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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.

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. How important mtDNA polymorphism is for adaptation is still unclear. This study tests 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 beetles. Our results demonstrate natural selection on mtDNA haplotypes, with some support for thermal environment influencing mtDNA evolution through mitonuclear epistasis. We also test for sex‐specific consequences of mtDNA evolution on reproductive success, given that mtDNA mutations can have sexually antagonistic fitness effects, but find that the changes in fitness were aligned in the sexes.

1. Because males and females of internally inseminating species interact directly during mating, adaptations in one sex in primary reproductive traits may trigger an evolutionary response in the other sex. Divergent postcopulatory sexual selection is considered the main driving force behind the evolution of many male and female reproductive traits, generating unique morphologies and physiologies that can contribute to reproductive isolation and, ultimately, speciation. 2. The focus of most previous studies of the evolution of primary reproductive characters has been male reproductive traits and ejaculate or sperm characteristics. However, in order to more fully understand the evolution of primary reproductive characters it is crucial that we also include female traits. 3. In insects, both the size and the composition of the ejaculate have been shown to influence female reproduction in numerous ways by affecting female remating behaviour, female fecundity and female life span. Here, we employ a phylogenetic comparative approach to assess correlated evolution between primary reproductive characters in males and those in females in a group of seed beetles (Chrysomelidae: Bruchinae). We further explore correlated evolution between ejaculate size and female fitness in these insects. 4. Our analyses revealed positive correlated evolution between three internal female reproductive traits and ejaculate weight as well as correlated evolution between ejaculate weight and female fitness. We discuss the causal factors behind this correlated evolution and suggest that the evolution of larger ejaculates, primarily by postcopulatory sexual selection, causes selection for larger primary sexual traits in females to allow females to more rapidly process ejaculates. This may then feedback on postcopulatory selection in males, reinforcing selection for larger ejaculates. 5. Our results show that the primary reproductive traits of males and females show correlated evolution and suggest that intersexual co-evolution may affect the evolution of female fitness.

Male seminal fluid proteins are known to affect female reproductive behavior and physiology by reducing mating receptivity and by increasing egg production rates. Such substances are also though to increase the competitive fertilization success of males, but the empirical foundation for this tenet is restricted. Here, we examined the effects of injections of size-fractioned protein extracts from male reproductive organs on both male competitive fertilization success (i.e., P2 in double mating experiments) and female reproduction in the seed beetle Callosobruchus maculatus. We found that extracts of male seminal vesicles and ejaculatory ducts increased competitive fertilization success when males mated with females 1 day after the females' initial mating, while extracts from accessory glands and testes increased competitive fertilization success when males mated with females 2 days after the females' initial mating. Moreover, different size fractions of seminal fluid proteins had distinct and partly antagonistic effects on male competitive fertilization success. Collectively, our experiments show that several different seminal fluid proteins, deriving from different parts in the male reproductive tract and of different molecular weight, affect male competitive fertilization success in C. maculatus. Our results highlight the diverse effects of seminal fluid proteins and show that the function of such proteins can be contingent upon female mating status. We also document effects of different size fractions on female mating receptivity and egg laying rates, which can serve as a basis for future efforts to identify the molecular identity of seminal fluid proteins and their function in this model species.

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.

Abstract When different alleles are favored in different environments, dominance reversal where alternate alleles are dominant in the environment in which they are favored can generate net balancing selection. The sexes represent two distinct genetic environments and sexually antagonistic (SA) selection can maintain genetic variation, especially when the alleles involved show sex-specific dominance. Sexual dimorphism in gene expression is pervasive and has been suggested to result from SA selection. Yet, whether gene-regulatory variation shows sex-specific dominance is poorly understood. We tested for sex-specific dominance in gene expression using three crosses between homozygous lines derived from a population of a seed beetle, where a previous study documented a signal of dominance reversal for fitness between the sexes. Overall, we found that the dominance effects of variants affecting gene expression were positively correlated between the sexes (r = 0.33 to 0.44). Yet, 586 transcripts showed significant differences in dominance between the sexes. Sex-specific dominance was significantly more common in transcripts with more sex-biased expression, in two of three of our crosses. Among transcripts showing sex-specific dominance, lesser sexual dimorphism in gene expression among heterozygotes was somewhat more common than greater. Gene ontology enrichment analyses showed that functional categories associated with known SA phenotypes in Callosobruchus maculatus were overrepresented among transcripts with sex-specific dominance, including genes involved in metabolic processes and the target-of-rapamycin pathway. Our results support the suggestion that sex-specific dominance of regulatory variants contributes to the maintenance of genetic variation in fitness mediated by SA selection in this species.

Insect genitalia exhibit rapid divergent evolution. Truly extraordinary structures have evolved in some groups, presumably as a result of post-mating sexual selection. To increase our understanding of this phenomenon, we studied the function of one such structure. The male genitalia of Callosobruchus subinnotatus (Coleoptera: Bruchinae) contain a pair of jaw-like structures with unknown function. Here, we used phenotypic engineering to ablate the teeth on these jaws. We then experimentally assessed the effects of ablation of the genital jaws on mating duration, ejaculate weight, male fertilization success and female fecundity, using a double-mating experimental design. We predicted that copulatory wounding in females should be positively related to male fertilization success. However, we found no significant correlation between genital tract scarring in females and male fertilization success. Male fertilization success was, however, positively related to the amount of ejaculate transferred by males and negatively related to female ejaculate dumping. Ablation of male genital jaws did not affect male relative fertilization success but resulted in a reduction in female egg production. Our results suggest that postmating sexual selection in males indeed favors these genital jaws, but not primarily through an elevated relative success in sperm competition but by increasing female egg production.

Reproductive conflict between the sexes is thought to be a key force in the evolution of many reproductive characters, but persuasive evidence for its significance is still scarce. The spectacular evolution of male genitalia that impose physical injury on females during mating has often been suggested to be a product of sexually antagonistic coevolution, but our understanding of these extraordinary adaptations is very limited, and there are no direct data addressing their evolutionary elaboration. We show that more spiny male genitalia causes more harm to females during copulation and provide comparative evidence for the correlated evolution between these antagonistic adaptations in males and a female counteradaptation (the amount of connective tissue in the copulatory duct) in a group of insects. By combining comparative and experimental methods, we demonstrate that imbalance of relative armament of the sexes affects evolution of the economics of reproduction: as males evolve genitalia that are more harmful relative to the level of female counteradaptation, costs associated with mating for females increase and population fitness is depressed. Our results unveil a coevolutionary arms race between the sexes and are consistent with a proposed link between sexual conflict, species' viability, and the risk of extinction.

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. 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. 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.