Extreme heterochiasmy and high rates of sex-reversed recombination result in large yet homomorphic sex chromosomes in the Emei moustache toad

Abstract

Unlike the highly degenerated sex chromosomes in birds and mammals, many amphibians possess homomorphic sex chromosomes, which may result from high rates of sex chromosome turnover and/or occasional recombination between the X and Y (or Z and W) Chromosomes. Yet, the molecular basis for maintaining homomorphy remains elusive, particularly the power of rare recombination events to arrest sex chromosome divergence. Here, we identified sex chromosomes of the Emei moustache toad and examined potential mechanisms of maintaining homomorphy. Although the sex chromosomes are homomorphic, we observed an extensive region of X–Y genetic differentiation, spanning ∼349 Mb, among the largest known to date in vertebrates. Despite this large size and the assumption that inversions catalyze recombination suppression between the X and Y Chromosomes, we found little evidence of XY structural variation. Using a high-density linkage map, we revealed that the large region of X–Y divergence was likely owing to the emergence of sex determining factors in the region of ancestrally low male recombination. Population genetic data showed high rates of sex-reversed XY-type females, and recombination between the X and Y Chromosomes in these individuals helps maintain the integrity of sequence and gene expression on the Y Chromosome. Finally, we revealed modest sexualization of gene expression within the sex chromosomes, and identified candidate genes involved in gonadal development. Our results not only show remarkable maintenance of vast sex differentiated regions under ancestral low recombination but also emphasize the sustaining power of X–Y recombination for homomorphic chromosomes over large genomic regions.