Altruism Researchers Must Cooperate Biologists Studying the Evolution of Social Behaviour Are at Loggerheads

COMMENT PHYSICS How the media COLLECTIVES Leadership EXHIBITION New show EVOLUTION Responses to misconstrued Steven tips learned from house- highlights 300 years of recent reappraisal of kin Hawking’s latest book p.657 hunting bees p.658 science in Berlin p.660 selection p.661 Altruism researchers must cooperate Biologists studying the evolution of social behaviour are at loggerheads. The disputes — mainly over methods — are holding back the field, says Samir Okasha. ast month, 30 leading evolutionary now calling for a radical rethink, arguing that I contend that there is little to argue about. biologists met in Amsterdam to discuss kin selection is theoretically problematic, and Much of the current antagonism stems a burgeoning controversy. The question has insufficient empirical support, and that from the fact that different researchers are PARKINS D. Lof how altruistic behaviour can arise through alternative models better account for the evo- focusing on different aspects of the same phe- natural selection, once regarded as settled, is lution of social behaviour2. Others regard kin nomenon, and are using different methods. In again the subject of heated debate. selection as solid, and the rethink as unneces- allowing a plurality of approaches — a healthy The question dividing biologists is the sary and potentially retrograde. thing in science — to descend into tribal- degree to which inclusive fitness theory, or kin Rival camps have emerged, each endors- ism, biologists risk causing serious damage selection, explains the evolution of altruism ing a different approach to social evolution. to the field of social evolution, and potentially — in which an animal provides a benefit to Heated exchanges have occurred at confer- to evolutionary biology in general. another at a cost to itself. This theory, that nat- ences, on blogs and in journals, and have ural selection can sometimes favour animals even been reported in The New York Times. Darwin’s PUZZLE that behave altruistically towards relatives, has Biologists have accused each other of misun- Charles Darwin realised that altruism dominated empirical work on social behav- derstanding, of failing to cite previous studies poses a special problem for his theory of iour since it was devised by W. D. Hamilton in appropriately, of making unwarranted claims evolution. He was particularly troubled by the 1960s and 1970s1. Yet some biologists are to novelty and of perpetuating confusions. Yet the sterile workers in colonies of social 7 OCTOBER 2010 | VOL 467 | NATURE | 653 © 2010 Macmillan Publishers Limited. All rights reserved COMMENT Examples of favouring kin are widespread: Japanese macaques spend more time grooming their closer relatives and meerkats share feeding and guard duties. insects, which devote their lives to help- closely related recipients. This means that a relative5. Similarly, rhesus and Japanese L.COM ing a queen reproduce at the expense of animals should behave in ways that maxi- macaques are more likely to groom rela- P EA.COM D URE having offspring themselves. One possible mize not their personal fitness (or number tives than non-relatives, and to help them T explanation, hinted at by Darwin, is that of surviving offspring), but rather their in disputes6. /NA DT groups containing many altruists might inclusive fitness — Several biologists, however, have recently RN A . out-compete groups containing fewer. a measure that also questioned the importance of kin selection in I “Many biologists DRESSLER/AR T. This idea of ‘group selection’ fell out of regard kin takes into account explaining social behaviour. Edward O. Wil- favour in the 1960s when George Williams selection theory the offspring of son, famous for his empirical work on insect argued that it was unlikely to be a powerful as a resounding their relatives. societies and once a forceful advocate of kin evolutionary force compared to individual Inclusive fitness selection, now argues that kinship plays selection, and was not needed to explain empirical theory predicts a minor part in the evolution of ant, bee, empirical observations3. success.” that animals should termite and other social insect colonies7–9. Inclusive fitness theory, most biologists behave more altru- More important, he says, are the ecological now believe, provides the solution to Dar- istically towards kin than non-kin. This has factors that make social living so successful. win’s puzzle. Hamilton realised that a gene been amply confirmed in diverse species, An easy-to-defend nest and a nearby food that causes an animal to behave altruisti- from microbes to primates4, leading many supply, for instance, may make it beneficial cally can spread by natural selection as long biologists to regard kin selection theory as a for animals to live in groups. Recently, Wil- as the beneficiaries are relatives, and so have resounding empirical success. In many bird son, along with theoretical biologists Martin a chance of carrying the same gene. In short, species, such as scrub jays and dunnocks, Nowak and Corina Tarnita, have argued that altruism can evolve if the cost to the actor for example, breeding pairs receive aid inclusive fitness theory rests on a number is offset by sufficient benefit to sufficiently from a non-breeding ‘helper’ bird, typically of assumptions that greatly limit its appli- cability — such as that natural selection is relatively weak2. Still others argue that multi- GLOSSARY level selection — a modern-day version of group selection — best explains the evolu- Coming to terms with social evolution tion of altruism (although many biologists remain suspicious of appeals to group, rather Altruism Group selection than individual, advantage). Behaviour that is costly for an animal The idea that natural selection favours traits The root of the problem is the existence to perform but benefits others. Costs because they benefit whole groups, rather of several different frameworks for model- and benefits are measured in terms of than individuals. ling the evolution of social behaviour. These reproductive success. include numerous variants of kin selection Multi-level selection theory theory; multi-level selection; evolutionary Inclusive fitness The idea, closely related to group game theory; and an approach from quan- A generalization of Darwinian fitness, which selection, that natural selection can titative genetics based on the notion of takes into account the effect of an individual’s operate on more than one hierarchical ‘indirect genetic effects’. The relationships actions on the reproductive success of their level, for instance at the level of the between these frameworks are sometimes relatives, as well as on their own. individual, group or species. ambiguous, and biologists disagree about which is most fundamental and which most Kin selection theory Social evolution useful empirically (see ‘Coming to terms The idea that natural selection shapes Darwinian theory as applied to an animal’s with social evolution’). individuals’ behaviour according to the social behaviour, that is behaviour affecting All this disagreement creates the impres- effect it has on relatives. other individuals in the population. sion of a field in massive disarray. In reality, many of the players involved are arguing at 654 | NATURE | VOL 467 | 7 OCTOBER 2010 © 2010 Macmillan Publishers Limited. All rights reserved COMMENT Eciton burchelli army ant workers can form living bridges for other colony members to cross. Older moorhen chicks sometimes help feed their young siblings. A P cross purposes. Nowak and his colleagues, over fundamentals. Most agreed that inclu- serious damage to the field. Up-and-coming L for instance, have developed a mathematical sive fitness theory has been extremely valu- researchers are unlikely to be attracted to a L.COM P URES/F model that they claim provides a more direct able for empirical biologists, but that it is not discipline plagued by controversy. Moreo- URE T way to calculate the evolutionary dynamics of the only way to model social evolution. ver, if the experts cannot agree about what T 2 EN PIC EN ION/NA D a social trait such as altruism . However, they theoretical framework works best, the T IN UC M overlook the fact that inclusive fitness theory BUILDING BRIDGES supply of research funding may eventually / D TT E explains what organisms are trying to maxi- Much of the current antagonism could be threatened. Also worrying is the pos- FF O mize. It is not just a tool for calculating when easily be resolved — for example, by sibility that onlookers perceive the central M URE PRO URE . T A M a social trait will evolve. researchers situating their work clearly in question of social evolution theory — how Likewise, in arguing that ecological factors, relation to existing literature; using existing altruism can evolve — as unresolved, even N rather than kinship, are key to the evolution terminology, conceptual frameworks and though it was answered decades ago. Dur- of social-insect colonies, Wilson is imposing taxonomic schemes unless there is good ing the ‘sociobiology wars’ of the 1970s and a false dichotomy4. To fully understand how reason to invent new ones; and avoiding 1980s, creationists proved adept at seizing these colonies evolve, researchers need to unjustified claims of novelty or of the supe- on and exaggerating the differences in consider ecological factors and relatedness. riority of one perspective over another. opinion between biologists for their own Whether they stress the importance of one It is strange that such basic good practice ends. It would be a disaster if the same were over the other will depend on the question is being flouted. The existence of equivalent to happen again. ■ SEE CORRESPONDENCE P.661 they are asking. For example, relatedness has formulations of a theory, or of alternative proved crucial to understanding conflicts modelling approaches, does not usually lead Samir Okasha is in the Department of between the queen and her workers over the to rival camps in sci- Philosophy, University of Bristol, Bristol production of male versus female offspring “Evolutionary ence.

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