Where did the Y chromosome in the spiny rat go, and how did it get there?

The XX/XY sex chromosome system is highly conserved across mammals, with rare exceptions where males lack a Y chromosome. Among these is the genus Tokudaia, a group of spiny rats comprising three species with unique sex chromosome systems deviating from the typical XX/XY pattern. While T. osimensis and T. tokunoshimensis have completely lost the Y chromosome, they retain some Y-linked genes on the X chromosome. In contrast, T. muenninki retains large sex chromosomes where both the X and Y chromosomes have fused with an autosome pair, carrying multi-copied Y-linked genes, including Sry. In this study, we generated chromosome-level genome assemblies for male individuals of all three Tokudaia species. By investigating loci typically associated with rodent Y-linked genes, we characterized sequences derived from the Tokudaia Y-chromosomal most recent common ancestor (Tokudaia Y-MRCA) and traced their evolutionary trajectories. Our analyses revealed that an initial X-to-Y translocation of a sequence containing the Boundary-Associated Segmental Duplication (BASD) in a common ancestor of Tokudaia marked the beginning of their unique sex chromosome evolution. The BASD, uniquely multi-copied in Tokudaia, facilitated further rearrangements through non-allelic homologous recombination and duplications. These processes culminated in subsequent Y-to-X translocations and duplications, leading to the complete loss of the Y chromosome as a distinct entity while preserving Y-linked genes in a multicopy state on the X chromosome. These findings highlight Tokudaia’s rapid sex chromosome evolution within three million years and provide insights into the mechanisms underlying Y chromosome loss, contributing to a broader understanding of sex chromosome evolution in rodents.