Males compete over mating and fertilization, and often harm females in the process. Inclusive fitness theory predicts that increasing relatedness within groups of males may relax competition and discourage male harm of females as males gain indirect benefits. Recent studies in Drosophila melanogaster are consistent with these predictions, and have found that within-group male relatedness increases female fitness, though others have found no effects. Importantly, these studies did not fully disentangle male genetic relatedness from larval familiarity, so the extent to which modulation of harm to females is explained by male familiarity remains unclear. Here we performed a fully factorial design, isolating the effects of male relatedness and larval familiarity on female harm. While we found no differences in male courtship or aggression, there was a significant interaction between male genetic relatedness and familiarity on female reproduction and survival. Relatedness among males increased female lifespan, reproductive lifespan and overall reproductive success, but only when males were familiar. By showing that both male relatedness and larval familiarity are required to modulate female harm, these findings reconcile previous studies, shedding light on the potential role of indirect fitness effects on sexual conflict and the mechanisms underpinning kin recognition in fly populations.

Sex differences in lifespan are ubiquitous, but the underlying causal factors remain poorly understood. Inter- and intrasexual social interactions are well known to influence lifespan in many taxa, but it has proved challenging to separate the role of sex-specific behaviours from wider physiological differences between the sexes. To address this problem, we genetically manipulated the sexual identity of the nervous system—and hence sexual behaviour—in Drosophila melanogaster, and measured lifespan under varying social conditions. Consistent with previous studies, masculinization of the nervous system in females induced male-specific courtship behaviour and aggression, while nervous system feminization in males induced male–male courtship and reduced aggression. Control females outlived males, but masculinized female groups displayed male-like lifespans and male-like costs of group living. By varying the mixture of control and masculinized females within social groups, we show that male-specific behaviours are costly to recipients, even when received from females. However, consistent with recent findings, our data suggest courtship expression to be surprisingly low cost. Overall, our study indicates that nervous system-mediated expression of sex-specific behaviour per se—independent of wider physiological differences between the sexes, or the receipt of aggression or courtship—plays a limited role in mediating sex differences in lifespan.

Intra-locus sexual conflict, or sexual antagonism, occurs when alleles have opposing fitness effects in the two sexes. Previous theory suggests that sexual antagonism is a driver of genetic variation by generating balancing selection. However, these studies assume that populations are well-mixed, neglecting the effects of spatial subdivision. Here we use mathematical modelling to show that limited dispersal can fundamentally change evolution at sexually antagonistic autosomal and X-linked loci due to inbreeding and sex-specific kin competition. We find that if the sexes disperse at different rates, kin competition within the philopatric sex biases intralocus conflict in favour of the more dispersive sex. Furthermore, kin competition diminishes the strength of balancing selection relative to genetic drift, reducing genetic variation in small subdivided populations. Meanwhile, by decreasing heterozygosity, inbreeding reduces the scope for sexually antagonistic polymorphism due to non-additive allelic effects, and this occurs to a greater extent on the X-chromosome than autosomes. Overall, our results demonstrate that spatial structure is an important factor in predicting where to expect sexually antagonistic alleles. We suggest that observed interspecific and intragenomic variation in sexual antagonism may be explained by sex-specific dispersal ecology and demography.

Sexual conflict can arise when males evolve traits that improve their mating success but in doing so harm females. By reducing female fitness, male harm can diminish offspring production in a population and even drive extinction. Current theory on harm is based on the assumption that an individual’s phenotype is solely determined by its genotype. But the expression of most sexually selected traits is also influenced by variation in biological condition (condition-dependent expression), such that individuals in better condition can express more extreme phenotypes. Here, we developed demographically explicit models of sexual conflict evolution where individuals vary in their condition. Because condition-dependent expression readily evolves for traits underlying sexual conflict, we show that conflict is more intense in populations where individuals are in better condition. Such intensified conflict reduces mean fitness and can thus generate a negative association between condition and population size. The impact of condition on demography is especially likely to be detrimental when the genetic basis of condition coevolves with sexual conflict. This occurs because sexual selection favors alleles that improve condition (the so-called good genes effect), producing feedback between condition and sexual conflict that drives the evolution of intense male harm. Our results indicate that in presence of male harm, the good genes effect in fact easily becomes detrimental to populations.