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Genome Biol
2018 Oct 05;191:156. doi: 10.1186/s13059-018-1548-4.
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Evolutionary and developmental dynamics of sex-biased gene expression in common frogs with proto-Y chromosomes.
Ma WJ
,
Veltsos P
,
Sermier R
,
Parker DJ
,
Perrin N
.
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BACKGROUND: 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. 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.
RESULTS: We 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.
CONCLUSIONS: The 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.
31003A_166323 Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, CRSII3_147625 Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CH)
Fig. 1
Sex bias in gene expression across developmental stages in Rana temporaria. The number of genes with significant sex bias (corrected for multiple testing) increases drastically in the late developmental stages (G43 and G46), corresponding to the morphological differentiation of gonads. At these stages, female-biased genes (reddish) significantly outnumber male-biased genes (blueish), mostly for the highly biased categories (|log2FC| â¥â2 and â¥â3). Drawings of frog tadpoles and larvae are reprinted from [80], with permission of the editors
Fig. 2
Female-biased genes (red) and male-biased genes (blue) in froglets (G46) show the same distribution patterns on the sex chromosomes (Chr01, left) as on autosomes (Chr02 to 10, right, shaded area)
Fig. 3
XX and XY° male froglets (G46) show similar patterns of gene expression, with a no specific signature of sex chromosomes (Chr01, red, left) relative to ausosomes (boxplots of Log2(XY°/XX) gene expression ratio) and b no difference around the sex-determining region (Manhattan plot of log2(XY°/XX) gene expression ratio along the sex chromosome, with a sliding window of 40 genes; Dmrt1 position marked by the blue dotted line)
Fig. 4
Heatmaps and hierarchical clustering of differentially expressed genes (FDRâ<â0.05) for XX females, XY° males, XX with testes, and XY° with ovaries at stages G46 (a) and G43 (b). Blue and red colors represent high and low expression, respectively. On each node of the clustering tree, bootstrap support values are shown from 10,000 replicates
Fig. 5
Boxplots of ratios of non-synonymous to synonymous substitutions (dN/dS) for XX-biased, XY°-biased, and unbiased genes identified at stages G43 and G46. Codes for levels of significance are 0.001 â***â, 0.05 â*â
Fig. 6
The ratios of non-synonymous to synonymous substitutions dN/dS a do not differ between sex chromosomes (red) and autosomes and b show no special pattern around the sex-determining region (the horizontal blue line shows the average dN/dS ratio of a sliding window of 40 genes; Dmrt1 position marked by the vertical blue dotted line). Codes for significance level is not significant âNSâ
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