Directional and disruptive selection in populations structured by class and continuous ontogeny under incomplete plasticity
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Many organisms undergo ontogeny, whereby individuals change in state (e.g. in size, morphology, or condition) as they age. Understanding the evolution of traits influencing ontogeny is challenging because their fitness effects unfold across an individual’s lifetime and may differ between classes such as sexes. Here, we analyze selection on non-plastic traits (e.g., fixed resource allocation strategies) that determine the development of dynamical states throughout life (e.g., body size), with consequences for fecundity and survival in age- and class-structured populations. Using invasion analysis, we derive expressions for directional and quadratic selection that decompose into age- and class-specific components. This allows us to identify convergence stable trait values, assess whether they are uninvadable or potentially experience evolutionary branching, and pinpoint the age and class pathways through which correlational and disruptive selection act. Applying our results to a model of growth under size-mediated sexual selection, we show how developmental trade-offs and sex-specific constraints can generate disruptive selection on male growth and favour the evolution of alternative male life histories. More broadly, our results highlight how adaptation is mediated by the interaction of development and demography, and provide tools to investigate how conflicts across ages and classes influence senescence, sexual dimorphism, and the diversification of ontogenetic strategies.
Author Summary
How does natural selection shape traits that influence how organisms develop through their lifetime? This question is difficult because the effects of such traits unfold dynamically as individuals change in states such as size or condition, which in turn influence survival and reproduction throughout life. We developed a mathematical model that follows these causal links and characterises the gradual evolution of developmental traits. Our results apply to populations with different classes, such as males and females, that follow distinct developmental and demographic paths. Our model reveals when selection is stabilizing, holding populations fixed for an optimal trait value, and when it is disruptive, favouring trait diversification into alternative life-history strategies. As an illustration, we analyse the evolution of sex-specific growth under size-based sexual selection. We show how developmental trade-offs and demographic differences can generate disruptive selection on male growth, leading to the coexistence of fast-growing short-lived males and slow-growing long-lived ones. More broadly, our results link development, demography, and adaptation, and show how their interplay shapes biological diversity both within and between populations.
