Evolution of maternal effect senescence

Abstract

Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton's evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton's age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species.S enescence is the age-related deterioration of organismal function and fitness. Evolutionary theory explains its pervasiveness as the result of age-related declines in the strength of natural selection to preserve survival and reproduction (1). Genes deleterious to survival or fertility in late life can persist or even come to fixation as a result of this weakening of selection in old age (2-4). To date, most theoretical and empirical research into the evolution of senescence has focused on age-specific survival and fertility (vital rates), as these rates are most proximate to fitness. Both age-related declines in survival (actuarial senescence) and fertility (reproductive senescence) can evolve independently from initially nonsenescent life histories (1).These vital rates are a product of complex interactions among different physiological systems, phenotypic traits, and their environment. One important source of environmental contributions involves social interactions. The influence of other individuals in the environment on a particular phenotype can itself be heritable, and the importance of these so-called "indirect genetic effects" (IGEs) is now established within evolutionary biology (5-7). IGEs are known to readily alter the evolutionary predictions of standard quantitative genetic models incorporating only direct genetic ...

Evaluating the diversity of maternal age effects upon neonatal survival across animal species

“…As with the classical evolutionary theory of senescence (Williams 1957;Hamilton 1966;Charlesworth 1994), the evolutionary model of maternal effect senescence demonstrates that age-attenuated selection is inevitable late-in-life (Moorad & Nussey 2016). However, natural selection can shape evolution only to the degree made available by the underlying genetic architecture (Lande 1979).…”

“…Finally, it should be emphasized that future conceptual advancements in evolutionary theory could provide better models to explain maternal effect senescence, perhaps by embellishing upon the relative simple population genetic model of Moorad and Nussey (2016). There are many features known to be important to reproductive and actuarial senescence that are not included in this model, such as across-age genetic pleiotropy (Williams 1957;Charlesworth 2001), selective disappearance (Vaupel et al 1979;Vaupel & Yashin 1985;van de Pol & Verhulst 2006), mutational bias (Moorad & Promislow 2008), density-and condition-dependent effects (Abrams 1993;Williams & Day 2003), and within-age trade-offs (Charlesworth & León 1976).…”

“…Hughes and Charlesworth 1994), and in particular, population genetic models of mutation accumulation predict Gompertz mortality in adults (Charlesworth 2001). More recently, Moorad and Nussey (2016) applied this approach to quantify how age changes the strength of selection for age-specific maternal effects and to show how these changes cause maternal effects upon neonatal survival to evolve. They predicted that evolved demographic patterns of this manifestation of senescence are qualitatively different from actuarial or reproductive senescence.…”

“…In this paper, we address conspicuous gaps in our understanding of maternal effect senescence by performing an extensive systematic review of the literature using metaanalytical methodology. We have chosen neonatal survival as our focus for several reasons: 1) this trait's relationship to fitness is profound and well-understood conceptually (Hamilton 1966); 2) evolutionary theory explicitly models age-specific maternal effects on this trait (Moorad & Nussey 2016); 3) conventional demographic models of actuarial senescence can be adapted to describe maternal-age trajectories; and 4) associations between the trait and maternal age are observed with sufficient frequency to enable meta-analyses. This study asks two sets of questions about the nature of maternal effect senescence as it manifests on neonatal survival rates:…”

Maternal Effect Senescence and Fitness: A Demographic Analysis of a Novel Model Organism

“…Maternal effect senescence refers to reduced success or quality of offspring with advancing age of the mother [7]. Advanced maternal age has known negative effects on offspring health, lifespan and fertility in humans and other species [8][9][10][11][12][13][14][15][16].…”