Y chromosomes are thought to undergo progressive degeneration due to stepwise loss of recombination and subsequent reduction in selection efficiency. However, the timescales and evolutionary forces driving degeneration remain unclear. To investigate the evolution of sex chromosomes on multiple timescales, we generated a high-quality phased genome assembly of the massive older (<10MYA) and neo (<200,000 years) sex chromosomes in the XYY cytotype of the dioecious plant Rumex hastatulus and a hermaphroditic outgroup R. salicifolius. Our assemblies, supported by fluorescence in situ hybridization, confirmed that the neo-sex chromosomes were formed by two key events: an X-autosome fusion and a reciprocal translocation between the homologous autosome and the Y chromosome. The enormous sex-linked regions of the X (296 MB) and two Y chromosomes (503 MB) both evolved from large repeat-rich genomic regions with low recombination; however, the complete loss of recombination on the Y still led to over 30% gene loss and major rearrangements. In the older sex-linked region, there has been a significant increase in transposable element abundance, even into and near genes. In the neo sex-linked regions, we observed evidence of extensive rearrangements without gene degeneration and loss. Overall, we inferred significant degeneration during the first 10 million years of Y chromosome evolution but not on very short timescales. Our results indicate that even when sex chromosomes emerge from repetitive regions of already-low recombination, the complete loss of recombination on the Y chromosome still leads to a substantial increase in repetitive element content and gene degeneration.

中文翻译：

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新性染色体的阶段性组装揭示了酸模中广泛的Y变性和快速的基因组进化

由于重组的逐步丧失和随后选择效率的降低，Y染色体被认为会经历进行性退化。然而，驱动退化的时间尺度和进化力量仍不清楚。为了研究性染色体在多个时间尺度上的进化，我们对雌雄异株植物 Rumex hastatulus 的 XYY 细胞型中的大量旧性染色体（<10MYA）和新性染色体（<200,000 年）进行了高质量的定相基因组组装，雌雄同体的外群 R. salicifolius。我们的组装在荧光原位杂交的支持下证实了新性染色体是由两个关键事件形成的：X常染色体融合以及同源常染色体和Y染色体之间的相互易位。 X (296 MB) 和两条 Y 染色体 (503 MB) 的巨大性连锁区域均是从低重组、富含重复的大型基因组区域进化而来；然而，Y 上重组的完全丧失仍然导致超过 30% 的基因丢失和重大重排。在较古老的性连锁区域，转座元件丰度显着增加，甚至进入基因和基因附近。在新性别连锁区域，我们观察到广泛重排的证据，但没有基因退化和丢失。总体而言，我们推断在 Y 染色体进化的前 1000 万年中发生了显着的退化，但在非常短的时间尺度上并没有发生。我们的结果表明，即使性染色体从重组已经很低的重复区域中出现，Y染色体上重组的完全丧失仍然会导致重复元件含量和基因退化的大幅增加。