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

Abstract Sexual dimorphism in immunity is believed to reflect sex-differences in 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 data 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 as a result of sex-biased expression of genes in the proPO activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (relative to natural polygamy) rapidly decreases female (but not male) PO activity. The evolution of decreased PO in monogamous females was accompanied by increased tolerance to bacterial infection unrelated to mating. This implies that female responses to costly mating may trade off with other aspects of immune defence. Finally, female (but not male) PO activity show 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 results thus provide a proximate and ultimate understanding of the links between sexual selection and sexual dimorphism in immunity.