Population Ecology Group, Institute of Ecology and Evolution, Friedrich Schiller University Jena, Jena, Germany.
Department of Organismal Biology-Systematic Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
Mol Ecol. 2024 Dec;33(23):e17567. doi: 10.1111/mec.17567. Epub 2024 Oct 30.
The early evolution of sex chromosomes has remained obscure for more than a century. The Vandiemenella viatica species group of morabine grasshoppers is highly suited for studying the early stages of sex chromosome divergence and degeneration of the Y chromosome. This stems from the fact that neo-XY sex chromosomes have independently evolved multiple times by X-autosome fusions with different autosomes. Here, we generated new chromosome-level assemblies for two chromosomal races representing karyotypes with and without neo-sex chromosomes (P24XY and P24X0), and sequence data of a third chromosomal race with a different neo-XY chromosome system (P25XY). Interestingly, these two neo-XY chromosomal races are formed by different X-autosome fusions (involving chr1 and chrB, respectively), and we found that both neo-Y chromosomes have partly ceased to recombine with their neo-X counterpart. We show that the neo-XY chromosomes have diverged through accumulation of SNPs and structural mutations, and that many neo-Y-linked genes have degenerated since recombination ceased. However, the non-recombining regions of neo-Y chromosomes host non-degenerated genes crucial for sex determination, such as sex-lethal and transformer, alongside genes associated with spermatogenesis, fertility, and reproduction, illustrating their integrative role as a masculinizing supergene. Contrary to expectations, the neo-Y chromosomes showed (slightly) lower density of transposable elements (TEs) compared to other genomic regions. The study reveals the unique dynamics of young sex chromosomes, with evolution of recombination suppression and pronounced decay of (some) neo-sex chromosome genes, and provides a compelling case illustrating how chromosomal fusions and post-fusion mutational processes contribute to the evolution of supergenes.
性染色体的早期演化在一个多世纪以来一直不为人知。Vandiemenella viatica 种组的拟步行虫非常适合研究性染色体分化和 Y 染色体退化的早期阶段。这源于这样一个事实，即新的 X-Y 性染色体通过不同的常染色体与 X-染色体融合独立进化了多次。在这里，我们为两个具有和不具有新性染色体的染色体种群（P24XY 和 P24X0）生成了新的染色体水平组装，并为具有不同新 X-Y 染色体系统的第三个染色体种群（P25XY）生成了序列数据。有趣的是，这两个新的 X-Y 染色体种群是由不同的 X-常染色体融合形成的（分别涉及 chr1 和 chrB），我们发现两个新的 Y 染色体都已经部分停止与新的 X 染色体配对重组。我们表明，新的 X-Y 染色体通过 SNP 和结构突变的积累而分化，并且许多新的 Y 连锁基因自重组停止以来已经退化。然而，非重组的新 Y 染色体区域拥有对于性别决定至关重要的非退化基因，例如 sex-lethal 和 transformer，以及与精子发生、生育力和生殖相关的基因，这表明它们作为一个雄性化超级基因的综合作用。与预期相反，新的 Y 染色体与其他基因组区域相比显示出（略）较低的转座元件（TE）密度。该研究揭示了年轻性染色体的独特动态，包括重组抑制的进化和（一些）新性染色体基因的明显退化，并提供了一个引人注目的案例，说明了染色体融合和融合后的突变过程如何促进超级基因的进化。
