The evolution of seminal fluid gene expression and postmating reproductive isolation in Drosophila.

Seminal fluid protein (Sfp) genes show, in general, a higher rate of sequence divergence than genes from other categories, which is often attributed to forms of postcopulatory sexual selection or sexual conflict. Recently, relaxation of selective constraints has been proposed as an alternative explanation for rapid sequence evolution of Sfps, and other genes with sex-limited expression. The expression of Sfp genes is a likely target of selection, but the evolution of differences in their expression levels is less understood. Here we explore both polymorphism and divergence in Sfp genes expression between D. melanogaster and D. simulans, how selection might have influenced their expression, and whether changes in expression might trigger the evolution of reproductive isolating barriers. In our analysis, Sfp genes showed higher divergence, but not higher polymorphism, in expression than the average male reproductive glands gene. Sfp genes with reproductive-tissue specific expression were enriched for both directional and stabilizing selection while relaxed selection was the predominant mode of evolution among Sfp genes with any other non-reproductive tissue specific or with non-tissue specific expression. The knock down of single genes known to affect intraspecific sperm competition, and with patterns of expression divergence and polymorphism suggestive of directional selection, was not enough to breakdown postmating reproductive isolation barriers between species. Our results identify the expression of male-specific Sfp genes as an enriched target of selection and suggests a complex molecular relationship between postcopulatory sexual selection on single gene's expression and its effect on the onset of speciation.

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