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.

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

“…However, the III M males have elevated heterozygosity on the X chromosome ( Figure 1; P = 8.32´10 -13 in a Wilcoxon rank sum test comparing the X chromosome with chromosomes I, II, IV, and V). Elevated X chromosome heterozygosity in III M males was also observed in a comparison with Y M males (Meisel et al 2017), and its cause remains unresolved. One possible explanation for elevated X chromosome heterozygosity is that the III M chromosome was created by a fusion between the third chromosome and the Y M chromosome.…”

“…One possible explanation for elevated X chromosome heterozygosity is that the III M chromosome was created by a fusion between the third chromosome and the Y M chromosome. Because Y M has nearly identical gene content as the X chromosome (Meisel et al 2017), a III-Y M fusion would cause III M males to have three copies of X chromosome genes, increasing the likelihood that III M males are heterozygous at any given site on the X chromosome. This hypothesis remains to be tested.…”

“…Second, the other common proto-Y (known as Y M ) has fewer than 100 genes, which is over one order of magnitude less than III M (Meisel et al 2017;. More genes on the third chromosome gives us greater power to detect divergence between the proto-Y and proto-X.…”

Temperature-dependent effects of house fly proto-Y chromosomes on gene expression

“…RealignerTargetCreator to identify and IndelRealigner to realign the indels. We used BaseRecalibrator and variant calls from a previous RNA-seq analysis (R. P. Meisel et al, 2017) to recalibrate the realigned reads. The realigned reads were then used for variant calling with…”

“…Mdmd can be found on multiple different chromosomes in house fly (Sharma et al, 2017) , and it is most commonly found on the third (III M ) and Y (Y M ) chromosomes (Hamm et al, 2015) . These Mdmd-bearing chromosomes are young proto-Y chromosomes that are minimally differentiated from their homologous X chromosomes (Meisel, Gonzales, & Luu, 2017) . The proto-Y chromosomes are clinally distributed-with III M most common at southern latitudes and Y M most common at northern latitudes-across multiple continents (Denholm, Franco, Rubini, & Vecchi, 1986;Hamm, Shono, & Scott, 2005;Hiroyoshi, 1964;Mcdonald et al, 1975) .…”