Does perception of female cues modulate male short-term fitness components in Drosophila melanogaster?

Phenotypic plasticity in reproductive behavior can be a strong driver of individual fitness. In species with high intra-sexual competition, changes in socio-sexual context can trigger quick adaptive plastic responses in males. In particular, a recent study in the vinegar fly (Drosophila melanogaster) shows that males derive net fitness benefits from being shortly exposed to female cues ahead of access to mating (termed sexual perception), but the underlying mechanisms of this phenomenon remain unknown. Here, we investigated the short-term effects of female perception on male pre- and post-copulatory components of reproductive performance: (a) mating success, (b) mating latency and duration, (c) sperm competitiveness, and (d) ejaculate effects on female receptivity and reproductive rate. We found that brief sexual perception increased mating duration, but had no effect on the other main pre- and post-copulatory fitness proxies recorded. This suggests that perception of female cues may not yield net fitness benefits for males in the short-term, but we discuss alternative explanations and future avenues of research.

Male Adaptive Plasticity Can Explain the Evolution of Sexual Perception Costs.

AbstractSensory perception of environmental cues has been shown to trigger plastic responses that can induce important fitness costs, including the dramatic modulation of aging across distant taxa. For example, male Drosophila melanogaster suffer a marked decrease in fitness, characterized by faster reproductive and actuarial aging, if they perceive female cues but fail to mate shortly after (aging via sexual perception). While this has been a breakthrough for our understanding of the mechanisms of aging, it raises the question of why such plastic responses evolved. Here, we used D. melanogaster to ask whether sexual perception costs may be a by-product of adaptive plastic responses to female cues. We found that (a) short-term perception (1 day) of female cues before mating opportunities increases male relative lifetime reproductive success in a competitive environment, (b) medium-term perception (3-7 days) is neutral, and (c) long-term perception (15 days) leads to reproductive costs. We then ran mathematical simulations under a wide range of sociosexual and demographic scenarios to show that such plastic male responses can be adaptive whenever mating rates fluctuate within the range experienced by D. melanogaster and other insects in the wild, suggesting that this may be a widespread strategy in nature. Finally, we show that, because the short-term benefits of plastic responses will be acquired mostly by high-quality males while long-term costs will be paid mostly by low-quality males, sexual perception can significantly magnify sexual selection (15%-27% average increase in the opportunity for selection).

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.