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

Abstract

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.

Gene-level, but not chromosome-wide, divergence between a very young house fly proto-Y chromosome and its homologous proto-X chromosome

“…In contrast, old Y chromosomes are more likely to have only retained genes with male-specific functions or recruited genes associated with testis expression from other autosomes (Koerich et al 2008;Kaiser et al 2011;Mahajan and Bachtrog 2017). Our results suggest that changes in the expression of individual Y-linked genes that were retained from the ancestral autosome could have important phenotypic effects during early Y chromosome evolution, consistent with gene-by-gene divergence on the young Y chromosomes (Wei and Bachtrog 2019).…”

Gene-Level, but Not Chromosome-Wide, Divergence between a Very Young House Fly Proto-Y Chromosome and Its Homologous Proto-X Chromosome

“…Our subsequent analyses suggest that the house fly III M proto-Y chromosome is differentiated in sequence and expression from its homologous proto-X chromosome at individual genes, but not chromosome-wide. This is consistent with previous work that found evidence for gene-by-gene divergence in a young neo-Y chromosome ( Wei and Bachtrog 2019 ). For example, we only identified two genomic loci (containing a total of seven genes) that are sufficiently differentiated to assemble into separate proto-X and proto-Y contigs ( fig.…”

“…2011 ; Mahajan and Bachtrog 2017 ). Our results suggest that changes in the expression of individual Y-linked genes that were retained from the ancestral autosome could have important phenotypic effects during early Y chromosome evolution, consistent with gene-by-gene divergence on the young Y chromosomes ( Wei and Bachtrog 2019 ).…”

“…We are especially interested in how gene expression differences accumulate between the proto-Y and proto-X chromosomes. As the proto-Y and proto-X chromosomes diverge, it is expected that alleles on the proto-Y chromosome are up- or downregulated because of cis -regulatory sequence differences that contribute to proto-Y gene expression ( Zhou and Bachtrog 2012a , 2012b ; Wei and Bachtrog 2019 ). These cis -regulatory effects may be especially important for the expression of sexually antagonistic (male-beneficial/female-deleterious) alleles and degeneration of functional genes ( Rice 1984 ; Zhou and Bachtrog 2012a ).…”

“…These cis -regulatory effects may be especially important for the expression of sexually antagonistic (male-beneficial/female-deleterious) alleles and degeneration of functional genes ( Rice 1984 ; Zhou and Bachtrog 2012a ). Degeneration of Y-linked genes has been shown to be accompanied by decreased expression as a result of relaxed selective constraints ( Zhou and Bachtrog 2012a ; Wei and Bachtrog 2019 ). However, the accumulation of gene expression differences separately from degeneration during the very earliest stages of sex chromosome evolution is not well understood.…”