THE

r

The Beauty, Elegance, and Strangeness of Insect Societies

Bert Holldobler and E. O.WilsonWINNERS 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', withMartinLindauer, editors (1985)

Herbivory ofLeafCuttingAnts, 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, withWilliam 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, withCharles 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 HyperdiverseAntGenus (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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^•-nfrti"1

Frontispiece: Plate 1.Weaver ants (Oecophylla smaragdina) cooperate inarranging leaves during the construction of theirleaftent nests.Copyright© 2009 by BertHoUdobler and Edward O. Wilson

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Library of Congress Cataloging-in-Publication Data

HoUdobler, Bert, 1936-

The superorganism : the beauty, elegance, andstrangeness of insect societies / BertHoUdoblerand Edward O. Wilson ; linedrawings 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 2009595.7'1782—dc22

2008038547

W. W. Norton & Company, Inc.500 Fifth Avenue, New York, N.Y. 10110

www.wwnorton.com

W. W. Norton & Company Ltd.Castle House, 75/76 Wells Street, London WIT 3QT

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FOR MARTIN LINDAUER, our colleague andfriend, whosepioneering work andinspiration inexperimentalsociobiobgy contributedgreatly to the conception ofaninsect society as afunctional superorganism

Let him who boasts the knowledge of

actually existing things, first tellusof the

nature of the ant.

-ST. BASIL

CONTENTS

NOTE TO THE GENERAL READER

CHAPTER 1 THE CONSTRUCTION OF A SUPERORGANISM

Why ColoniesAreSuperior

The Construction of Superorganisms

The Levels of Organization

Eusociality and the Superorganism

A BriefHistoryof Insect Sociobiology

CHAPTER 2 GENETIC SOCIAL EVOLUTION

AnAbridged History of theGenetic Theory ofSocial EvolutionMultilevel Natural Selection

The Evolution of Eusociality

Crossing the Eusociality Threshold

Countervailing Forces of Selection

Passing the Point of No Return

CHAPTER 3 SOCIOGENESIS

The Colony Life Cycle

Social Algorithms

Self-Organization and EmergencePhylogenetic Inertiaand Dynamic Selection

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CHAPTER 4 THE GENETIC EVOLUTION OF DECISION RULES

The Genetic Origin andFurther Evolution ofEusocialitySociogenetics and Sociogenomics

Honeybee Sociogenomics

Sociogenomic Conservation

The Fire Ant Case

Genetic Variation and Phenotypic Plasticity

CHAPTER 5 THE DIVISION OF LABOR

Parallels: Organism andSuperorganismThe Ecology of Caste Systems

The Evolution of Caste: Principles

Dominance Orders in Caste Determination

Temporal Castes

The Physiology ofTemporal Castes

GeneticVariability in Caste Differentiation

Memory in Division of Labor

Task Switching and Behavior Plasticity

Child Labor

Genetic Caste Determination

Nongenetic Caste Determination

Worker Subcastes

The Physiology and Evolution of Physical CastesAdaptive Demography

Teamwork

The Larger Picture

CHAPTER 6 COMMUNICATION

Dance Communication in Honeybees

Communication in Ant Societies

The Evolution ofAnt Recruitment Signals andTrail GuidesDesign and Functional Efficiency of Pheromones

Behavioral Modes of Recruitment Communication

The Extreme Multiple Recruitment System ofWeaver AntsMultimodal Signals, Parsimony, and Ritualization

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Message and Meaning

Modulatory Communication

Motor Displays in Recruitment Communication

Environmental Correlates of Recruitment Systems

The Measurement of Information

TactileCommunication and Trophallaxis

The Social Bucket

Visual Communication

Anonymity and Specificity of Chemical Signals

Necrophoric Behavior

Nestmate Recognition

Within-Colony Recognition

Recognition of Brood

Communicating Resource-Holding Potential AmongColonies

Conclusion

CHAPTER 7 THE RISE OF THE ANTS

The Origin of Ants

The Early Radiation of the Ants

The Cenozoic Radiation

The Ponerine Paradox

The Tropical Arboreal Ants

The Dynastic-Succession Hypothesis

CHAPTER 8 PONERINE ANTS: THE GREAT RADIATION

The Social Regulation of Reproduction

Harpegnathos: Life Cycle ofa Colonial ArchitectDinoponera: Giant "Worker Queens"

Queens, Workers, Gamergates in Permutations

Diacamma: Regulating Reproduction byMutilationStreblognathus-. Dominance and Fertility Uncoupled

Gamergates versus Ergatoid Queens

Pachycondylafochi: Mass Termite Raiders

Ergatoid Queensand Army Ants

Pachycondyla: Sociobiologically the Most Diverse Ant Genus

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Platythyreapunctata: Extreme Plasticity in Reproduction

Aggression and Dominance: Origin and Loss

Harpegnathos: Resilience in Reproductive Behavior

Colony Size asan Ecological Adaptation

Pachycondyla: Hyperdiversity Summarized

CHAPTER 9 THE ATTINE LEAFCUTTERS:

THE ULTIMATE SUPERORGANISMS

The Attine Breakthrough

The Ascent of the Leafcutters

The AttaLifeCycle

The AttaCaste System

Harvesting Vegetation

Communication in Atta

The Ant-Fungus Mutualism

Hygiene in the Symbiosis

Waste Management

Agropredators and Agroparasites

Leafcutter Nests

Trails and Trunk Routes

CHAPTER 10 NEST ARCHITECTURE AND HOUSE HUNTING

The Analysis of NestArchitecture

How Architecture Is Achieved

The Process of Stigmergy

HouseHunting and Colony Emigration

EPILOGUE

ACKNOWLEDGMENTS

GLOSSARY

INDEX

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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 surelyinclude something like the following: This planet is teeming with more than 1,000trillion highly social creatures, representing at least 20,000 species! Their final reportwould surely contain thefollowing key points:

• Most of the highly social forms are insects (six legs, two antennae on the head,threebodyparts). All live on the land, none in the sea.

• Atmaturity, each colony contains as few as 10 members toas many as 20 millionmembers, according to species.

• The members ofeach colony are divided into two basic castes: oneor at most asmall number ofreproductives and a larger number ofworkers who conduct thelabor inan altruistic manner and do not, as a rule, attempt tobreed.

• In the great majority of the colonial species—namely, those belonging to theorder Hymenoptera (ants, bees, wasps)—the colony members are all female.They produce and care for males during short periods oftime prior to the matingseason. The males do no work. After the mating season, any ofthese drones thatremain in the nest are expelled or killed by their worker sisters.

• On the other hand, in a minority ofthe highly social species, belonging to theorder Isoptera (termites), a king typically lives with the queen, the reproductivefemale. Unlike hymenopteran workers, those of termites often belong to bothsexes, and in some species, labor is divided to some degree between the sexes.

• More than 90 percent of the signals used in communication by these strangecolonial creatures are chemical. The substances, the pheromones, are released

XVI

from exocrine glands located in various parts of the body. When smelled ortasted byothercolony 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 ofpheromones. Some signals are complex, combining smell,taste, vibration (sound), and touch. Notable examples are the waggle dance of

honeybees, the recruitment trails offire ants, andthemultimodal communication

ofweaver ants.

• Thesocial insects distinguish theirownnestmates from members ofothercolonies

byusing receptors on theirantennae to smell thehydrocarbons 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 andcaste-based 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 thecolony have full reproductive potential and there is considerable interindividualreproductive competition within each colony. Highly advanced grades are

represented, for example, by the leafcutter ant genera Atta andAcromyrmex andthe Oecophylla weaver ants, where the queen caste is the sole reproductive, andthe 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.

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o • The superorganism exists at a level of biological organization between theorganisms thatform its units andtheecosystems, such as a forest patch, ofwhichit is a unit. This is why the social insects are important to the general study ofbiology.

Such isthearray ofphenomena onwhich we two Earth-born biologists will nowexpand. The ants, bees, wasps, and termites are among the most socially advancednonhuman organisms ofwhich we have knowledge. In biomass and impact on ecosystems, 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 anequivalentspan of timepreviously, but were relatively much less common. Some of the ants, in

particular, were similar tothose living today. Itgives pleasure to think that they stungor sprayed formic acid on many a dinosaur thatcarelessly trampled their nests.

The modern insect societies have a vast amount to teach us today. They showhow it is possible to "speak" incomplex messages with pheromones. And they illustrate, through thousands of examples, howthe 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 incomputersand 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 Harvard University, said when he bestowed an honorary degree on thegreat myrmecol-ogist William Morton Wheeler in the 1920s, has demonstrated that these insects,

"likehuman beings, can create civilizations without the useof reason."

The superorganisms are theclearest window through which scientists can witness the emergence of one level of biological organization from another. This isimportant, because almost all of modern biology consists of a process of reductionof complex systems followed by synthesis. During reductive research, thesystem is

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enable members ofcolonies to construct complex nests with superior defensive ram

parts and interior microclimate control.

Endowed with the advantages of colonial life, the social insects have managedto displace solitary insects, such as cockroaches, grasshoppers, and beetles, from themost favored nest sites and defensible foraging ranges. In the most general terms,

w 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 occupythe peripheral twigs, leaf surfaces, mudflats, and wet or very dry and crumbling portions of dead wood. In short, solitary forms tend to prevail over social insects onlyin 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 biology: How does asuperorganism arisefrom the combined operation oftiny andshort-livedminds? The answer is relevant to studies of lower levels of biological organizationand the related question thatalso presents itself: How does an organism arisefrom thecombined operation oftiny andshort-lived cells?

The object of most research conducted on social insects during the past halfcentury can be expressed in a single phrase: the construction ofsuperorganisms. Thefirst level ofconstruction is sociogenesis, thegrowth of thecolony by the creation ofspecialized castes that act together as a functional whole. Castes are created by algorithms of development, the sequential decision rules that guide the body growthof 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 isroughly as follows. At the first decision point, depending on its physiological condition, 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 tomore extended growth and development, it will turn into a queen upon reaching

5| General accounts ofthe dominance ofsocial insects and the reasons for it are given in E. O.Wilson, Success andDominance in Ecosystems: The Case ofthe Social Insects (Oldendorf/Luhe, Germany: Ecology institute, 1990); andB. 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 H

X

mend up a worker. In some species of ants, the worker-bound larva encounters a sec- oo

ond decision point on the road to adulthood, from whichone path leads it to matu- z

rity 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 9.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 o

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 behaviorof 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 theastronomically 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 worldas 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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z> primary or secondary targets of natural selection. For example, the genes that dis-

lu tinguish the Africanized honeybee (or "killer bee"), which was accidentally intro-i

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

duced 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 byshifts in climate or byanyother 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 arealtered, with eventual consequences for the inherited traits of at

least someof the species.

The dynamism of ecosystems is consequently eternal. Biological hierarchies arereverberating systems within which, depending on the histories of the species and

the environmental niches theyoccupy, social order mayor 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 theflux ofchanging gene frequencies across generations. That flux in turn reflects the complex interplay of behavior both by coloniesand 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