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: AStory ofScientific Exploration (1994)
ALSO BY BERT HOLLDOBLER
Experimental Behavioral Ecology and Sociobiology', withMartinLindauer, editors
(1985)
Herbivory ofLeafCuttingAnts, withRainer Wirth, Hubert Herz, Ronald J. Ryel,
and Wolfram Beyschlag (2003)
ALSO BY EDWARD O. WILSON
The Theory ofIslandBiogeography, with Robert H. MacArthur (1967); new preface, 2001
APrimer ofPopulation Biology, withWilliam H. Bossert (1971)
TheInsect Societies (1971)
Sociobiology: The New Synthesis (1975); new edition, 2000
OnHumanNature (1978); Pulitzer Prize, General Nonfiction, 1979
Caste andEcology inthe 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 inEcosystems: 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: AHyperdiverseAnt 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 Bert HoUdobler andEdward O. Wilson
All rightsreserved
Printed in the United States of America
First Edition
For information about permission to reproduce selections from thisbook, writeto
Permissions, W. W. Norton& Company, Inc., 500Fifth Avenue, NewYork, NY 10110
For information aboutspecial discounts for bulk purchases, please contact
W W. Norton Special Sales at specialsales@wwnonon.com or 800-233-4830
Manufacturing by RR Donnelley, Willard, OH
Bookdesign 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 ; 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 2009
595.7'1782dc22
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
1234567890
FOR MARTIN LINDAUER, our colleague andfriend, whose
pioneering work andinspiration inexperimental
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.
-ST. BASIL
CONTENTS
NOTE TO THE GENERAL READER
CHAPTER 1 THE CONSTRUCTION OF A SUPERORGANISM
Why Colonies AreSuperior
The Constructionof Superorganisms
The Levels of Organization
Eusociality and the Superorganism
ABriefHistoryof Insect Sociobiology
CHAPTER 2 GENETIC SOCIAL EVOLUTION
AnAbridged History of theGenetic Theory ofSocial Evolution
Multilevel Natural Selection
The Evolution of Eusociality
Crossing the Eusociality Threshold
Countervailing Forces of Selection
Passing the Point of No Return
CHAPTER 3 SOCIOGENESIS
The ColonyLife Cycle
Social Algorithms
Self-Organization and Emergence
Phylogenetic Inertiaand Dynamic Selection
XVI
5
6
7
8
10
15
16
24
29
31
42
42
51
53
53
58
60
CHAPTER 4 THE GENETIC EVOLUTION OF DECISION RULES
The Genetic Origin andFurther Evolution of Eusociality
Sociogenetics and Sociogenomics
Honeybee Sociogenomics
Sociogenomic Conservation
The Fire Ant Case
Genetic Variation and Phenotypic Plasticity
CHAPTER 5 THE DIVISION OF LABOR
Parallels: Organism andSuperorganism
The Ecology of Caste Systems
The Evolution of Caste: Principles
Dominance Orders in Caste Determination
Temporal Castes
The Physiology ofTemporal Castes
GeneticVariability in CasteDifferentiation
Memory in Divisionof Labor
Task Switching and Behavior Plasticity
Child Labor
Genetic Caste Determination
Nongenetic Caste Determination
Worker Subcastes
The Physiology andEvolution of Physical Castes
Adaptive Demography
Teamwork
The Larger Picture
CHAPTER 6 COMMUNICATION
Dance Communication in Honeybees
Communication in Ant Societies
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
69
70
71
73
75
77
79
83
84
85
89
93
97
103
116
117
120
125
129
136
139
147
152
159
164
167
169
178
183
206
214
218
221
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-ColonyRecognition
Recognition of Brood
Communicating Resource-Holding Potential AmongColonies
Conclusion
CHAPTER 7 THE RISE OF THE ANTS
The Origin of Ants
The EarlyRadiation 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 of a Colonial Architect
Dinoponera: Giant "Worker Queens"
Queens, Workers, Gamergates in Permutations
Diacamma: Regulating Reproduction byMutilation
Streblognathus-. Dominance and Fertility Uncoupled
Gamergates versus Ergatoid Queens
Pachycondylafochi: Mass Termite Raiders
Ergatoid Queensand Army Ants
Pachycondyla: Sociobiologically theMost Diverse Ant Genus
XIII
229
231
235
247
251
252
259
267
270
273
275
288
299
301
309
313
315
318
320
322
328
330
333
334
336
355
364
366
373
376
378
380
382
Platythyreapunctata: Extreme Plasticity in Reproduction
Aggression and Dominance: Origin and Loss
Harpegnathos: Resilience in Reproductive Behavior
ColonySize as an 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
HarvestingVegetation
Communication in Atta
The Ant-Fungus Mutualism
Hygiene in the Symbiosis
WasteManagement
Agropredators and Agroparasites
Leafcutter Nests
Trails and Trunk Routes
CHAPTER 10 NEST ARCHITECTURE AND HOUSE HUNTING
The Analysis of Nest Architecture
How Architecture Is Achieved
The Process of Stigmergy
HouseHunting and Colony Emigration
EPILOGUE
ACKNOWLEDGMENTS
GLOSSARY
INDEX
XIV
394
397
397
398
404
407
408
411
412
426
430
439
445
449
454
456
457
463
469
470
473
479
481
501
503
505
515
< NOTE TO THE GENERAL READER
magine that 1million 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,
threebodyparts). 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 tospecies.
The members of each colony are divided intotwo basic castes: oneor 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 tobreed.
In the great majority of the colonial speciesnamely, 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 byother colony members, theyevoke a particular response, such as alarm,
attraction, assembly, or recruitment. Sound or substrate-borne vibrations
and
touch are also used by manyspecies 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, andthemultimodal communication
of weaver 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, andages 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 the
colony have full reproductive potential and there is considerable interindividual
reproductive competition within each colony. Highly advanced grades
are
represented, for example, bythe 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 that form 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 andimpact oneco
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
anequivalent
span of timepreviously, but were relatively much less common. Some of the ants, in
particular, were similar tothose living today. It gives pleasure tothink that they
stung
or sprayed formic acid onmany adinosaur that carelessly trampled their nests.
The modern insect societies have a vast amount to teach us today. They show
how it is possible to"speak" incomplex messages with pheromones. And they illus
trate, throughthousands of examples, howthe division of laborcanbe crafted with
flexible behavior programs to achieve an optimal efficiency of a working
group.
Their networks ofcooperating individuals have suggested new designs incomputers
andshed lighton how neurons of the brain might interact in the creation of mind.
Theyare in many ways an inspiration. Thestudy of ants, President Lowell, of Har
vard University, said when he bestowed an honorary degree on thegreat myrmecol-
ogist WilliamMorton Wheeler in the 1920s, has demonstrated that these insects,
"likehuman beings, cancreate civilizations without the useof reason."
Thesuperorganisms are theclearest 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 toaddress aclassic question of
biol
ogy: Howdoes asuperorganism arisefrom the combinedoperation oftiny andshort-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 it are
given in E. O. Wilson, Success and
Dominance inEcosystems: 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 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 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
blyinstructions 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 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
T
in
z
<
o
a
O
LU
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 inductionof 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 newones 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 are
reverberating 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 intheflux 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