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Kin selection is the key to altruism

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Research FocusKin selection is the key to altruismKevin R. Foster1,2, Tom Wenseleers2,3and Francis L.W. Ratnieks2,41Laboratory of Ecological and Evolutionary Dynamics, Department of Biological and Environmental Sciences,University of Helsinki, Helsinki, 00014, Finland2Wissenschaftskolleg zu Berlin, Institute for Advanced Study, Berlin, 14193, Germany3Zoological Institute, University of Leuven, B-3000 Leuven, Belgium4Laboratory of Apiculture and Social Insects, Department of Animal and Plant Sciences, University of Sheffield,Sheffield, UK, S10 2TNKin selection theory, also known as inclusive fitnesstheory, has been the subject of much debate andmisunderstanding. Nevertheless, the idea that related-ness among individuals can drive the evolution ofaltruism has emerged as a central paradigm in evol-utionary biology. Or has it? In two recent articles, E.O.Wilson argues that kin selection should no longer beconsidered the main explanation for the evolution ofaltruism in insect societies. Here, we discuss what thesearticles say about kin selection and how it relates to thetheory. We conclude that kin selection remains the keyexplanation for the evolution of altruism in eusocialinsects.What is kin selection?The first glimmers of kin selection theory (see Glossary)were comments made by Haldane and Fisher that kinshipcan be important in social actions ([1,2] and refs therein).However, it was Hamilton wh o showed th e generalimportance of relatedness in evolution [1]. His theorytakes its most accessible form in the inequality known asHamilton’s rule, which predicts that altruistic action willbe favoured when brOc, where c and b are the cost andbenefit to actor and recipient, respectively, and r is theirrelatedness. Hamilton called his new and general prin-ciple of natural selection ‘inclusive fitness theory’ [1], butit is often known by the term ‘kin selection’, coined byMaynard Smith ([3] and refs therein).The fall of kin selection?E.O. Wilson [2] and E.O. Wilson and Ho¨lldobler [4] criticisethe kin selection explanatio n for altruism on severalgrounds (Table 1). E.O. Wilson [2] emphasises problemswith one idea that arose from kin selection thinking, knownas the haplodiploidy hypothesis [1], and argues that kinselection is similarly limited. In addition, both papers [2,4]criticise kin selection because it neglects ecological factors,predicts conflict rather than altruism and does not accountfor important colony-level effects. It is also argued that,contrary to kin selection predictions, altruism can evolvewithout relatedness. Alternatives to kin selection areprovided in the form of a modified Hamilton’s rule [2] anda scenario where having a ‘eusocial allele’ rather than highfamily relatedness causes individuals to behavealtruistically [4]. Here, we show that E.O. Wilson’scriticisms are based upon commonly made errors in eitherthe definiti on or applic ation of kin selection t heory(Table 1). Uncovering these errors makes it clear that hisideas are not true alternatives to kin selection theory, andthat the E.O. Wilson and Ho¨lldobler [4] scenario for theorigin of eusociality is probably incorrect.The haplodiploidy hypothesis and kin selection theoryare not equivalentIn his 1964 papers [1], Hamilton suggested that theunusually high relatedness among full sisters (rZ0.75) inthe haplodiploid Hymenoptera (bees, ants and wasps)relative to that among diploids (rZ0.5) helps to explainwhy eusociality is so freq uent in the Hymenoptera.Howev er, this idea, known as the ‘haplodiploidy’ or‘3⁄4relatedness’ hypothesis [5], neglected the lower related-ness of sisters to brothers (rZ0.25) in haplodiploids. Whenaveraged out, the relatedness of daughter Hymenopterato their full siblings is the same as it is to their offspring(rZ0.5), as seen in diploids. As a result, the haplodiploidyhypothesis has, for many years, been considered lessGlossaryAltruism: action that, on average, decreases the lifetime direct fitness of anactor and benefits one or more recipients; also ‘strong’ altruism [10].Altruism (weak): cooperative investment in a group by a group member, wherethe cost to the individual is outweighed by the feedback benefit to the individualfrom group membership (decreases within-group fitness of an actor butincreases its fitness in the population) [10].Cooperation: action that benefits one or more recipients.Direct fitness: fitness from personal reproduction.Eusociality: social groups in which some individuals specialise in work or helpto enhance the direct reproduction of others (see [3] for a full definition).Group selection: selection caused by the differential productivity and/orsurvival of whole groups, including colonies, demes, species and communities.Haplodiploidy hypothesis: idea that the3⁄4relatedness among full sisters inhaplodiploids predisposes them to eusociality with female workers [1,3,5,13].Inclusive fitness: direct plus indirect fitness [3,13,15].Indirect fitness: fitness component received from effects on the reproduction ofrelatives.Kin selection: selection affected by relatedness among individuals (also usedas an abbreviation of kin selection theory) [3,12,13].Kin selection or inclusive fitness theory: theory that models social traits with afocus on the individual (group effects are often implicit) and uses relatednesscoefficients to capture effects of genetic correlations among individuals [1,3,13].Relatedness: genetic correlation among individual loci or organisms [3,12,13].Trait-group selection theory (also multi-level selection or levels of selectiontheory): theory that models social traits in terms of effects on the individual andthe group; it often uses between-group genetic variance as an equivalent torelatedness [10,14].Corresponding author: Foster, K.R. ([email protected]).DTD 5 ARTICLE IN PRESSUpdate TRENDS in Ecology and Evolution Vol.xx No.xx 0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2005.11.020important than it was initially [3,5,6]. E.O. Wilson takesthis to mean that kin selection theory is similarly limited[2]. However, the haplodiploidy hypothesis is just oneapplication of the broader theory of kin selection. Itslimitations have no bearing on either the validity of kinselection theory or the key insight that relatedness canselect for altruistic actions [3,5]. This is well illustrated byrecent evidence for kin selection in the evolution of helpingin

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