The House Fly Y Chromosome is Young and Minimally Differentiated from its Ancient X Chromosome Partner

Abstract

Canonical ancient sex chromosome pairs consist of a gene rich X (or Z) chromosome and a male- (or female-) limited Y (or W) chromosome that is gene poor. In contrast to highly differentiated sex chromosomes, nascent sex chromosome pairs are homomorphic or very similar in sequence content. Nascent sex chromosomes arise frequently over the course of evolution, as evidenced by differences in sex chromosomes between closely related species and sex chromosome polymorphisms within species. Sex chromosome turnover typically occurs when an existing sex chromosome becomes fused to an autosome or an autosome acquires a new sex-determining locus/allele. Previously documented sex chromosome transitions involve changes to both members of the sex chromosome pair (X and Y, or Z and W). The House fly has sex chromosomes that resemble the ancestral fly karyotype that originated 100 million years ago, and therefore house fly is expected to have X and Y chromosomes with different gene content. We tested this hypothesis using whole genome sequencing and transcriptomic data, and we discovered little evidence for genetic differentiation between the X and Y in house fly. We propose that house fly has retained the ancient X chromosome, but the ancestral Y was replaced by an X chromosome carrying a male determining gene. Our proposed hypothesis provides a mechanisms for how one member of a sex chromosome pair can experience evolutionary turnover while the other member remains unaffected.