Rapid male benefit adaptation in response to sex-limitation, mates, and genetic context in Drosophila melanogaster

Abstract Intralocus sexual conflict (IaSC) arises when selection favours different trait values in females and males despite their shared genetic architecture. In the presence of IaSC, sex-limited selection is expected to resolve this conflict by allowing one sex to adapt without constraint from selection acting on the other sex, with intersexual genetic correlations predicted to drive a decline in the fitness of the opposite sex. In a recent study, we found that male-limited (ML) selection produced the predicted decline in female fitness, but male fitness improvement was sensitive to genetic background, suggesting unintended sources of adaptation. Here we dissect these evolutionary responses using a fully factorial assay spanning control-like and selection-like conditions, explicitly accounting for the unusual genetic features of the clone-generator (CG) breeding system and the specialized (CG) females used to enforce male-limited inheritance of nuclear genetic variation. Evolved male fitness increased by more than 100% (relative to controls) when tested with all the features of the CG breeding system. Retaining the CG genetic background while replacing CG females with control females yielded an approximately 66% fitness increase. In a control-like genetic background, male fitness increased by 26% when males competed for the CG females they had potentially adapted to, but only by a marginal 6% otherwise. Despite this strong context dependence, the underlying phenotypic responses were remarkably consistent: selected male improvements were driven by enhanced precopulatory traits; greater attractiveness, reflected in higher mating success and shorter mating latency; while postcopulatory traits, including sperm offense (P2) and fecundity induced in mates, remained unchanged. Intriguingly, evolved males also inflicted substantially less mate harm on CG females, contrary to findings from an earlier ML selection experiment. Together, these findings provide clearer evidence of intralocus sexual conflict, expressed as male-benefit adaptations alongside previously established costs to females, but demonstrate that these adaptations were also shaped by the genetic manipulations and mating context of the experimental design.