Gene Expression and Alternative Splicing Dynamics Are Perturbed in Head Transcriptomes of Heterospecifically Mated Females

Abstract Background Despite the growing interest in the female side of copulatory interactions, the roles played by alternative splicing mechanisms of pre-RNA and the epistatic effects of these interactions on tissues outside of the reproductive tract have remained largely unknown. Here we addressed these questions in the context of con- vs heterospecific matings between Drosophila mojavensis and its sister species, D. arizonae. We analyzed transcriptional responses in female heads using an integrated investigation of genome-wide patterns of gene expression, including differential expression (DE), alternative splicing (AS) and intron retention (IR). Results Our results indicated that early transcriptional responses were largely congruent between con- and heterospecific matings but are substantially perturbed over time. Conspecific matings induced functional pathways related to amino acid balance previously associated with the brain’s physiology and female postmating behavior. Heterospecific matings often fail to activate regulation of some of these genes and induce expression of additional genes when compared with those of conspecifically-mated females. These results are consistent for all transcriptional mechanisms with some distinctions: DE genes were mostly linked to pathways of proteolysis and nutrient homeostasis, while AS genes are more related to photoreception and muscle assembly pathways. Conclusions IR seem to be an important mechanism of DE regulation during the female postmating response. While AS genes evolve at slower evolutionary rates than the genome background, DE genes evolve at much higher rates, similar or even higher than those of seminal fluid proteins, which unveil their potential role for reproductive barriers and the extent of sexual conflict.