Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Abstract

Sexual dimorphism in morphological, physiological, and behavioral traits is pervasive in animals, as is the observation of strong sexual dimorphism in genomewide patterns of gene expression in the few species where this has been studied. Studies of transcriptome divergence show that most interspecific transcriptional divergence is highly sex dependent, an observation consistent with the action of sex-dependent natural selection during species divergence. However, few transcriptome evolution studies have been conducted between recently diverged species (<1 MY). Here, we present analyses of sex-biased transcriptome divergence in sexually mature adults of three recently diverged species of Drosophila: Drosophila pseudoobscura, D. persimilis, and D. pseudoobscura bogotana. Data were collected using a custom designed Agilent oligonucleotide. Expression was detected in 12,507 genes. About 80% of the expressed genes show sex-biased expression in each species. Across species, 21% of the transcriptome shows switches between nonsex bias and sex bias, and just 0.9% of the transcriptome shows reversals of sex-biased expression. Over 80% of the expression divergence between species is due to changes in one sex only. About 15% of the expression divergence between species is due to changes in the same direction in both sexes and just 2% is due to changes in both sexes but in opposite directions. In agreement with previous studies, we observe a high level of sex-dependent transcriptome divergence and strong demasculinization of the two arms of the X chromosome in all species. However, in contrast to previous studies we find that male-biased genes do not have higher levels of expression divergence than non-sex-biased genes, and sex-biased genes show higher levels of expression divergence in the alternate sex, suggesting that sex-biased genes endure stronger selection when expressed in the alternate sex.