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Kin Selection and the Evolutionary Theory of Aging ANRV328-ES38-05 ARI 24 September 2007 8:51 Kin Selection and the Evolutionary Theory of Aging Andrew F.G. Bourke School of Biological Sciences, University of East Anglia, Norwich, Norfolk NR4 7TJ, United Kingdom; email: [email protected] Annu. Rev. Ecol. Evol. Syst. 2007. 38:103–28 Key Words First published online as a Review in Advance on kin conflict, life history, longevity, senescence, social evolution July 3, 2007 The Annual Review of Ecology, Evolution, and Abstract Systematics is online at http://ecolsys.annualreviews.org Researchers are increasingly recognizing that social effects influence the evolution of aging. Kin selection theory provides a framework This article’s doi: 10.1146/annurev.ecolsys.38.091206.095528 for analyzing such effects because an individual’s longevity and mor- tality schedule may alter its inclusive fitness via effects on the fitness Copyright c 2007 by Annual Reviews. All rights reserved of relatives. Kin-selected effects on aging have been demonstrated both by models of intergenerational transfers of investment by care- by UNIVERSITY OF ILLINOIS - CHICAGO on 06/05/08. For personal use only. 1543-592X/07/1201-0103$20.00 givers and by spatially explicit population models with limited dis- persal. They also underlie coevolution between the degree and form Annu. Rev. Ecol. Evol. Syst. 2007.38:103-128. Downloaded from arjournals.annualreviews.org of sociality and patterns of aging. In this review I critically examine and synthesize theory and data concerning these processes. I pro- pose a classification, stemming from kin selection theory, of social effects on aging and describe a hypothesis for kin-selected conflict over parental time of death in systems with resource inheritance. I conclude that systematically applying kin selection theory to the analysis of the evolution of aging adds considerably to our general understanding of aging. 103 ANRV328-ES38-05 ARI 24 September 2007 8:51 INTRODUCTION The evolutionary theory of aging provides an explanation for aging based on natural Aging (senescence): selection. The theory proposes that aging occurs because extrinsic mortality reduces decrease in an individual’s the relative size of cohorts of older individuals, causing the potential genetic contri- performance, survivorship, bution of older cohorts to future generations to fall. Therefore, any gene increasing or fecundity as age survival or fecundity is more strongly selected for when its phenotypic effects oc- increases, occurring as a result of intrinsic changes cur at younger ages, and conversely, any gene decreasing survival or fecundity is less strongly selected against when its phenotypic effects occur at greater ages. As a result, Kin selection: natural selection of genes for social age-specific phenotypic effects tend to evolve whereby genes for increased survival or actions via the sharing of fecundity have an effect at younger ages and genes for decreased survival or fecundity these genes between the have an effect at greater ages, so explaining the occurrence of aging. The evolutionary actor and its relatives theory of aging was initially formulated in the mid-twentieth century as an amalgam of contributions from R.A. Fisher, J.B.S. Haldane, P.B.Medawar, G.C. Williams, and W.D. Hamilton, with the last three authors having made the major contributions (reviewed in Charlesworth 2000, Rose 1991). The early theorists also identified two principal genetic routes to aging. The first, antagonistic pleiotropy, proposes that aging stems from selection of pleiotropic genes having a positive effect on survival and fecundity early in life and a negative effect late in life. The second, mutation ac- cumulation, proposes that aging stems from lack of selection against genes of purely negative effect, where these effects occur only late in life (e.g., Hughes & Reynolds 2005, Kirkwood & Austad 2000). A major area of research has developed on the basis of the evolutionary theory of aging (e.g., Arking 2006, Austad 1997a, Carey 2003, Charlesworth 1980, Finch 1990, Rose 1991), with more derived versions of the original theory having been con- structed to account for various complicating factors (e.g., for the case when extrinsic mortality reduces population density and so increases resource availability for older age classes; Abrams 1993). The theory has also been integrated with the general study of life history evolution because finite resources entail the occurrence of trade-offs between somatic maintenance and reproduction (Barnes & Partridge 2003, Kirkwood 1977), and because the age at first reproduction represents the critical period beyond which aging is predicted to occur (Charlesworth 1980, Rose 1997, Stearns 1992). Overall, empirical work has provided strong support for the evolutionary theory of aging from several sources. These include comparative analyses of life histories as by UNIVERSITY OF ILLINOIS - CHICAGO on 06/05/08. For personal use only. a function of the strength of extrinsic mortality and experimental manipulations of schedules of reproduction (e.g., Hughes & Reynolds 2005, Kirkwood & Austad 2000, Annu. Rev. Ecol. Evol. Syst. 2007.38:103-128. Downloaded from arjournals.annualreviews.org Rose 1991, Stearns 1992), although results from some studies have proved more con- sistent with derived versions of the theory than with the original theory (Reznick et al. 2004, Williams et al. 2006). Related studies have provided better support for antagonistic pleiotropy than for mutation accumulation as genetic routes to aging (e.g., Campisi 2005, Hughes & Reynolds 2005, Kirkwood & Austad 2000, Leroi et al. 2005, Partridge & Barton 1993, Partridge & Gems 2002a, Rose 1991), with some phenomena not readily reconcilable with either route (Mitteldorf 2004). Another major body of evolutionary theory, kin-selection theory (Hamilton 1964, Lehmann & Keller 2006, Michod 1982, West-Eberhard 1975), has sought to explain 104 Bourke ANRV328-ES38-05 ARI 24 September 2007 8:51 the evolution of social behavior as a function of the genetic relatedness of interacting individuals. Kin selection theory is based on Hamilton’s rule (Grafen 1985, Hamilton 1964), which states that a social action is naturally selected when the sum of rb and c Relatedness: probability exceeds zero, where r is the relatedness of the interactants, b is the change in offspring that two individuals share a number of the recipient of the act, and c is the change in offspring number of the gene as the result of kinship social actor. Although controversial in some of its applications (Alonso & Schuck- Social action: an action by Paim 2002, Wilson & Holldobler¨ 2005), kin selection is widely accepted as a powerful one individual (the actor) and robust explanation for various forms of social behavior across many taxa (e.g., affecting the survivorship or Bourke 2005, Emlen 1995, Foster et al. 2006, Trivers1985). These forms include kin- offspring output of another selected conflict, whereby individuals within social groups differ in their relatedness individual (the recipient) to the group’s progeny, and hence in their fitness optima, leading to potential within- Inclusive fitness: in kin group conflict (Ratnieks & Reeve 1992, Trivers 1974). A central tenet of the theory is selection theory, the fitness of a focal individual that an individual’s fitness (its inclusive fitness) depends upon its own offspring output incorporating effects of its plus its effects (through social actions) on the offspring output of relatives (Hamilton social actions toward 1964). A key prediction is that altruism (entailing lifetime reproductive costs) cannot relatives evolve unless interactants are related (Hamilton 1964, Lehmann & Keller 2006). Altruism: social action in The evolutionary theory of aging, including its derived versions, has traditionally which the actor experiences considered patterns of aging with reference to an individual’s fitness evaluated in the a loss in survivorship or absence of social effects (e.g., Hughes & Reynolds 2005, Rose 1991). However, kin offspring output and the recipient a gain selection theory predicts that social effects will influence patterns of aging because a focal individual’s longevity and mortality schedule may affect the fitness of other individuals. If the interacting individuals are relatives, the focal individual’s inclusive fitness will be altered, and hence patterns of aging in the focal individual will, in principle, be subject to kin selection. Recently, researchers have incorporated social and kin-selected effects into evolutionary models of aging (e.g., Lee 2003, Travis 2004), albeit implicitly in some cases. In a related development, researchers have argued that social organisms exhibit a complex, coevolutionary relationship between the trajectory of social evolution and patterns of aging (e.g., Alexander et al. 1991, Carey & Judge 2001). Nonetheless, patterns of aging stemming from social effects have not been systematically considered in the synthetic, overarching framework provided by kin selection theory. Applying this framework is an important exercise because it allows social hypotheses of aging to be classified and rigorously assessed. It also reveals hitherto underappreciated possibilities, such as the occurrence of potential kin-selected conflict over the timing of death and aging. In addition, explorations of by UNIVERSITY OF ILLINOIS - CHICAGO on 06/05/08. For personal use only. coevolution between sociality and aging have tended to proceed independently of one another. Annu. Rev. Ecol. Evol. Syst. 2007.38:103-128.
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