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Evolution of Maternal Effect Senescence

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Evolution of Maternal Effect Senescence Evolution of maternal effect senescence Jacob A. Moorad1 and Daniel H. Nussey Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, United Kingdom Edited by James W. Vaupel, Max Planck Institute for Demographic Research, Rostock, Germany, and approved December 4, 2015 (received for review October 23, 2015) Increased maternal age at reproduction is often associated with Amid the many studies of senescing traits, a clear pattern is decreased offspring performance in numerous species of plants emerging that relates maternal age to the health, fitness, and life- and animals (including humans). Current evolutionary theory considers span of their progeny across widely diverse taxa including humans such maternal effect senescence as part of a unified process of (8), birds (9, 10), mammals (11, 12), Drosophila species (13–15) and reproductive senescence, which is under identical age-specific selective other arthropods (16–18), and plants (19). Although observations pressures to fertility. We offer a novel theoretical perspective by com- suggest that maternal effect senescence may not proceed at the – bining William Hamilton’s evolutionary model for aging with a quan- same rate as fertility senescence (12, 20 24), there is no evolu- titative genetic model of indirect genetic effects. We demonstrate that tionary theory yet capable of explaining maternal effect senescence fertility and maternal effect senescence are likely to experience differ- or its distinction from fertility senescence. Biologists have assumed ent patterns of age-specific selection and thus can evolve to take di- that the age-related decline in selection that shapes fertility and survival generalizes to traits under the influence of IGEs, including vergent forms. Applied to neonatal survival, we find that selection for ’ maternal effects. To address this deficiency in the theory, we de- maternal effects is the product of age-specific fertility and Hamilton s velop a general model incorporating IGEs into age-specific phe- age-specific force of selection for fertility. Population genetic models notypic evolution. We then focus our attention upon maternal show that senescence for these maternal effects can evolve in the effects that influence neonatal survival with the aim to: (i)un- absence of reproductive or actuarial senescence; this implies that ma- derstand how increases in maternal age will alter the strength of ternal effect aging is a fundamentally distinct demographic manifesta- selection for neonatal survival IGEs and (ii) predict how neonatal tion of the evolution of aging. However, brief periods of increasingly survival will change with maternal age when populations are at a beneficial maternal effects can evolve when fertility increases with age mutation–selection equilibrium. faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework Model with which to model, measure, and compare the evolutionary deter- The conventional model of phenotypic evolution describes the minants of the social manifestations of aging. Extension of our mater- relationship between the fitness, phenotypes, and genotypes of nal effects model to other ecological and social contexts could provide individuals. The phenotype of some individual i is the sum of a important insights into the drivers of the astonishing diversity of life- breeding value (a transmissible genetic quantity) gi and a non- spans and aging patterns observed among species. heritable environmental residual ei expressed as deviations from the population mean μ. Relative fitness is the numerical repre- aging | demography | indirect genetic effects | selection | social sentation of the focal individual in the next generation, usually quantified by the number of zygotes produced; it can be de- scribed in terms of a function of a phenotype of interest, enescence is the age-related deterioration of organismal function and fitness. Evolutionary theory explains its perva- S w = μ + βfw, zg + e . [1] siveness as the result of age-related declines in the strength of i i natural selection to preserve survival and reproduction (1). Genes β{w, z} is a selection gradient, the slope of the regression of deleterious to survival or fertility in late life can persist or even relative fitness on phenotypes, and ei is the residual fitness not come to fixation as a result of this weakening of selection in old age explained by the trait. The response to selection is the change in (2–4). To date, most theoretical and empirical research into the the population mean over one generation owing to selection for evolution of senescence has focused on age-specific survival and fertility (vital rates), as these rates are most proximate to fitness. Significance Both age-related declines in survival (actuarial senescence) and fertility (reproductive senescence) can evolve independently from Evolutionary theory underpins our understanding of the aging initially nonsenescent life histories (1). process. The many aspects of reproduction that decline with These vital rates are a product of complex interactions among maternal age in animals include number of offspring born, different physiological systems, phenotypic traits, and their environ- offspring size, and neonatal survival. Current theories of aging ment. One important source of environmental contributions involves ignore potential differences in the evolutionary pressures on social interactions. The influence of other individuals in the envi- these traits. Here, we combine two important branches of ronment on a particular phenotype can itself be heritable, and the evolutionary theory to allow consideration of age-dependent importance of these so-called “indirect genetic effects” (IGEs) is now selection at both offspring and maternal levels. We show that established within evolutionary biology (5–7). IGEs are known to we should actually expect the rates of age-related decline in readily alter the evolutionary predictions of standard quantitative female fertility and offspring performance to diverge under genetic models incorporating only direct genetic effects (DGEs). In selection. Our model has the potential to significantly improve age-structured populations, social interactions among individuals of our understanding of the evolution of reproductive senescence different ages are likely to be commonplace, but it is not known how and, more generally, the variability of aging patterns in nature. age-dependent IGEs influence the evolution of senescence. Here we incorporate IGEs into the evolutionary theory of aging to provide the Author contributions: J.A.M. and D.H.N. designed research, performed research, and necessary conceptual and statistical framework with which to un- wrote the paper. derstand how social interactions among individuals of different ages The authors declare no conflict of interest. can shape aging patterns. We then develop our model to specifically This article is a PNAS Direct Submission. deal with one particular social interaction of central biological im- Freely available online through the PNAS open access option. portance: maternal effects influencing neonatal survival. 1To whom correspondence should be addressed. Email: [email protected]. 362–367 | PNAS | January 12, 2016 | vol. 113 | no. 2 www.pnas.org/cgi/doi/10.1073/pnas.1520494113 Downloaded by guest on September 25, 2021 trait z. Following the conventional quantitative genetic assump- to the ages of the focal individual and the social interactors, tion of no covariance between genotype and environment (25), respectively. Thus, the phenotype of the focal individual taking this response follows from the definition of phenotype and [1], into account the influence of social partners of only age xI is Δz = βfw, zgvarfgg. [2] niðXxD, xI Þh i ziðxD, xI Þ = μ + gDiðxDÞ + eDiðxDÞ + gIjðxD, xI Þ + eIjðxD, xI Þ . var{g} is the additive genetic variance. j=1 [8] Response with Indirect Genetic Effects. Social interactions alter the response to selection when the phenotype of one individual is Using this age-specific notation, we can rewrite the genetic modified by the genotype of another. We can define the phenotype response to selection [6]. However, the determination of selection to incorporate the effects of social interactions by considering some gradients becomes more complicated in age-structured populations breeding value gDi that predicts the phenotype of the bearer i (the with overlapping generations. Here we consider a demographic DGE) and the breeding value gIj of a social partner j that modifies model with discrete time units. When populations are at a steady ’ the focal individual s phenotype (the IGE). Following ref. 26, the state with respect to age structure, these can be identified by partial phenotype of individual i with some number of social interactors ni is regression coefficients estimated by conventional multiple regres- sion approaches (27), provided that the relative fitness of individuals Xni P is defined as wi = expð−rxÞliðxÞmiðxÞ (33, 34), where the summa- zi = μ + gDi + eDi + gIj + eIj . [3] j=1 tion continues to the last possible age of reproduction (34, 35), liðxÞmiðxÞ is the individual’s reproductive output at age x,andr is ’ e and e are environmental error terms arising from the focal the population s Malthusian growth rate (35). Di Ij In the special case where one is interested in multivariate individual and each of its interactors, respectively. A change in the ’ phenotype due
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