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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.

SUBMITTER: Jiang ZF

PROVIDER: S-EPMC2778969 | biostudies-literature | 2009 Nov

REPOSITORIES: biostudies-literature

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Evolution of sex-dependent gene expression in three recently diverged species of Drosophila.

Jiang Zi-Feng ZF Machado Carlos A CA

Genetics 20090831 3

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 stud ...[more]

PMID: 19720861

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Project description:Sexually dimorphic phenotypes are thought to largely result from sex differences in gene expression, and genes with sex-biased expression have been well characterized in adults of many species. Although most sexual dimorphisms manifest in adults, many result from sex-specific developmental trajectories, implying that juveniles may exhibit significant levels of sex-biased expression. However, it is unclear how much sex-biased expression occurs before reproductive maturity and whether preadult sex-biased genes should exhibit the same evolutionary dynamics observed for adult sex-biased genes. In order to understand the continuity, or lack thereof, and evolutionary dynamics of sex-biased expression throughout the life cycle, we examined sex-biased genes in pre-gonad tissue of two preadult stages and compared them with the adult gonad of Drosophila melanogaster. We found that the majority of the genome is sex-biased at some point in the life cycle, with some genes exhibiting conserved sex-biased expression and others displaying stage-specific sex bias. Our results also reveal a far more complex pattern of evolution for sex-biased genes throughout development. The most rapid evolutionary divergence occurred in genes expressed only in larvae within each sex, compared with continuously expressed genes. In females-but not males-this pattern appeared to be due to relaxed purifying selection in larva-limited genes. Furthermore, genes that retained male bias throughout life evolved more rapidly than stage-specific male-biased genes, due to stronger purifying selection in stage-specific genes. However, female-biased genes that were specific to larvae evolved most rapidly, a pattern that could not be definitively attributed to differences in adaptive evolution or purifying selection, suggesting that pleiotropic constraints on protein-coding sequences can arise when genes are broadly expressed across developmental stages. These results indicate that the signature of sex-specific selection can be detected well before reproductive maturity and is strongest during development.

Dataset Information

Evolution of sex-dependent gene expression in three recently diverged species of Drosophila.

Publications

Evolution of sex-dependent gene expression in three recently diverged species of Drosophila.

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