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Ecology, Not the Genetics of Sex Determination, Determines Who Helps in Eusocial Populations

2013; Elsevier BV; Volume: 23; Issue: 23 Linguagem: Inglês

10.1016/j.cub.2013.10.013

1879-0445

Laura Ross, Andy Gardner, Nate B. Hardy, Stuart A. West,

Evolutionary Game Theory and Cooperation

In eusocial species, the sex ratio of helpers varies from female only, in taxa such as the social Hymenoptera (ants, bees, and wasps) [1Wilson E.O. Sociobiology. Belknap Press, Harvard1975Google Scholar], to an unbiased mixture of males and females, as in most termites [2Thorne B.L. Evolution of eusociality in termites.Annu. Rev. Ecol. Syst. 1997; 28: 27-54Crossref Scopus (221) Google Scholar]. Hamilton suggested that this difference owes to the haplodiploid genetics of the Hymenoptera leading to females being relatively more related to their siblings [3Hamilton W.D. Altruism and related phenomena, mainly in social insects.Annu. Rev. Ecol. Syst. 1972; 3: 193-232Crossref Google Scholar]. However, it has been argued that Hamilton's hypothesis does not work [4Charlesworth B. Some models of the evolution of altruistic behaviour between siblings.J. Theor. Biol. 1978; 72: 297-319Crossref PubMed Scopus (88) Google Scholar, 5Charnov E.L. Evolution of eusocial behavior: offspring choice or parental parasitism?.J. Theor. Biol. 1978; 75: 451-465Crossref PubMed Scopus (83) Google Scholar, 6Trivers R.L. Hare H. Haploidploidy and the evolution of the social insect.Science. 1976; 191: 249-263Crossref PubMed Scopus (915) Google Scholar, 7Craig R. Evolution of male workers in the Hymenoptera.J. Theor. Biol. 1982; 94: 95-105Crossref Scopus (15) Google Scholar, 8Pamilo P. Evolution of the sterile caste.J. Theor. Biol. 1991; 149: 75-95Crossref PubMed Scopus (25) Google Scholar, 9Bourke A.F.G. Franks N.R. Social Evolution in Ants. Princeton University Press, Princeton1995Google Scholar] and that the sex of helpers could instead be explained by variation in the ecological factors that favor eusociality [10Queller D.C. Strassmann J.E. Kin Selection and Social Insects.Bioscience. 1998; 48: 165-175Crossref Scopus (424) Google Scholar]. Here we test these two competing hypotheses, which focus on the possible importance of different terms in Hamilton's rule [2Thorne B.L. Evolution of eusociality in termites.Annu. Rev. Ecol. Syst. 1997; 28: 27-54Crossref Scopus (221) Google Scholar, 11Hamilton W.D. The genetical evolution of social behaviour. I.J. Theor. Biol. 1964; 7: 1-16Crossref PubMed Scopus (9581) Google Scholar], with a comparative study across all sexual eusocial taxa. We find that the sex ratio of helpers (1) shows no significant correlation with whether species are haplodiploid or diploid and (2) shows a strong correlation with the ecological factor that had favored eusociality. Specifically, when the role of helpers is to defend the nest, both males and females help, whereas when the role of helpers is to provide brood care, then helpers are the sex or sexes that provided parental care ancestrally. More generally, our results confirm the ability of kin selection theory to explain the biology of eusocial species, independently of ploidy, and add support to the idea that haplodiploidy has been more important for shaping conflicts within eusocial societies than for explaining its origins [6Trivers R.L. Hare H. Haploidploidy and the evolution of the social insect.Science. 1976; 191: 249-263Crossref PubMed Scopus (915) Google Scholar, 12Ratnieks F.L. Foster K.R. Wenseleers T. Conflict resolution in insect societies.Annu. Rev. Entomol. 2006; 51: 581-608Crossref PubMed Scopus (472) Google Scholar, 13Gardner A. Alpedrinha J. West S.A. Haplodiploidy and the evolution of eusociality: split sex ratios.Am. Nat. 2012; 179: 240-256Crossref PubMed Scopus (43) Google Scholar, 14West S. Sex Allocation. Princeton University Press, Princeton2009Crossref Google Scholar, 15Alpedrinha J. West S.A. Gardner A. Haplodiploidy and the evolution of eusociality: worker reproduction.Am. Nat. 2013; 182: 421-438Crossref PubMed Scopus (16) Google Scholar, 16Boomsma J.J. Lifetime monogamy and the evolution of eusociality.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009; 364: 3191-3207Crossref PubMed Scopus (276) Google Scholar, 17Hughes W.O.H. Oldroyd B.P. Beekman M. Ratnieks F.L.W. Ancestral monogamy shows kin selection is key to the evolution of eusociality.Science. 2008; 320: 1213-1216Crossref PubMed Scopus (475) Google Scholar, 18Boomsma J.J. Beyond promiscuity: mate-choice commitments in social breeding.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013; 368: 20120050Crossref PubMed Scopus (97) Google Scholar, 19Boomsma J.J. Kin selection versus sexual selection: why the ends do not meet.Curr. Biol. 2007; 17: R673-R683Abstract Full Text Full Text PDF PubMed Scopus (201) Google Scholar].