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

Abstract

Whether sexual selection impedes or aids adaptation has become an outstanding question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics. 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 be either avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes 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 stressful environments (elevated temperature and a host plant shift). We found evidence that sexual selection on males had positive genetic effects on female fitness components across environments, supporting good‐genes sexual selection. Interestingly, however, when males evolved under sexual selection with fecundity selection removed, they became more robust to both temperature and host plant stress compared to their conspecific females and males from the other evolution regimes that applied fecundity selection. We quantified the population‐level consequences of this sex‐specific adaptation and found evidence that the cost of sociosexual interactions in terms of reduced offspring production was higher in the regime applying only sexual selection to males. Moreover, the cost tended to be more pronounced at the elevated temperature to which males from the 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 the relative efficacies of sexual selection and fecundity selection can cause inherent sex differences in environmental robustness that may impact demography of maladapted populations.

The ecology of sexual conflict: Temperature variation in the social environment can drastically modulate male harm to females

“…On the one hand, several studies over the last few years have shown that IASC can be strongly modulated by the environment so that inter‐sexual correlations in fitness can change significantly across environments (Berger et al, ; Long, Agrawal, & Rowe, ; Punzalan, Delcourt, & Rundle, , but see Delcourt, Blows, & Rundle, ; Martinossi‐Allibert, Savkovic et al, ; Punzalan et al, ). On the other, a few studies have also shown that IRSC can be similarly affected by the environment (Martinossi‐Allibert, Thilliez, Arnqvist, & Berger, ). For example, using Drosophila melanogaster , Arbuthnott, Dutton, Agrawal, and Rundle () showed that evolution of male harm and female resistance is conditioned by the environment, and Yun et al showed that the physical environment (i.e., small and simple vs. large and complex) drastically affects sexual interactions and male harm in the same species (Yun et al, ).…”

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

“…The polygamy and monogamy regime show differences consistent with generally positive effects of sexual selection on genetic quality: already following 16 generations of experimental evolution, polygamy lines showed higher individual lifetime reproductive success compared to monogamy lines (Martinossi‐Allibert et al. ). Moreover, at generations 20 (Martinossi et al.…”

“…), and experimental evolution (Martinossi‐Allibert et al. ) to demonstrate substantial standing genetic variation in behavior, life‐history, and sex‐specific life time reproductive success. Preliminary screening of mitochondrial haplotypes in these lines (D. Berger, unpublished data) show extreme levels of polymorphism, as expected given large population sizes and that the lines originate from the center of the species range (Tuda et al.…”

“…The lines used in this study are thoroughly described in Martinossi‐Allibert et al. (). In brief, the lines and the outbred base population from which they originate were maintained under controlled temperature (29°C), humidity (50%RH), and light cycle (12L: 12D), and were reared on the preferred host plant Vigna unguiculata (black‐eyed bean) (Tuda et al.…”

“…Effective population size in each regime was kept approximately equal ( N e = 150, N monogamy = 246, and N polygamy = 300) and the number of beans provided as egg laying substrate in each regime was standardized to give the same, relatively low, juvenile density (2–4 eggs/bean) to minimize (and equalize) larval competition (Martinossi‐Allibert et al. ). The polygamy and monogamy regime show differences consistent with generally positive effects of sexual selection on genetic quality: already following 16 generations of experimental evolution, polygamy lines showed higher individual lifetime reproductive success compared to monogamy lines (Martinossi‐Allibert et al.…”