Sexual selection, environmental robustness, and evolutionary demography of maladapted populations: A test using experimental evolution in seed beetles

Whether sexual selection impedes or aids adaptation has become a pressing question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics and viability. The net effect of sexual selection on population viability results from a balance between genetic benefits of good genes effects and costs of sexual conflict. Depending on how these facets of sexual selection are affected under environmental change, extinction of maladapted populations could either be avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes (polygamy, monogamy and male-limited selection) to disentangle the contributions of sexual selection, fecundity selection and male-female coevolution to individual reproductive success and population fitness. We compared these contributions between the ancestral environment and two new stressful environments (temperature and host plant shift). Evolution under polygamy resulted in the highest individual reproductive success in competitive context for both sexes. Moreover, females evolving only via sexual selection on their male siblings in the male-limited regime had similar reproductive success and higher fertility than females evolving under monogamy, suggesting that sexual selection on males had positive effects on female fitness components. Interestingly, male-limited sexual selection resulted in males that were robust to stress, compared to males from the two evolution regimes applying fecundity selection. We quantified the population-level consequences of this sex-specific adaptation and found evidence that costs of socio-sexual interactions were higher in male-limited lines compared to polygamous lines, and that this difference was particularly pronounced at elevated temperature to which males from the male-limited regime were more robust compared to their conspecific females. These results illustrate the tension between individual-level adaptation and population-level viability in sexually reproducing species and suggest that sex-specific selection can cause differences in environmental robustness that may impact population demography under environmental change.