Y chromosomes are thought to undergo progressive degeneration due to stepwise loss of recombination and subsequent reduction in selection efficiency. However, the timescales over which degeneration occurs and the evolutionary forces driving degeneration remain unclear. In order to characterize the evolution of sex chromosomes on multiple timescales, we generated a high-quality phased genome assembly of the massive older (7-9 MYA) and neo (<200,000 years) sex chromosomes in the XYY cytotype of the plant Rumex hastatulus, along with a hermaphroditic outgroup Rumex salicifolius. Our assemblies confirmed 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 the two Y chromosomes (503 MB) both arose in a large repeat-rich genome with low recombination, however the complete loss of recombination on the Y still led to over 30% gene loss and massive rearrangements over a short timescale. In the older sex-linked region, there has been a major increase in the abundance of transposable elements, including into and near genes. In the neo sex-linked regions, we observe evidence of extensive chromosome rearrangements before gene degeneration and loss. Overall, we observe extensive degeneration during the first 10 million years of Y chromosome evolution, but not immediate genomic degeneration on very short timescales. Our results highlight 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.

Phased assembly of neo-sex chromosomes reveals extensive Y degeneration and rapid genome evolution in Rumex hastatulus