Abstract
BackgroundThe patterns of gene expression on highly differentiated sex chromosomes differ drastically from those on autosomes, due to sex-specific patterns of selection and inheritance. As a result, X chromosomes are often enriched in female-biased genes (feminization) and Z chromosomes in male-biased genes (masculinization). However, it is not known how quickly sexualization of gene expression and transcriptional degeneration evolve after sex-chromosome formation. Furthermore, little is known about how sex-biased gene expression varies throughout development.ResultsWe sample a population of common frogs (Rana temporaria) with limited sex-chromosome differentiation (proto-sex chromosome), leaky genetic sex determination evidenced by the occurrence of XX males, and delayed gonadal development, meaning that XY individuals may first develop ovaries before switching to testes. Using high-throughput RNA sequencing, we investigate the dynamics of gene expression throughout development, spanning from early embryo to froglet stages. Our results show that sex-biased expression affects different genes at different developmental stages and increases during development, reaching highest levels in XX female froglets. Additionally, sex-biased gene expression depends on phenotypic, rather than genotypic sex, with similar expression in XX and XY males; correlates with gene evolutionary rates; and is not localized to the proto-sex chromosome nor near the candidate sex-determining gene Dmrt1.ConclusionsThe proto-sex chromosome of common frogs does not show evidence of sexualization of gene expression, nor evidence for a faster rate of evolution. This challenges the notion that sexually antagonistic genes play a central role in the initial stages of sex-chromosome evolution.
Highlights
The patterns of gene expression on highly differentiated sex chromosomes differ drastically from those on autosomes, due to sex-specific patterns of selection and inheritance
Sexualization of proto-sex chromosomes Unlike studies of organisms with differentiated sex chromosomes, we found no clear evidence for sexualization of the proto-sex chromosomes in R. temporaria, even at developmental stages that display strong sex bias in gene expression. (i) Sex-biased genes were not more common on proto-sex chromosome than on autosomes, nor around the candidate sex-determining locus compared to the rest of the sex chromosome
There was no difference when analyzing separately the genes with significant male- or female-biased expression, and their distribution was uniform along the sex chromosome. (iii) We found no evidence for faster-X effect, as the dN/dS ratio did not differ between sex-linked and autosomal genes, and no specific pattern was found along the sex chromosomes. (iv) We found negligible differences in expression between XX and XY° males at Gosner stages 23 (G46): only 0.06% of genes had significantly different expression
Summary
The patterns of gene expression on highly differentiated sex chromosomes differ drastically from those on autosomes, due to sex-specific patterns of selection and inheritance. In proto-sex chromosomes (where X and Y chromosomes differ only at the sex-determining locus), male-beneficial mutations on the Y may spread even if detrimental to females, because linkage with the sex-determining locus makes them more likely to be transmitted to sons than to daughters. These might be mutations affecting coding sequences or promoter regions, and DNA methylation or heterochromatinization affecting transcriptional activity, such that alleles from one gametolog (e.g., X) might be upregulated, and those of the other gametolog downregulated. While the sex-biased expression of autosomal genes is thought to result from sexual conflict alone, sex-biased expression of sex-linked genes potentially arises from a combination of sexualization and decay [11]
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