Inclusive fitness forces of selection in an age-structured population

Abstract

Current evolutionary theories of senescence predict that the force of selection on survival will decline from maturity to zero at the age of last reproduction, and the force of selection on reproduction will decline monotonically from birth. These predictions rest upon the assumption that individuals within a population do not interact with one another. This assumption, however, is violated in social species, where an individuals survival and/or reproduction may shape the fitness of other group members. In such species, it is inclusive fitness that natural selection optimises. Yet, it remains unclear how the forces of selection on survival and reproduction might be modified when inclusive fitness, rather than population growth rate, is considered the appropriate metric for fitness. Here, we derive inclusive fitness forces of selection for hypothetical populations of social species. We show that selection on survival is not always constant before maturity, and can remain above zero in post-reproductive age classes, contrary to conventional models of senescence. We also show how the trajectory of the force of selection on reproduction does not always decline monotonically from birth, as predicted by classical theory, but instead depends on the balance of benefits to direct fitness and costs to indirect fitness. Our theoretical framework provides the unique opportunity to expand our understanding of senescence across social species, with important implications to species with variable life histories.

Sexual antagonism in sequential hermaphrodites

“…Such asymmetric fitness effects too may bias the invasion of sexually antagonistic alleles in one direction or another. Analogous to this is the analysis of the force of selection in the study of senescence, where researchers, by incorporating different mutational effects [68], or indirect fitness effects [69,70], find that the force of selection does not appear to decline with age as classically suggested [26,71,72], but may show a much more complex pattern depending on the further assumptions made. Yet, while these additional effects may shift the balance of sexually antagonistic (or antagonistically pleiotropic) alleles in particular cases, reproductive value continues to provide the underlying weightings to these effects.…”

Current perspectives and future directions in animal life history evolution

“…To quantify this relative fitness, researchers often use reproductive value: the discounted contribution of an individual to future offspring (for a thorough explanation, see: Etheridge, 2011 andGrafen, 2006). Using reproductive value, researchers are able to build hypotheses as to the evolution of life history strategies in structured populations (e.g., senescence in age-structured populations (Newton & Rothery, 1997;Roper et al, 2021), the evolution of sociality (Roper et al, 2023), bet-hedging (Grafen, 1999) and parasitism (Andersson, 2017)).…”

Evolution in a Complicated World

“…In 2003, Lee presented a model incorporating energy transfers between family members that demonstrated the potential for the force of selection to increase during successive juvenile stages. Roper et al (2022), who considered a spatial model with an explicit focus on kin selection, under certain conditions also observed an increasing force of selection at the juvenile stage. Both models incorporate a large amount of mechanistic detail regarding the interactions between family members, and the generality of these findings with respect to the force of selection is presently unclear.…”

“…The supposed constant force of selection during infancy however contrasts with extensive evidence that mortality decreases towards maturity ('ontogenescence', Levitis and Martínez 2013). Age-structured models generally assume offspring to become independent the moment they are born, and thereby ignore dependencies between parents and offspring (although see Kahn et al 2015;Roper et al 2022). Indeed, offspring of many taxa crucially depend on their parents during substantial parts of ontogeny, and parents are often prevented from beginning a new reproductive cycle while taking care of their young.…”

“…Such extensions are feasible, but the specification of costs and benefits of parental care becomes nontrivial, with different modelling options to be explored. The models that so far have observed an increasing force of selection before the age of first reproduction were in fact mechanistic models that considered interactions between relatives in greater detail Roper et al, 2022). And finally, because the model considers adult reproductive stages rather than age classes, vital rates are independent of parental age.…”