Ancestral male recombination in Drosophila albomicans produced geographically restricted neo-Y chromosome haplotypes varying in age and onset of decay

Author summary Sex chromosomes evolve from autosomes yet harbor many unique characteristics that differentiate them from autosomes and from each other. Male-specific Y-chromosomes degenerate: they lose most of their protein-coding genes and accumulate repetitive DNA. How Y chromosomes evolve these unique features is poorly understood, especially during the initial stages of Y decay. Here, we use genome-wide polymorphism data to study the unusual neo-sex chromosomes of D. albomicans. Its neo-Y is the youngest neo-sex chromosome analyzed to date, which allows us to examine the molecular changes and evolutionary processes initiating Y degeneration. We find both coding and non-coding changes contributing to early neo-Y decay, and genes on the neo-Y are starting to become down-regulated. Genes with testis-biased expression are more likely to be preserved on the neo-Y, indicating that genes important for male function are shielded from degeneration early on. Most intriguingly, we find that this sex chromosome formed in an ancestor where males (and thus the neo-Y) were recombining, and males reverted back to achiasmy only some time after the establishment of the neo-sex chromosomes. This resulted in several unusual patterns of neo-Y evolution, and allowed us to study the complex interplay of recombination, selection and population structure on neo-Y decay. Male Drosophila typically have achiasmatic meiosis, and fusions between autosomes and the Y chromosome 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 ancestral recombination 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, the neo-Y chromosomes fail to form a monophyletic clade in sliding window trees outside of the region proximal to the fusion. Based on tree topology changes, we inferred the recombination breakpoints that produced haplotypes specific to each neo-Y type. We show that recombination became suppressed at different time points for the different neo-Y haplotypes. Haplotype age correlates with onset of neo-Y decay, and 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-expressed genes across all haplotypes. This indicates that genes important for male function are initially 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.