Male recombination produced multiple geographically restricted neo-Y chromosome haplotypes of varying ages that correlate with onset of neo-Y decay in Drosophila albomicans

Abstract

Male Drosophila typically have achiasmatic meiosis, and fusions between autosomes and the Y have repeatedly created non-recombining neo-Y chromosomes that degenerate. Intriguingly, Drosophila nasuta males recombine, but their close relative D. albomicans reverted back to achiasmy after evolving neo-sex chromosomes. Here we use genome-wide polymorphism data to reconstruct the complex evolutionary history of neo-sex chromosomes in D. albomicans and examine the effect of recombination and its cessation on the initiation of neo-Y decay. Population and phylogenomic analyses reveal three distinct neo-Y types that are geographically restricted. Due to meiotic exchange with the neo-X, overall nucleotide diversity on the neo-Y is similar to the neo-X but severely reduced within neo-Y types. Consistently, outside of the region proximal to the fusion, the neo-Ys fail to form a monophyletic clade in sliding window trees. Based on tree topology changes, we inferred the recombinant breakpoints that produced haplotypes specific to each neo-Y type and estimated their ages revealing that recombination became suppressed at different time points for the different neo-Y haplotypes. Although there are no evidence of chromosome-wide differentiation between the neo-sex chromosomes, haplotype age correlates with onset of neo-Y decay. Older neo-Y haplotypes show more fixed gene disruption via frameshift indels and down-regulation of neo-Y alleles. Genes are downregulated independently on the different neo-Ys, but are depleted of testes-biased genes across all haplotypes, indicating that genes important for male function are shielded from degeneration. Our results offer a time course of the early progression of Y chromosome evolution, showing how the suppression of recombination, through the reversal to achiasmy in D. albomicans males, initiates the process of degeneration.