The consequences of sexual selection in well-adapted and maladapted populations of bean beetles.

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modeling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex-specific strengths of selection and IaSC by cross-rearing the two experimental evolution regimes on the alternative hosts and estimating within-population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male-bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.This is the peer reviewed version of the following article: Martinossi-Allibert I, Savković U, Đorđević M, Arnqvist G, Stojković B, Berger D. The consequences of sexual selection in well-adapted and maladapted populations of bean beetles, which has been published in final form at [https://doi.org/10.1111/evo.13412]. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving

Sexual Selection and Adaptation to Novel Environments

The work included in this thesis aims at exploring the environmental sensitivity of benefits and costs of sexual selection through a combined empirical and theoretical effort, to increase our understanding of the impact of environmental change on sexually reproducing populations.Can sexual selection promote adaptation to novel environments? Sexual selection for good genes should accelerate adaptation by granting higher reproductive success to individuals of high genetic quality. However, sexual conflict is a frequent outcome of sexual reproduction and may often be detrimental to population fitness. Experimental evolution has shown that the role of sexual selection in adaptation is variable, because of a complex balance between the detrimental and beneficial effects described above.The present thesis is investigating the role of sexual selection in adaptation by focusing on the sex-specific strength of selection and the intensity of intralocus sexual conflict (IaSC) in ancestral and novel environments. The sex-specific strength of selection is a valuable proxy for the benefits of sexual reproduction, since a male-bias in selection caused by sexual selection should allow efficient purging of deleterious alleles with little impact on female fecundity and cost to population fitness.This thesis investigates both sex-specific selection and IaSC across benign and novel environments in two species of seed beetles, Callosobruchus maculatus and Acanthoscelides obtectus, and includes a theoretical model of the effect of environmental change on of sexual selection. The empirical part of my results indicates that, generally, selection at the adult stage is male biased but that this male bias may be reduced under stress, pointing towards reduced benefits of sexual selection under rapid environmental change. Additional simulations suggest that the frequency dependent nature of sexual selection alone could explain this trend. No empirical support was found for the reduction of IaSC under stress.It is becoming crucial today to understand the impact of environmental change on natural populations. This thesis brings new material adding to our understanding of the role of sexual selection within that particular issue. The outcome of sexual selection is dependent on a variety of mechanisms, such as good genes processes and sexual conflict, which are very likely to be dependent on ecological factors and specificity of the system studied. For that reason, carefully controlled experiments on laboratory systems and mathematical modelling are necessary steps that should ultimately lead to the study of similar questions in natural systems

Female-specific resource limitation does not make the opportunity for selection more female biased

Competition for limiting resources and stress can magnify variance in fitness and therefore selection. But even in a common environment, the strength of selection can differ across the sexes, as their fitness is often limited by different factors. Indeed, most taxa show stronger selection in males, a bias often ascribed to intense competition for access to mating partners. This sex bias could reverberate on many aspects of evolution, from speed of adaptation to genome evolution. It is unclear, however, whether stronger opportunity for selection in males is a pattern robust to sex-specific stress or resource limitation. We test this in the model speciesCallosobruchus maculatusby comparing female and male opportunity for selection (i) with and without limitation of quality oviposition sites, and (ii) under delayed age at oviposition. Decreasing the abundance of the resource key to females or increasing their reproductive age was challenging, as shown by a reduction in mean fitness, but opportunity for selection remained stronger in males across all treatments, and even more so when oviposition sites were limiting. This suggests that males remain the more variable sex independent of context, and that the opportunity for selection through males is indirectly affected by female-specific resource limitation

Data from: Sex-specific selection under environmental stress in seed beetles

Sexual selection can increase rates of adaptation by imposing stronger selection in males, thereby allowing efficient purging of the mutation load on population fitness at a low demographic cost. Indeed, sexual selection tends to be male-biased throughout the animal kingdom, but little empirical work has explored the ecological sensitivity of this sex difference. In this study, we generated theoretical predictions of sex-specific strengths of selection, environmental sensitivities and genotype-by-environment interactions, and tested them in seed beetles by manipulating either larval host plant or rearing temperature. Using fourteen isofemale lines, we measured sex-specific reductions in fitness components, genotype-by-environment interactions, and strength of selection (variance in fitness) in the juvenile and adult stage. As predicted, variance in fitness increased with stress, was consistently greater in males than females for adult reproductive success (implying strong sexual selection), but was similar in the sexes in terms of juvenile survival across all stress-levels. While genetic variance in fitness increased in magnitude under severe stress, heritability decreased, and particularly so in males. Moreover, genotype-by-environment interactions for fitness were common but specific to the type of stress and each sex and life stage, suggesting that new environments may change the relative alignment and strength of selection in males and females. Our study thus exemplifies how environmental stress can influence the relative forces of natural and sexual selection, as well as concomitant changes in genetic variance in fitness, which are predicted to have consequences for rates of adaptation in sexual populations

Fitness data

Juvenile survival and adult reproductive success for isofemale lines of C. maculatus in 5 different environments

Data from: 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 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 either be 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 socio-sexual 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

Data from: The efficacy of good genes sexual selection under environmental change

Sexual selection can promote adaptation if sexually selected traits are reliable indicators of genetic quality. Moreover, models of good genes sexual selection suggest that, by operating more strongly in males than in females, sexual selection may purge deleterious alleles from the population at a low demographic cost, offering an evolutionary benefit to sexually reproducing populations. Here, we investigate the effect of good genes sexual selection on adaptation following environmental change. We show that the strength of sexual selection is often weakened relative to fecundity selection, reducing the suggested benefit of sexual reproduction. This result is a consequence of incorporating a simple and general mechanistic basis for how sexual selection operates under different mating systems, rendering selection on males frequency-dependent and dynamic with respect to the degree of environmental change. Our model illustrates that incorporating the mechanism of selection is necessary to predict evolutionary outcomes and highlights the need to substantiate previous theoretical claims with further work on how sexual selection operates in changing environments

Mathematica code.

The mathematica code used to build the model described in that article