Gene expression and alternative splicing dynamics are perturbed in female head transcriptomes following heterospecific copulation

Fernando Diaz,Jeremy M Bono,Luciano M Matzkin,Therese Ann Markow,Carson W Allan

doi:10.1186/s12864-021-07669-0

Abstract

BackgroundDespite the growing interest in the female side of copulatory interactions, the roles played by differential expression and alternative splicing mechanisms of pre-RNA 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).ResultsOur 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 failed to activate regulation of some of these genes and induced expression of additional genes when compared with those of conspecifically-mated females. These mechanisms showed functional specializations with DE genes mostly linked to pathways of proteolysis and nutrient homeostasis, while AS genes were more related to photoreception and muscle assembly pathways. IR seems to play a more general role in DE regulation during the female postmating response.ConclusionsWe provide evidence showing that AS genes substantially perturbed by heterospecific matings in female heads evolve at slower evolutionary rates than the genome background. However, DE genes evolve at evolutionary rates similar, or even higher, than those of male reproductive genes, which highlights their potential role in sexual selection and the evolution of reproductive barriers.

Highlights

Despite the growing interest in the female side of copulatory interactions, the roles played by differential expression and alternative splicing mechanisms of pre-RNA on tissues outside of the reproductive tract have remained largely unknown
Pervasive perturbation of differential expression (DE) and alternative splicing (AS) following heterospecific matings Experimental design consisted of conspecific and heterospecific matings between the species D. mojavensis and D. arizonae considering three biological replicates composed of 20 pooled dissected heads (Fig. 1)
We found evidence for gene expression changes when comparing mated with virgin samples (Fig. 2a)

Summary

Introduction

Despite the growing interest in the female side of copulatory interactions, the roles played by differential expression and alternative splicing mechanisms of pre-RNA on tissues outside of the reproductive tract have remained largely unknown. We addressed these questions in the context of con- vs heterospecific matings between Drosophila mojavensis and its sister species, D. arizonae. Transcriptional changes induced by con- or heterospecific matings have been explored in a number of species [8,9,10,11,12,13,14,15,16], most of these studies have not considered alternative splicing (AS) as an additional mechanism by which genes responsible for postmating changes might be regulated [17]. Recent comparisons of Drosophila species show that AS diversification contributes to lineage-specific adaptation [19], with sex-biased splicing and IR rates [20] in several tissues including the brain [18], suggesting that this mechanism might be important in female behavioral responses

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Conclusion