CURRENT TRENDSIN SCIENCE

PLATINUM JUBILEE SPECIAL

Edited by

N Mukunda

INDIAN ACADEMY OF SCIENCESBAN GALORE

CURRENT TRENDSIN SCIENCE

Why are animals (and humans) nice to each other?*

Centre for Ecological Sciences and Centre for Contemporary Studies, Indian Institute of Science,Bangalore 560 012, India.

andEvolutionary and Organismal Biology Unit, Jawaharlal Nehru Centre for Advanced Scientific Research,

Jakkur, Bangalore 560 064, India.e-mail: ragh@ces.iisc.ernet.in

It usually comes as a surprise to my friends,especially to those in the humanities, that amajor problem that we evolutionary biologists areobsessed with is why animals and humans are sonice, i.e., cooperative and altruistic, toward eachother. Why not investigate selfishness, conflict andback-stabbing that is so widespread, they plead.It may indeed sound strange, even malicious, tolabel nicety as a mystery. But that's just whatit is for evolutionary biologists, who like to labeleverything that they cannot easily explain throughDarwin's theory of natural selection, as a mystery.Of course, the motivation for labelling somethingas a mystery is to provoke deeper study of thephenomenon and, where appropriate, a modifica-tion of the theory to fit the new facts. Darwin'stheory of natural selection, graphically describedby his phrase "the preservation of favoured racesin the struggle for life", prepares us to expectcompetitive selfishness rather than cooperationand altruism. After all how can an individual thatpays a cost in order to help another individual, beexpected to win the race to survive and reproduce?And yet we find many examples of animals doingjust that. Honey bee workers kill themselves in the

*Expanded and modified (with permission) fromGadagkar R (2008) Why are animals nice to each other?In: The Seventy Mysteries of the Natural World -unlocking the secrets of our planet, (ed.) MichaelJ Benton, Thames and Hudson Ltd., London.

process of stinging predators that might destroytheir nest. Helpers at the nest of the bee-eater post-pone rearing their own offspring and spend timeand energy in assisting their parents to raise addi-tional brood. Ground squirrels risk attracting theattention of the predator to themselves by givingan alarm call to warn their neighbours. How cannatural selection promote such behaviour? Whydon't such individuals get eliminated by virtue oftheir lowering their own chances of survival andreprod uction?

Not surprisingly, humans have displayed anabsorbing fascination for cases of cooperation andaltruism in the animal world, long before the evolu-tionary puzzle associated with them became evi-dent. Indeed, freedom from precise evolutionarythinking accommodated all manner of untenabletheories about cooperation and altruism, in thepast. While Thomas Henry Huxley believed thatcooperation and altruism were only possible amongclose kin, Peter Kropotkin saw "mutual aid" every-where he looked, unconnected with any sort ofkinship. W C Allee and V C Wynne Edwardsand many others succumbed to a naIve form ofgroup selection - the notion that cooperation andself-sacrifice existed because they were good forthe group and the species - never mind that theywere harmful to the individuals displaying them[1]. There was unfortunately a long period dur-ing which such 'naIve group selection' and vague'good of the species' arguments prevailed. TheNobel Laureate Konrad Lorenz wrote for example

that 'Darwin had already raised the question ofthe survival value of fighting, and he has givenus an enlightening answer: It is always favourableto the future of a species if the stronger of tworivals takes possession either of the territory or thedesired female' [2]. Ironically such arguments wereneither logically sound nor were they attributableto Darwin who was a clear individual selectioniststating unambiguously that 'Natural selection, itshould never be forgotten, can act solely throughand for the advantage of each being.' Apart fromobfuscating the true significance of many biologi-cal phenomena, naive good of the species rhetoricreadily lent itself to the vindication of socialDarwinism and such other evils that purported tojustify such human social inequalities as racism andgenocide, in the name of natural selection. Naivegroup selection came to an abrupt end in the 1960sat least among evolutionary biologists due to somesimple but precise thinking by a handful of people;for a brief review, see [3].

Precise evolutionary thinking on this matter canbe traced back to the famous 20th century biolo-gist J B S Haldane who became an Indian citi-zen in the 1960s. Haldane appears to have beenthe first person to realize the arithmetic truth thatrisking one's life to save drowning relatives canindeed be favoured by natural selection, providedthat more copies of genes that give rise to suchbehaviour are recovered in the saved relatives thanare lost in the risk-taker (figure 1). The Englishbiologist W D Hamilton formalized essentially thesame idea in what has since come to be known asHamilton's Rule (box 1). The rule, usually writ-ten as [b· r > c] states that an altruistic gene willspread in a population when the benefit [b] to therecipient, devalued by the coefficient of relatednessbetween altruist and recipient [r], is greater thanthe cost incurred by the altruist [c]. In the wordsof Edward 0 Wilson, 'How can altruism, which bydefinition reduces personal fitness, possibly evolveby natural selection? The answer is kinship.' Thusthe alarm calling behaviour of the ground squirrelis no longer a mystery if the probability of savingindividuals carrying genes for alarm calling behavi-our is greater than the probability of losing onecopy of such a gene due to the death of the caller.Similarly, the helping behaviour of the bee-eater isno longer a mystery if its help at its parents' nestresults in the rearing of more additional siblingsthan the number of offspring it might have pro-duced instead of helping. Not only does this theoryprovide a logical explanation for why cooperationevolves more easily among kin, it also shows why

----~------ -- - --- --~--- -.....---- ---- --------'- --- ---- ----------"----~---

Figure 1. Cartoon illustrating the theme ofJ B S Haldane's story. The shaded portions of the drowningindividuals indicate the proportion of their genes which arealso present in the altruist standing on the bank. Noticethat the altruist is willing to risk his life when the numbersof his genes expected to be rescued is greater than thenumber in his body likely to be lost. (Drawing by SudhaPremnath; reprinted from [3].

close kinship is not always essential. If the benefitis very much greater than the cost, even low geneticrelatedness will do.

The theory is elegant indeed but the hard partis to show that animals behave as if theyobey Hamilton's Rule, i.e., whether they behavealtruistically only when Hamilton's Rule is satis-fied and behave selfishly when the rule is not satis-fied. Here most empiricists have chosen the easyoption of assuming that the cost and benefit termsare equal and of testing the simpler prediction thataltruism is more often directed towards close rela-tives than it is to distant relatives or non-relatives.Perhaps the most famous example of such a lim-ited test, based merely on the measurement ofrelatedness, has been carried out in the honey bee.Because of their peculiar haplodiploid genetics,honey bee workers are more closely related to theirnephews than they are to their brothers, as longas their mother mates with a single male. But therelatedness to nephews becomes less than that totheir brothers if the queen mates with more thantwo males. Because honey bee queens are known toroutinely mate with several males, worker bees areexpected to be less related to their nephews thanto their brothers and thus are expected to destroyany nephew eggs that their sister workers mightsneak into the nest and rear only their brothereggs laid by the queen. There is now good evi-dence that worker bees undertake such policingof each other and destroy most worker laid eggs

OJ'".D~ Cannot be tested as~ honey bee queens alwaysiii mate multiplyo

Figure 2. Because of their peculiar haplodiploid genetics,workers in hymenopteran insect societies are more closelyrelated to their nephews than they are to their brothers,as long as their mother mates with a single male. Butthe relatedness to nephews becomes less than that to theirbrothers if the queen mates with more than two males. Thustheory predicts that workers should prefer nephews overbrothers when their mother mates singly but should pre-fer brothers over nephews when their mothers mate multi-ply (upper panel). One part of this theoretical prediction isupheld in experiments with honey bees, because honey beequeens mate with multiple males. There is now good evi-dence that worker bees police each other and destroy mostworker laid eggs; in experiments where honey bee work-ers were offered queen-laid haploid eggs which are normallyexpected to be their brothers, and worker laid eggs (whichare normally expected to be their nephews), only 0.7% ofthe worker laid eggs survived while 42% of the queen-laideggs survived (lower panel; see [4]. Because honey bee queensalways mate with multiple males, the other part of the pre-diction that workers should prefer nephews over brotherscannot be tested in the honey bee.

(figure 2) [4]. Nevertheless, because the proximatecues used by the workers to distinguish worker-laideggs from queen-laid eggs are not well understood,there is always a lingering doubt that destruction ofworker eggs may have been selected for some reasonother than relatedness based, indirect fitnessbenefits [5].

An excessive and often exclusive focus on measure-ment of relatedness and the neglect of the costand benefit terms in empirical studies, has some-times given the false impression that Hamilton'sRule is inadequate to explain altruism. Wherethe cost and benefit terms have been measured,Hamilton's Rule has indeed provided a powerfultool to understand altruism. Studies on the white-fronted bee-eater in Kenya have shown that not

Figure 3. Typical nests of the primitively eusocial waspsRopalidia marginata (upper panel) and Ropalidia cyathi-formis (lower panel) (see text and [6]).

only the presence of helpers at the nest but alsothe bizarre behaviour of fathers harassing theirsons to return and act as helpers, are consistentwith the predictions of Hamilton's Rule. In anattempt to answer the question whether animalsbehave as if they obey Hamilton's Rule, I andmy students have chosen the locally abundantsocial wasps Ropalidia marginata and Ropalidiacyathiformis (figure 3). These wasps live in rel-atively small colonies consisting of less than ahundred individuals among which only one indivi-dual (referred to as the queen) reproduces whilethe rest function as altruistic sterile workers andspend their whole lives rearing the queen's off-spring. An important feature of these wasps is thatthey are primitively social, meaning that they canstill pursue a solitary life style, i.e., a lone femalewasp can build a nest, lay eggs and bring her off-spring to adulthood, all by herself. The remarkablefact of course is that most wasps nevertheless pre-fer to nest in groups and lead the life of a sterile

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Figure 4. Pedigrees of queens in four colonies ofR. margin at a, involved in a long-term study. The relation-ship between queen 1 (Q1) and queen 2 (Q2) is unknown forcolonies T08 and Tll because both Q1 and Q2 were amongthe wasps present on the nest at the time of its collectionand transplantation (Reprinted from [6]).

worker, helping to rear the queen's brood. Ourresearch has uncovered some rather remarkablefacts concerning the lives of these wasps and hasprovided novel insights into the evolutionary forcesthat mould the evolution of altruism. For exam-ple, we were able to construct royal pedigrees ofthe queens in these wasps (figure 4) and discover toeveryone's surprise, that altruism in these coloniesis not merely directed towards close genetic rela-tives such as brothers and sisters but also directedto nieces and nephews, cousins, cousins' offspring,mother's cousins, mother's cousins' offspring andeven mother's cousin's grand-offspring. I often jokethat these wasps will put any Indian joint familyto shame (table 1). We also find that altruism inthese wasps is very context dependent - not allwasps are altruistic, the same wasp is not altru-istic at all times, altruism depends on geneticrelatedness to the recipient and even more impor-tantly, altruism depends on the ecological situa-tion the wasps find themselves in. Perhaps ourmost important discovery is that, contrary to con-ventional wisdom, altruism is not just a matterof kinship; it is shaped by complex ecological fea-tures of the environment and complex physiologicaland demographic features of the wasps themselves.Our research has now reached a level of sophisti-cation that allows us to correctly predict the pro-portion of the population of wasps that should optfor a selfish, solitary nesting strategy and the pro-portion that should opt for an altruistic, workerstrategy [6].

Table 1. Genetic relationships between successivequeens and between workers and brood observed in thefour colonies (Reprinted from reference [6]).

Relationship betweenqueens and theirimmediate predecessors

Relationship betweenworkers andbrood

(a) Daughters(b) Sisters(c) Nieces(d) Cousins

(1) Sisters(2) Brothers(3) Nieces and nephews(4) Cousins(5) Cousins' offspring(6) Mother's cousins(7) Mother's cousins'

offspring(8) Mother's cousins'

grand-offspring

David Sloan Wilson has all along kept alive interestin a certain unobjectionable form of group selec-tion, better termed as 'trait-group selection' or'intrademic group selection' [7,8]. It is now beingrecognised that selection could act in principle atvarious levels of biological organization. Attemptsare being made to develop models of multi-levelselection, to address such fundamental questionsas how selection at lower levels of organizationsuch as that of individuals create higher levels oforganization such as societies and, how selectionat one level affects selection at other levels [9].More recently, a different and more controversialattempt is being made to resurrect group selec-tion. There are several reasons why this has cre-ated something of a turmoil in the field. First,group selection is being touted as an alternativeto kin selection and not just as an alternativeto individual selection. Second, it is being spear-headed by E 0 Wilson [10], the very man whocreated the field of sociobiology based largely onkin selection. Third, the new group selection ideasare being most forcefully applied to the evolutionof insect societies, the traditional bastion of kinselection. Indeed, the claim is that' ... group selec-tion is the strong binding force in eusocial evo-lution; individual selection, the strong dissolutiveforce; and kin selection , either a weak bindingor weak dissolutive force ' [11]. And fourth, itis being claimed that genetic relatedness is notessential for the evolution of altruism [12]. Thelast point is probably the most useful part of thedebate because we can make precise and mutuallyexclusive predictions. Indeed, Foster et al [13]havetaken up the gauntlet with the words ' ... the dis-covery of true altruism that evolved in the absenceof relatedness would be strong evidence against

kin selection theory, paralleling Darwin's statementthat altruism between species would reject naturalselection ... '. One can therefore hope that at leastthis point will soon be settled one way or another,unless of course people keep changing the very def-initions of altruism and relatedness.

Humans are indeed a special case because we oftencooperate with and behave altruistically towardnon-kin. Robert Trivers [14]proposed the theory ofreciprocal altruism to explain altruism toward non-kin. The idea is that 'I will do you a favour today,at a cost to myself if there is a reasonable guaran-tee that you will return the favour tomorrow, whenI am in need'. And 'if you don't, then I punishyou of course by not helping you the next time youare in need'. This sounds like a good idea but ithas been hard to document in animals. Cognitiveabilities to recognise past helpers so as to selec-tively return favours and even more importantly,to remember, recognise and punish cheaters whotake help and do not reciprocate, may be absent orlimited in animals. Reciprocal altruism may workmore effectively in humans because of our well-developed cognitive abilities and social networksbut we still cannot explain many acts of altruismthat are directed at strangers without a history ofspecifically helping the altruist. Indirect reciprocityor the idea that A helps B because B is known tohave helped C, may be somewhat easier to evolvebecause it depends on reputations of individuals as'altruistic, helping individuals' [15,16]. Neverthe-less, human altruism remains a puzzle because weoften behave altruistically not only to geneticallyunrelated strangers in large groups but also whenreputation gains or cues are entirely absent. Thisis a uniquely human dimension of cooperation andaltruism that appears to be absent in any otheranimal species.

An exciting new paradigm for investigating theevolutionary puzzle of human cooperation andaltruism is beginning to develop and promises toprovide what might be a uniquely human solutionto a uniquely human problem [17]. There are seve-ral other most interesting and unique features ofthis new paradigm. One is that it is being deve-loped as a collaborative effort between evolutionarybiologists, psychologists and economists. Anotheris that the primary methodology in use consists of'economic games' played with human volunteers.Many games are being used and I will mention twoof the most common ones.

One game, called the Ultimatum game, inventedby the German economist Werner Giith some three

decades ago, has become something of the 'labora-tory rat' in this line of research. The game isplayed between two anonymous players who haveto decide on how to split a sum of money givenby the experimenter. One player, the proposeroffers a certain proportion of the sum to the otherplayer, the responder. If the responder, who isaware of the total sum, agrees to the proposed divi-sion of the money, the deal goes through and thegame is over with money distributed between theproposer and responder as agreed. If the respon-der rejects the offer, nobody gets any money andthe game is nevertheless over. The excitement asso-ciated with this game has to do with the fact thatthe results obtained when played with real peopleare in stark violation of the theoretical predictionmade by economists. Economists have implicitly orexplicitly postulated the concept of Homo econo-micus, meaning that humans behave as rationalmaximizers of individual selfish gains. Thus theresponder is expected to accept even the smallestnon-zero sum offered to him because somethingis better than nothing. Knowing this, as the pro-poser is also a member of Homo economicus, heought to always offer the smallest non-zero sumand keep the rest to himself. But real people donot play that way. Generally people offer 40 to50% of the total sum and offers below 30% areoften rejected. This is a remarkably robust resultthat appears to be largely unaffected by the cul-tural background or literacy of the players and evenmore surprisingly, it does not seem to be affectedby the magnitude of the total sum involved. Indeedresearchers have had to travel to remote cultures inAfrica, South America and the Pacific Islands, todetect any significant variation in the sums offeredby proposers and in the sums rejected by respon-ders. The broad conclusion is that humans do notbehave as Homo economicus. People often rejectgrossly unfair offers and the proposers know thisso that they offer a fair or nearly fair proportion.The world average for offers seems to be about45%. People appear to have a sense of fairness andbehave in an 'other-regarding' way.

The results of another game, the so-called PublicGoods game are even more striking. In this game,the experimenter offers say Rs. 100 to each of4 players. The players are anonymous to each otherand each has to independently decide how muchof his or her Rs. 100 to keep and how much toinvest in a common pool which brings benefit toall the players. To simulate the benefits accruingfrom the common pool, the experimenter doublesthe common pool and distributes it equally amongall four players. Thus if each player invested Rs. 50in the common pool, Rs. 200 would accumulatein the common pool and the investigator doublesthis to Rs. 400 and gives Rs. 100 back to each

player. Thus everyone gets back twice what heor she had invested in the common pool. Clearly,it is good to invest in the common pool, i.e.,good to cooperate. However consider the situa-tion where one player contributes nothing to thecommon pool and keeps his Rs. 100 to himself.Since the other three players invest Rs. 50 each,the common pool now has Rs. '150, which theinvestigator doubles to Rs. 300 and gives backRs. 75 to each player (note that the player whodid not contribute to the common pool also getsan equal share of the benefit). Thus the three play-ers who contributed to the common pool end upwith Rs. 50 + 75 = 125 each, while the player whodid not contribute anything to the common pooltakes home a booty of Rs. 100 + 75 = 175. Clearly,it pays even more to be selfish, not to contributeanything to the common pool and reap the benefitsof other people's generosity. Thus the Homo eco-nomicus model of human behaviour predicts thatnobody should contribute anything to the commonpool and that nobody should go home with anymore than their initial Rs. 100. But again, real peo-ple do not play that way. Most people contributenearly half their initial sum to the common pool.But why do people play this way? Why are peoplenot as selfish as predicted by the Homo economi-cus model. Why do people cooperate and behavealtruistically?

A possible answer suggests itself when the publicgoods game is played with an interesting twist.When players were offered the opportunity topunish their (anonymous) co-players who did notcontribute enough to the common pool in previousrounds, many were eager to do so even if they hadto incur a cost to themselves. For example, a playercould impose a fine of Rs. 10 on a co-player but inorder for this punishment to be executed the puni-sher had to pay say, Rs. 5 so that both the Rs. 10and the Rs. 5 went back to the experimenter. It wasremarkable the players were willing to punish theirco-players at a cost to themselves even when theywere unaware of the identity of the co-players andeven when they were aware that they would notencounter the same players again. In games thathad such an option to punish, all players seemedto fear punishment because contributions to thecommon pool went up. Fehr and Giichter [18] whoperformed these experiments conclude that peopleseem to derive a 'primal pleasure' in punishing free-riders and that it may be in our genes to do so.In other words they suggest that human coopera-tion and altruism may be maintained more becauseof fear of punishment rather than due to any innatetendency to cooperate. These are intriguing resultsand intriguing suggestions, by no means defini-tive, but clearly worthy of further investigation.

Taken at face value these results suggest that theevolution of human cooperation and altruism maybe based on quite different forces as compared towhat we have seen for other animals. Unless ofcourse we begin to find that animals also showgeneralised reciprocity, other-regarding behaviourand a tendency to punish free-riders. Recent exam-ples of very clever experiments with rats, capuchinmonkeys and chimpanzees promise to engage withthese questions in the near future [19-21].

While more needs to be done on the theoreti-cal front, empirical studies compatible with test-ing modern theoretical predictions (arising out ofHamilton's Rule, group selection of different kinds,multilevel selection and reciprocity of various hues)are now probably the rate limiting step in clinchingour understanding of the evolution of cooperationand altruism. But I would hazard a guess that weare poised to demystify the evolution of nicety inthe natural world - animal and human.

My research is supported by the Department ofScience and Technology, Department of Biotech-nology, Ministry of Environment and Forests andCouncil for Scientific and Industrial Research,Government of India.

b = benefit to recipientc = cost to donorr = genetic relatedness between donor and recipient

or

ni = No. of relatives rearedri = relatedness to relativesno = No. of offspring rearedr 0 = relatedness to offspring

Hamilton's Rule defines the condition for the evo-lution of altruism. The upper form is useful topredict when an individual will be selected to sacri-fice its life to help others. The lower form is useful

to predict when a sterile individual who rears rela-tives will be selected over a fertile individual whorears offspring.

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[2] Lorenz K 1966 On aggression ( ew York: BantamBooks, Inc) pp. xiv+306.

[3] Gadagkar R 1997 Survival strategies - cooperationand conflict in animal societies (Cambridge, Mass.;Hyderabad, India: Harvard University Press andUniversities Press) pp. x+196.

[4] Ratnieks F L W, Foster K Rand Wenseleers T2006 Conflict resolution in insect societies; Ann. Rev.Entomol. 51 581-608.

[5] Gadagkar R 2004 Why do honey bee workers destroyeach other's eggs?; J. Biosci. 29 213~217.

[6] Gadagkar R 2001 The social biology of Ropa-lidia marginata: Toward understanding the evolutionof eusociality (Cambridge, Massachusetts.: HarvardUniversity Press) pp. xiii+368.

[7] Sober E and Wilson D S 1998 Unto others: The evolu-tion and psychology of unselfish behavior (Cambridge:Harvard University Press) pp. 394.

[8] Wilson D S 1980 The natural selection of populations fjcommunities (California: The Benjamin/CummingsPublishing Company, Inc.) pp. xv+186.

[9] Keller L (ed.) 1999 Levels of selection in evolution(Princeton: Princeton University Press) pp. 318.

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