Sexual selection and population spatial structure interact to shape sex-specific evolutionary responses in physiology

Different selection pressures acting on females and males arising from sexual selection and sexual conflict may lead to sex-specific phenotypic expression of physiological traits. Importantly, sexual selection is affected by ecological and demographic factors. We explored whether population spatial structure modulates the effect of sexual selection on male and female standard metabolic rates and oxidative stress. For this purpose, we used selection lines of the seed beetle Callosobruchus maculatus subjected to divergent evolutionary regimes in the intensity of sexual selection (high vs. low, in polygamous vs. enforced monogamous populations, respectively) and the presence of metapopulation structure (absent vs. present). We found that the evolutionary treatments impacted physiological traits in a complex way. While in the selection regimes simulating metapopulation structure (i.e., divided populations) both sexes had similar metabolic rates, in undivided (unstructured) populations males had lower rates than females. Males from polygamous and undivided populations showed the lowest levels of antioxidant enzymes quantified as superoxide dismutase (SOD), resulting in strong sexual dimorphism in SOD levels in this selection regime. The oxidative damage to lipids measured as thiobarbituric acid reactive substances levels, instead, was highest for both males and females from monogamous and undivided populations. On the whole, our results reveal two key insights. First, physiological traits evolve differently in females and males in response to sexual selection intensity and population spatial structure. Second, such sex-specific physiological responses are linked to selective pressures acting mostly on males. We highlight the importance of considering ecological and demographic factors when evaluating whether sexual selection drives sex-specific trait evolution.