Divergent evolutionary trajectories shape the postmating transcriptional profiles of conspecific and heterospecifically mated females

Abstract

Postmating-prezygotic (PMPZ) reproductive isolation is hypothesized to result from divergent coevolutionary trajectories of sexual selection and/or sexual conflict in isolated populations (coevolutionary divergence model). However, the genetic basis of PMPZ incompatibilities between species is poorly understood. Here, we use a comparative framework to test predictions of the coevolutionary divergence model using a large transcriptomic dataset generated from con- and heterospecifically mated Drosophila mojavensis and D. arizonae female reproductive tracts. We found striking divergence between the species in the female postmating transcriptional response to conspecific mating, including differences in differential expression (DE), alternative splicing (AS), and intron retention (IR). As predicted, heterospecific matings produced disrupted transcriptional profiles, but the overall patterns of misregulation were different between the reciprocal crosses. Moreover, we found a positive correlation between postmating transcriptional divergence between species and levels of transcriptional disruption in heterospecific crosses, indicating that mating-responsive genes that have diverged more in expression also have more disrupted transcriptional profiles in heterospecifically mated females. Overall, our results are consistent with predictions of the coevolutionary divergence model and lay the foundation for future studies aimed at identifying specific genes involved in PMPZ incompatibilities and the evolutionary forces that have contributed to their divergence in closely related species.