Thermal phenotypic plasticity of pre- and post-copulatory male harm buffers sexual conflict in wild Drosophila melanogaster.

Strong sexual selection frequently leads to sexual conflict and ensuing male harm, whereby males increase their reproductive success at the expense of harming females. Male harm is a widespread evolutionary phenomenon with a strong bearing on population viability. Thus, understanding how it unfolds in the wild is a current priority. Here, we sampled a wild Drosophila melanogaster population and studied male harm across the normal range of temperatures under which it reproduces optimally in nature by comparing female lifetime reproductive success and underlying male harm mechanisms under monogamy (i.e. low male competition/harm) vs. polyandry (i.e. high male competition/harm). While females had equal lifetime reproductive success across temperatures under monogamy, polyandry resulted in a maximum decrease of female fitness at 24°C (35%), reducing its impact at both 20°C (22%), and 28°C (10%). Furthermore, female fitness components and pre- (i.e. harassment) and post-copulatory (i.e. ejaculate toxicity) mechanisms of male harm were asymmetrically affected by temperature. At 20°C, male harassment of females was reduced, and polyandry accelerated female actuarial aging. In contrast, the effect of mating on female receptivity (a component of ejaculate toxicity) was affected at 28°C, where the mating costs for females decreased and polyandry mostly resulted in accelerated reproductive aging. We thus show that, across a natural thermal range, sexual conflict processes and their effects on female fitness components are plastic and complex. As a result, the net effect of male harm on overall population viability is likely to be lower than previously surmised. We discuss how such plasticity may affect selection, adaptation and, ultimately, evolutionary rescue under a warming climate.

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.

No evidence that relatedness or familiarity modulates male harm in Drosophila melanogaster flies from a wild population.

Sexual selection frequently promotes the evolution of aggressive behaviors that help males compete against their rivals, but which may harm females and hamper their fitness. Kin selection theory predicts that optimal male-male competition levels can be reduced when competitors are more genetically related to each other than to the population average, contributing to resolve this sexual conflict. Work in Drosophila melanogaster has spearheaded empirical tests of this idea, but studies so far have been conducted in laboratory-adapted populations in homogeneous rearing environments that may hamper kin recognition, and used highly skewed sex ratios that may fail to reflect average natural conditions. Here, we performed a fully factorial design with the aim of exploring how rearing environment (i.e., familiarity) and relatedness affect male-male aggression, male harassment, and overall male harm levels in flies from a wild population of Drosophila melanogaster, under more natural conditions. Namely, we (a) manipulated relatedness and familiarity so that larvae reared apart were raised in different environments, as is common in the wild, and (b) studied the effects of relatedness and familiarity under average levels of male-male competition in the field. We show that, contrary to previous findings, groups of unrelated-unfamiliar males were as likely to fight with each other and harass females than related-familiar males and that overall levels of male harm to females were similar across treatments. Our results suggest that the role of kin selection in modulating sexual conflict is yet unclear in Drosophila melanogaster, and call for further studies that focus on natural populations and realistic socio-sexual and ecological environments.