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

X and Y chromosomes are derived from a pair of homologous autosomes, which then diverge from each other over time. Although Y-specific features have been characterized in sex chromosomes of various ages, the earliest stages of Y chromosome evolution are poorly understood. In particular, we do not know whether early stages of Y chromosome evolution consist of changes to individual genes or happen via chromosome-scale divergence from the X.

To address this question, we used house fly, Musca domestica, as a model because it has very young sex chromosomes that are still segregating as polymorphisms within natural populations. To identify early differentiation between the very young X and Y chromosomes, we compared genotypic (XY) and sex-reversed (XX) males in gene sequence and gene expression using RNA-seq and Oxford Nanopore sequencing data. There is an excess of genes with divergent expression between the X and Y copies, but the number of genes is small. This suggests that individual Y genes, but not the entire Y chromosome, have diverged from their homologous X-linked alleles.

We identified one gene, encoding an axonemal dynein assembly factor (which functions in sperm motility), that has higher expression in the abdomens of XY males than XX males because of a disproportionate contribution of the Y allele to gene expression. The up-regulation of the Y-linked copy of this gene may be favored in males because of its function in spermatogenesis, consistent with sexually antagonistic selection affecting the expression evolution of individual genes during early Y chromosome evolution.