), and to make some predictions about the origins and inferences of such an adaptation.

2. ISOTOPIC EVIDENCE FOR C4 IN HOMININ DIETS The primary distinction in application of stable carbon isotopes to hominin diets is the difference in 13C/12C (expressed as d13C)1 between C3 and C4 plants. In the African environments they typically occupied, where the growing (wet) season is warm, all carbon dietary sources from trees, bushes, shrubs and forbs are distinctly lower in d13C compared with those from tropical grasses and some sedges. The primary exception is in tropical forest ecosystems where C3 subcanopy (shaded) plants are even more depleted in 13 C (i.e. lower d13C), while vegetation in clearings Phil. Trans. R. Soc. B (2010)

and in the canopy (including fruits) is slightly less depleted (van der Merwe & Medina 1989; Cerling et al. 2004). Dietary d13C values are reflected in all tissues, including enamel, so that fossil enamel d13C values provide opportunities to test hypotheses about the dietary habits of extinct animals (e.g. Lee-Thorp et al. 1989; Cerling et al. 1997). Most published isotope hominin dietary research has so far focused on the South African hominins (Lee-Thorp et al. 1994; Sponheimer & Lee-Thorp 1999; Sponheimer et al. 2005, 2006b; Lee-Thorp & Sponheimer 2006), although this situation is beginning to change. Comparisons between the two South African australopiths were also a starting point for the development of occlusal enamel microwear comparisons (Grine 1981, 1986). This and subsequent studies using less subjective, more quantifiable methods (Scott et al. 2005) suggested that, in spite of significant overlap, P. robustus microwear showed subtly more complexity or pitting in occlusal enamel wear compared with Australopithecus africanus. Therefore, the inference is that the former included a higher proportion of harder food items that required more processing and caused more pitting and fewer directional scratches (Grine 1986). These results were thought to be consistent with the widely held view that Paranthropus was a specialist vegetarian (Grine 1986). The microwear distinctions are quite subtle and may also be influenced by differences in enamel prism orientation between the two taxa (Macho & Shimizu 2009). Nevertheless, the microwear findings provide a useful framework for hypothesis-testing using stable isotopes since the data essentially suggest diets that would be classed as C3 (i.e. hard fruits and nuts). The prediction would be that A. africanus and P. robustus should be indistinguishable in their d13C values from C3 feeders, such as browsers and frugivores. The results, however, flatly contradict this prediction. Analysis of more than 40 hominin specimens from the sites Makapansgat, Sterkfontein, Kromdraai and Swartkrans, spanning a period of about 3 – 1.5 Ma, demonstrate that d13C values of both australopiths are indistinguishable from each other, but distinct from that of coexisting C3 consumers (figure 1). Surprisingly, the proportions of C4 in enamel, on average, remain relatively constant in spite of the passage of time and marked shifts in environments, from relatively closed to far more open landscapes, by about 1.8 Ma (Vrba 1985; Reed 1997; Lee-Thorp et al. 2007). On average, both taxa obtained 25 – 35% of their carbon from C4 sources. These resources must have been obtained either directly from grasses or sedges, or indirectly from animals that ate these plants. Since few of the fine scratches characterizing consumption of grass are present in their microwear (Grine 1986; Scott et al. 2005), it was deduced that direct consumption of grass blades was less plausible (although not ruled out) (Lee-Thorp & Sponheimer 2006). C4 sedges, grass rhizomes and the proposed consumption of grass-eating termites (and other small animal foods) may be implicated (Sponheimer et al. 2005; Yeakel et al. 2007), but

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Isotopes and hominin diets Makapansgat M3

Sterkfontein M4

Swartkrans M1

–14

–12

–10

–8

–6

–4

–2

0

2

4

δ13C‰ Figure 1. Data for all the South African hominins are summarized as means d13C (black boxes) and standard deviations compared with means and standard deviations for the browsing and grazing fauna. The sites are given in sequence from oldest (top) to youngest (bottom). Makapansgat Member 3 is about 2.7–3 Ma, Sterkfontein Member 4 is usually considered to be about 2.2 –2.5 Ma and Swartkrans Member 1 is younger than 2 Ma. These ages based on biostratigraphy are imprecise, but sufficient for our purposes. More precise chronometric studies based on Pb/U isotopes have recently been completed (R. Pickering 2009, personal communication), but do not change the overall sequence. All the hominin data show significant C4 contributions compared with C3 feeders, in spite of large shifts, from closed to open, in the environments (Reed 1997). Adapted from Lee-Thorp & Sponheimer (2006).

when examined individually, none of these resources offers a completely satisfactory solution. For instance, it has been shown that in this part of southern Africa the proportion of sedges following the C4 pathway is modest (Stock et al. 2004), and likewise few termite species seem to be C4 specialists (Sponheimer et al. 2005). The most plausible explanation is that they utilized C4 resources quite broadly, including both C4 plant and animal resources. Although the results say little about the rest of the diet (i.e. the major C3 portion), they hint that neither of these australopiths were plant specialists. These results were also unexpected because extant great apes consume minimal or no C4 resources even when they live in relatively open habitats. Several studies have shown that even ‘savannah’ chimpanzees, who live in the more open parts of the Pan range, consume few, if any, C4 resources (Schoeninger et al. 1999; Sponheimer et al. 2006a). Most forest-dwelling chimpanzees and gorillas reveal distinct low d13C values, indicative of the use of resources located in shaded understorey vegetation (Carter 2001; Cerling et al. 2004; Sponheimer et al. 2009; J. A. Lee-Thorp, Y. Warren & G. A. Macho 2009, unpublished data). It is this engagement with C4 resources, which were becoming increasingly available in the Plio-Pleistocene, that indicates a fundamental niche difference between the australopiths and extant apes. Phil. Trans. R. Soc. B (2010)

J. A. Lee-Thorp et al.

3391

3. VARIABILITY BETWEEN AND WITHIN INDIVIDUALS The foregoing discussion relies on broad averages, and we now turn to examine patterns in individuals. Where sufficient australopith d13C values exist within any one site, or members within that site, the data are quite variable, which suggests a degree of dietary opportunism and flexibility. This observation leads to the question of whether hominins shifted their diets on annual or even seasonal time scales, and whether the C4 contributions observed in bulk tooth enamel measurements mask short-term dietary variability. Tooth enamel is an incremental tissue that can be sampled to investigate temporal changes in both climate and diet using stable isotope analysis. Developments in laser ablation techniques now permit high-resolution sequential sampling of enamel crowns, with minimal visible damage (Passey & Cerling 2006). However, the sequential chronological resolution that can be attained, no matter how small the sample spot, is severely constrained by overprinting during maturation of the enamel. Enamel maturation occurs for many months, even years, after primary mineralization during prism formation (Suga 1982; Balasse 2002). Recovery of primary dietary signals has been successfully accomplished using a forward and inverse model only in continuously growing teeth and where the growth and enamel maturation parameters are well characterized (Passey et al. 2005). The patterns of enamel maturation in modern human tooth crowns are poorly understood, and those of early hominins even less so. However, it is evident that the nature of crown formation and enamel maturation inevitably produces a mixture of isotope signals, from both the initial primary mineralization and the maturation periods, so that there will be dampening or overprinting of the original signals. Nevertheless, three statements can be made with certainty: (i) the isotope profile from crown to root preserves an ordered time series extending from earlier (crown) to later (root) in time, (ii) the mimimum time duration of any single spot-sample within a tooth is equivalent to the ‘maturation time’, or time required for enamel to cure into its fully mineralized form (probably months in primates), and (iii) the total time duration of an isotopic profile across a tooth is the sum of the crown enamel deposition time (for example, as recorded by perikymata) and the maturation time of the last enamel increment deposited. Notwithstanding the constraints imposed by maturation patterns and by lower analytical precision, laser ablation has been applied to sample the external surface along the growth trajectory of four P. robustus tooth crowns (Sponheimer et al. 2006b) (figure 2b). The results showed that d13C values, and the pattern or temporal change, differed between individuals and, most startling, showed differences of up to 5‰ within a given P. robustus tooth. Given that the signal is attenuated or even scrambled as described above, these data still suggest a very large shift from a diet dominated by C3 to a diet dominated by C4 resources in certain individuals. Variability is observed at several time scales—intra- and inter-annual.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3392

J. A. Lee-Thorp et al.

(a)

Isotopes and hominin diets

0

(b)

–2

δ13C

–4 –6 –8 –10 –12 0

2

4

6 8 10 scan number

12

14

0

2

4

6

8 10 12 scan number

14

16

18

Figure 2. High-resolution laser ablation d13C sequences for (a) A. africanus and (b) P. robustus plotted against sample (scan) number. Sample increments were approximately 0.3 mm. The Paranthropus data are from Sponheimer et al. (2006b), where the data were plotted according to a time-sequence model based on perikymata counts. In this case, we avoided the application of a time sequence based on perikymata because the lengthy maturation time introduces not only a longer time period but also more uncertainty. (a) Open diamonds, STS 2518 max RM3; filled circles, STS 31 max RM3; filled triangles, STS 2253 mand RM1. (b) Open diamonds, SKW 6427 M; filled circles, SKW 5939 M; filled triangles, SK 24606 RM2 or 3; squares with crosses, SK 24606 RM3.

Four A. africanus molar crowns from Sterkfontein Member 4 were analysed using the same methods. The results for one tooth were omitted because of concerns about the interference of glue on the surface, observed as puffs of gas during ablation. Although the age of Member 4 is uncertain, biostratigraphic evidence indicates that it is considerably older than Swartkrans, and with several taxa—including A. africanus—in common with the older site of Makapansgat (Vrba 1985). As was the case for the P. robustus crowns, all teeth are lightly to moderately worn molars. The tooth assignments are shown in figure 2, although some in figure 2b were too fragmentary to allow determination other than that they are molars. The analytical methods for the A. africanus molars followed exactly those reported in Sponheimer et al. (2006b). Each tooth was cleaned mechanically and chemically (with acetone), and then thoroughly dried in a low-temperature oven. Samples were purged with helium inside the laser chamber for several minutes or hours as required for the rate of CO2 outgassing to fall below appropriate levels. Small amounts (10– 30 nmol) of CO2 were generated using a CO2 laser (10.6 mm) operating at 5 – 15 W and 8.5 ms pulse duration in a He atmosphere. The CO2 was cryogenically purified and ‘focused’ prior to introduction to a continuous-flow GC-IRMS (MAT 252). Systematic isotope fractionation and fractionation associated with laser ablation production of CO2 were monitored by analyses of injected aliquots of CO2 and by analysis of a suite of internal tooth enamel standards, both calibrated against NBS-19 gas (d13C ¼ 1.95‰). The laser-carbonate isotope fractionation (1*LASER-carb) for fossil herbivore samples from several South African hominin sites was – 1.3 + 1.5‰ (1s). Enamel was sampled at ca 0.3 mm intervals, encompassing about four perikymata for each laser ablation track (or scan) and the space between tracks. The length of each sampling trajectory varied Phil. Trans. R. Soc. B (2010)

depending on the available tooth surface, with between nine and 12 scans for the three reported molars. Based on a periodicity of 7 days per striae of Retzius (observed externally as perikymata) as calculated in Lacruz et al. (2006), the period of primary mineralization in the sampled area is over a year for two specimens (STS 2253 and STS 31) and just under a year for the third (STS 2518). However, as discussed above, the time represented in the isotope profile is much longer when enamel maturation is taken into account, and additionally the measured values represent an attenuated signal of higher amplitude. Variability in the proportions of C3 and C4 resources between and within individuals is on a similar scale for A. africanus compared with P. robustus (figure 2). At least one individual, STS 2518, indicates a more or less uniform C3 resource base, while another, STS 31, shows values varying by over 6‰ from a C3 to a predominantly C4 resource base. As emphasized above, it is difficult to ascertain the precise time scales over which this variation occurred. However, given that the enamel underlying the sampling arrays mineralized and matured over a period of over a year in each case, the differences between individuals cannot be ascribed to sampling of a single season in one case and multiple seasons in another. The results suggest that C4 resources formed an important but highly variable component of hominin diets, extending at least as far back as A. africanus at Sterkfontein. There is no reason to believe that the dietary ecology of A. africanus at the earlier site of Makapansgat Member 3 would be significantly different.

4. ORIGINS AND TIME DEPTH OF THE C4 PATTERN IN HOMININ DIETS Few analyses have been performed on eastern African material to allow us to definitively address the question of the origins of engagement with C4 resources. Clues from several sources may hint at an origin associated

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Isotopes and hominin diets with the emergence of the genus Australopithecus, but at present there are no data to address the period prior to emergence of A. africanus. Recently published d13C data for two Paranthropus boisei individuals from Olduvai revealed a strong dependence on C4 resources (van der Merwe et al. 2008). This was unexpected since the similarity of the ‘nutcracker’ dental and masticatory complex to that of South African P. robustus led to the expectation of a broadly similar dietary adaptation. Such high d13C values cannot be explained by consumption of C4 animal foods alone since they would require a highly unlikely dietary scenario that included almost exclusive consumption of the flesh of grazing (C4) animals. The results demand an alternative explanation. The authors suggested that P. boisei, or at least these two individuals, probably specialized in exploitation of C4 sedges, which are far more abundant in East African wetlands than they are in South Africa (van der Merwe et al. 2008). Additionally, a recent microwear study of P. boisei occlusal enamel showed little evidence for the pitting associated with hard object feeding (Ungar et al. 2008). These data seem inconsistent with their strongly developed masticatory complex, widely considered to be an adaptation for the consumption of hard foods. However, their diets were clearly abrasive when the degree of wear is considered (Tobias 1967). In combination, the high C4 resource consumption and the lack of a hardobject microwear pattern may require that we rethink the functional significance of the australopith masticatory package. Interestingly, microwear patterns for Australopithecus afarensis and Australopithecus anamensis also lack evidence for hard-object feeding (Ungar 2004; Grine et al. 2006), but rather resemble patterns seen in apes, especially gorillas. These results could also be considered as inconsistent with an evolutionary trajectory for larger molars and thicker enamel, which seem to suggest adaptation to increasingly more xeric habitats (Grine et al. 2006). However, other evidence points in a similar direction. It has been argued that the biomechanical masticatory complex of both A. anamensis (Macho et al. 2005) and A. afarensis (Rak et al. 2007) is more gorilla-like. Furthermore, modern humans and gorillas share life-history characteristics including non-seasonal breeding (Knott 2005), which in turn carries implications for a pattern of seasonal resource exploitation that ensures maximum infant survival. No isotope data exist for these older australopiths that would allow us to test whether C4 exploitation formed part of an increasingly seasonal foraging round as suggested by Macho et al. (2003). If they did engage with such resources, it will be important to understand the seasonal variation. While no isotopic data yet exist for A. anamensis and A. afarensis, recently published data for Aramis suggest that Ardipithecus ramidus, at 4.4 Ma, included few, if any, C4 resources in the diet (White et al. 2009b). Rather their isotopic composition most closely resembles that of savannah chimpanzees which avoid C4 resources, and contrasts with that observed in A. africanus at Makapansgat (figure 3). Although the authors lay stress on the woody nature of the Aramis Phil. Trans. R. Soc. B (2010)

J. A. Lee-Thorp et al.

3393

Aramis 4.4 Ma

hyaenids

Makapansgat ca 2.8–3 Ma

hyaenids –14

–12

–10

–8

–6

–4

–2

0

2

4

δ13C‰ Figure 3. A summary comparison of the hominin data for Aramis (above), and Makapansgat (below), plotted as means (black boxes) and standard deviations with mean values for C3 and C4 feeders shown for comparison. Data for carnivores (hyaenids) are also shown (white boxes; n ¼ 2 for Makapansgat), because they are effectively integrators for the values of all the fauna they consume. These data are shifted towards values more enriched in 13C in Aramis, suggesting more open, C4 elements in the environment compared with Makapansgat, where the faunal assemblage consists largely of C3 feeders. In spite of this difference, Ar. ramidus remains relatively depleted in 13C, quite unlike the patterns for A. africanus seen at Makapansgat. Data for Aramis are from White et al. (2009b), and for Makapansgat are from Sponheimer (1999).

environment, the d13C values for the fauna, taken together, show that a good deal of C4 grassy vegetation was present in the environs. Therefore, the important point is not that ‘Ar. ramidus was a denizen of woodland’ (White et al. 2009a), but that Ar. ramidus focused almost exclusively on C3 resources while avoiding nearby C4 resources, which were present. In contrast, the Makapansgat hominins clearly had moved to exploit C4 resources (figure 3), in spite of the relatively closed nature of that environment (Reed 1997). The Aramis data would certainly suggest that, if an engagement with C4 foods marked a fundamental shift in hominin evolution as we have argued, then such a shift occurred post Ar. ramidus, or elsewhere. Further evidence for a possible ecological shift between Aramis and Makapansgat may reside in a comparison of the combined d13C and d18O data (figure 4). The d18O composition of enamel provides a potential source of information about dietary ecology because, in addition to the influences of hydrology and isotopic composition of precipitation, an animal’s d18O value is affected by dietary ecology, drinking behaviour and thermophysiology (Bocherens et al. 1996; Kohn 1996; Kohn et al. 1996; Sponheimer & Lee-Thorp 2001). It has been shown that suids, some primates and in particular all faunivores have relatively low d18O compared with herbivores (Lee-Thorp & Sponheimer 2005). The reasons are not yet clear and almost certainly differ for these groups. In the case of suids, it may reflect reliance on underground storage

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3394

J. A. Lee-Thorp et al. (a)

Isotopes and hominin diets

8 Kuseracolobus Pliopapio Deinotherium Giraffidae Tragelaphini Neotragini Simatherium Eurygnathohippus Aepyceros Nyanzachoerus Kolpochoerus Hyaenidae Ardipithecus

6 4

δ18OVPDB

2 0 –2 –4 –6 –8 (b)

8 6 Cercopithecoides Parapapio Diceros Giraffids Tragelaphini Neotragini Simatherium Hipparion Aepyceros Suidae Hyaenidae Australopithecus

4

δ18OVPDB

2 0 –2 –4 –6 –8 –16

–14

–12

–10

–8

–6

–4

–2

0

2

4

δ13C‰ Figure 4. Bivariate d13C and d18O comparisons of similar taxa in (a) Aramis and (b) Makapansgat shown as means and standard deviations. Several significant differences are observed. On average, d18O values for Makapansgat fauna are about 2‰ lower than at Aramis, which is consistent with their relative geographical positions and associated values for hydrology. However, the Aramis data are more variable, with some exceptional and unusually low values for Deinotherium in particular. Australopithecus africanus data are relatively enriched in 13C and depleted in 18O, and occupy the same isotopic ‘space’ as the hyaenids, quite unlike Ar. ramidus. The other primate species are also more enriched in 13C, unlike Aramis, but the impala (Aepyceros) has higher d13C values at Aramis. Although impalas are generally considered to be mixed feeders, a recent study showed high d13C and almost exclusive grazing habits for Aepyceros in the nutritious grasslands of Rwanda (Copeland et al. 2009). The data for Nyanzochoerus at Aramis are remarkably similar to those for the Suidae at Makapansgat, suggesting a similar ecological niche. Data for Aramis are from White et al. (2009b) and for Makapansgat from Sponheimer (1999).

organs, and for faunivores, a high proportion of dietary lipids and proteins, or a very heavy reliance on drinking water. Australopith d18O data from Makapansgat overlap with those of carnivores in the same strata (figure 4). Similarly low d18O values—compared with other taxa in the Aramis faunal assemblage—are not observed for Ar. ramidus. Whatever the underlying contributors to the lower d18O values for hominins at Makapansgat (and we do not imply that they are necessarily the same), these observations call for further study and explanation.

5. CONCLUSIONS Carbon isotope data have demonstrated that australopiths in South Africa increased their dietary breadth by Phil. Trans. R. Soc. B (2010)

consuming C4 resources, while in East African P. boisei, this involvement might rather be regarded as a specialization. The exact nature of these C4 resources remains unclear, and cannot be deduced from the d13C values alone, but they most plausibly included various C4 resources, in varying proportions. Among the South African australopiths at least, consumption of C4 resources varied strongly between individuals and within individuals, in both A. africanus and P. robustus. The australopith pattern is quite unlike that seen in modern chimpanzees, and indeed in early Pliocene Ar. ramidus, and we argue that it represented a fundamental shift in dietary ecology that increased dietary breadth. Additionally, the exact foods that contributed to the observed C4 signals in australopith enamel are not clear. We cannot yet

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Isotopes and hominin diets pinpoint when the shift occurred because no published data yet exist for A. anamensis and A. afarensis, but certainly further research should target the period between 4 and 3 Ma. We thank Alan Walker and Chris Stringer for organizing the Royal Society Symposium on the ‘First four million years of human evolution’, the Royal Society for sponsoring the meeting, Debbie Guatelli-Steinberg for her work on the perikymata and many colleagues for their assistance and helpful discussions over the course of many years spent exploring the fascinating discipline of isotope ecology.

ENDNOTE 1

By convention, 13C/12C ratios are expressed in the delta (d) notation relative to the PDB standard, as follows: d13C (‰) ¼ (Rsample/Rstandard 2 1)1000, where R ¼ 13C/12C, and similarly, 18 O/16O ratios are expressed as d18O relative to PDB or SMOW (we use PDB in this paper).

REFERENCES Balasse, M. 2002 Reconstructing dietary and environmental history from enamel isotopic analysis: time resolution of intra-tooth sequential sampling. Int. J. Osteoarch. 12, 155 –165. (doi:10.1002/oa.601) Bocherens, H., Koch, P. L., Mariotti, A., Geraads, D. & Jaeger, J. 1996 Isotopic biogeochemistry (13C, 18O) of mammalian enamel from African Pleistocene hominid sites. PALAIOS 11, 306 –318. (doi:10.2307/3515241) Carter, M. L. 2001 Sensitivity of stable isotopes (13C, 15N, and 18O) in bone to dietary specialization and niche separation among sympatric primates in Kibale National Park, Uganda. PhD dissertation, University of Chicago. Cerling, T. E., Harris, J. M., MacFadden, B. J., Leakey, M. G., Quade, J., Eisenman, V. & Ehleringer, J. R. 1997 Global vegetation change through the Miocene/ Pliocene boundary. Nature 389, 153–158. (doi:10.1038/ 38229) Cerling, T. E., Hart, J. A. & Hart, T. B. 2004 Stable isotope ecology in the Ituri Forest. Oecologia 138, 5–12. (doi:10. 1007/s00442-003-1375-4) Copeland, S. R., Sponheimer, M., Spinage, C. A., Lee-Thorp, J. A., Codron, D., Codron, J. & Reed, K. 2009 Stable isotope evidence for impala Aepyceros melampus diets at Akagera National Park, Rwanda. Afr. J. Ecol. 47, 490– 501. (doi:10.1111/j.1365-2028.2008.00969.x) Dart, R. A. 1925 Australopithecus africanus: the man-ape of South Africa. Nature 115, 195 –199. (doi:10.1038/ 115195a0) Dart, R. A. 1926 Taungs and its significance. Nat. Hist. 26, 315 –327. DeNiro, M. J. & Epstein, S. 1978a Influences of diet on the carbon isotope distribution in animals. Geochim. Cosmochim. Acta 42, 495– 506. (doi:10.1016/00167037(78)90199-0) DeNiro, M. J. & Epstein, S. 1978b Carbon isotopic evidence for different feeding habits in two hyrax species occupying the same habitat. Science 201, 906 –908. (doi:10.1126/ science.201.4359.906) Elias, R. W., Hirao, Y. & Patterson, C. C. 1982 The circumvention of the natural biopurification of calcium along nutrient pathways by atmospheric inputs of industrial lead. Geochim. Cosmochim. Acta 46, 2561–2580. (doi:10.1016/0016-7037(82)90378-7) Ericson, J. E., Sullivan, C. H. & Boaz, N. T. 1981 Diets of Pliocene mammals from Omo deduced from carbon isotopic ratios in tooth apatite. Palaeogeogr. Phil. Trans. R. Soc. B (2010)

J. A. Lee-Thorp et al.

3395

Palaeoclimatol. Palaeoecol. 36, 69–73. (doi:10.1016/ 0031-0182(81)90049-3) Grine, F. E. 1981 Trophic differences between gracile and robust australopithecines. South Afr. J. Sci. 77, 203 –230. Grine, F. E. 1986 Dental evidence for dietary differences in Australopithecus and Paranthropus. J. Hum. Evol. 15, 783–822. (doi:10.1016/S0047-2484(86)80010-0) Grine, F. E., Ungar, P. S., Teaford, M. F. & El-Zaatari, S. 2006 Molar microwear in Praeanthropus afarensis: evidence for dietary stasis through time and under diverse paleoecological conditions. J. Hum. Evol. 51, 297 –319. (doi:10.1016/j.jhevol.2006.04.004) Knott, C. D. 2005 Energetic responses to food availability in the great apes: implications for hominin evolution. In Seasonality in primates (eds D. K. Brockman & C. P. van Schaik), pp. 351 –378. Cambridge, UK: Cambridge University Press. Kohn, M. J. 1996 Predicting animal d18O: accounting for diet and physiological adaptation. Geochim. Cosmochim. Acta 60, 4811–4829. (doi:10.1016/S00167037(96)00240-2) Kohn, M. J., Schoeninger, M. J. & Valley, J. W. 1996 Herbivore tooth oxygen isotope composition: effects of diet and physiology Geochim. Cosmochim. Acta 60, 3889–3896. (doi:10.1016/0016-7037(96)00248-7) Lacruz, R. S., Rozzi, F. R. & Bromage, T. G. 2006 Variation in enamel development of South African fossil hominids. J. Hum. Evol. 51, 580 –590. (doi:10.1016/j.jhevol.2006. 05.007) Lee-Thorp, J. A. & Sponheimer, M. 2005 Opportunities and constraints for reconstructing palaeoenvironments from stable light isotope ratios in fossils. Geol. Q. 49, 195 –204. Lee-Thorp, J. A. & Sponheimer, M. 2006 Biogeochemical approaches to investigating hominin diets. Yrbk Phys. Anthropol. 49, 131– 148. Lee-Thorp, J. A. & van der Merwe, N. J. 1987 Carbon isotope analysis of fossil bone apatite. South Afr. J. Sci. 83, 712 –715. Lee-Thorp, J. A., van der Merwe, N. J. & Brain, C. K. 1989 Isotopic evidence for dietary differences between two extinct baboon species from Swartkrans. J. Hum. Evol. 18, 183 –190. Lee-Thorp, J. A., van der Merwe, N. J. & Brain, C. K. 1994 Diet of Australopithecus robustus at Swartkrans deduced from stable carbon isotope ratios. J. Hum. Evol. 27, 361–372. (doi:10.1006/jhev.1994.1050) Lee-Thorp, J. A., Sponheimer, M. & Luyt, J. C. 2007 Tracking changing environments using stable carbon isotopes in fossil tooth enamel: an example from the South African hominin sites. J. Hum. Evol. 53, 595–601. (doi:10.1016/j.jhevol.2006.11.020) Macho, G. A. & Shimizu, D. 2009 Dietary adaptations of South African australopiths: inference from enamel prism attitude. J. Hum. Evol. 57, 241–247. (doi:10. 1016/j.jhevol.2009.05.003) Macho, G. A., Leakey, M. G., Williamson, D. K. & Jiang, Y. 2003 Palaeoenvironmental reconstruction: evidence for seasonality at Allia Bay, Kenya, at 3.9 million years. Palaeogeogr. Palaeoclimatol. Palaeoecol. 199, 17–30. (doi:10.1016/S0031-0182(03)00483-8) Macho, G. A., Shimizu, D., Jiang, Y. & Spears, I. R. 2005 Australopithecus anamensis: a finite-element approach to studying the functional adaptations of extinct hominins. Anat. Rec. 283A, 310–318. (doi:10.1002/ar.a.20175) Parker, R. & Toots, H. 1980 Trace elements in bones as paleobiological indicators. In Fossils in the making (eds A. K. Behrensmeyer & A. Hill), pp. 197– 207. Chicago, IL: University of Chicago Press. Passey, B. H. & Cerling, T. E. 2006 In situ stable isotope analysis (d13C, d18O) of very small teeth using

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3396

J. A. Lee-Thorp et al.

Isotopes and hominin diets

laser ablation GC/IRMS. Chem. Geol. 235, 238 –249. (doi:10.1016/j.chemgeo.2006.07.002) Passey, B. H., Cerling, T. E., Schuster, G. T., Robinson, T. F., Roeder, B. L. & Krueger, S. K. 2005 Inverse methods for estimating primary input signals from timeaveraged isotope profiles. Geochim. Cosmochim. Acta 69, 4101–4116. (doi:10.1016/j.gca.2004.12.002) Rak, Y., Ginzburg, A. & Geffen, E. 2007 Gorilla-like anatomy on Australopithecus afarensis mandibles suggests Au. afarensis link to robust australopiths. Proc. Natl Acad. Sci. USA 104, 6568–6572. (doi:10.1073/pnas. 0606454104) Reed, K. 1997 Early hominid evolution and ecological change through the African Plio-Pleistocene. J. Hum. Evol 32, 289–322. (doi:10.1006/jhev.1996.0106) Schoeninger, M. J., Moore, J. & Sept, M. 1999 Subsistence strategies of two ‘savanna’ chimpanzee populations: the stable isotope evidence. Am. J. Primatol. 49, 297– 314. (doi:10.1002/(SICI)1098-2345(199912)49:4,297:: AID-AJP2.3.0.CO;2-N) Scott, R. S., Ungar, P. S., Bergstrom, T. S., Brown, C. A., Grine, F. E., Teaford, M. F. & Walker, A. 2005 Dental microwear texture analysis shows within-species dietary variability in fossil hominins. Nature 436, 693 –695. (doi:10.1038/nature03822) Sillen, A. 1988 Elemental and isotopic analysis of mammalian fauna from southern Africa and their implications for paleodietary research. Am. J. Phys. Anthropol. 76, 49–60. (doi:10.1002/ajpa.1330760106) Sillen, A. 1992 Strontium–calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. J. Hum. Evol. 23, 495 –516. (doi:10.1016/ 0047-2484(92)90049-F) Sponheimer, M. 1999 Isotopic ecology of the Makapansgat Limeworks fauna. PhD dissertation, Rutgers University. Sponheimer, M. & Lee-Thorp, J. A. 1999 Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283, 368 –370. (doi:10.1126/science.283.5400. 368) Sponheimer, M. & Lee-Thorp, J. A. 2001 The oxygen isotope composition of mammalian enamel carbonate from Morea Estate, South Africa. Oecologia 126, 153 –157. (doi:10.1007/s004420000498) Sponheimer, M. & Lee-Thorp, J. A. 2006 Enamel diagenesis at South African Australopith sites: implications for paleoecological reconstruction with trace elements. Geochim. Cosmochim. Acta 70, 1644–1654. (doi:10. 1016/j.gca.2005.12.022) Sponheimer, M., Lee-Thorp, J. A., de Ruiter, D., Codron, D., Codron, J., Baugh, A. T. & Thackeray, J. F. 2005 Hominins, sedges, and termites: new carbon isotope data from the Sterkfontein valley and Kruger National Park. J. Hum. Evol. 48, 301– 312. (doi:10.1016/j.jhevol. 2004.11.008) Sponheimer, M., Loudon, J. E., Codron, D., Howells, M. E., Pruetz, J. D., Codron, J., de Ruiter, D. & Lee-Thorp, J. A. 2006a Do ‘savanna’ chimpanzees consume C4 resources? J. Hum. Evol. 51, 128 –133. (doi:10.1016/j. jhevol.2006.02.002) Sponheimer, M., Passey, B. H., de Ruiter, D. J., GuatelliSteinberg, D., Cerling, T. E. & Lee-Thorp, J. A. 2006b

Phil. Trans. R. Soc. B (2010)

Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science 314, 980–982. (doi:10.1126/science.1133827) Sponheimer, M., Codron, D., Passey, B. H., De Ruiter, D. J., Cerling, T. E. & Lee-Thorp, J. A. 2009 Using carbon isotopes to track dietary change in modern, historical, and ancient primates. Am. J. Phys. Anthropol. 140, 661 –670. (doi:10.1002/ajpa.21111) Stock, W. D., Chuba, D. K. & Verboom, G. A. 2004 Distribution of South African C-3 and C-4 species of Cyperaceae in relation to climate and phylogeny. Aust. Ecol. 29, 313–319. (doi:10.1111/j.1442-9993.2004.01368.x) Suga, S. 1982 Progressive mineralization pattern of developing enamel during the maturation stage. J. Dent. Res. 61, 1532–1542. Sullivan, C. H. & Krueger, H. W. 1981 Carbon isotope analysis of separate chemical phases in modern and fossil bone. Nature 292, 333–335. (doi:10.1038/292333a0) Tobias, P. V. 1967 The cranium and maxillary dentition of Australopithecus (Zinjanthropus) boisei. Olduvai Gorge, vol. 2. Cambridge, UK: Cambridge University Press. Ungar, P. S. 2004 Dental topography and diets of Australopithecus afarensis and early Homo. J. Hum. Evol. 46, 605–622. (doi:10.1016/j.jhevol.2004.03.004) Ungar, P. S., Grine, F. E. & Teaford, M. F. 2008 Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS ONE 3, e2044. (doi:10.1371/journal.pone.0002044) van der Merwe, N. J. & Medina, E. 1989 Photosynthesis and 13C/12C ratios in Amazonian rain forests. Geochim. Cosmochim. Acta 53, 1091–1094. van der Merwe, N. J. & Vogel, J. C. 1978 Content of human collagen as a measure of prehistoric diet in Woodland North America. Nature 276, 815 –816. (doi:10.1038/ 276815a0) van der Merwe, N. J., Masao, F. T. & Bamford, R. J. 2008 Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. S. Afr. J. Sci. 104, 153–155. Vogel, J. C. 1978 Isotopic assessment of the dietary habits of ungulates. S. Afr. J. Sci. 74, 298–301. Vrba, E. S. 1985 Early hominids in southern Africa: updated observations on chronological and ecological background. In Hominid evolution: past, present and future (ed. P. V. Tobias), pp. 195–200. New York, NY: Alan R. Liss. Walker, A. 1981 Dietary hypotheses and human evolution. Phil. Trans. R. Soc. Lond. B 292, 57–64. (doi:10.1098/ rstb.1981.0013) White, T. D., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, C. O., Suwa, G. & WoldeGabriel, G. 2009a Ardipithecus ramidus and the paleobiology of early hominids. Science 326, 64. (doi:10.1126/science.1175802) White, T. D. et al. 2009b Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 87–93. See www.sciencemag.org/cgi/content/full/326/ 5949/67/DC1. Yeakel, J. D., Bennett, N. C., Koch, P. L. & Dominy, N. J. 2007 The isotopic ecology of African mole rats informs hypotheses on the evolution of human diet. Proc. R. Soc. B 274, 1723–1730. (doi:10.1098/rspb.2007.0330)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3397–3410 doi:10.1098/rstb.2010.0052

Review

Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past M. Christopher Dean* Department of Cell and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK A chronology of dental development in Pan troglodytes is arguably the best available model with which to compare and contrast reconstructed dental chronologies of the earliest fossil hominins. Establishing a time scale for growth is a requirement for being able to make further comparative observations about timing and rate during both dento-skeletal growth and brain growth. The absolute timing of anterior tooth crown and root formation appears not to reflect the period of somatic growth. In contrast, the molar dentition best reflects changes to the total growth period. Earlier initiation of molar mineralization, shorter crown formation times, less root length formed at gingival emergence into functional occlusion are cumulatively expressed as earlier ages at molar eruption. Things that are similar in modern humans and Pan, such as the total length of time taken to form individual teeth, raise expectations that these would also have been the same in fossil hominins. The best evidence there is from the youngest fossil hominin specimens suggests a close resemblance to the model for Pan but also hints that Gorilla may be a better developmental model for some. A mosaic of great ape-like features currently best describes the timing of early hominin dental development. Keywords: hominin evolution; dental development; incremental markings; tooth root growth; enamel; dentine

1. BACKGROUND The lives of all living organisms can be divided into stages. This allows comparisons to be made between them. There are many reasons for studying the stage or period of growth in primates in a comparative context, which include identifying those ontogenetic changes shared by all primates and those that are unique to modern humans (Schultz 1937). Relative comparisons of the stages of skeletal or dental growth have proved to be a useful way of defining similarities and differences between both living and fossil primates. When chronological age is known, then the length of the phases of growth as well as the rates of growth of individuals can be compared. Dental development is just one measure of biological maturity, but is arguably the most stable, and it occurs over an unusually long period of time from before birth to maturity. Besides enabling us to discover things about the evolutionary history of our own growth period, studies of comparative dental development provide us with an opportunity for investigating the biological processes that govern tooth formation from the initial mineralization of teeth to the completion of their roots (Swindler 1985).

*[email protected] One contribution of 14 to a Discussion Meeting Issue ‘The first four million years of human evolution’.

Smith (1989) has shown that certain key marker events during dental development actually correlate better with important variables that describe lifehistory variation than any of these life-history variables do with each other. Because of this, some tentative inferences can be made about the way fossil primates lived their lives compared with living primates that go beyond simple relative dento-skeletal comparisons. A powerful aspect of dental biology is that tooth tissues preserve an incremental record of their growth, which remains literally embodied within the microstructure of enamel and dentine. This offers an opportunity to reconstruct the period of maturation in fossil primates and compare them in real time with living primates. Even if it may never be possible to retrieve information about many life-history variables from the fossil record, it should be possible to reconstruct a time scale for growth in the past.

2. INCREMENTAL GROWTH OF ENAMEL AND DENTINE The cells that form enamel and dentine (ameloblasts and odontoblasts) secrete their matrix in a rhythmic manner (Bromage 1991; Smith 2006; Bromage et al. 2009). A circadian rhythm in cell function is expressed as a daily slowing of secretion during enamel and dentine formation and is still manifest in the enamel and dentine microstructure of fully formed teeth as a

3397

This journal is # 2010 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3398

M. C. Dean Review. Dental development in early hominins

(a)

(b)

Figure 1. Scanning electron micrograph showing perikymata on the upper lateral incisor of MLD 11 (Au. africanus) from Makapansgat, South Africa (a). Their spacing becomes closer towards the cervix. Two or three regions of enamel hypoplasia are evident indicating periods of slowed enamel growth during tooth formation. (b) Transmitted polarized light micrograph of enamel incremental markings seen in a longitudinal ground section of a probable second molar fragment (Ward et al. 2001) attributed to Au. anamensis (KNMER 30748) from Allia Bay, Kenya. Coarse oblique long period incremental markings (approx. 35 mm apart) run from bottom left to top right and emerge at the surface within perikymata troughs. Along prisms, that run left to right in this image, are short period daily increments marked by fine cross striations approximately 5 mm apart. In this specimen, there are seven daily increments between adjacent long period striae.

daily incremental marking (Boyde 1976, 1979, 1989, 1990a; Shinoda 1984). Thin sections of teeth prepared for histological analysis, or even polished or naturally fractured surfaces of fossil teeth that are suitable for examination with various kinds of microscopy (figure 1) can be used to reveal these markings in enamel and dentine (Boyde 1989, 1990b; Dean 2000, 2006; Lacruz et al. 2006, 2008). Counts of daily incremental markings in the teeth of individuals with known dates of birth and death match very closely with the number of days of life (Antoine et al. 2009). The daily increments of enamel secretion in great ape and fossil hominin teeth cumulate at a faster rate than they do in modern human tooth enamel (Dean et al. 2001). Enamel measuring 200 mm thick over the cusp of a great ape tooth, takes on average between 55 and 65 days to form, whereas in modern humans this takes 70 – 80 days (Dean et al. 2001; Dean 2009; Smith et al. 2006). Daily rates of dentine formation, however, are more similar in great apes and humans and take between 80 and 100 days to form 200 mm close to the root surface (Dean 2009, in press). Another, but longer period rhythm, that also slows dental hard tissue formation in a regular way is superimposed upon this daily rhythm (figure 1). In modern humans this coarser more prominent marking usually occurs every 7, 8, 9 or 10 days with a modal value of 8 days (Smith et al. 2006). Long-period incremental markings are aligned along the original mineralizing tissue front in both enamel and dentine. The slope of these incremental markings, with respect to the Phil. Trans. R. Soc. B (2010)

junction between enamel and dentine, provides a way of estimating past rates of differentiation of new secretory cells during tooth formation (Boyde 1963, 1964, 1990b; Shellis 1984; Dean 1985; Risnes 1986). The rate of increase in both tooth crown height and root height can be reconstructed by dividing increments of tooth crown length along the enamel dentine junction (EDJ), or cement dentine junction (CDJ) by the time intervals taken to form them (Boyde 1963; Risnes 1986; Dean 2006, 2009). In figure 2, consecutive 200 mm-thick increments of enamel and dentine have been used to plot increasing tooth height against time from the dentine horn to a point as close to completion of the root as possible (Dean 2009). The number of daily increments between longperiod markings appears always to be the same in each of the teeth of an individual but it varies between individuals. In large samples of individuals there are also outliers with a long-period rhythm of 6 or 11 or even perhaps 12 days. We now know that these longperiod markings (first described by Anders Retzius (1837) and, therefore, also referred to as Retzius lines) occur in the enamel of other primates including early fossil hominins (figure 1). Of 29 australopiths examined so far, 17 (59%) showed a mean periodicity of 7 days and of seven early Homo specimens examined so far, two had long-period lines 7 days apart, four were 8 days apart and one was 9 days apart (Lacruz et al. 2008). Fossil teeth, however, are precious and it is only rarely possible to employ partially destructive techniques to retrieve data about their growth. Nevertheless, long-period markings also create a furrow or trough on the external surface of permanent tooth enamel. These so-called perikymata (waves around the tooth) first defined by Preiswerk (1895) in ungulate enamel are well preserved on many early hominin teeth and they can be counted with scanning electron microscopy (figure 1) or even in obliquereflected light. They can be used to estimate enamel formation times in fossil teeth since counts of perikymata are equivalent to counts of long-period striae within the tooth but their periodicity may not be known unless the internal structure of the enamel can be visualized.

3. CONSTRUCTING A COMPARATIVE MODEL FOR EARLY HOMININ MATURATION Recent evidence about DNA sequence analysis and from molecular biology suggests that modern humans and chimpanzees are more closely related to each other than to any other living ape (Goodman et al. 1994; Ruvolo 1994; Bradley 2008). It is, therefore, not an unreasonable assumption that the last common ancestor of the Pan – Homo clade had a life history more like that of modern chimpanzees than modern humans (Robson & Wood 2008). It is nonetheless equally likely that among the species of early hominins there were many different life-history strategies that spanned what we know today about life history in modern orangutans, chimpanzees, bonobos and gorillas. One key question that we can then ask is whether there is any evidence among early hominins

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Dental development in early hominins

tooth height along EDJ (mm)

(a) 25 000

M. C. Dean

3399

(b)

20 000 15 000 10 000 5000

0

2

4

6 8 10 12 14 tooth formation time (years)

16

18

0

2

4

6 8 10 12 14 tooth formation time (years)

16

18

Figure 2. Plots of M1, M2 and M3 formation time (years) against increasing tooth height (mm) along the mesiobuccal (protoconid) EDJ (red open circles), continued along the CDJ (open blue circles) for (a) Pan troglodytes and (b) modern human molars. The mean length (+1 s.d.) of mesiobuccal root formed at gingival emergence in free-living Pan specimens given in Kelley et al. (2009), M1, 4.2 mm; M2, 5.2 mm; M3, 6.8 mm has been used to generate a likely range of root lengths (and thereby corresponding ages) where molars in Pan might have emerged into the mouth (yellow filled circles). Arrows denote the median ages of gingival emergence. The rates of crown and root growth, as well as the total tooth formation times in modern humans and Pan, are similar but earlier initiation times compress Pan molar development into approximately 12 years rather than approximately 18 years. Distance curves for a single Gorilla M1, a short M1 fragment of KNM-ER 30749 and a longer M2 fragment of KNM-ER 30748 (both attributed to Au. anamensis, Ward et al. 2001) are superimposed over the Pan M1 and M2 molars (filled black circles, crown; filled blue circles, root). Rates of root extension in Gorilla and Au. anamensis are faster than in Pan.

for a period of maturation that differs from that known today for modern chimpanzees. Another feasible question is whether there is evidence among the various species of early hominins for any differences between them in the timing of dental development that might point to the presence of different life-history strategies existing together during the first four million years of human evolution. If this were so it might point to interesting links with climate change or diet. To answer these questions requires a detailed knowledge of the chronology of dental development in modern great apes and an assessment of how early fossil hominins do or do not compare with this. Since this is realistically only presently possible for Pan troglodytes, it makes sense to try and construct a model that brings together everything that is known about the timing of dental development in P. troglodytes and use this to examine the timing of dental development in early hominins.

4. THE CHRONOLOGY OF DENTAL DEVELOPMENT IN PAN TROGLODYTES Early studies of dental development in great apes were made on single individuals or on samples of animals brought to zoos or acquired for comparative skeletal collections (Keith 1899; Schultz 1924, 1935, 1940; Zuckerman 1928; Krogman 1930; Bennejeant 1940; Clements & Zuckerman 1953). Few of the living animals studied were actually born in captivity and so their chronological age was rarely known. While some early studies identified differences in the sequence of dental eruption between great apes and humans and also noted earlier ages for the eruption of certain teeth, others found no differences in the timing of dental development between great apes and Phil. Trans. R. Soc. B (2010)

modern humans (Zuckerman 1928). In recent years many issues have been clarified through studies on samples of captive animals of known chronological age. Parallel histological studies of enamel and dentine growth in great apes have also helped to build a better picture of the chronology of dental development in a comparative context. What follows is a synthesis of those studies.1 (a) Permanent tooth eruption times in Pan In two classic longitudinal studies on chimpanzee dental emergence, Nissen & Riesen (1945, 1964) presented the first reliable data for ages of gingival emergence (eruption) in captive chimpanzees. They showed that the deciduous dentition was fully emerged into functional occlusion by approximately one year of age (Nissen & Riesen 1945) and that for eight males and seven females combined (Nissen & Riesen 1964), the mean ages of emergence for M1 were 3.3 years (range, 2.6 – 3.8); M2, 6.7 years (range, 5.6 – 7.8); and M3, 10.8 years (range, 9.0 – 13.6). All of these molar eruption ages are much earlier than those known for modern humans. Interestingly, however, the equivalent data for incisors and canines are indistinguishable from those known for modern humans. Mean gingival emergence ages for those teeth are, respectively, I1: 5.7 years (range, 4.5 – 7.0); I2: 6.4 years (range, 5.0 – 8.3); C: 9.0 years (range, 7.6 – 10.1). Kuykendall et al. (1992) in a study of 22 male and 36 female laboratory born and raised chimpanzees aged between 1 and 10 years observed median emergence times for permanent teeth that were rarely more than a month or two different from the data of Nissen & Riesen (1964). One exception was the permanent canine that in both the mandible and maxilla erupted a year earlier at approximately

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

(b) Environmental effects on dental development in great apes An important issue that is still not well understood is the effect on great ape dental development of being born and raised in captivity and perhaps more significantly, the effect of being nursed and raised by the mother in captivity or being hand-nursed and bottlefed by humans. Zihlman et al. (2004, 2007) have presented a range of data for free-living chimpanzees that demonstrate a slower rate of behavioural, somatic and dental development than for captive animals. They place M1 emergence at approximately 4 years, M2 between 6 and 8 years, canine emergence between 10 and 11 years and M3 emergence at approximately 12.5 years. Smith et al. (2006) have also illustrated a wild-born chimpanzee aged 4.4 years (fig. 6 in Smith et al. 2006), where M1 is still far from functional occlusion. Phillips-Conroy & Jolly (1988) and Kahumbu & Ely (1991) also recorded later eruption times in free-living than in captive baboons. Even if the degree of difference is both population- and sample size-sensitive, some degree of difference is certainly real. Kelley et al. (2009) used the extrinsic staining on newly emerged cusps of molar teeth to indicate gingival emergence in wild-collected great ape skulls. In figure 2, the mean lengths for mesiobuccal roots (+1 s.d.) measured at gingival emergence in that study are plotted individually onto each Pan molar root (M1, n ¼ 14; M2, n ¼ 10; M3, n ¼ 8). The age ranges generated for these root lengths have been used to simulate a likely range and median age of attainment for gingival emergence in the predominantly wild-collected Pan specimens represented in figure 3. The results are a close match with those of Zihlman et al. (2004) for M1 and to some extent for M2 with simulated median age of attainment of M1 at approximately 4.0 years, M2 at approximately 7.0 years and M3 at approximately 10 years. Interestingly, they also fall close to the 32.6, 59.4 and 86 per cent of the total time to complete dental development that Swindler (1985) calculated for modern human molar eruption times, assuming that this total time is approximately 12 years in P. troglodytes. However, with the exception of M1, these simulated median ages of attainment for molar gingival emergence still fall within the ranges reported for captive chimpanzees. Kelley & Schwartz (2009) have drawn attention to the wide range of ages likely for gingival emergence in free-living great apes but Smith et al. (2010) have suggested that ages for gingival emergence may be influenced more by free-living or captive rearing than crown or root formation are. Phil. Trans. R. Soc. B (2010)

M3 M3

M3

M3 M3

M2 M2 M2 M2 M2

8 years (range 6.5 – 8.7). Unfortunately, the age sample of Kuykendall et al. (1992) did not extend to individuals with emerging M3s, but the general consistency for dental emergence ages between these samples of laboratory-raised chimpanzees is remarkable. However, these data are not so closely reflected by those derived from a much smaller sample of free-living chimpanzees of known chronological age originally described by Zihlman et al. (2004) but subsequently revisited by Smith et al. (2009, 2010).

M1 M1 M1 M1 M1

M. C. Dean Review. Dental development in early hominins

100 80 percentile

3400

60 40 20 0 2

3

4

5

6

7

8

9

10

11

12

age at tooth eruption (years) Figure 3. Predicted median ages of attainment (50th percentile) for molar gingival emergence ages in Pan (M1, 4.1 years; M2, 6.9 years; M3, 10.1 years). These are derived from the times corresponding to root lengths formed at gingival emergence shown as yellow filled circles in figure 2. The interquartile age ranges (vertical lines) of attainment were simulated by using 1 s.d. of root formed at gingival emergence. The median values are represented by central vertical lines. A spread of initiation times over a lower age range, which in reality seems likely, would, reduce these estimates slightly.

What lies behind this difference is likely to be multifactorial but certainly to a large extent nutritional. Lippert (1977) showed that captive hand-reared infant apes double their birth weight by three months, whereas mother-nursed infants do not do so until six months. This difference persists until at least 21 months and probably continues as a trend into adulthood (Nissen & Riesen 1945; Fooden & Izor 1983). Nissen & Riesen (1945), Marzke et al. (1996) and Winkler et al. (1991) have all noted advanced deciduous tooth emergence ages between mother-nursed and formula-fed infant great apes. Marzke et al. (1996) specifically made the point that data from mother-nursed captive animals are likely to be more directly relevant to free-living conditions than data for hand-reared great apes. The available data for great ape dental development needs, therefore, to be considered carefully in this light if a model for dental development in fossil hominins is to be realistic. (c) Tooth initiation times, sequences and overlaps Swindler (1985), Anemone et al. (1991), Anemone & Watts (1992), Kuykendall (1996) and Reid et al. (1998) have all noted that the times for initial mineralization of the permanent incisors and canines in Pan are very similar to those described for humans (Kronfeld 1935) and that the sequence of mineralization is identical. Lower permanent incisors initiate at approximately 3 –4 m after birth and canines at 4– 5 m although both earlier and later times have been recorded (Kronfeld 1935; Anemone et al. 1991; Kuykendall 1996; Winkler 1996; Schwartz et al. 2006). Winkler (1995) demonstrated that direct observations of tooth germs can pick up earlier initiation

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Dental development in early hominins times than radiography as Hess et al. (1932) and Beynon et al. (1998) also observed. Reid et al. (1998) have nonetheless noted generally similar initiation times in Pan from histological studies for lower I1 (range, 1.8–5.6 m), lower I2 (range, 2.3–8.5 m) lower canines (range, 4.6–6.9 m) as well as for P3 and P4 initiation (range, 1.1–1.95 years) something also observed by Anemone et al. (1991) and Kuykendall (1996) to between 1.4 and 1.8 years in Pan. Understanding the differences in dental development that exist between great apes that take approximately 12 years to grow up and modern humans that take approximately 18 years to grow up is fundamental to our being able to interpret juvenile fossil hominin material. It is molar development that reflects these somatic growth differences most closely. While the sequence of molar initiation is also always identical in great apes and humans (M1, M2, M3), the timing of molar initiation has been much debated. Molar formation is drawn out in modern humans between birth and approximately 18 years. Initiation of M1 around birth is followed by M2 initiation at approximately 3 years and M3 initiation at approximately 8 years with each molar then taking about 10 years to form. Dean & Wood (1981) suggested that molar initiation times were compressed together in great apes (M1 close to birth, M2 at 2.5 years and M3 at 5 years) and that total molar formation times were shorter, with M3 root formation completing between 11 and 12 years. Certainly, studies of dissected M1 germs in great apes have usually, but not always, demonstrated three or four mineralizing cusps at birth (Oka & Kraus 1969; Tarrant & Swindler 1972; Moxham & Berkovitz 1974; Winkler 1996). Schwartz et al. (2006) have described an extreme case of M1 initiation in a captive hand-raised gorilla as early as 90 days before birth. However, Anemone et al. (1991) and Anemone (1995) in the first longitudinal radiographic studies of dental development in captive P. troglodytes, showed that for 16 individuals, the proposal of Dean & Wood (1981) for M2 and M3 initiation in Pan was incorrect. They demonstrated even earlier initiation times for M2 at 1.5 years and M3 at 3.5 – 4.0 years. Subsequently, Kuykendall (1996) in an extensive cross-sectional radiographic study imaged stages of tooth formation in 118 captive chimps and reported even younger median ages of molar initiation: M2, 1.3 years (range, 1.15– 1.48) and M3, 3.2 years (range, 3.0 – 4.6). Despite the supposed advantage of picking up initial mineralization of tooth germs earlier in histological studies, Reid et al. (1998) estimated M2 initiation in Pan at between 1.7 and 1.9 years and M3 initiation between 3.6 and 3.8 years. In figure 2, for consistency, and because for isolated teeth initiation times can never be known, histological estimates for molar initiation times have been used and fixed at the average age for molar tooth types estimated in Reid et al. (1998): M1, birth; M2, 1.75 years; M3, 3.69 years. The issue of early molar initiation in great apes has become confused with observations about the degree of overlap in crown formation periods between sequential molars. Overlap of crown formation periods Phil. Trans. R. Soc. B (2010)

M. C. Dean

3401

has as much to do with how long or short the crown formation period of the earlier forming molar is as it has to do with the early or late initiation of the subsequent forming molar. Smith et al. (2006) noted the potential effect earlier or later molar initiation might have on eruption timing and highlighted the need to document the degree of molar overlap in free-living versus captive animals and in hand-reared versus mother-nursed animals. Indeed in figure 2, a spread of molar initiation times towards earlier ages would reduce the simulated estimates for median emergence times in figure 3. Winkler et al. (1996) studied a much larger originally free-living sample of 89 orangutans and concluded that sequential molars in orangutans had usually begun to mineralize by the time a previous molar had reached crown completion but that variability was too high to consistently predict that crown initiation had always commenced prior to crown completion of a preceding molar. Smith et al. (2006) in a histological study of Pan molars from the same individuals again noted variability in the degree of molar overlap but that more often than not this was considerable. The effects of captive rearing, therefore, cannot yet be resolved.

(d) Total tooth and root formation times Kuykendall (1996) made the important observation that the overall duration of crown and root formation in chimpanzee permanent incisors and canines is comparable with that in modern humans. Some of the best summary data for mean age at entering a formation stage for modern humans (Liversidge 2009) places apex closure for mandibular I1 (8.04 years), I2 (8.69 years), canines (12.2 years) and M1 (9.38 years) at very close to the recorded ranges reported for Pan (Anemone et al. 1991; Anemone 1995; Kuykendall 1996). The median values and ranges of ages for root apex completion in Pan are: I1, 9.55 years (range, 7.99– 10.75); I2, 9.69 years (range 8.35 – 10.75); C, approximately 12 years. When initiation times are taken into account, total molar formation times in Pan appear to come close to those for modern human molars (approx. 10 years). Data for 30 observations of mean M1 apex closure (M1, 8.14 years, range 6.47 – 10.75 years) given in Kuykendall (1996) and data for M2 and M3 from Anemone et al. (1991) and Anemone (1995) also suggest overlap in total M2 and M3 formation times with modern humans (M2, 6.5 – 9.8 years; M3, 11 – 13 years). Kuykendall (1996), however, concluded that, unlike incisors and canines, total molar formation times in Pan were in fact slightly shorter than those known for modern humans but since no longitudinal studies exist with sufficient samples of older animals this remains speculative. Nevertheless, the wide range of ages reported for molar apex closure in great apes is noteworthy. Beynon et al. (1991) illustrated a gorilla with an open M1 apex at approximately 6 years with a little more root growth to come (see also the additional gorilla M1 in figure 2) and Schwartz et al. (2006) yet another gorilla at the same stage but aged only 3.2 years. These data suggest that total molar formation times in Gorilla may be shorter than

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3402

M. C. Dean Review. Dental development in early hominins n=2

n=2 5.5

5.8 5.5 5.1

5.2 4.8 4.2

4.6 4.0 3.4

3.5 2.8 2.3

2.9 2.5 1.0 1.5 2.2 2.9 3.7 4.4 5.1 5.8 6.5

1.0

1.8

2.1 1.8

1.4 1.0

1.5

0.7 0.7 0.8

1.4

1.1

1.8

1.4

2.4

1.8

3.0

2.3

3.6 4.2 4.9 5.5

1.0 1.2 1.5 1.9 2.4

2.9

2.9

3.4

3.4

4.1

4.0

4.6

4.4

5.0

4.7

7.0

6.1

5.4

7.3 male n = 10

6.5 female n = 8

n=7

n=6

Figure 4. Anterior crown formation times in Pan troglodytes. Crown heights are divided into deciles and an average chronological age of attainment for each decile of height has been calculated from estimates of enamel formation time made from counts of daily cross striations and long period striae in longitudinal ground sections of teeth. (Data from Reid et al. 1998, 2000; Schwartz & Dean 2001; Schwartz et al. 2001.)

those reported for Pan but sample size and these data for captive animals may be misleading.

(e) Crown formation times Perhaps, the most debated aspect of great ape dental development is the time taken to form enamel, or crown formation time. The reason for this is that it bears heavily on whether early fossil hominins can be judged ‘ape-like’ or ‘human-like’ with respect to this formation time. However, enamel formation time may be defined differently in radiographic studies and histological studies of tooth development (Beynon et al. 1998; Kuykendall 2001) and an added complication is that in histological studies, different enamel formation times are often estimated for each cusp of a molar tooth (Smith et al. 2006). For these reasons and others many comparisons of enamel formation times between modern humans and great apes have often been either unconvincing or incomparable (Kuykendall 2001). With the exception of lower canines (Schwartz & Dean 2001; Schwartz et al. 2001), the data for anterior crown formation times in great apes is very poor. Figure 4 summarizes what is known for a few Phil. Trans. R. Soc. B (2010)

specimens of Pan with data taken from Reid et al. (1998, 2000), Schwartz & Dean (2001) and Schwartz et al. (2001). However, the data for one or two specimens of Gorilla published by Beynon et al. (1991) and Schwartz et al. (2006) suggest crown formation times for incisors may sometimes be as short as 2.7 years suggesting that Pan may be atypical in this sense. Once again this raises the question of potentially advanced dental development in captive animals or perhaps of significant differences between Pan and Gorilla that are currently unappreciated and in addition, whether a Pan-like model for dental development is actually the most appropriate for early hominins. Knowing something about anterior crown formation times allows us to link periodic linear hypoplastic banding patterns on anterior teeth that are common in many Pan and Gorilla specimens collected from locations in West Africa (Gabon, Cameroon) with two rainy seasons each year (Skinner & Hopwood 2003). Besides being generally under the weather in colder wetter conditions, chimpanzees in particular are more susceptible to increased intestinal parasite loads (Lilly et al. 2002) since damp soil and sporadic forest floor flooding present prefect conditions for eggs, protozoa and

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Dental development in early hominins

crown and root extension rate (mm d–1)

40 35 30 25 20 15 10 5 0 –1

0

1

2

3

4

5

6

7

8

9

tooth formation time (years)

Figure 5. Extension rates for the same sample of Pan M1s shown in figure 2. Rates are high in the cusps of the crown but then quickly fall to values between 4 and 8 mm d21 (see also Dean 2009). These data for 14 teeth are each aligned (arrow) around the mean age (3.8 years) of peak height velocity (PHV) for this sample, which displaces the initiation and completion of tooth formation to earlier or later ages but highlights the root spurt more clearly. The mean chronological age and range of ages at which PHV occurs during early root formation (3.01– 4.65 years, s.d. 0.48) broadly mirrors those ages reported for gingival emergence in Pan M1s.

helminths to flourish. Seasonal fluctuations such as this increase the likelihood of individuals succumbing to any number of conditions that are known to underlie linear enamel hypoplasias (particularly prolonged bouts of diarrhoea or dysentery) and are a likely explanation for many wild-collected great ape permanent canines having, for example, 15 or so faint bands on canine crowns that took close to 7.5 years to form enamel. The data presented in figure 2 for molar crown (protoconid) formation times in Pan are for slightly bigger sample sizes than previous studies (but comparable to those of Smith et al. 2006, 2010) although they are not based on counts or error-prone periodicities of long period incremental markings but only on counts of daily increments close to the EDJ: M1, 2.3 years (range 1.78 – 2.66); M2, 2.38 years (range 1.72– 3.19); M3, 2.71 years (range 2.19 – 3.34). Mean values for modern human (protoconid) formation times (Reid & Dean 2005) are greater than these: M1 (3.1 years), M2 (3.2 years) and M3 (3.27 years) but there is overlap in the ranges (for example, see Reid & Dean 2005 and Mahoney 2008) such that an individual molar tooth could not always be attributed to Pan or Homo on the basis of molar crown formation time alone. (f) Rates of root formation and the timing of gingival emergence All hominoid teeth show a pattern of change in extension rate that is dominated by an initial high rate in the cusps of the crown but which then quickly reduces to a more constant rate in the lateral enamel (Dean 2009). The transition from cervical enamel formation to cervical root formation in hominoid teeth appears to occur without any abrupt change to the rate of growth in tooth length (figure 5). In many teeth, but Phil. Trans. R. Soc. B (2010)

M. C. Dean

3403

not all, the root extension rate then rises to a peak and falls off again. In very long tooth root, there may again be a rise in root extension rate towards apex completion. In the small sample of Pan, M1 mesiobuccal roots plotted in figure 5, the mean age at which this early peak in root extension rate occurs (3.8 years, range ¼ 3.01 – 4.65 years, s.d. 0.48) is close to that reported for gingival emergence. While this apparent signature for gingival emergence is unlikely to be a simple epigenetic reflection of tooth movement through the bone, it is intuitive that root extension rates should begin to fall off at the time of initial functional occlusion. When the data for extension rates are aligned around this early mean peak height velocity (PHV) rather than plotted with respect to initiation at birth, this small rise in root extension rate is more easily seen and not smoothed out (figure 5). For this sample of Pan M1s, PHV is 8.7 mm d21 (range 6.1 – 10.2 mm d21). The expression of this peak in early root growth becomes weaker distally in M2s and M3s but is still there although it occurs later into root formation. PHV in this sample of M2s was 6.7 mm d21 and occurred at 4.7 years (range 3.4 – 6.4 years, s.d. 0.85) into tooth formation. (g) Summary points about dental development in P. troglodytes The sequence and times of initiation as well as total tooth formation times of incisors and canines are little different from modern humans. The ages of gingival emergence of incisors and canines are also little different. Anterior crown formation times (with the exception of male canines crowns which take longer to form) are only slightly longer than average modern human crown formation times. It is the initiation times and eruption times of the molar dentition in modern humans that are drawn out to later ages with prolongation of the growth period. The greatest shift in timing appears to be in eruption times, which can be observed both at later stages of root formation in modern humans as well as at later ages than in Pan. This is most marked in M3 that initiates approximately 4.5 years later in modern humans than in Pan and which erupts into functional occlusion approximately 8 years later at close to 18 years of age. Average total molar tooth formation times in Pan are shorter than those in modern humans, but it only seems by between one and two years, and while molar crown formation times are also shorter on average, this is only by six to nine months with overlapping ranges. It appears (figure 2) that there is little or no difference in the rate of growth in height of the molar crowns or roots between Pan and modern humans. Besides these comparisons of timing in tooth formation, it may well be that great ape teeth contain information about seasonality and perhaps even about their own eruptive history. 5. THE EVIDENCE FOR A CHRONOLOGY OF DENTAL DEVELOPMENT IN FOSSIL HOMININS (a) Molar eruption times Bromage & Dean (1985) estimated the age at death of four early hominin specimens with M1 just prior to or at functional occlusion (Sts 24, Australopithecus

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3404

M. C. Dean Review. Dental development in early hominins

africanus; LH 2, Au. afarensis; SK 62 and SK 63, Paranthropus robustus) to be 3.2 – 3.5 years on the basis of perikymata counts on lower permanent incisors. Subsequently, a histological study of SK 63 (Dean et al. 1993) placed gingival emergence nearer to 4 years. More recently, Lacruz et al. (2005) estimated M1 emergence into occlusion and age at death of the Taung child (Au. africanus) to be between 3.73 and 3.93 years on the basis of M1 enamel formation times and length of mesial root formed (5 – 6 mm: Conroy & Vannier 1991a,b). The only evidence for the status of the developing dentition in Australopithecus of any species around the age of M2 eruption comes from scans and radiographs of MLD 2 and Stw 327, both of which are described as having M2s recently in functional occlusion (Skinner & Sperber 1982; Conroy & Vannier 1991a). While the M3 crypt of MLD 2 is only partially preserved, CT scans of Stw 327 show a completed M3 crown (Conroy & Vannier 1991a). Skinner & Sperber (1982) have drawn attention to the permanent canines of MLD 2, which are still deep in their crypts and that on CT scans (Conroy & Vannier 1991a) have less root length formed than crown length. However, no histological age estimates are possible for either of these specimens. But if the timing of canine root length formed could be shown to match that known for Pan, then the standards defined by Kuykendall (1996) would provide a median age estimate of 7.6 years for MLD 2 (range 6.10– 8.75)—but this is speculative. This age range, however, spans the range of histological estimates for age at death of KNMWT 15000 (attributed to Homo erectus at 1.5 Ma), where M2s were also just in functional occlusion and where the one preserved upper M3 crown was also just complete (Dean & Smith 2009).

(b) Molar initiation times The approximately 3-year-old infant hominin dated to 3.3 Ma from Dikika, Ethiopia (Dik-1-1), and attributed to Au. afarensis had M1 crown complete with just 1.6 mm of mesiobuccal root formation (Alemseged et al. 2006). The occlusal surface of the M2 crown had already formed. This is clear evidence for early initiation of M2 and of overlap in molar enamel formation. KNM-ER 1477, a juvenile P. boisei mandible roughly the same chronological age, preserves the mesial portion of what may have been a well-formed M2 crypt. However, this is the only other potential evidence in any early hominin specimen that M2 may already have been mineralizing at the time of M1 crown completion. The mineralizing P4 in this specimen would be expected to match M2 but this cannot be known. A number of juvenile P. boisei or P. robustus specimens exist with M1 at or close to crown completion (Skinner & Sperber 1982; Dean 1987; Conroy & Vannier 1991b; Lacruz 2006). Relative to this stage of M1 formation several of the P. robustus specimens (SK 438, SK 64, SK 3978) appear to show delayed premolar formation when compared with the P. boisei specimens (KNM-ER 1477, KNMER 1820) and one explanation for this might be shorter M1 crown formation times in P. robustus. Phil. Trans. R. Soc. B (2010)

Unlike Pan no evidence exists to show early initiation of M3 in fossil hominins. Stw 151, from the late Member 4 breccia deposit at Sterkfontein, is described as a specimen with a dentition ‘not fully distinct from that of Au. africanus but with a cranial morphology more derived in some characters’ (Moggi-Cecchi et al. 1998). While there is a small mandibular M3 crypt in Stw 151, it is still too small to have accommodated a mineralizing tooth germ, which must, therefore, have initiated after M2 crown completion. Another specimen (SK 63, attributed to P. robustus) contains M2 crowns that are not quite completed but at this stage, only incipient M3 crypt depressions in the root of the ascending mandibular rami are present. Certainly, M3 initiation could not have occurred prior to M2 crown completion in this specimen.

(c) Total tooth formation times The evidence for total anterior tooth formation times in early hominins is lacking but what there is suggests little difference from Pan. Median ages for combined sexes in Pan for lower incisors at the same developmental stage (Kuykendall 1996) would estimate age at death of Stw 151 at 4.95 years (range 4.61 – 5.22). This is very close to the histological estimate of 5.2 – 5.3 years for this specimen (Moggi-Cecchi et al. 1998). There is then no evidence to suggest that the timing of root formation in this early hominin was different from that observed in Pan. Both standards for lower lateral incisors in modern humans (8.0 years, s.d. 0.99; Liversidge 2009) and Pan (8.04 years, inter-quartile range 7.66– 8.86; Kuykendall 1996) also each give median age at death estimates that match histological estimates for the H. erectus youth from Nariokotome (7.6 – 8.8 years, Dean & Smith 2009). Again this suggests that there is no evidence for any change in total incisor tooth formation times in early hominins, but histological evidence for ages of hominin specimens with near completed canine roots are needed to show that this also holds true for canines. Stw 151 is aged histologically to between 5.2 and 5.3 years at death (Moggi-Cecchi et al. 1998). It had M1s with one or more incomplete root apex at the time M2, premolar and canine crowns had just completed enamel formation. This age implies that root apex closure of M1 was at the earliest end of the age range reported for Pan and occurred close to M2 crown completion. The end of M2 crown completion in KNM-WT 15000 (H. erectus) was also estimated to have completed between 4.2 and 4.9 years on the basis of perikymata counts (Dean & Smith 2009). Other early hominin specimens from Laetoli, LH 3 and LH 6 (attributed to Au. afarensis) consist only of isolated teeth (White 1977). However, in both specimens, the upper M1 is at a similar stage of root apex formation as Stw 151 and each have permanent canine and premolar crowns close to or just completed. Close correspondence of the canine crown perikymata counts (Stw 151 ¼ 140 and LH 6 ¼ 134) suggests that LH 6 was close in age with the same pattern of tooth formation and the same early age for

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Dental development in early hominins M1 root completion. No M2s are preserved for comparison in either of these specimens from Laetoli. While speculative, a tooth fragment from Allia Bay, Kenya, attributed to Au. anamensis (KNM-ER 30748) may contain information about molar eruption in early hominins. It is plotted in figure 2 as an M2, since it has an enamel formation time (2.7 years) beyond the range of the Pan M1s sampled here (see also Ward et al. 2001). It contains a marked early root spurt of 9.8 mm d21 at 4.2 years into tooth formation that is within the M2 range for Pan (3.44 – 6.38 years). If M2 initiation in Au. anamensis was close to 1.75 years, as in Pan, and if early root PHV actually reflects the eruptive process, then this would place functional occlusion of this tooth towards the lower end of the range reported for M2 in Pan (5.6 – 7.8 years) (Nissen & Riesen 1964). A number of chronologically older hominin specimens exists with incomplete M3 roots. KNM-ER 1802 has a left M3 with just one wear facet on the protoconid and a ca 9 mm long mesial root impression in the alveolar bone for the right M3. Sts 52 (attributed to Au. africanus), OH5 and KNM-WT 17400 both attributed to P. boisei, are specimens closer to dental maturity but there is no histological evidence at all to estimate their chronological age, only a hint from periapical radiographs of the upper canine of OH5 that this root apex may have been recently completed by age at death (Skinner & Sperber 1982).

(d) Crown formation times Perikymata counts on hominin incisors and canines, especially those attributed to Paranthropus, all point to anterior crown formation times having been shorter than those known for modern humans and for Pan (Dean et al. 1993, 2001; Dean & Reid 2001). One lower canine tooth attributed to Au. africanus (Sts 50) has 170 perikymata suggesting a crown formation time of around four years or more (Dean & Reid 2001) but in general the anterior teeth with the greatest crown formation times appear to be those of Au. anamensis and Au. afarensis. Here, canine enamel formation times come closest to those known for modern humans. Suwa et al. (2009a) counted 193 perikymata on the upper canine of ARA-VP-6/1 (the holotype of Ardipithecus ramidus and a probable male). This suggests that canine crown formation took between 4.3 and 4.8 years in this specimen (Suwa et al. 2009a) and so was potentially within the range recorded for female Gorilla and Pongo, but below the range so far recorded for female Pan canines (Schwartz & Dean 2001). The several clear regularly spaced hypoplastic bands illustrated on this specimen in Suwa et al. (2009b) are reminiscent of what are likely to be seasonally related cycles of poor growth on living great ape canines (Skinner & Hopwood 2003). If there were eight or nine such bands on ARA-VP-6/ 1 and on other Ar. ramidus canines, this would strongly suggest that Ar. ramidus existed in a seasonal environment with two colder wetter seasons per year. At least seven juvenile specimens attributed to P. boisei (KNM-ER 1477, KNM-ER 812, KNM-ER 1820, OH 30) or P. robustus (KB 5223, SK 64, Phil. Trans. R. Soc. B (2010)

M. C. Dean

3405

SK 3978) have M1 at or close to crown completion (Skinner & Sperber 1982; Dean 1987; Conroy & Vannier 1991b; Lacruz 2006). Some have been aged on the basis of perikymata counts on anterior tooth germs at between 2.5 and 3.0 years of age at death (Dean 1987) but with some root formation. This fits well with a histologically derived estimate of 2.4 years for M1 crown formation time in SK 63 (P. robustus) from Swartkrans, South Africa (Dean et al. 1993). Lacruz & Ramirez Rozzi (2010) have made histological estimates of metaconid as well as total crown formation times of two Au. afarensis molar fragments (AL 333-52 and AL 336-1) at between 2.2 and 2.4 years. Beynon & Wood (1987) calculated a range of molar crown formation times of 2.12 – 2.59 years in P. boisei, while Ramirez Rozzi (1993, 1995) found ranges of 1.93– 2.49 years for P. aethiopicus but a greater range for enamel formation times of P. boisei molars of all types (2.67 – 3.43 years). In P. robustus from Kromdraai, Lacruz (2006) calculated protoconid formation times at between 1.98 and 2.38 years and metaconid time to be near identical (1.92 –2.37 years) but Lacruz et al. (2006) reported protocone formation times in two Au. africanus molars to be greater than this (M1, 2.74 years and M2, 3.0 – 3.2 years). These latter two crown formation times are very close to mean modern human values. In general, molar crown formation times in early hominins are less than those in modern humans and more similar to those of Pan but there is considerable overlap in the ranges and still insufficient data to compare sample mean values statistically.

(e) Summary points about dental development in early hominins The cumulative rates of enamel formation follow a similar trajectory in both Pan and early hominins (irrespective of enamel thickness and crown formation times) that is faster than that in modern humans (Dean et al. 2001; Lacruz et al. 2008). Estimates for gingival emergence times for M1 in several early hominin specimens all fall within the range expected for Pan, and in fact are all earlier than the time proposed for free-born, free-living chimpanzees. There is, however, no direct evidence at all for ages of M2 and M3 eruption among the earliest hominins. The evidence for molar initiation times provides only one example (Dikika: Dik-1-1) where there is clear early M2 initiation with respect to M1 and there is no evidence at all for M3 initiation occurring prior to completion of M2 enamel formation in any early hominin specimen. Total molar tooth formation times have only been estimated in three hominin specimens, and appear to fall closest to the earlier ages known for Pan. In contrast, those of incisors appear similar to those observed in Pan. Anterior crown formation times are almost always consistently less than those known for Pan with the shortest crown formation times occurring in Paranthropus. Enamel (crown) formation times in molars are generally within the ranges known for Pan molars (but occasionally also fall well within modern human ranges).

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3406

M. C. Dean Review. Dental development in early hominins

6. DISCUSSION Constructing a chronology for dental development in P. troglodytes as a comparative model for early hominins is useful for a number of reasons. First, it highlights the processes whereby dental development is likely to have kept pace with prolongation of the period of general growth during hominid evolution. These seem to be confined to the sequence of molar development and to have involved shifts in the timing of initial mineralization, slightly faster crown formation rates and particularly, earlier times of tooth emergence into functional occlusion. The cumulative effects of each of these are most fully expressed in molar emergence times, which appear to be the clearest measure of comparative development than any one of the components that contribute to it. Estimates of M1 emergence times in fossil hominins, as well as observations of early molar initiation, and in some cases shorter crown formation times, resemble Pan more closely than modern humans. However, too few specimens exist to provide clear evidence for early initiation or earlier gingival emergence times of M2 or M3 among australopith specimens, although the evidence for this is a little better in early Homo (Dean et al. 2001; Dean & Smith 2009). The model reveals, however, that the key indicators of a Pan-like dental maturation pattern would include early M3 initiation with respect to M2 crown formation time and a lesser proportion of root formed at gingival emergence in all molar tooth types than in modern humans. A second point to emerge from the model for Pan is that some things appear to be little different between Pan and Homo and, it follows, might not be expected to differ in early hominins. Total anterior tooth formation times, and maybe also those for molars, fall within the same range, all be it a broad range. Few radiographic studies of molar development in Pan have included older animals and few of the individual plots in figure 2 extend all the way to root apex closure and moreover, it is the distobuccal root (not the mesiobuccal root shown in figure 2) in both Pan and Gorilla that on radiographs completes formation last (Dean & Wood 2003). It is highly likely, therefore, that future studies will show total molar formation times to be equal in Pan and Homo. In this respect, the evidence for at least three individual australopith specimens suggests that total M1 and M2 formation time may have been at the low end of the range reconstructed for Pan. The plot of M2 (figure 2) attributed to Au. anamensis (KNM-ER 30748) has a crown formation time at the upper limit of the M2 range for Pan (2.66 years) but a total tooth formation time of only 5.5 years (but with a little root still to form) and a faster rate of root formation generally than in Pan that might prove to be more typical of Gorilla. Shorter anterior crown formation times in many australopiths and earlier times for root completion might also turn out to fit a Gorilla model better than a Pan model. This mosaic of great ape-like dental development among australopiths is perhaps what one ought to expect given the gorilla-like anatomy of the scapula of Dikika, Dik-1-1 (Alemseged et al. 2006) and the gorilla-like mandibular morphology of Au. afarensis mandibles (Rak et al. 2007). Phil. Trans. R. Soc. B (2010)

A third observation about the chronological model of dental development in Pan compared with that in early hominins is that anterior tooth growth does not appear to reflect general somatic growth. While total anterior tooth formation times appear to be little different, anterior crown formation times in australopiths are very variable but always shorter than in Pan (Dean & Reid 2001; Dean et al. 2001). In this respect, the comparative chronological model for anterior tooth crown formation times in Pan differs completely from that reconstructed for australopiths. Crown formation time does not relate in any simple way to crown height (Dean 2009) within a tooth type. For example, there is nothing to distinguish the enamel formation times of smaller P. robustus canines from taller canines of H. erectus (Dean et al. 1993, 2001). The fact that both enamel thickness and anterior tooth crown height, characters that can be broadly linked to dietary specialization, are not tightly linked to the time taken to form crowns is interesting. If in fact total anterior tooth formation times are relatively more stable than anterior tooth morphology appears to be, then perhaps crown formation times might be a better candidate for exploring phylogenetic relatedness among closely related species of early hominins than tooth morphology. An interesting case in point worth further consideration is the short time taken to form the reduced canine crown heights of Ar. ramidus (Suwa et al. 2009a). All observations made so far on fossil and living apes and on early hominins indicate that M1 eruption times would have fallen within the simulated ranges for free-living Pan shown in figure 3 and none appear to fall within the ranges known for modern humans. Interestingly, all predictions so far for M1 emergence in fossil apes (Kelley 1997, 2002; Kelley & Smith 2003; Dean 2006) actually fall below the simulated median age of attainment for M1 emergence predicted in figure 3 as indeed do most estimates for early hominins. This raises questions about how different great ape dental development in the Late Miocene might have been to that known today for modern P. troglodytes and how good a model modern Pan is for comparisons with the earliest hominins. It also highlights the need to reconstruct a chronology for dental development in Gorilla to place that for Pan in a better modern comparative perspective. It remains a real possibility that the chronological dental development in the earliest hominins was more similar to that in modern Gorilla than to modern Pan. Were this the case it would raise very interesting issues about early hominin lifehistory strategies of the kind discussed by Kelley & Schwartz (2009). The issue of advanced dental maturity in captive hand-reared great apes suggests that even M1 emergence times of approximately 4.5 years predicted for H. erectus (Dean et al. 2001; Dean & Smith 2009) would still fall comfortably within the simulated range for wild-born chimpanzees (figure 3) as has been suggested by Zihlman et al. (2004) but predictions for M2 and M3 eruption of approximately 8 and approximately 14 years, respectively, in H. erectus would not. No convincing evidence exists for any differences in the chronology of molar development and emergence

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Dental development in early hominins between early hominin taxa, but estimates of chronological age in specimens around 2.5 years and younger make it clear that tooth wear was excessive in some infant and juvenile late australopiths. Even thicker deciduous dental enamel was insufficient to compensate for this, resulting in extensive islands of dentine exposure on deciduous teeth very early in development (Aiello et al. 1991). Moggi-Cecchi et al. (2010) describe an infant P. robustus hemi-mandible from Drimolen (DNH-44) with an unworn erupting Rdm2 where islands of dentine are exposed on the Rdc and on four out of five cusps of the Rdm1, arguably within a year or so of birth. The obvious inference that some early hominin juveniles were taking considerable quantities of supplementary foods at a very early age cannot, at the moment, be extended to assuming they were also weaned early and that interbirth intervals were relatively short in these later australopiths, although this is one interpretation of those observations (Aiello et al. 1991; Dean 2006). Once again, there is the tantalizing suggestion that a Gorilla-like life-history model may be a better match for some, but not all, early hominins. Many life-history variables in Gorilla such as age at weaning (reviewed in Aiello et al. 1991) age at first reproduction and interbirth interval (Watts 1991; Robson & Wood 2008; Kelley & Schwartz 2009) are reported to be earlier than in Pan and Pongo (Wich et al. 2004). However, a firm link with these variables and earlier dental development remains illusive (Kelley & Schwartz 2009; Humphrey 2010). In the future, combined studies of tooth microstructure that put a chronological time scale to more sophisticated models of changing infant diets may shed more light on early life-history events such as these during the first four million years of human evolution (Humphrey et al. 2008; Humphrey 2010). I thank Alan Walker and Chris Stringer for inviting me to contribute to this discussion meeting. Much of the research underpinning this paper has been supported by the Leverhulme Trust and the Royal Society through grants to me. I thank Don Reid and Gary Schwartz for helping with the construction of figure 4 and I am especially grateful to Louise Humphrey, Jay Kelley, Helen Liversidge and Holly Smith for discussions that have helped develop some of the ideas set out here.

ENDNOTE 1

For consistency and clarity, ages given in the literature are cited here as follows: Prenatal and postnatal ages up to 1 month are given in days, those between 1 month and 1 year in months and those greater than this in years.

REFERENCES Aiello, L. C., Montgomery, C. & Dean, C. 1991 The natural history of deciduous tooth attrition in hominoids. J. Hum. Evol. 21, 397–412. (doi:10.1016/0047-2484(91)90114-B) Alemseged, Z., Spoor, F., Kimbel, W. H., Bobe, R., Geraads, D., Reed, D. & Wynn, J. 2006 Juvenile early hominin skeleton from Dikika, Ethiopia. Nature 443, 296 –301. (doi:10.1038/nature05047) Anemone, R. L. 1995 Dental development in chimpanzees of known chronological age; implications for understanding the age at death of Plio-Pleistocene hominids. Phil. Trans. R. Soc. B (2010)

M. C. Dean

3407

In Aspects of dental biology; palaeontology, anthropology and evolution (ed. J. Moggi-Cecchi), pp. 201–215. Florence, Italy: International Institute for the Study of Man. Anemone, R. L. & Watts, E. S. 1992 Dental development in apes and humans: a comment on Simpson, Lovejoy and Meindl (1990). J. Hum. Evol. 22, 149–153. (doi:10. 1016/0047-2484(92)90035-8) Anemone, R. L., Watts, E. S. & Swindler, D. R. 1991 Dental development of known age chimpanzees Pan troglodytes (Primates, Pongidae). Am. J. Phys. Anthropol. 86, 229–241. (doi:10.1002/ajpa.1330860211) Antoine, D., Hillson, S. & Dean, M. C. 2009 The developmental clock of dental enamel: a test for the periodicity of prism cross-striations and an evaluation of the likely sources of error in histological studies of this kind. J. Anat. 214, 45–55. (doi:10.1111/j.1469-7580.2008.01010.x) Bennejeant, C. 1940 La chronologie de la dentition chez les anthropoids. Mammalia 4, 41–45. (doi:10.1515/mamm. 1940.4.2.41) Beynon, A. D. & Wood, B. A. 1987 Patterns and rates of molar crown formation times in East African fossil hominids. Nature 326, 493–496. (doi:10.1038/326493a0) Beynon, A. D., Dean, M. C. & Reid, D. J. 1991 Histological study on the chronology of the developing dentition in gorilla and orangutan. Am. J. Phys. Anthropol. 86, 189–203. (doi:10.1002/ajpa.1330860208) Beynon, A. D., Clayton, C. B., Ramirez Rozzi, F. V. & Reid, D. J. 1998 Radiographic and histological methodologies in estimating the chronology of crown development in modern humans and great apes; a review, with some applications for studies on juvenile hominids. J. Hum. Evol. 35, 351 –370. (doi:10.1006/jhev.1998.0234) Boyde, A. 1963 Estimation of age at death of young human skeletal remains from incremental lines in dental enamel. Third Int. Meeting in Forensic Immunology, Medicine, Pathology and Toxicology, April 16th–24th, Excerpta Medica (Int. Congress Series no. 80) Plenary Session IIA, London, pp. 36–46. Boyde, A. 1964 The structure and development of mammalian enamel. PhD Thesis, University of London, London, UK. Boyde, A. 1976 Amelogenesis and the structure of enamel. In Scientific foundations of dentistry (eds B. Cohen & I. R. H. Kramer), pp. 335–352. London, UK: W. Heinemann Medical Books Ltd. Boyde, A. 1979 Carbonate concentration, crystal centres, core dissolution, caries, cross striation, circadian rhythms and compositional contrast in the SEM. J. Dent. Res. 58b, 981–983. Boyde, A. 1989 Enamel. In Handbook of microscopic anatomy. Vol. 2: Teeth (eds A. Oksche & L. Vollrath), pp. 309 –473. Berlin, Germany: Springer. Boyde, A. 1990a Developmental interpretations of dental microstructure. In Primate life history and evolution: monographs in primatology, vol. 14 (ed. C. Jean De Rousseau), pp. 229–267. New York, NY: Wiley-Liss Inc. Boyde, A. 1990b Confocal optical microscopy. In Modern microscopies: techniques and applications (eds P. J. Duke & A. G. Michette), pp. 185– 204. New York, NY: Plenum Press. Bradley, B. J. 2008 Reconstructing phylogenies and phenotypes: a molecular view of human evolution. J. Anat. 212, 337–353. (doi:10.1111/j.1469-7580.2007.00840.x) Bromage, T. G. 1991 Enamel incremental periodicity in the pig-tailed macaque; a polychrome fluorescent labelling study of dental hard tissues. Am. J. Phys. Anthropol. 86, 205–214. (doi:10.1002/ajpa.1330860209) Bromage, T. G. & Dean, M. C. 1985 Re-evaluation of the age at death of immature fossil hominids. Nature 317, 525–527. (doi:10.1038/317525a0)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3408

M. C. Dean Review. Dental development in early hominins

Bromage, T. G. et al. 2009 Lamellar bone is an incremental tissue reconciling enamel rhythms, body size and organismal life history. Cal. Tissue Int. 84, 388 –404. (doi:10.1007/s00223-009-9221-2) Clements, E. M. B. & Zuckerman, S. 1953 The order of eruption of the permanent teeth in the Hominoidea. Am. J. Phys. Anthropol. 11, 313–337. (doi:10.1002/ajpa. 1330110309) Conroy, G. C. & Vannier, M. W. 1991a Dental development in South African australopithecines. Part I: problems of pattern and chronology. Am. J. Phys. Anthropol. 86, 121 –136. (doi:10.1002/ajpa.1330860204) Conroy, G. C. & Vannier, M. W. 1991b Dental development in South African australopithecines. Part II: dental stage assessment. Am. J. Phys. Anthropol. 86, 137 –156. (doi:10.1002/ajpa.1330860205) Dean, M. C. 1985 Variation in the developing root cone angle of the permanent mandibular teeth of modern man and certain fossil hominids. Am. J. Phys. Anthropol. 68, 233 –238. (doi:10.1002/ajpa.1330680210) Dean, M. C. 1987 The dental developmental status for six East African juvenile hominids. J. Hum. Evol. 16, 197 –213. (doi:10.1016/0047-2484(87)90076-5) Dean, M. C. 2000 Progress in understanding hominoid dental development. J. Anat. 197, 77–101. (doi:10. 1046/j.1469-7580.2000.19710077.x) Dean, M. C. 2006 Tooth microstructure tracks the pace of human life history evolution. Proc. R. Soc. B 273, 2799–2808. (doi:10.1098/rspb.2006.3583) Dean, M. C. 2009 Growth in tooth height and extension rates in modern human and fossil hominin canines and molars. In Frontiers of oral biology; interdisciplinary dental morphology (eds T. Koppe, G. Meyer & K. W. Alt), pp. 68–73. Basel, Switzerland: Karger. Dean, M. C. In press. Daily rates of dentine formation and root extension rates in Paranthropus boisei, KNM-ER 1817, from Koobi Fora, Kenya. In African Genesis Symp. Proc. (eds S. Reynolds & C. Menter). South Africa: University of Witwatersrand Press. Dean, M. C. & Reid, D. J. 2001 Anterior tooth formation times in Australopithecus and Paranthropus. In Twelfth Int. Symp. on Dental Morphology (ed. A. Brooks), pp. 135 –149. Sheffied, UK: Sheffield Academic Press. Dean, M. C. & Smith, B. H. 2009 Growth and development in the Nariokotome Youth, KNM-WT 15000. In The first humans: origin of the genus Homo (eds F. E. Grine, J. C. Fleagle & R. E. Leakey), pp. 101 –120. New York, NY: Springer. Dean, M. C. & Wood, B. A. 1981 Developing pongid dentition and its use for ageing individual crania in comparative cross-sectional growth studies. Folia Primatol. 36, 111 –127. (doi:10.1159/000156011) Dean, M. C. & Wood, B. A. 2003 A digital radiographic atlas of the great ape skull and dentition. In Digital archives of human paleobiology (eds L. Bondioli & R. Macchiarelli). Milano, Italy: ADS Solutions/Consiglio Nazionale delle Ricerche. Dean, M. C., Beynon, A. D., Thackeray, J. F. & Macho, G. A. 1993 Histological reconstruction of dental development and age at death of a juvenile Paranthropus robustus specimen, SK 63, from Swartkrans, South Africa. Am. J. Phys. Anthropol. 91, 401–419. (doi:10.1002/ajpa. 1330910402) Dean, M. C., Leakey, M. G., Reid, D. J., Schrenk, F., Schwartz, G. T., Stringer, C. & Walker, A. 2001 Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414, 628 –631. (doi:10.1038/414628a) Fooden, J. & Izor, R. J. 1983 Growth curves, dental emergence norms, and supplementary morphological Phil. Trans. R. Soc. B (2010)

observations on known-age captive orangutans. Am, J. Primatol. 5, 285–301. (doi:10.1002/ajp.1350050402) Goodman, M., Bailey, W. J., Hayasaka, K., Stanhope, M. J., Slightom, J. & Czelusniak, J. 1994 Molecular evidence on primate phylogeny from DNA sequences. Am. J. Phys Anthropol. 94, 3–24. (doi:10.1002/ajpa.1330940103) Hess, A. F., Lewis, J. M. & Roman, B. 1932 A radiographic study of calcification of the teeth from birth to adolescence. Dent. Cosmos 74, 1053–1061. Humphrey, L. T. 2010 Weaning behaviour in human evolution. Semin. Cell Dev. Biol. 21, 453–461. Humphrey, L. T., Dean, M. C., Jeffries, T. E. & Penn, M. 2008 Unlocking evidence of early diet from tooth enamel. Proc. Natl Acad. Sci. USA 105, 6834 –6839. (doi:10.1073/pnas.0711513105) Kahumbu, P. & Ely, R. M. 1991 Teeth emergence in wild olive baboons in Kenya and formulation of a dental schedule for ageing wild baboon populations. Am. J. Primatol. 23, 1–9. (doi:10.1002/ajp.1350230102) Keith, A. 1899 On the chimpanzees and their relationship to the gorilla. Proc. Zool. Soc. Lond. 67, 296 –312. (doi:10. 1111/j.1469-7998.1899.tb06859.x) Kelley, J. 1997 Paleobiological and phylogenetic significance of life history in Miocene hominoids. In Function, phylogeny, and fossils: miocene hominoid evolution and adaptations (eds D. R. Begun, C. V. Ward & M. D. Rose), pp. 173 –208. New York, NY: Plenum Press. Kelley, J. 2002 Life history evolution in Miocene and extant apes. In Human evolution through developmental change (eds N. Minugh-Purvis & K. J. McNamara), pp. 223– 248. Baltimore, MD: Johns Hopkins University Press. Kelley, J. & Schwartz, G. T. 2009 Dental development and life history in living African and Asian apes. Proc. Natl Acad. Sci. USA 107, 1035– 1040. (doi:10.1073/pnas. 0906206107) Kelley, J. & Smith, T. M. 2003 Age at first molar emergence in early Miocene Afropithecus turkanensis and life-history evolution in the Hominoidea. J. Hum. Evol. 44, 307 –329. (doi:10.1016/S0047-2484(03)00005-8) Kelley, J., Dean, M. C. & Ross, S. 2009 Root growth during molar eruption in extant great apes. In Frontiers of oral biology; interdisciplinary dental morphology (eds T. Koppe, G. Meyer & K. W. Alt), pp. 128 –133. Basel, Switzerland: Karger. Krogman, W. M. 1930 Studies in growth changes in the skull and face of anthropoids. I. The eruption of teeth in anthropoids and Old World apes. Am. J. Anat. 46, 303 –313. (doi:10.1002/aja.1000460205) Kronfeld, R. 1935 Development and calcification of the human deciduous and permanent dentition. The Bur 35, 18–25. Kuykendall, K. L. 1996 Dental development in chimpanzees (Pan troglodytes): the timing of tooth calcification stages. Am. J. Phys. Anthropol. 99, 135– 157. (doi:10.1002/ (SICI)1096-8644(199601)99:1,135::AID-AJPA8.3.0. CO;2-#) Kuykendall, K. L. 2001 On radiographic and histological methods for assessing dental development in chimpanzees: comments on Beynon et al. (1998) and Reid et al. (1998). J. Hum. Evol. 40, 67–76. (doi:10.1006/jhev.2000.0445) Kuykendall, K. L., Mahoney, C. J. & Conroy, G. C. 1992 Probit and survival analysis of tooth emergence ages in a mixed-longitudinal sample of chimpanzees (Pan troglodytes). Am. J. Phys. Anthropol. 89, 379–399. (doi:10.1002/ajpa.1330890310) Lacruz, R. S. 2006 Enamel microstructure of the hominid KB 5223 from Kromdraai, South Africa. Am. J. Phys. Anthropol. 132, 175 –182. (doi:10.1002/ajpa.20506) Lacruz, R. S., Ramirez Rozzi, F. & Bromage, T. G. 2005 Dental enamel hypoplasia, age at death, and weaning in the Taung child. S. Afr. J. Sci. 101, 567 –569.

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Review. Dental development in early hominins Lacruz, R. S., Ramirez Rozzi, F. & Bromage, T. G. 2006 Variation in enamel development of South African fossil hominids. J. Hum. Evol. 51, 580 –590. (doi:10.1016/j. jhevol.2006.05.007) Lacruz, R. S., Dean, M. C., Ramirez Rozzi, F. & Bromage, T. G. 2008 Megadontia, striae periodicity and patterns of enamel secretion in Plio-Pleistocene fossil hominins. J. Anat. 213, 148 –158. (doi:10.1111/j.1469-7580.2008. 00938.x) Lacruz, R. S. & Ramirez Rozzi, F. V. 2010 Molar crown development in Australopithecus afarensis. J. Hum. Evol. 58, 201– 206. (doi:10.1016/j.jhevol.2009.11.007) Lilly, A. A., Mehlmann, P. T. & Doran, D. 2002 Intestinal parasites in gorillas, chimpanzees and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 23, 555–573. (doi:10.1023/A:1014969617036) Lippert, W. 1977 Erfahrungen bei der Aufzucht von OrangUtans (Pongo pygmaeus) im Tierpark Berlin. Der Zoologische Garten (N.F.) 47, 209–225. Liversidge, H. M. 2009 Permanent tooth formation as a method of estimating age. In Frontiers of oral biology; interdisciplinary dental morphology (eds T. Koppe, G. Meyer & K. W. Alt), pp. 153 –157. Basel, Switzerland: Karger. Mahoney, P. 2008 Intraspecific variation in M1 enamel development in modern humans: implications for human evolution. J. Hum. Evol. 55, 130 –146. Marzke, M. W., Young, D. L., Hawkey, D. E., Su, S. M., Fritz, J. & Alford, P. L. 1996 Comparative analysis of weight gain, hand/wrist maturation, and dental emergence rates in chimpanzees aged 0 –24 months from varying captive environments. Am. J. Phys. Anthropol. 99, 175 –190. (doi:10.1002/(SICI)10968644(199601)99:1,175::AID-AJPA10.3.0.CO;2-K) Moggi-Cecchi, J., Tobias, P. V. & Beynon, A. D. 1998 The mixed dentition and associated skull fragments of a juvenile fossil hominid from Sterkfontein, South Africa. Am J. Phys. Anthropol. 106, 425–465. (doi:10.1002/(SICI)10968644(199808)106:4,425::AID-AJPA2.3.0.CO;2-I) Moggi-Cecchi, J., Mentor, C., Boccone, S. & Keyser, A. 2010 Early hominin dental remains from the PlioPleistocene site of Drimolen, South Africa. J. Hum. Evol. 58, 374–405. (doi:10.1016/j.jhevol.2010.01.006) Moxham, B. J. & Berkovitz, B. K. B. 1974 The circumnatal dentitions of a gorilla (Gorilla gorilla) and a chimpanzee (Pan troglodytes). J. Zool. Lond. 173, 271–276. (doi:10. 1111/j.1469-7998.1974.tb03137.x) Nissen, H. W. & Riesen, A. H. 1945 The deciduous dentition of the chimpanzee. Growth 9, 265 –274. Nissen, H. W. & Riesen, A. H. 1964 The eruption of the permanent dentition of chimpanzees. Am. J. Phys. Anthropol. 22, 285– 294. (doi:10.1002/ajpa.1330220315) Oka, S. W. & Kraus, B. S. 1969 The circumnatal status of molar crown maturation among the hominoidea. Archs. Oral Biol. 14, 639–659. (doi:10.1016/00039969(69)90187-3) Phillips-Conroy, J. & Jolly, C. 1988 Dental eruption schedules of wild and captive baboons. Am. J. Primatol. 15, 17–29. (doi:10.1002/ajp.1350150104) Preiswerk, G. 1895 Beitra¨ge zur Kenntniss de Schmelzstrustur bei Sa¨ugethieren mit besonderer beru¨cksichtigung der Ungulaten. Basel, Switzerland: Akadenische Buchhandlung. C. F. Lendorff. Rak, Y., Ginzburg, A. & Geffen, E. 2007 Gorilla-like anatomy on Australopithecus afarensis mandibles suggests Au. afarensis link to robust australopiths. Proc. Natl Acad. Sci. 104, 6568–6572. (doi:10.1073/pnas.0606454104) Ramirez Rozzi, F. V. 1993 Tooth development in East African Paranthropus. J. Hum. Evol. 24, 429–454. (doi:10.1006/jhev.1993.1030) Phil. Trans. R. Soc. B (2010)

M. C. Dean

3409

Ramirez Rozzi, F. V. 1995 Time of crown formation in PlioPleistocene hominid teeth. In Aspects of dental biology; palaeontology, anthropology and evolution. (ed. J. Moggi-Cecchi), pp. 217 –238. Florence, Italy: International Institute for the Study of Man. Reid, D. J. & Dean, M. C. 2005 Variation in modern human enamel formation times. J. Hum. Evol. 50, 329– 346. (doi:10.1016/j.jhevol.2005.09.003) Reid, D. J., Schwartz, G. T., Dean, M. C. & Chandrasekera, M. S. 1998 A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes. J. Hum. Evol 35, 427 –448. (doi:10.1006/jhev.1998.0248) Reid, D. J., Hillson, S. & Dean, M. C. 2000 Defining chronological growth standards for known fractions of tooth crown height in primate anterior teeth. Am. J. Phys. Anthropol. Suppl. 30, 260. Retzius, A. 1837 Bemerkungen u¨ber den inneren Bau der Za¨hne, mit besonderer Ru¨cksicht auf dem in Zahnknochen vorkommenden Ro¨hrenbau. (Mu¨llers). Arch. Anat. Physiol. 1837, 486–566. Risnes, S. 1986 Enamel apposition rate and the prism periodicity in human teeth. Scand. J. Dent. Res. 94, 394–404. Robson, S. L. & Wood, B. A. 2008 Hominin life history: reconstruction and evolution. J. Anat. 212, 394 –425. (doi:10.1111/j.1469-7580.2008.00867.x) Ruvolo, M. 1994 Molecular evolutionary processes and conflicting gene trees; the hominoid case. Am. J. Phys. Anthropol. 94, 89–113. (doi:10.1002/ajpa.1330940108) Schultz, A. H. 1924 Growth studies on primates bearing upon man’s evolution. Am. J. Phys. Anthropol. 7, 149–164. (doi:10.1002/ajpa.1330070218) Schultz, A. H. 1935 Eruption and decay of the permanent teeth of primates. Am. J. Phys. Anthropol. 19, 480–581. Schultz, A. H. 1937 Fetal growth and development of the rhesus monkey. Contrib. Embryol. Carneg. Inst. 26, 71–97. Schultz, A. H. 1940 Growth and development of the chimpanzee. Contrib. Embryol. Carneg. Inst. 28, 1–63. Schwartz, G. T. & Dean, M. C. 2001 Ontogeny of canine dimorphism in extant hominoids. Am. J. Phys. Anthropol. 115, 269–283. (doi:10.1002/ajpa.1081) Schwartz, G. T., Reid, D. J. & Dean, M. C. 2001 Developmental aspects of sexual dimorphism in hominoid canines. Int. J. Primatol. 22, 837–860. (doi:10.1023/ A:1012073601808) Schwartz, G. T., Dean, M. C., Reid, D. J. & Zihlman, A. L. 2006 A faithful record of stressful life events preserved in the dental developmental record of a juvenile gorilla. Int. J. Primatol. 27, 1– 19. Shellis, R. P. 1984 Variations in growth of the enamel crown in human teeth and a possible relationship between growth and enamel structure. Archs. Oral Biol. 29, 697– 705. (doi:10.1016/0003-9969(84)90175-4) Shinoda, H. 1984 Faithful records of biological rhythms in dental hard tissues. Chem. Today 162, 34–40. [In Japanese.] Skinner, M. F. & Hopwood, D. 2003 Hypothesis for the causes and periodicity of repetitive linear enamel hypoplasia in large, wild African (Pan troglodytes and Gorilla gorilla) and Asian (Pongo pygmaeus) apes. Am. J. Phys. Anthropol. 123, 216– 235. (doi:10.1002/ajpa.10314) Skinner, M. F. & Sperber, G. H. 1982 Atlas of radiographs of early man. New York, NY: A. R. Liss Inc. Smith, B. H. 1989 Dental development as a measure of life history in primates. Evolution 43, 683–688. (doi:10.2307/ 2409073) Smith, T. M. 2006 Experimental determination of the periodicity of incremental features in enamel. J. Anat. 208, 99–113. (doi:10.1111/j.1469-7580.2006.00499.x)

Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3410

M. C. Dean Review. Dental development in early hominins

Smith, T. M., Reid, D. J., Dean, M. C., Olejniczak, A. J. & Martin, L. B. 2006 Molar development in common chimpanzees (Pan troglodytes). J. Hum. Evol. 52, 201 – 206. (doi:10.1016/j.jhevol.2006.09.004) Smith, T. M., Smith, B. H. & Boesch, C. 2009 Dental development in the Taı¨ forest chimpanzees reappraised. Am. J. Phys. Anthropol. 138, 243. Smith, T. M., Smith, B. H., Reid, D. J., Siedel, H., Vigilant, L., Hublin, J.-J. & Boesch, C. 2010 Dental development of the Taı¨ Forest chimpanzees revisited. J. Hum. Evol. 58, 363 –373. (doi:10.1016/j.jhevol.2010.02.008) Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, O. C. & White, T. D. 2009a Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 94–99. Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, O. C. & White, T. D. 2009b Author’s summaries. Paleobiological implications of the Ardipithecus ramidus dentition. Science 326, 69. (doi:10.1126/science.1175824) Swindler, D. R. 1985 Nonhuman primate dental development and its relation to human dental development. In Nonhuman primate models for human growth and development (ed. E. S. Watts), pp. 67–94. New York, NY: A. R. Liss. Tarrant, L. H. & Swindler, D. R. 1972 The state of the deciduous dentition of a chimpanzee fetus (Pan troglodytes). J. Dent. Res. 51, 677. Ward, C. V., Leakey, M. G. & Walker, A. 2001 Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J. Hum. Evol. 41, 255–368. (doi:10.1006/jhev. 2001.0507) Watts, D. P. 1991 Mountain gorilla reproduction and sexual behavior. Am. J. Primatol. 24, 211– 226. (doi:10.1002/ ajp.1350240307)

Phil. Trans. R. Soc. B (2010)

White, T. D. 1977 New fossil homininds from Laetolil, Tanzania. Am. J. Phys. Anthropol. 48, 197 –229. Wich, S. A., Utami-Atmoko, S. S., Mitra Setia, T., Rijkesen, H. D., Schurmann, C., van Hooff, J. A. R. A. M. & van Schaik, C. P. 2004 Life history of wild Sumatran orangutans (Pongo abelii). J. Hum. Evol. 47, 385–398. (doi:10.1016/j.jhevol.2004.08.006) Winkler, L. A. 1996 A comparison of radiographic and anatomical evidence of tooth development in infant apes. Folia Primatol. 65, 1 –13. (doi:10.1159/000156864) Winkler, L. A., Schwartz, J. H. & Swindler, D. R. 1991 Aspects of dental development in the orangutan prior to eruption of the permanent dentition. Am. J. Phys. Anthropol. 86, 255 –271. (doi:10.1002/ajpa. 1330860213) Winkler, L. A., Schwartz, J. H. & Swindler, D. R. 1996 Development of the orang utan permanent dentition: Assessing patterns and variation in tooth development. Am. Phys. Anthropol. 99, 205–220. (doi:10.1002/ (SICI)1096-8644(199601)99:1,205::AID-AJPA12.3.0. CO;2-R) Zihlman, A., Bolter, D. & Boesch, C. 2004 Wild chimpanzee dentition and its implications for assessing life history in immature hominin fossils. Proc. Natl Acad. Sci. USA 101, 10541–10543. (doi:10.1073/pnas.0402635101) Zihlman, A., Bolter, D. & Boesch, C. 2007 Skeletal and dental growth and development in chimpanzees of the Taı¨ National Park, Coˆte D’Ivoire. J. Zool. 273, 63–73. (doi:10.1111/j.1469-7998.2007.00301.x) Zuckerman, S. 1928 Age changes in the chimpanzee, with special reference to growth of the brain, eruption of the teeth and estimation of age; with a note on the Taungs ape. Proc. Zool. Soc. Lond. 96, 1 –42.

RSTB_365_1556_Cover.qxd

9/7/10

10:42 AM

Page 2

GUIDANCE FOR AUTHORS

Editor Professor Georgina Mace Publishing Editor Joanna Bolesworth Editorial Board Neuroscience and Cognition Dr Brian Billups Dr Andrew Glennerster Professor Bill Harris Professor Trevor Lamb Professor Tetsuro Matsuzawa Professor Andrew Whiten Cell and developmental biology Professor Makoto Asashima Dr Buzz Baum Professor Martin Buck Dr Louise Cramer Dr Anne Donaldson Professor Laurence Hurst Professor Fotis Kafatos Professor Elliot Meyerowitz Professor Dale Sanders Dr Stephen Tucker

Publishing Editor: Joanna Bolesworth (tel: +44 (0)20 7451 2602; fax: +44 (0)20 7976 1837; [email protected]) Production Editor: Jessica Mnatzaganian 6–9 Carlton House Terrace, London SW1Y 5AG, UK rstb.royalsocietypublishing.org

Organismal, environmental and evolutionary biology Professor Spencer Barrett Professor Nick Barton Dr Will Cresswell Professor Georgina Mace Professor Yadvinder Malhi Professor Manfred Milinski Professor Peter Mumby Professor Karl Sigmund Health and Disease Professor Zhu Chen Professor Mark Enright Professor Michael Malim Professor Angela McLean Professor Nicholas Wald Professor Joanne Webster

Publishing format Phil. Trans. R. Soc. B articles are published regularly online and in print issues twice a month. Along with all Royal Society journals, we are committed to archiving and providing perpetual access. The journal also offers the facility for including Electronic Supplementary Material (ESM) to papers. Contents of the ESM might include details of methods, derivations of equations, large tables of data, DNA sequences and computer programs. However, the printed version must include enough detail

to satisfy most non-specialist readers. Supplementary data up to 10Mb is placed on the Society's website free of charge. Larger datasets must be deposited in recognised public domain databases by the author.

Conditions of publication Articles must not have been published previously, nor be under consideration for publication elsewhere. The main findings of the article should not have been reported in the mass media. Like many journals, Phil. Trans. R. Soc. B employs a strict embargo policy where the reporting of a scientific article by the media is embargoed until a specific time. The Executive Editor has final authority in all matters relating to publication.

Electronic Submission details For full submission guidelines and access to all journal content please visit the Phil. Trans. R. Soc. B website at rstb.royalsocietypublishing.org.

AIMS AND SCOPE Each issue of Phil. Trans. R. Soc. B is devoted to a specific area of the biological sciences. This area will define a research frontier that is advancing rapidly, often bridging traditional disciplines. Phil. Trans. R. Soc. B is essential reading for scientists working across the biological sciences. In particular, the journal is focused on the following four cluster areas: neuroscience and cognition; organismal and evolutionary biology; cell and developmental biology; and health and disease. As well as theme issues, the journal publishes papers from the Royal Society’s biological discussion meetings. For information on submitting a proposal for a theme issue, consult the journal‘s website at rstb.royalsocietypublishing.org.

ISBN: 978-0-85403-847-3

Copyright © 2010 The Royal Society Except as otherwise permitted under the Copyright, Designs and Patents Act, 1988, this publication may only be reproduced, stored or transmitted, in any form or by any other means, with the prior permission in writing of the publisher, or in the case of reprographic reproduction, in accordance with the terms of a licence issued by the Copyright Licensing Agency. In particular, the Society permits the making of a single photocopy of an article from this issue (under Sections 29 and 38 of this Act) for an individual for the purposes of research or private study. SUBSCRIPTIONS In 2011 Phil. Trans. R. Soc. B (ISSN 0962-8436) will be published twice a month. Full details of subscriptions and single issue sales may be obtained either by contacting our journal fulfilment agent, Portland Customer Services, Commerce Way, Colchester CO2 8HP; tel: +44 (0)1206 796351; fax: +44 (0)1206 799331; email: [email protected] or by visiting our website at http://royalsocietypublishing.org/info/subscriptions. The Royal Society is a Registered Charity No. 207043.

Selection criteria The criteria for selection are scientific excellence, originality and interest across disciplines within biology. The Editors are responsible for all editorial decisions and they make these decisions based on the reports received from the referees and/or Editorial Board members. Many more good proposals and articles are submitted to us than we have space to print, we give preference to those that are of broad interest and of high scientific quality.

The Royal Society, the national academy of science of the UK and the Commonwealth, is at the cutting edge of scientific progress. We support many top young scientists, engineers and technologists, influence science policy, debate scientific issues with the public and much more. We are an independent, charitable body and derive our authoritative status from over 1400 Fellows and Foreign Members. During 2010, we are celebrating the Royal Society’s 350th anniversary. As part of this, there will be an exciting programme of activities – exhibitions, lectures, conferences, a new book, a vast science festival on the South Bank in London, television and radio broadcasting and much more besides. Our mission: to expand knowledge and further the role of science and engineering in making the world a better place.

Subscription prices 2011 calendar year

Europe

USA & Canada

All other countries

Electronic access only

£2145/€2788

$4058

£2317/US$4153

• invest in future scientific leaders and in

Printed version plus electronic access

£2574/€3345

$4869

£2780/US$4983

• influence policymaking with the best scientific

For further information on the Society’s activities, please contact the following departments on the extensions listed by dialling +44 (0)20 7839 5561, or visit the Society’s Web site (www.royalsociety.org). Research Support (UK grants and fellowships) Research Appointments (Fellowships): 2542 Research Grants: 2223 International travel Grants: 2555 Newton International Fellowships: 2559 Science Advice Science Policy Centre: 2550 Science Communication General enquiries: 2573 Library and Information Services Library/archive enquiries: 2606

The Royal Society’s strategic priorities are to: innovation, advice,

• invigorate science and mathematics education, • increase access to the best science internationally, and

Typeset in India by Techset Composition Limited, Salisbury, UK. Printed by Latimer Trend, Plymouth. This paper meets the requirements of ISO 9706:1994(E) and ANSI/NISO Z39.48-1992 (Permanence of Paper) effective with volume 335, issue 1273, 1992. Philosophical Transactions of the Royal Society B (ISSN: 0962-8436) is published twice a month for $4058 per year by the Royal Society, and is distributed in the USA by Agent named Air Business, C/O Worldnet Shipping USA Inc., 149-35 177th Street, Jamaica, New York, NY11434, USA. US Postmaster: Send address changes to Philosophical Transactions of the Royal Society B, C/O Air Business Ltd, C/O Worldnet Shipping USA Inc, 149-35 177th Street Jamaica, New York, NY11414.

• inspire an interest in the joy, wonder and excitement of scientific discovery.

Cover image: Sahelanthropus tchadensis: Toumaï chest, drawing (by S. Riffaut) of the sculpture (by E. Daynes); copyright MPFT.

RSTB_365_1556_Cover.qxd

9/7/10

10:42 AM

Page 1

volume 365

. number 1556 . pages 3263–3410

The first four million years of human evolution Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer Introduction The first four million years of human evolution A. Walker & C. Stringer

3265

Articles In search of the last common ancestor: new findings on wild chimpanzees W. C. McGrew More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure A. C. Stone, F. U. Battistuzzi, L. S. Kubatko, G. H. Perry Jr, E. Trudeau, H. Lin & S. Kumar

3267

3277 3289

Arboreality, terrestriality and bipedalism R. H. Crompton, W. I. Sellers & S. K. S. Thorpe

3301

Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction M. Brunet

3315

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia) Y. Haile-Selassie

3323

Anterior dental evolution in the Australopithecus anamensis–afarensis lineage C. V. Ward, J. M. Plavcan & F. K. Manthi

3333

Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis P. S. Ungar, R. S. Scott, F. E. Grine & M. F. Teaford

3345

An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar to modern humans P. L. Reno, M. A. McCollum, R. S. Meindl & C. O. Lovejoy

3355

The cranial base of Australopithecus afarensis: new insights from the female skull W. H. Kimbel & Y. Rak

3365

Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000 F. Spoor, M. G. Leakey & L. N. Leakey

3377

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene J. A. Lee-Thorp, M. Sponheimer, B. H. Passey, D. J. de Ruiter & T. E. Cerling

3389

Retrieving chronological age from dental remains of early fossil hominins to reconstruct human growth in the past M. C. Dean

Founded in 1660, the Royal Society is the independent scientific academy of the UK, dedicated to promoting excellence in science Registered Charity No 207043

3397

volume 365

number 1556

pages 3263–3410

In this Issue

The first four million years of human evolution Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer

The first four million years of human evolution

Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip–bent-knee gait C. O. Lovejoy & M. A. McCollum

Phil. Trans. R. Soc. B | vol. 365 no. 1556 pp. 3263–3410 | 27 Oct 2010

27 October 2010

ISSN 0962-8436

The world’s first science journal

rstb.royalsocietypublishing.org 27 October 2010

Published in Great Britain by the Royal Society, 6–9 Carlton House Terrace, London SW1Y 5AG See further with the Royal Society in 2010 – celebrate 350 years