Department of Ecology and Evolution, University of Lausanne, CH 1015, Lausanne, Switzerland.
Current address: Department of Biology, Amherst College, Amherst, MA, USA.
Genome Biol. 2018 Oct 5;19(1):156. doi: 10.1186/s13059-018-1548-4.
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.
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.
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.
由于选择和遗传的性别特异性模式，高度分化的性染色体上的基因表达模式与常染色体上的模式有很大的不同。因此，X 染色体通常富集雌性偏性基因（雌性化），Z 染色体富集雄性偏性基因（雄性化）。然而，目前尚不清楚基因表达的性化和转录退化在性染色体形成后是如何快速进化的。此外，人们对性别偏性基因表达在整个发育过程中的变化知之甚少。
我们对具有有限性染色体分化的普通青蛙（Rana temporaria）种群进行了采样（原性染色体），遗传性别决定存在渗漏，表现为 XX 雄性的出现，以及性腺发育延迟，这意味着 XY 个体可能首先发育成卵巢，然后再发育成睾丸。我们使用高通量 RNA 测序技术，研究了从早期胚胎到青蛙阶段的整个发育过程中的基因表达动态。我们的结果表明，性别偏性表达在不同的发育阶段影响不同的基因，并随着发育的进行而增加，在 XX 雌性青蛙中达到最高水平。此外，性别偏性基因表达取决于表型，而不是基因型性别，XX 和 XY 雄性之间的表达相似；与基因进化率相关；并且不限于原性染色体，也不在候选性别决定基因 Dmrt1 附近。
普通青蛙的原性染色体没有表现出基因表达性化的证据，也没有证据表明进化速度更快。这挑战了性拮抗基因在性染色体进化的初始阶段起核心作用的观点。
