THE
r The Beauty, Elegance, and Strangeness of Insect Societies
Bert Holldobler and E. O.Wilson WINNERS
OF
THE
PULITZER
PRIZE
FOR
THE ANTS
THE
SUPERORGANISM
BOOKS BY THE AUTHORS
ALSO BY BERT HOLLDOBLER AND EDWARD O. WILSON
TheAnts (1990); Pulitzer Prize, General Nonfiction, 1991
Journey tothe Ants: A Story ofScientific Exploration (1994)
ALSO BY BERT HOLLDOBLER
Experimental Behavioral Ecology and Sociobiology', with Martin Lindauer, editors (1985) Herbivory ofLeafCutting Ants, with Rainer Wirth, Hubert Herz, Ronald J. Ryel, and Wolfram Beyschlag (2003)
ALSO BY EDWARD O. WILSON
The Theory ofIsland Biogeography, with Robert H. MacArthur (1967); new preface, 2001 A Primer ofPopulation Biology, with William H. Bossert (1971) TheInsect Societies (1971)
Sociobiology: The New Synthesis (1975); new edition, 2000 On Human Nature (1978); Pulitzer Prize, General Nonfiction, 1979
Caste and Ecology in the Social Insects, with George E Oster (1978) Genes, Mind, and Culture, with CharlesJ. Lumsden (1981)
Promethean Fire: Reflections on the Origin ofMind, with Charles J. Lumsden (1983) Biophilia (1984) Success andDominance in Ecosystems: The Case ofthe Social Insects (1990) The Diversity ofLife (1992) Naturalist(1994); new edition, 2006
InSearch ofNature (1996)
Consilience: The Unity ofKnowledge (1998) Biological Diversity: The Oldest Human Heritage (1999)
The Future ofLife (2002) Pheidole in the NewWorld: A Hyperdiverse Ant Genus (2003)
From So Simple a Beginning: The Four Great Books ofDarwin, edited with introductions (2005) Nature Revealed: Selected Writings, 1949-2006 (2006) The Creation: An Appeal to Save Life on Earth (2006)
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Frontispiece: Plate 1.Weaver ants (Oecophylla smaragdina) cooperate in arranging leaves during the construction of theirleaftent nests. Copyright© 2009 by BertHoUdobler and Edward O. Wilson
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[email protected] or 800-233-4830 Manufacturing by RR Donnelley, Willard, OH Book design by AbbateDesign Production manager: Anna Oler Library of Congress Cataloging-in-Publication Data HoUdobler, Bert, 1936-
The superorganism : the beauty, elegance, andstrangeness of insect societies / BertHoUdobler and Edward O. Wilson ; line drawings by Margaret C. Nelson. — 1sted. p. cm.
Includes bibliographical references and index. ISBN 978-0-393-06704-0 (hardcover) 1. Insect societies. I. Wilson, Edward O. II. Title.
QL496.H65 2009 595.7'1782—dc22 2008038547
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FOR MARTIN LINDAUER, our colleague andfriend, whose pioneering work andinspiration in experimental sociobiobgy contributedgreatly to the conception ofan insect society as afunctional superorganism
Let him who boasts the knowledge of actually existing things, first tell us of the nature of the ant.
- S T . BASIL
CONTENTS
NOTE TO THE GENERAL READER
CHAPTER 1
THE CONSTRUCTION OF A SUPERORGANISM
Why Colonies Are Superior The Construction of Superorganisms The Levels of Organization Eusociality and the Superorganism
CHAPTER 2
CHAPTER 3
XVI
5 6
7 8
A BriefHistory of Insect Sociobiology
10
GENETIC SOCIAL EVOLUTION
15
AnAbridged History of the Genetic Theory ofSocial Evolution
16
Multilevel Natural Selection
24
The Evolution of Eusociality Crossing the Eusociality Threshold Countervailing Forces of Selection Passing the Point of No Return
29 31 42
42
SOCIOGENESIS
51
The Colony Life Cycle Social Algorithms Self-Organization and Emergence Phylogenetic Inertiaand Dynamic Selection
53
53 58 60
CHAPTER 4
CHAPTER 5
THE GENETIC EVOLUTION OF DECISION RULES
69
The Genetic Origin and Further Evolution of Eusociality
70
Sociogenetics and Sociogenomics Honeybee Sociogenomics Sociogenomic Conservation
73
The Fire Ant Case
77
Genetic Variation and Phenotypic Plasticity
79
THE DIVISION OF LABOR
83
Parallels: Organism and Superorganism The Ecology of Caste Systems The Evolution of Caste: Principles
75
84 85 89
Dominance Orders in Caste Determination
93
Temporal Castes
97
The Physiology ofTemporal Castes Genetic Variability in Caste Differentiation Memory in Division of Labor
103 116 117
Task Switching and Behavior Plasticity
120
Child Labor
125
Genetic Caste Determination
129
Nongenetic Caste Determination
136
Worker Subcastes
139
The Physiology and Evolution of Physical Castes Adaptive Demography
CHAPTER 6
71
147 152
Teamwork
159
The Larger Picture
164
COMMUNICATION
167
Dance Communication in Honeybees
169
Communication in Ant Societies
178
The Evolution ofAnt Recruitment Signals andTrail Guides Design and Functional Efficiency of Pheromones Behavioral Modes of Recruitment Communication
The Extreme Multiple Recruitment System of Weaver Ants Multimodal Signals, Parsimony, and Ritualization
XII
183 206 214
218 221
Message and Meaning Modulatory Communication Motor Displays in Recruitment Communication Environmental Correlates of Recruitment Systems
229 231 235 247
The Measurement of Information
251
Tactile Communication and Trophallaxis
252
The Social Bucket
259
Visual Communication
267
Anonymity and Specificity of Chemical Signals Necrophoric Behavior
270 273
Nestmate Recognition
CHAPTER 7
275
Within-Colony Recognition Recognition of Brood Communicating Resource-Holding Potential AmongColonies
299
Conclusion
309
THE RISE OF THE ANTS
301
313
The Origin of Ants The Early Radiation of the Ants
CHAPTER 8
288
315 318
The Cenozoic Radiation
320
The Ponerine Paradox
322
The Tropical Arboreal Ants The Dynastic-Succession Hypothesis
328 330
PONERINE ANTS: THE GREAT RADIATION
333
The Social Regulation of Reproduction Harpegnathos: Life Cycle of a Colonial Architect Dinoponera: Giant "Worker Queens" Queens, Workers, Gamergates in Permutations Diacamma: Regulating Reproduction by Mutilation Streblognathus-. Dominance and Fertility Uncoupled Gamergates versus Ergatoid Queens Pachycondylafochi: Mass Termite Raiders Ergatoid Queens and Army Ants Pachycondyla: Sociobiologically the Most Diverse Ant Genus
334 336 355 364 366 373 376
378 380
382
XIII
Platythyreapunctata: Extreme Plasticity in Reproduction Aggression and Dominance: Origin and Loss Harpegnathos: Resilience in Reproductive Behavior Colony Size as an Ecological Adaptation Pachycondyla: Hyperdiversity Summarized CHAPTER 9
397 397 398
404
THE ATTINE LEAFCUTTERS: THE ULTIMATE SUPERORGANISMS
407
The Attine Breakthrough
408
The Ascent of the Leafcutters
411
The AttaLife Cycle The AttaCaste System
426
Harvesting Vegetation
430
Communication in Atta
439
The Ant-Fungus Mutualism Hygiene in the Symbiosis Waste Management Agropredators and Agroparasites
CHAPTER 10
394
412
445 449 454 456
Leafcutter Nests
457
Trails and Trunk Routes
463
NEST ARCHITECTURE AND HOUSE HUNTING
469
The Analysis of Nest Architecture
470
How Architecture Is Achieved
473
The Process of Stigmergy House Hunting and Colony Emigration EPILOGUE
479 481
501
ACKNOWLEDGMENTS
503
GLOSSARY
505
INDEX
XIV
515
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NOTE TO THE GENERAL READER
magine that 1 million years ago, long before theorigin ofhumanity, a team of alien scientists landed on Earth to study its life-forms. Their first report would surely
include something like the following: This planet is teeming with more than 1,000 trillion highly social creatures, representing at least 20,000 species! Their final report would surely contain thefollowing key points: • Most of the highly social forms are insects (six legs, two antennae on the head, threebody parts). All live on the land, none in the sea.
• Atmaturity, each colony contains as few as 10 members toas many as 20 million members, according to species. • The members of each colony are divided into two basic castes: one or at most a small number ofreproductives and a larger number ofworkers who conduct the
labor inan altruistic manner and do not, as a rule, attempt to breed.
• In the great majority of the colonial species—namely, those belonging to the order Hymenoptera (ants, bees, wasps)—the colony members are all female.
They produce and care for males during short periods oftime prior to the mating season. The males do no work. After the mating season, any ofthese drones that remain in the nest are expelled or killed by their worker sisters.
• On the other hand, in a minority ofthe highly social species, belonging to the order Isoptera (termites), a king typically lives with the queen, the reproductive female. Unlike hymenopteran workers, those of termites often belong to both sexes, and in some species, labor is divided to some degree between the sexes.
• More than 90 percent ofthe signals used in communication by these strange colonial creatures are chemical. The substances, the pheromones, are released
XVI
from exocrine glands located in various parts of the body. When smelled or tasted by other colony members, theyevoke a particular response, such as alarm, attraction, assembly, or recruitment. Sound or substrate-borne vibrations and touch are also used by many species in communication, but ordinarily just to augment theeffects of pheromones. Some signals are complex, combining smell, taste, vibration (sound), and touch. Notable examples are the waggle dance of honeybees, the recruitment trails offire ants, andthe multimodal communication of weaver ants.
• Thesocial insects distinguish theirownnestmates from members ofothercolonies byusing receptors on theirantennae to smell the hydrocarbons in theouterlayer of their hard-shelled cuticles. They use different blends of these chemicals to identify different castes, life stages, and ages among their nestmates.
• Each colony isintegrated tightly enough byits communication system and castebased division of labor to be called a superorganism. The social organizations, however, vary greatly among the social insect species, and we can recognize
different evolutionary grades ofsuperorganismic organization. A"primitive" (less derived) grade is represented byseveral ponerine species, where members of the colony have full reproductive potential and there is considerable interindividual reproductive competition within each colony. Highly advanced grades are represented, for example, by the leafcutter ant genera Atta andAcromyrmex and the Oecophylla weaver ants, where the queen caste is the sole reproductive, and the hundreds of thousands of sterile workers occur as morphological subcastes
that are tightly integrated in division of labor systems. These societies exhibit the ultimate superorganism states, where interindividual conflict within the colony is minimal or nonexistent.
XVII
o
• The superorganism exists at a level of biological organization between the organisms thatform its units andtheecosystems, such as a forest patch, ofwhich it is a unit. This is why the social insects are important to the general study of biology.
Such isthearray ofphenomena onwhich we two Earth-born biologists will now expand. The ants, bees, wasps, and termites are among the most socially advanced nonhuman organisms ofwhich we have knowledge. In biomass and impact on eco systems, their colonies have been dominant elements of most of the land habitats
for at least 50 million years. Social insect species existed for more than an equivalent span of timepreviously, but were relatively much less common. Some of the ants, in
particular, were similar tothose living today. It gives pleasure to think that they stung or sprayed formic acid on many a dinosaur thatcarelessly trampled their nests. The modern insect societies have a vast amount to teach us today. They show how it is possible to "speak" in complex messages with pheromones. And they illus trate, through thousands of examples, how the division of laborcan be crafted with
flexible behavior programs to achieve an optimal efficiency of a working group. Their networks ofcooperating individuals have suggested new designs in computers and shed lighton how neurons of the brain might interact in the creation of mind. Theyare in many ways an inspiration. The study of ants, President Lowell, of Har vard University, said when he bestowed an honorary degree on the great myrmecologist William Morton Wheeler in the 1920s, has demonstrated that these insects, "like human beings, can create civilizations without the use of reason."
The superorganisms are the clearest window through which scientists can wit ness the emergence of one level of biological organization from another. This is important, because almost all of modern biology consists of a process of reduction of complex systems followed by synthesis. During reductive research, thesystem is
XVIII
enable members of colonies to construct complex nests with superior defensive ram parts and interior microclimate control.
Endowed with the advantages of colonial life, the social insects have managed
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to displace solitary insects, such as cockroaches, grasshoppers, and beetles, from the most favored nest sites and defensible foraging ranges. In the most general terms, social insects control the center of the land environment, while solitary insects pre-
dominate in the margins. Where social insects take territorial possession ofthe larger and more enduring spaces of the vegetation and ground, the solitary forms occupy the peripheral twigs, leaf surfaces, mudflats, and wet or very dry and crumbling por tions of dead wood. In short, solitary forms tend to prevail over social insects only in the more remote and transient of living spaces.5
THE CONSTRUCTION OF SUPERORGANISMS
Reflection on thesuccess ofsocial life allows us to address a classic question of biol ogy: How does a superorganism arisefrom the combined operation oftiny and short-lived minds? The answer is relevant to studies of lower levels of biological organization and the related question thatalso presents itself: How does an organism arisefrom the combined operation oftiny andshort-lived cells?
The object of most research conducted on social insects during the past half century can be expressed in a single phrase: the construction ofsuperorganisms. The first level ofconstruction is sociogenesis, thegrowth of thecolony by the creation of specialized castes that act together as a functional whole. Castes are created by algo rithms of development, the sequential decision rules that guide the body growth
of each colony member step by step until the insect reaches its final, adult stage. In the social hymenopterans (ants, social bees, and social wasps), the sequence is roughly as follows. At the first decision point, depending on its physiological con dition, the developing female egg or larva is shunted onto one or the other of two
paths of physical development. If the immature insect takes the path leading to more extended growth and development, it will turn into a queen upon reaching
5 | General accounts ofthe dominance ofsocial insects and the reasons for itare given in E. O. Wilson, Success and Dominance in Ecosystems: The Case ofthe Social Insects (Oldendorf/Luhe, Germany: Ecology institute, 1990); and B. HoUdobler and E.O. Wilson, The Ants (Cambridge, MA: The Belknap Press of Harvard University Press, 1990).
the adult .stage. If it takes the other path, it will curtail growth and development and end up a worker. In some species of ants, the worker-bound larva encounters a second decision point on the road to adulthood, from which one path leads it to maturity as a major worker ("soldier") and the other to maturity as a minor worker. These specialists, working together as a functional unit, are guided by sets of behavioral rules that operate in the following manner. If in a given context the worker encounters a certain stimulus, it predictably performs one act, and if the same stimalus is received in a different context, the worker performs a different act.
For example, if a hungry larva is encountered in the brood chamber, the worker offers it food; if a larva is found elsewhere, the worker carries it, whether hungry or not, to the brood chamber and places it with other larvae. And so on through
a repertory of a few dozen acts. The totality of these relatively sparse and simple responses defines the social behavior of the colony. Nothing in the brain of a worker ant represents a blueprint of the social order. There is ro overseer or "brain caste" who carries such a master plan in its head. Instead, colony life is the product of self-organization. The superorganism exists in the separaze programmed responses of the organisms that compose it. The assem bly instructions the organisms follow are the developmental algorithms, which cre ate the castes, together with the behavioral algorithms, which arc responsible for moment-to-moment behavior of the caste members.
The algorithms of caste development and behavior are the first level in the con struction of a superorganism. The second level of construction is the genetic evo
lution of the algorithms themselves. Out of all possible algorithms, generating the astronomically numerous social patterns they might produce, at least in theory, only an infinitesimal fraction have in fact evolved. The sets of algorithms actually real ized, each of which is unique in some respect to a living species, are the winners in the arena of natural selection. They exist in the world as a select group that emerged in response to pressures imposed by the environment during the evolutionary his tory of the respective species.
THE LEVELS OF ORGANIZATION
Life is a self-replicating hierarchy of levels. Biology is the study of the levels that compose the hierarchy. No phenomenon at any level can be wholly characterized without incorporating other phenomena that arise at all levels. Genes prescribe
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proteins, proteins self-assemble into cells, cells multiply and aggregate to form organs, organs arise as parts of organisms, and organisms gather sequentially into societies, populations, and ecosystems. Natural selection that targets a trait at any of these levels ripples in effect across all the others. All levels of organization are primary or secondary targets of natural selection. For example, the genes that distinguish the Africanized honeybee (or "killer bee"), which was accidentally introduced into Brazil in the 1950s, include induction of restless and aggressive behavior in workers. Under free-living conditions, Africanized colonies outcompcte those of other strains. To some extent, they also penetrate and alter wild environments, includingespecially the canopies of tropical forests. As ecosystems change by biological invasions, such as those of the Africanized honeybees, or by shifts in climate or by any other means, the relative abundances of the species composing the ecosystems also change. Some species are likely to drop out and new ones invade. As a consequence, the selection pressures on the individu als and societies are altered, with eventual consequences for the inherited traits of at least some of the species.
The dynamism of ecosystems is consequently eternal. Biological hierarchies are reverberating systems within which, depending on the histories of the species and the environmental niches theyoccupy, social order may or may not evolve. The principal target of natural selection in the social evolution of insects is the colony, while the unit of selection is the gene. Because the traits of the colony are summed products of the traits of the colony members and those traits differ geneti cally among the members, as well as from one colony to the next, the evolution of
thesocial insects is grounded in the flux ofchanging gene frequencies across genera tions. That flux in turn reflects the complex interplay of behavior both by colonies and the individual members that compose them.
EUSOCIALITY AND THE SUPERORGANISM
The sociobiology of insects is most effectively constructed with the concept of the superorganism, with reference to both its origin and evolution. Which or the insect societies deserve to be designated a superorganism? In the broadest sense, the term superorganism is appropriate for any insect colony that is eusocial, or "truly social," and that means combining three traits: first, its adult members are divided into reproductive castes and partially or wholly nonrcproductive workers; second, the
