THE

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)
k^c

^•-nfrti"1
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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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 XVI

CHAPTER 1 THE CONSTRUCTION OF A SUPERORGANISM

Why Colonies Are Superior 5

The Construction of Superorganisms 6

The Levels of Organization 7

Eusociality and the Superorganism 8

A BriefHistory of Insect Sociobiology 10

CHAPTER 2 GENETIC SOCIAL EVOLUTION 15

AnAbridged History of the Genetic Theory ofSocial Evolution 16

Multilevel Natural Selection 24

The Evolution of Eusociality 29

Crossing the Eusociality Threshold 31

Countervailing Forces of Selection 42

Passing the Point of No Return 42

CHAPTER 3 SOCIOGENESIS 51

The Colony Life Cycle 53

Social Algorithms 53

Self-Organization and Emergence 58

Phylogenetic Inertiaand Dynamic Selection 60

CHAPTER 4 THE GENETIC EVOLUTION OF DECISION RULES 69

The Genetic Origin and Further Evolution of Eusociality 70

Sociogenetics and Sociogenomics 71

Honeybee Sociogenomics 73

Sociogenomic Conservation 75

The Fire Ant Case 77

Genetic Variation and Phenotypic Plasticity 79

CHAPTER 5 THE DIVISION OF LABOR 83

Parallels: Organism and Superorganism 84

The Ecology of Caste Systems 85

The Evolution of Caste: Principles 89

Dominance Orders in Caste Determination 93

Temporal Castes 97

The Physiology ofTemporal Castes 103

Genetic Variability in Caste Differentiation 116

Memory in Division of Labor 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 147

Adaptive Demography 152

Teamwork 159

The Larger Picture 164

CHAPTER 6 COMMUNICATION 167

Dance Communication in Honeybees 169

Communication in Ant Societies 178

The Evolution ofAnt Recruitment Signals andTrail Guides 183

Design and Functional Efficiency of Pheromones 206

Behavioral Modes of Recruitment Communication 214

The Extreme Multiple Recruitment System of Weaver Ants 218

Multimodal Signals, Parsimony, and Ritualization 221

XII
 Message and Meaning 229

Modulatory Communication 231

Motor Displays in Recruitment Communication 235

Environmental Correlates of Recruitment Systems 247

The Measurement of Information 251

Tactile Communication and Trophallaxis 252

The Social Bucket 259

Visual Communication 267

Anonymity and Specificity of Chemical Signals 270

Necrophoric Behavior 273

Nestmate Recognition 275

Within-Colony Recognition 288

Recognition of Brood 299

Communicating Resource-Holding Potential AmongColonies 301

Conclusion 309

CHAPTER 7 THE RISE OF THE ANTS 313

The Origin of Ants 315

The Early Radiation of the Ants 318

The Cenozoic Radiation 320

The Ponerine Paradox 322

The Tropical Arboreal Ants 328

The Dynastic-Succession Hypothesis 330

CHAPTER 8 PONERINE ANTS: THE GREAT RADIATION 333

The Social Regulation of Reproduction 334

Harpegnathos: Life Cycle of a Colonial Architect 336

Dinoponera: Giant "Worker Queens" 355

Queens, Workers, Gamergates in Permutations 364

Diacamma: Regulating Reproduction by Mutilation 366

Streblognathus-. Dominance and Fertility Uncoupled 373

Gamergates versus Ergatoid Queens 376

Pachycondylafochi: Mass Termite Raiders 378

Ergatoid Queens and Army Ants 380

Pachycondyla: Sociobiologically the Most Diverse Ant Genus 382

XIII
 Platythyreapunctata: Extreme Plasticity in Reproduction 394

Aggression and Dominance: Origin and Loss 397

Harpegnathos: Resilience in Reproductive Behavior 397

Colony Size as an Ecological Adaptation 398

Pachycondyla: Hyperdiversity Summarized 404

CHAPTER 9 THE ATTINE LEAFCUTTERS:

THE ULTIMATE SUPERORGANISMS 407

The Attine Breakthrough 408

The Ascent of the Leafcutters 411

The AttaLife Cycle 412

The AttaCaste System 426

Harvesting Vegetation 430

Communication in Atta 439

The Ant-Fungus Mutualism 445

Hygiene in the Symbiosis 449

Waste Management 454

Agropredators and Agroparasites 456

Leafcutter Nests 457

Trails and Trunk Routes 463

CHAPTER 10 NEST ARCHITECTURE AND HOUSE HUNTING 469

The Analysis of Nest Architecture 470

How Architecture Is Achieved 473

The Process of Stigmergy 479

House Hunting and Colony Emigration 481

EPILOGUE 501

ACKNOWLEDGMENTS 503

GLOSSARY 505

INDEX 515

XIV
< 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 caste-
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 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 myrmecol-
ogist 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
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,
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 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 H
X

m
end up a worker. In some species of ants, the worker-bound larva encounters a sec- o
o
ond decision point on the road to adulthood, from which one 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
T

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
in
proteins, proteins self-assemble into cells, cells multiply and aggregate to form
z
<
organs, organs arise as parts of organisms, and organisms gather sequentially into
o
a societies, populations, and ecosystems. Natural selection that targets a trait at any
O

LU
of these levels ripples in effect across all the others. All levels of organization are
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
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 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