Evolving the ingredients for reciprocity and spiteIntroductionReciprocal altruismSpiteConclusionsReferencesdoi: 10.1098/rstb.2009.0116, 3255-3266364 2009 Phil. Trans. R. Soc. B Marc Hauser, Katherine McAuliffe and Peter R. Blake Evolving the ingredients for reciprocity and spite Supplementary datamlhttp://rstb.royalsocietypublishing.org/content/suppl/2009/10/05/364.1533.3255.DC1.ht "Audio supplement"Referenceshttp://rstb.royalsocietypublishing.org/content/364/1533/3255.full.html#related-urls Article cited in: http://rstb.royalsocietypublishing.org/content/364/1533/3255.full.html#ref-list-1 This article cites 73 articles, 21 of which can be accessed freeRapid responsehttp://rstb.royalsocietypublishing.org/letters/submit/royptb;364/1533/3255 Respond to this articleSubject collections (1578 articles)evolution  (292 articles)cognition  (1157 articles)behaviour  Articles on similar topics can be found in the following collectionsEmail alerting service hereright-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the top http://rstb.royalsocietypublishing.org/subscriptions go to: Phil. Trans. R. Soc. BTo subscribe to This journal is © 2009 The Royal Society on April 9, 2010rstb.royalsocietypublishing.orgDownloaded fromEvolving the ingredients forreciprocity and spiteMarc Hauser1,2,*, Katherine McAuliffe2and Peter R. Blake31Department of Psychology,2Department of Human Evolutionary Biology, and3Graduate School ofEducation, Harvard University, Cambridge, MA, USADarwin never provided a satisfactory account of altruism, but posed the problem beautifully in lightof the log ic of natural selection. Hamilton and Williams delivered the necessary satisfaction byappealing to kinship, and Trivers showed that kinship was not necessary as long as the originallyaltruistic act was conditionally reciprocated. From the late 1970s to the present, the kinship theoriesin particular have been supported by considerable empirical data and elaborated to explore anumber of other social interactions such as cooperation, selfishness and punishment, giving uswhat is now a rich description of the nature of social relationships among organisms. There are,however, two forms of theoretically possible social interactions—reciprocity and spite—thatappear absent or nearly so in non-human vertebrates, despite considerable research efforts on awide diversity of species. We suggest that the rather weak comparative evi dence for these inter-actions is predicted once we consider the requisite socioecological pressures and psychologicalmechanisms. That is, a consideration of ultimate demands and proximate prerequisites leads tothe prediction that reciprocity and spite should be rare in non-human animals, and common inhumans. In particular, reciprocity and spite evolved in humans because of adaptive demands oncooperation among unrelated individuals living in large groups, and the integrative capacities ofinequity detection, future-oriented decision-making and inhibitory control.Keywords: reciprocal altruism; spite; ultimate pressures; proximal constraints1. INTRODUCTIONIn The descent of man, Darwi n (1871) pondered theevolutionary origins of altruism and self-sacrificeamong humans. The puzzle, as Darwin realized, wasthat such behaviours pose significant costs to the indi-vidual: ‘he who was ready to sacrifice his life, as many asavage has been, rather than betray his comrades,would often leave no offspring to inherit his noblenature’ (p.163). To solve this problem, Darwin ass-umed that self-sacrifice might payoff in the currencyof group benefits. He thus stated, if ‘a tribe includingmany members who ...were always ready to g ive aidto each other and sacrifice themselves for thecommon good, would be vic torious over most othertribes; and this would be natural selection’ (p.166).In other words, the costs to the individual of self-sacrifice and other altruistic behaviour could evolve ifthe individual’s group benefited relative to othergroups lacking such behaviours.As this history has been recounted many times, herewe simply reiterate the key ideas and findings intelegraphic form so as to set up the essential problemsdiscussed in this essay. In brief, sociobiologists raisedwhat Dawkins (1976) famously described as the pro-blem of subversion from within, that is, in a group ofself-sacrificial altruists, defectors immediately win asthey reap the benefits without paying the costs.Thus, group selection was attacked as, at best, aweak account of the evolution of altruistic behaviour.As an alternative, Hamilton (1964) and Williams(1966) proposed and developed a gene’s eye view ofaltruism, arguing that self-sacrifice would evolve ifthe costs to the individual were offset by benefits tothe individual’s close kin. What drives the evolutionof altruism, therefore, is a consideration of thedistribution of winning genes, rather than winningindividuals or groups. But what about altruisticbehaviour among genetically unrelated individuals?The solution, provided by Tr ivers (1971), was recipro-cal altruism: self-sacrifice is offset because the initialact of altruism is conditioned upon a reciprocatedact of altruism in the future.These brilliant ideas can be placed in the context of asocial matrix that considers the gains (benefits) andlosses (costs) of an act from the perspective of a donorand putative recipient or recipients (figure 1). Movingclockwise from the top left, altruism arises when thedonor incurs a loss but delivers a gain to the recipient.Spite occurs when both the donor and the recipientincur losses, but typically, the cost to the recipient out-weighs the cost to the donor. Cooper a tion arises whenboth donor and recipient accrue gains. Finally, selfishnessarises when the donor gains, but the recipient loses.Needless to say, there are several important distinctionswithin each of these cells, but critically for our purposes,are the differences within the cooperation cell. In par-ticular, some forms of cooperation entail joint actionand mutual, simultaneous benefit, whereas others (i.e.reciprocity) entail delays.* Author for correspondence ([email protected]).One contribution of 16 to a Discussion Meeting Issue ‘Theevolution of society’.Phil. Trans. R. Soc. B (2009) 364, 3255–3266doi:10.1098/rstb.2009.01163255 This journal is q 2009 The Royal Society on April 9, 2010rstb.royalsocietypublishing.orgDownloaded fromBased on the