Environmental complexity mitigates the demographic impact of sexual selection.

Sexual selection and the evolution of costly mating strategies can negatively impact population viability and adaptive potential. While laboratory studies have documented outcomes stemming from these processes, recent observations suggest that the demographic impact of sexual selection is contingent on the environment and therefore may have been overestimated in simple laboratory settings. Here we find support for this claim. We exposed copies of beetle populations, previously evolved with or without sexual selection, to a 10-generation heatwave while maintaining half of them in a simple environment and the other half in a complex environment. Populations with an evolutionary history of sexual selection maintained larger sizes and more stable growth rates in complex (relative to simple) environments, an effect not seen in populations evolved without sexual selection. These results have implications for evolutionary forecasting and suggest that the negative demographic impact of sexually selected mating strategies might be low in natural populations.

Experimental Life History Evolution Results in Sex-specific Evolution of Gene Expression in Seed Beetles.

The patterns of reproductive timing and senescence vary within and across species owing to differences in reproductive strategies, but our understanding of the molecular underpinnings of such variation is incomplete. This is perhaps particularly true for sex differences. We investigated the evolution of sex-specific gene expression associated with life history divergence in replicated populations of the seed beetle Acanthoscelides obtectus, experimentally evolving under (E)arly or (L)ate life reproduction for >200 generations which has resulted in strongly divergent life histories. We detected 1,646 genes that were differentially expressed in E and L lines, consistent with a highly polygenic basis of life history evolution. Only 30% of differentially expressed genes were similarly affected in males and females. The evolution of long life was associated with significantly reduced sex differences in expression, especially in non-reproductive tissues. The expression differences were overall more pronounced in females, in accordance with their greater phenotypic divergence in lifespan. Functional enrichment analysis revealed differences between E and L beetles in gene categories previously implicated in aging, such as mitochondrial function and defense response. The results show that divergent life history evolution can be associated with profound changes in gene expression that alter the transcriptome in a sex-specific way, highlighting the importance of understanding the mechanisms of aging in each sex.

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity.

BACKGROUND: Sexual dimorphism in immunity is believed to reflect sex differences in reproductive strategies and trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex differences in immunity as well as associated host-pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. RESULTS: We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex differences in the expression of genes in the prophenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and reduced sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females had evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. CONCLUSIONS: Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host-pathogen dynamics in sexually reproducing organisms.

An experimental test of temperature-dependent selection on mitochondrial haplotypes in Callosobruchus maculatus seed beetles.

Mitochondrial DNA (mtDNA) consists of few but vital maternally inherited genes that interact closely with nuclear genes to produce cellular energy. How important mtDNA polymorphism is for adaptation is still unclear. The assumption in population genetic studies is often that segregating mtDNA variation is selectively neutral. This contrasts with empirical observations of mtDNA haplotypes affecting fitness-related traits and thermal sensitivity, and latitudinal clines in mtDNA haplotype frequencies. Here, we experimentally test whether ambient temperature affects selection on mtDNA variation, and whether such thermal effects are influenced by intergenomic epistasis due to interactions between mitochondrial and nuclear genes, using replicated experimental evolution in Callosobruchus maculatus seed beetle populations seeded with a mixture of different mtDNA haplotypes. We also test for sex-specific consequences of mtDNA evolution on reproductive success, given that mtDNA mutations can have sexually antagonistic fitness effects. Our results demonstrate natural selection on mtDNA haplotypes, with some support for thermal environment influencing mtDNA evolution through mitonuclear epistasis. The changes in male and female reproductive fitness were both aligned with changes in mtDNA haplotype frequencies, suggesting that natural selection on mtDNA is sexually concordant in stressful thermal environments. We discuss the implications of our findings for the evolution of mtDNA.

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 species Callosobruchus maculatus by 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.