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 individual’s 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.

Effects of development and parental care on Hamilton’s force of selection

“…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 11 were in fact mechanistic models that considered interactions between relatives in greater detail (Lee 2003, Roper et al 2022. Further work remains to be done on the force of selection before maturity with regards to potential parent-offspring conflicts (Ronce & Promislow 2010, Kramer et al 2016) and the effect of density dependence (Mylius & Diekmann 1995, Pen & Weissing 2000, Kokko 2021).…”

“…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 (Lee 2003, Roper et al 2022). And finally, because the model considers adult reproductive stages rather than age classes, vital rates are independent of parental age.…”

“…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 2011, Levitis & Martínez 2013). Age-structured models generally assume offspring to become independent the moment they are born, and thereby ignore dependencies between parents and offspring (but see Lee 2003, 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.…”