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.
Highlights
Evolutionary rescue critically depends on genetic responses being rapid enough to allow populations to track changes in their environ‐ ment while the demographic cost of maladaptation remains small enough to avoid genetic drift and extinction (Bell & Gonzales, 2009, Carlson, Cunningham, & Westley, 2014; Derry et al, 2019; Gonzalez, Ronce, Ferriere, & Hochberg, 2013; Orr & Unckless, 2014; Walters, Blanckenhorn, & Berger, 2012)
In sexually reproducing spe‐ cies, these dynamics can become of particular importance, and be‐ cause while population growth often depends strongly on female egg production, adaptation in traits increasing male fertilization success may have only weak, and sometimes even negative, ef‐ fects on population viability (Arnqvist & Rowe, 2005; Clutton‐Brock & Parker, 1995; Rankin et al, 2011, see Fraser et al, 2019 of this special issue)
We observed a cost of sociosexual interactions in all evolution regimes at the ancestral temperature (Figure 3). We suggest that this effect is mainly medi‐ ated by interlocus sexual conflict (IeSC), given that there are well‐known costs to females of mating multiply and documented sexually antagonistic coevolution involving male and female genitalia in this species (Crudgington & Siva‐Jothy, 2000; Dougherty et al, 2017; Edvardsson & Tregenza, 2005; Gay et al, 2011; Rönn, Katvala, & Arnqvist, 2007)
Summary
Evolutionary rescue critically depends on genetic responses being rapid enough to allow populations to track changes in their environ‐ ment while the demographic cost of maladaptation remains small enough to avoid genetic drift and extinction (Bell & Gonzales, 2009, Carlson, Cunningham, & Westley, 2014; Derry et al, 2019; Gonzalez, Ronce, Ferriere, & Hochberg, 2013; Orr & Unckless, 2014; Walters, Blanckenhorn, & Berger, 2012). Hypotheses suggesting that sexual selection should increase population fitness assume that the expression and maintenance of these traits are energetically costly and reflect the bear‐ er's overall condition and genetic quality (Hamilton & Zuk, 1982; Jennions, Moller, Petrie, Mller, & Bernard, 2001; Zahavi, 1975) Such sexual selection for “good genes” could target large parts of the genome and purge deleterious mutations with pleiotropic ef‐ fects on survival and female fecundity (the genic capture hypothesis, Rowe & Houle, 1996; Tomkins, Radwan, Kotiaho, & Tregenza, 2004).
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