Upload
gabriel-andrus
View
66
Download
2
Embed Size (px)
DESCRIPTION
Eusocial animals
Citation preview
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)
k^c
^•-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
All rights reservedPrinted in the United States ofAmerica
First Edition
For information aboutpermission to reproduce selections from thisbook,writetoPermissions, W. W. Norton & Company, Inc., 500 Fifth Avenue, NewYork, NY 10110
For information aboutspecial discounts for bulk purchases, please contactW W. Norton Special Sales at [email protected] or 800-233-4830
Manufacturing by RR Donnelley, Willard, OHBookdesign by AbbateDesignProduction manager: Anna Oler
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
1234567890
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
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 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
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-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
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
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
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 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.
XVII
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
XVIII
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
T
in
z
<oa
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 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