Laurent Lehmann, Charles Mullon
Adaptive polymorphisms in quantitative traits are characterised by the coexistence of distinct genetically encoded phenotypes maintained by selection. Such intraspecific genetic and phenotypic variation makes a substantial contribution to biological diversity. Building on established results from invasion analysis, we analyse conditions under which adaptive polymorphism can emerge under long-term gradual evolution. We first note that, in general, fully characterising an adaptive polymorphism, including its number of morphs, trait values and frequencies, is a computationally hard problem. Nevertheless, standard invasion results reveal a unifying necessary condition for the gradual emergence of polymorphism: negative trait-dependent selection (NTDS), whereby the marginal fitness effect of increasing trait expression in a mutant depends negatively on the population-level trait expression, reflecting a negative interaction between mutant and population trait changes. We use NTDS as an organising principle to structure the pathways through which polymorphism can evolve. This is based on a decomposition of fitness that distinguishes production factors, the inputs to survival and reproduction that are endogenous to individuals, from regulating factors, the ecological, social or genetic inputs to fitness that are influenced in part by conspecifics. This decomposition allows us to clarify how NTDS arises across three broad classes of interactions: ecological, social and genetic; and to identify previously unrecognised adaptive polymorphisms in well-studied scenarios, including life-history, social preferences, and class-structured populations. More broadly, by integrating perspectives from population genetics, evolutionary ecology, adaptive dynamics, game theory and inclusive fitness theory, we aim to provide a common thread among the pathways through which selection favours intraspecific variation.