The Social Biology of Ropalidia marginata

TOWARD UNDERSTANDING

THE EVOLUTION OF

EU SOCIALITY

Raghavendra Gadagkar

HARVARD UNIVERSITY PRESS

Cambridge, Massachusetts 111< London, England 111< 2001

Copyright © 2001 by the President and Fellows of Harvard CollegeAll rights reservedPrinted in the United States of America

Library of Congress Cataloging-in-Publication Data

Gadagkar, Raghavendra.The social biology of Ropalidia marginata :toward understanding the evolution of eusociality / Raghavendra Gadagkar.

p.cm.Includes bibliographical references (p. ).ISBN 0-674-00611-9 (hardcover: alk. paper)1. Ropalidia marginata-Behavior.2. Insect societies. I. TitleQLS68.VS G34 2001595.79'8---<ic212001024420

CONTENTS

Preface

PART I Introduction

1 A Primer of Eusociality

2 In Praise of Ropalidia

p ART II Social Biology

ix

3

27

3 Some Methodological Necessities 35

4 Natural History 52

5 Behavioral Caste Differentiation 75

6 Dominance Behavior and Regulation of Worker Activity 98

7 Age and Division of Labor 128

PART III The Evolution ofEusodality

8 The Theoretical Framework 151

9 Genetic Predisposition I: Intracolony Genetic Relatedness 159

10 Genetic Predisposition II: Kin and Nestmate Recognition 180

11 Ecological Predisposition 216

12 Physiological Predisposition 234

13 Demographic Predisposition 248

14 Synthesis 267

15 Factors That Remain t'o Be Explored 276

viii Contents

PART IV Beyond Ropalidia marginata: Social Evolution, Forward and Reverse

16 A Route to Sociality

17 The Evolution of Caste Polymorphism

18 Reverse Social Evolution

Summary

References

Index

J

293

299

313

321

329

361

PREFACE

~ y most pleasant childhood memories are of collecting insects and tadpoles and watching them metamorphose and staring at drops of pond water under my uncle's microscope in his veterinary hospital. My interest

in insects persisted through my teenage years, and eventually I decided to study zoology. While in college, I read with fascination King Solomon's Ring by Konrad Lorenz and The Double Helix by James Watson, and became equally interested in animal behavior and molecular biology. But it did not occur to me that these two subjects could be considered opposite ends of the spectrum in biology.

During the five years that I spent earning my bachelor's and master's de­grees in zoology at what was then called Central College, in Bangalore, In­dia, I continued to observe insects: I spent many hours watching, with great curiosity, the wasp colonies that were on every window sill, but could not identify the wasps. For my Ph.D., I applied to the Indian Institute of Science, arguably the best place in Incfu to pursue scientific research. The Institute did not have a program in animal behavior, but it offered me the only slot available to study what was then called interdisciplinary molecu­lar biology. For the next five years I greatly enjoyed studying the mecha­nisms of interaction between bacteria and bacteriophages.

On my first day at what was then the Microbiology and Pharmacology Laboratory, I was assigned a desk on which somebody had left a copy of India's premier science magazine, Current Science, dated 5 August 1974. Opening it casually, I saw an article entitled "Caste differentiation in the paper wasp Ropalidia marginata (Lep.):' by M. Gadgil and A. Mahabal.

x Preface

After reading the paper, I suspected that the wasps [ had watched in the Zoology Department of Central College were Ropalidia marginata. Gadgil was at the Centre for Theoretical Studies in the Indian Institute of Science, and I had met him briefly at the previous year's meeting of the Ethological Society of India. I sought him out to tell him that [ knew of what I thought

was a population of the paper wasps that he was studying. We went to Central College on his scooter early the next Sunday morning, and he con­firmed that the wasps were indeed Ropalidia marginata, but disappointed me by saying that he no longer studied them. But then he said, "if you are interested, however, I can help you study them."

Thus I began to study Ropalidia marginata, by observing the colonies at

Central College and also by keeping some colonies in the Microbiology and Pharmacology Laboratory. But I could pursue these studies only as a hobby since I had just begun the Ph.D. program in molecular biology. Most of my wasp watching had to be done on weekends. But even so, my interest in these insects led me to explore behavioral ecology and socio­

biology and to read the works of W. D. Hamilton, E. 0. Wilson, and other leaders in those fields. Thanks to Gadgil, and to the patience and under­standing of my two supervisors, T. Ramakrishnan and K. P. Gopinathan, I was able to pursue my dual interests in molecular biology and animal be­havior.

In 1979, when I had obtained my Ph.D. and had decided to make the study of animal behavior and ecology my profession, I met Mary Jane West-Eberhard when she came to Bangalore. She taught me how to indi­vidually mark the wasps and make behavioral observations, an experience

which I cherish. The Centre for Theoretical Studies at the Indian Institute of Science offered me a research associateship for one year to analyze my data on Ropalidia marginata and write up the results. But Mary Jane West­Eberhard's visit had inspired me to begin new observations and my asso­ciateship was renewed repeatedly. I will always remain grateful to Madhav Gadgil, H. Sharat Chandra, E. C. G. Sudarshan, N. Mukunda, R. Rajara­

man, and others at the Centre for Theoretical Studies for believing in me. This book is the story of my adventures with Ropalidia marginata dur­

ing the last twenty years, of my dream of understanding the evolution of that pinnacle of social life in animals, eusociality. I begin the book with a primer of eusociality, show why social insects should be studied, and point out the benefits of studying my genus of choice-Ropalidia---and my spe-

Preface xi

des of choice, R. marginata. In the second part, I discuss general aspects of the social biology of R. marginata, including nesting biology, behavioral caste differentiation, dominance behavior, and age polyethism. The third part focuses directly on the evolution of eusociality. Beginning with a brief account of the theoretical framework adopted, I explore the genetic, eco­

logical, physiological, and demographic factors that influence the evolu­tion of eusociality. I wrap up this part with a first-approximation unified model that integrates various factors that influence the inclusive fitness of workers and solitary nesters, and point out the factors that remain to be considered. In the fourth part, I end with a discussion of some general is­sues, perhaps the most important of which is the possibility of reversal of social evolution.

Much of the work described here is the result of collaboration with many gifted students and colleagues: Maulishree Agrahari, H. S. Arathi, Seetha Bhagavan, J. T. Bonner, Partiba Bose, Swarnalatha Chandran, K. Chandrashekara, Madhav Gadgil, A. P. Gore, N. V. Joshi, Sujatha Kardile, A. S. Mahabal, Rashmi Malpe, K. Muralidharan, Padmini Nair, Dhrubajyothi Naug, Sumana Rao, Sudha Premnath, M. S. Shalla, Mallikarjun Shakarad, A. Shanubhogue, Anindya Sinha, Thresiamma Varghese, Arun Venkataraman, and C. Vmutha. I thank them for their friendship and their collaboration. This is our collective story and I have the privilege of being the spokesman.

Several people provided technical help while the research described in this book was being conducted: Doddaiah, Augustin Dorairaj, S. Ganesh, G. Jayashree, Milind Kolatkar, Sheela Menon, N. Murugeshachar, Padmini Nair, Sai Prabha, M. Ramachandran, Preeti Roy, N. Roopa, U. N. Shyamala, S. Uma, D. Vasantha, V. Venkatesh, C. Vinutha, and Harry William. I thank all of them. In writing this book, I have been ably assisted by Swarnalatha Chandran, who word-processed most of the innumerable drafts, and by Milind Kolatkar, who meticulously prepared all the illustrations at times when most human beings should be, and were, asleep.

I owe a special debt of gratitude to my wife, Geetha, and my son, Vikram, for admitting Ropalidia marginata into our family-we have had colonies all over our home, our newly built house was christened Ropalidia, and of course we have never ceased to talk about these wasps. Geetha has, on more than one occasion, cared for and fed hundreds of wasps when I was away from home.

xii Prefac.e

am grateful to Michael Fisher, Ann Downer-Hazell, and Nancy

Clemente of Harvard University Press for waiting with patience for the

manuscript to be delivered and for sending encouraging e-mails from time

to time. It has been a pleasure to work with them.

The following people read and commented on one or more chapters in

the book or on one or more research papers on which this book is based: J.

Altmann, S. A. Barnett, Sam Beshers, J. T. Bonner, R. M. Borges, S. Braude,

M. D. Breed, M. V. Brian, H. S. Chandra, E. L. Charnov, D. Cherix, M. Col­let, E. C. Cox, B. J. Crespi, R. H . Crozier, R. Dawkins, W. G. Eberhard, G. C.

Eickwort, W. Fortelius, N. Franks, M. Gadgil, S. Gadgil, G. J. Gamboa, W. Getz, D. Gordon, A. P. Gore, D. Haig, W. D. Hamilton, J. Heinze, J. M. Herbers, B. Holldobler, J. H. Hunt, Y. It6, R. L. Jeanne, Amitabh Joshi, N. V.

Joshi, L. Keller, W. Kirchner, B. Konig, M. Lehrer, E. G. Leigh, Jr., H. K.

Macwilliams, R. W. Matthews, C. D. Michener, V. Nanjundiah, P. Nonacs,

K. C. Noonan, i. Packer, P. Pamilo, C. Peeters, D. C. Queller, R. Rajase­

kharan, A. Stanley Rand, Photon Rao, Sumana Rao, H. K. Reeve, G. Robin­

son, K. G. Ross, D. W. Roubik, S. F. Sakagami, T. D. Seeley, K. Slessor, C. K. Starr, D. L. Stern, B. L. Thorne, K. Tsuji, S. Turillazzi, W. T. Wcislo, J. W. Wenzel, M. J. West-Eberhard, D. E. Wheeler, E. 0 . Wtlson, D. Windsor, M.

Winston, and D. Yanega. In the early stages of my work 0. W. Richards and J. van der Vecht helped identify specimens and patiently answered many

questions. I take this opportunity to thank all of them for their kindness. I thank J. M. Carpenter and J. W. Wenzel for granting permission to re­

produce certain illustrations. The following gave permission to reproduce

illustrations for which they hold the copyright: Academic Press, Birkhauser

Publishing Ltd., Blackwell Science Ltd., Cornell University Press, Indian

Academy of Sciences, Indian National Science Academy, Kluwer Academic/ Plenum Publishers, Oxford University Press, Springer-Verlag GmbH & Co.

KG, and the Royal Society of London.

While writing this book, I was first a Homi Bhabha Fellow, then a B. P.

Pal National Environment Fellow, and finally a Schering Fellow at the

Wissenschaftskolleg. I am happy to record my appreciation to the Homi

Bhabha Fellowships Council, the Ministry of Environment and Forests,

and the Schering Foundation and the Wissenschaftskolleg zu Berlin for

their generosity. My research has been generously supported by the De­

partment of Science and Technology, the Ministry of Environment and

Forests, the Department of Biotechnology, the Council for Scientific and

Preface xiii

Industrial Research, the Indian National Science Academy, the Jawaharlal Nehru Centre for Advanced Scientific Research, and the Centre for Theo­retical Studies and the Centre for Ecological Sciences of the Indian Insti­tute of Science. I am grateful to the authorities of all these organizations. I especially thank the successive directors of the Indian Institute of Science, S. Dhawan, S. Ramaseshan, C. N. R. Rao, G. Padmanaban, and Goverdhan

Mehta, for creating and sustaining an inspiring academic atmosphere. I hope to continue to study Ropalidia marginata and Ropalidia cyathi­

formis, and to continue to explore the evolutionary forces that influence

the balance between cooperation and conflict in these remarkable wasps. I would therefore welcome queries and comments from readers and potential social insect researchers; I can be reached by e-mail at < ragh@ces.iisc.ernet.in >.

SUMMARY

jiff oc1AL insects provide a unique opportunity to explore the ecological

consequences of sociality and to study the origin and evolution of social life in animals. Social insects exhibit great variety, not only in their life cy­

cles and habits but also in the extent of development of their social organi­zation, social integration, and division of labor. To deal with this social di­versity, various levels of sociality are recognized. The most highly evolved stage in social evolution is the eusocial; it is characterized by overlap of generations, cooperative brood care, and reproductive caste differentia­tion. Among insects, eusociality is seen in the hymenopteran families Formicidae (ants), Vespidae (wasps), Apidae (bees), Sphecidae (in the ge­nus Microstigmus), and Halictidae (sweat bees). Outside the Hymenoptera, eusociality is shown by all species of Isoptera (termites) and some species in the orders Hemiptera (aphids), Coleoptera (ambrosia beetles), Thysa­noptera (thrips) and class Crustacea (marine shrimp). There is also the now famous eusocial mammal, the naked mole rat.

Social insects are excellent model systems for the study of altruism. Re­productive caste differentiation implies that the worker castes of social in­sects behave altruistically inasmuch as they remain sterile and work for the welfare of their colonies. Such altruism was considered paradoxical until W. D. Hamilton proposed the theory of inclusive fitness. This idea, most conveniently expressed as Hamilton's rule, provides a powerful theoretical framework for investigating the evolution of eusociality and thus the evo­lution of altruism.

Among eusocial species, the primitively eusocial ones hold special promise because in these species queens and workers are not morphologi­cally differentiated and workers usually retain some reproductive options.

322 Summary

In many species new nests are founded either by a single female or by groups of females in which only one or a small number reproduces and the rest function as workers. By comparing the solitary and social nesting strategies within the same species researchers can measure the costs and benefits of social life. The social wasp genus Ropalidia has long been con­sidered crucial to understanding the evolution of hymenopteran sociality because it contains both independent-founding, primitively eusocial spe­cies that build small open nests and exhibit no morphological caste differ­entiation and swarm-founding, highly eusocial species that often build large, enveloped nests and may exhibit considerable queen-worker dimor­phism.

R. marginata, a primitively eusocial species occurring in the tropical cli­mate of southern India and exhibiting a perennial, indeterminate colony­founding cycle, is particularly attractive for studies of the evolution of eusociality. As in many other species, new nests are initiated by one or a small number of female wasps. The nest is made of paper_ carton whose hexagonal cells are used to rear brood. All colonies are strictly monog­ynous at any given time. Males eclosing on the nest leave within a few days to lead a nomadic life, mate, and die. Eclosing female wasps, however, have a number of options open to them; they may leave to found new nests by themselves or along with other wasps, they may remain in the natal nest and work for its welfare for the rest of their lives, or they may work for some time and then at an opportune movement drive away the original queen and become replacement queens.

Behavioral observations of individually marked wasps reveal a great deal of interindividual variability. Multivariate statistical analysis of time-activ­ity budgets reveals behavioral caste differentiation of the wasps in a colony into sitters, fighters, and foragers. Sitters are relatively docile individuals that do little or no foraging and participate in little or no dominance inter­actions, but do perform many intranidal activities. Fighters are aggressive individuals that, while participating in intranidal activities, show the high­est levels of dominance behaviors. Foragers are relatively subordinate indi­viduals that are responsible for most of the tasks of foraging for food, wa­ter, nectar, and building material. Queens in R. marginata always belong to the sitter caste. In a related species, R. cyathiformis, queens belong to the fighter caste. It appears that this difference between the behavioral caste of the queens in the two species is related to the fact that R. marginata queens,

Summary 323

face less reproductive threat from their nestmates than do R. cyathiformis queens. The system of behavioral caste differentiation into sitters, fighters, and foragers seems to permit the wasps to work for the welfare of their col­onies and gain indirect fitness without entirely dosing off their reproduc­tive options.

As in many primitively eusocial species, the wasps indulge in frequent dominance-subordinate interactions. On the basis of these interactions, most wasps in a colony can be arranged in a dominance hierarchy. In R.

marginata, the queen, unlike the queens in most other primitively eusocial species, is not at the top of the colony's dominance hierarchy. Consistent with her classification as a sitter, the queen may participate in few or no dominance interactions. But she is nevertheless completely successful in monopolizing reproduction. It seems likely therefore that she achieves this monopoly through the production of pheromones. But when she has to establish herself as a new queen, she resorts to striking levels of physical aggression quite uncharacteristic of R. marginata queens in mature nests but highly reminiscent of the behavior of queens of other primitively eusocial species. As might be expected in established colonies, R. margi­nata queens do not appear to regulate the activities of their workers, which appear to continue to bring food and feed larvae in the absence of the queen as efficiently as they do in her presence. There is some evidence that the dominance-subordinate interactions among the workers may serve to regulate their own activity levels by signaling hunger levels of the adults and the larvae in the colony.

Given the primitively eusocial status of R. marginata, there is a surpris­ingly well-developed age polyethism. Feeding larvae, building the nest, bringing pulp, and bringing food are four tasks performed sequentially by successively older wasps. More than the absolute age of the wasps, their relative position in the age distribution of the colony appears to strongly influence the task profile of an individual. The pattern of interindividual interactions, especially interactions not involving dominance or food ex­change, constitutes a plausible mechanism for the wasps to assess their rel­ative age in their colony. Computer simulations reveal that the so-called activator-inhibitor model proposed for the regulation of age polyethism in honey bees provides a suitable proximate mechanism for the organization of work in R. marginata colonies.

In an adaptation of Hamilton's rule to compare the inclusive fitness of

324 Summary

solitary nest foundresses and workers, I computed inclusive fitness as the product of an intrinsic productivity factor, the coefficient of genetic relat­edness, and a demographic correction factor. Then to make investigation easy, I measured inequalities between workers and solitary foundresses in adult-brood genetic relatedness (genetic predisposition), in intrinsic pro­ductivity levels (ecological and physiological predisposition), and in the demographic correction factors (demographic predisposition).

Haplodiploidy is expected to create genetic asymmetries such that full sisters are more closely related to each other than a mother would be to her offspring. In R. marginata, however, multiple mating by queens (polyan­dry) and frequent queen replacements (serial polygyny) break down these relatedness asymmetries to such an extent that, if anything, workers are less related to the brood they rear than a solitary foundress might be to her offspring. Thus there is no evidence for genetic predisposition for the evo­lution of eusociality in R. marginata. R. marginata does have a well-devel­oped system of nestmate discrimination, but it is based on recognition la­bels and templates acquired by the wasps after their eclosion and from sources outside their body. This makes it unlikely that intracolony kin rec­ognition helps the workers to be preferentially altruistic toward their close relatives. These results make it imperative to look for factors other than ge­netic relatedness in the evolution of eusociality.

There is considerable evidence that factors other than genetic related­ness do play a role in that evolution. During the pre-emergence phase of the colony cycle, wasps drift from one colony to other colonies. Even ma­ture colonies readily accept young intruders from alien colonies. These phenomena must result in considerable further reduction of intracolony genetic relatedness. Nevertheless, alien conspecifics become well integrated into their foster colonies and are not discriminated against; they even go on to become foragers and replacement queens in their foster colonies. Field studies have shown that only some 4 to 8% of the wasps nest soli­tarily, while the remainder nest in groups. Why should such a large pro­portion of wasps join multiple-foundress nests when doing so means most of them will be sterile? There is evidence that all wasps are not as efficient at raising offspring as solitary foundresses. Those that are not as efficient as solitary foundresses fare better as workers in multiple-foundress colonies. Field and laboratory experiments show that a subordinate cofoundress gains fitness by a factor of 2.9 by choosing not to found her own nest and

Summary 325

to work instead in another foundress' nest. It is this advantage that permits workers to rear brood quite distantly related to them. This is the ecological predisposition to the evolution of eusociality.

There is also evidence for considerable physiological predisposition. Un­der laboratory conditions, only about 50% of the wasps are capable of ini­tiating single-foundress nests and laying eggs. Both larval and adult nutri­tion play a role in such pre-imaginal caste bias. Individuals that are well fed as larvae enter a developmental pathway that makes them grow into adults that are hungry, eat more, develop their ovaries, and become egg layers. Conversely, poorly fed larvae enter a developmental pathway that makes them grow into adults that are not hungry, eat less, and become non-egg layers. It is reasonable to expect that, under natural conditions, egg layers have a better chance of capitalizing on opportunities to become queens than the non-egg layers, which are more likely to become workers.

There is also evidence for strong demographic predisposition to euso­ciality in R. marginata. Delayed reproductive maturation makes it advan­tageous for wasps to serve as workers in another individual's nest rather than to wait until they become reproductively mature and able to raise their own offspring. Variation between individuals in the time taken to at­tain reproductive maturity provides a mechanism by which some individ­uals (the early reproducers) can be selected to become solitary nest foun­dresses while others (the late reproducers) are selected to become workers. There is both theoretical and empirical evidence that wasps can follow mixed reproductive strategies-behaving as workers until they become re­productively mature and raising their own offspring later. If a solitary foundress dies before she brings the brood under her care to indepen­dence, she necessarily loses all her investment in them. But a worker has more assured fitness returns because even if she dies, another worker in the colony will continue to look after the brood that were under her care. Quantitative inclusive fitness models show that the advantage of such as­sured fitness returns can be greater than the maximum advantage pro­vided by haplodiploidy. In combination with delayed reproductive matu­ration, variation in age at reproductive maturity, and the possibility of mixed reproductive strategies, assured fitness returns leads to a significant demographic predisposition for the evolution of eusociality.

Although many factors that might tilt the inclusive fitness balance in fa­vor of workers are yet to be considered, a preliminary unified model com-

326 Summary

bining such genetic, ecological, physiological, and demographic factors as can now be quantified predicts that about 5% of the wasps should opt for the solitary nesting strategy, and that the remaining 95% should opt for the worker strategy. This result is remarkably close to the empirically ob­served proportions of solitary nest foundresses and workers in nature.

In addition to elucidating the relative roles of genetic, ecological, physi­ological, and demographic factors in promoting the evolution of euso­ciality, I have discussed the possible evolutionary route to eusociality, mechanisms for the evolution of caste polymorphism, and the possibility of reversal of social evolution. Perhaps the single most important point I have made is that ecological, physiological, and demographic factors can be more important in promoting the evolution of eusociality than the ge­netic relatedness asymmetries potentially created by haplodiploidy. Put in another way, the benefit and cost terms in Hamilton's rule deserve more attention than the relatedness term.