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Sex-biased gene expression and recent sex chromosome turnover.

ABSTRACT: Cichlids are well known for their propensity to radiate generating arrays of morphologically and ecologically diverse species in short evolutionary time. Following this rapid evolutionary pace, cichlids show high rates of sex chromosome turnover. We here studied the evolution of sex-biased gene (SBG) expression in 14 recently diverged taxa of the Lake Tanganyika Tropheini cichlids, which show different XY sex chromosomes. Across species, sex chromosome sequence divergence predates divergence in expression between the sexes. Only one sex chromosome, the oldest, showed signs of demasculinization in gene expression and potentially contribution to the resolution of sexual conflict. SBGs in general showed high rates of turnovers and evolved mostly under drift. Sexual selection did not shape the rapid evolutionary changes of SBGs. Male-biased genes evolved faster than female-biased genes, which seem to be under more phylogenetic constraint. We found a relationship between the degree of sex bias and sequence evolution driven by sequence differences among the sexes. Consistent with other species, strong sex bias towards sex-limited expression contributes to resolving sexual conflict in cichlids. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

SUBMITTER: Lichilin N

PROVIDER: S-EPMC8310714 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Sex-biased gene expression and recent sex chromosome turnover.

Lichilín Nicolás N El Taher Athimed A Böhne Astrid A

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20210726 1833

Cichlids are well known for their propensity to radiate generating arrays of morphologically and ecologically diverse species in short evolutionary time. Following this rapid evolutionary pace, cichlids show high rates of sex chromosome turnover. We here studied the evolution of sex-biased gene (SBG) expression in 14 recently diverged taxa of the Lake Tanganyika Tropheini cichlids, which show different XY sex chromosomes. Across species, sex chromosome sequence divergence predates divergence in ...[more]

PMID: 34304591

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Project description:BackgroundSex-biased gene expression is thought to drive the phenotypic differences in males and females in metazoans. Drosophila has served as a primary model for studying male-female differences in gene expression, and its effects on protein sequence divergence. However, the forces shaping evolution of sex-biased expression remain largely unresolved, including the roles of selection and pleiotropy. Research on sex organs in Drosophila, employing original approaches and multiple-species contrasts, provides a means to gain insights into factors shaping the turnover and magnitude (fold-bias) of sex-biased expression.ResultsHere, using recent RNA-seq data, we studied sex-biased gonadal expression in 10,740 protein coding sequences in four species of Drosophila, D. melanogaster, D. simulans, D. yakuba and D. ananassae (5 to 44 My divergence). Using an approach wherein we identified genes with lineage-specific transitions (LSTs) in sex-biased status (amongst testis-biased, ovary-biased and unbiased; thus, six transition types) standardized to the number of genes with the ancestral state (S-LSTs), and those with clade-wide expression bias status, we reveal several key findings. First, the six categorical types of S-LSTs in sex-bias showed disparate rates of turnover, consistent with differential selection pressures. Second, the turnover in sex-biased status was largely unrelated to cross-tissue expression breadth, suggesting pleiotropy does not restrict evolution of sex-biased expression. Third, the fold-sex-biased expression, for both testis-biased and ovary-biased genes, evolved directionally over time toward higher values, a crucial finding that could be interpreted as a selective advantage of greater sex-bias, and sexual antagonism. Fourth, in terms of protein divergence, genes with LSTs to testis-biased expression exhibited weak signals of elevated rates of evolution (than ovary-biased) in as little as 5 My, which strengthened over time. Moreover, genes with clade-wide testis-specific expression (44 My), a status not observed for any ovary-biased genes, exhibited striking acceleration of protein divergence, which was linked to low pleiotropy.ConclusionsBy studying LSTs and clade-wide sex-biased gonadal expression in a multi-species clade of Drosophila, we describe evidence that interspecies turnover and magnitude of sex-biased expression have been influenced by selection. Further, whilst pleiotropy was not connected to turnover in sex-biased gonadal expression, it likely explains protein sequence divergence.

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Sex-biased gene expression and recent sex chromosome turnover.

Publications

Sex-biased gene expression and recent sex chromosome turnover.

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