Experimental sexual selection reveals rapid divergence in male and female reproductive transcriptomes and their interactions

Mating causes substantial changes in females, altering male and female reproductive fitness. Some postmating effects are hypothesized to be at least partially mediated by gene expression changes, driven by postcopulatory sexual selection, which results in population divergence of reproductive proteins that could generate reproductive isolation. However, understanding of the direct role of sexual selection on gene expression divergence along with the subsequent molecular mismatches that could occur between diverging populations is limited. Here, we analyze gene expression divergence following over 150 generations of experimental evolution in which Drosophila pseudoobscura evolved under either elevated polyandry or enforced monogamy. We find that sexual selection rapidly impacted sex-, tissue-, and mating-specific responses, and not always in the predicted direction. Postmating female responses are either unique to each sexual selection treatment or exhibit asymmetric non-congruence, in which monogamy females upregulate and polyandry females downregulate the same genes following mating. This substantial population divergence of gene expression also gives rise to either unique or mismatched gene expression patterns in crosses between treatments. Many of these genes are involved in immune and stress responses, and non-congruent responses are particularly prevalent in the female reproductive tract, the main arena for postcopulatory sexual selection. In summary, we show that sexual selection has pervasive impacts on gene expression divergence acting both differentially between reproductive tissues of the same sex and asymmetrically in postmating female responses, and this divergence is highest in the female reproductive tract, the main arena for postcopulatory sexual selection. ### Competing Interest Statement The authors have declared no competing interest.