Editor's choice Female transcriptomic response to male genetic and nongenetic ejaculate variation

Postcopulatory variation in reproductive success is fundamental for sexual selection. Because evolutionary change is impossible without a heritable basis for variation, the study of postcopulatory variation has mainly focused on genetic differences between males, that is, the effect of sperm competition or differential female responses toward male genotypes (cryptic female choice). The role of environmental components in shaping postcopulatory variation in reproductive success is well known, for example, in the form of damaging lifestyle effects on sperm, but their effect on eliciting female responses has rarely been tested, as has its relative significance compared with male genotypic effects. Here we provide such a test in bedbugs, a species where cryptic female choice has been hypothesized to be directed toward specific sperm genotypes. We measured female transcriptomic responses after experimentally controlling the male genetic and environmental component of the ejaculate. For identical female genetic background and identical male age at mating, we analyzed female gene expression in response to insemination with sperm of 3 different inbred populations (genotypes), each exposed to 1 of 2 environmental treatments (sperm storage duration in the male). Females responded mainly to environmental variation: >15 times more genes were differentially expressed, including stress response genes, compared with male genotypic variation. Our results suggest that postcopulatory natural selection exists and plays a significant role in the evolution and diversification of reproductive traits. Our results add complexity to testing the cryptic female choice hypothesis and show that nongenetic ejaculate effects are an important but underappreciated source of variation in biology.