Drosophila female reproductive tract gene expression reveals coordinated mating responses and rapidly evolving tissue-specific genes

Abstract

Sexual reproduction in internally fertilizing species requires complex coordination between female and male reproductive systems and among the diverse tissues of the female reproductive tract (FRT). Here, we report a comprehensive, tissue-specific investigation of Drosophila melanogaster FRT gene expression before and after mating. We identified expression profiles that distinguished each tissue, including major differences between tissues with glandular or primarily non-glandular epithelium. All tissues were enriched for distinct sets of genes possessing secretion signals and exhibiting accelerated evolution, as might be expected for genes participating in molecular interactions between the sexes within the FRT extracellular environment. Despite robust transcriptional differences between tissues, post-mating responses were dominated by coordinated transient changes indicative of an integrated systems-level functional response. This comprehensive characterization of gene expression throughout the FRT identifies putative female contributions to post-copulatory events critical to reproduction and potentially reproductive isolation, as well as the putative targets of sexual selection and conflict.

Pronounced Postmating Response in the Drosophila Female Reproductive Tract Fluid Proteome

“…Notably, abundant fluid proteins tended to have higher and broader patterns of expression across the FRT. Those proteins may constitute a core fluid proteome to which all tissues contribute (107), which is consistent with evidence that most FRT tissues have secretory capacity (65,78,108) and the identification of FRT genes that are highly expressed across multiple FRT tissues (83). FRT tissues may contribute to the fluid through a variety of secretory mechanisms and our results are useful in beginning to identify these pathways.…”

“…Thus, in contrast to the reproductive fat body, the glandular spermatheca and parovaria appear to contribute a relatively small number of tissue-specific products to the FRT fluid. This pattern supports the hypothesis that the tightly associated FRT fat body, which was found to have a distinct transcriptomic profile relative to the remainder of FRT tissues, contributes a substantive number of proteins to the FRT lumen (83).…”

“…Our ability to compare the proteomic data to patterns of FRT gene expression (83) allowed us to begin to resolve how FRT tissues regulate extracellular luminal fluid composition.…”

“…To evaluate how the FRT tissues (i.e., bursa, oviduct, seminal receptacle, spermathecae, and parovaria) and reproductive fat body may contribute to the fluid composition, we compared the fluid proteome to our recent comprehensive analysis of gene expression across FRT tissues (83).…”

“…To investigate how the FRT tissue and fluid proteomes changed in response to mating we compared samples from unmated females to those 6hrs postmating, the time of maximal postmating transcriptomic response (64,83). A principal components (PC) analysis revealed that more than 85% of the variation among samples is explained by the first two PCs.…”