Experimental sexual selection reveals rapid evolutionary divergence in sex-specific transcriptomes and their interactions following mating

Postcopulatory interactions between the sexes in internally fertilizing species elicits both sexual conflict and sexual selection. Macroevolutionary and comparative studies have linked these processes to rapid transcriptomic evolution in sex-specific tissues and substantial transcriptomic postmating responses in females, patterns of which are altered when mating between reproductively isolated species. Here we test multiple predictions arising from sexual selection and conflict theory about the evolution of sex-specific and tissue-specific gene expression and the postmating response at the microevolutionary level. Following over 150 generations of experimental evolution under either reduced (enforced monogamy) or elevated (polyandry) sexual selection in Drosophila pseudoobscura , we found a substantial effect of sexual selection treatment on transcriptomic divergence in virgin male and female reproductive tissues (testes, male accessory glands, the female reproductive tract and ovaries). Sexual selection treatment also had a dominant effect on the postmating response, particularly in the female reproductive tract – the main arena for sexual conflict - compared to ovaries. This affect was asymmetric with monandry females typically showing more postmating responses than polyandry females, with enriched gene functions varying across treatments. The evolutionary history of the male partner had a larger effect on the postmating response of monandry females, but females from both sexual selection treatments showed unique patterns of gene expression and gene function when mating with males from the alternate treatment. Our microevolutionary results mostly confirm comparative macroevolutionary predictions on the role of sexual selection on transcriptomic divergence and altered gene regulation arising from divergent coevolutionary trajectories between sexual selection treatments.