Abstract
X and Y chromosomes are usually 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 remain elusive. 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 quantified divergence between young proto-X and proto-Y chromosomes in the house fly, Musca domestica. We compared proto-sex chromosome sequence and gene expression between genotypic (XY) and sex-reversed (XX) males. We find evidence for sequence divergence between genes on the proto-X and proto-Y, including five genes with mitochondrial functions. There is also an excess of genes with divergent expression between the proto-X and proto-Y, but the number of genes is small. This suggests that individual proto-Y genes, but not the entire proto-Y chromosome, have diverged from the proto-X. We identified one gene, encoding an axonemal dynein assembly factor (which functions in sperm motility), that has higher expression in XY males than XX males because of a disproportionate contribution of the proto-Y allele to gene expression. The upregulation of the proto-Y allele may be favored in males because of this gene’s function in spermatogenesis. The evolutionary divergence between proto-X and proto-Y copies of this gene, as well as the mitochondrial genes, is consistent with selection in males affecting the evolution of individual genes during early Y chromosome evolution.
Highlights
In many organisms with two separate sexes, a gene on a sex chromosome determines whether an individual develops into a male or female
We found that the genotypic males have an excess of heterozygous sites in third chromosome genes, relative to the sex-reversed males (Figure 1; P < 10-16 in a Wilcoxon rank sum test comparing percent heterozygous sites in genes on the third chromosome with genes on the other chromosomes). This is consistent with elevated third chromosome heterozygosity in a previous comparison between IIIM males and Y chromosome (YM) males
(Meisel et al 2017), and it suggests that the sequences of genes on the IIIM proto-Y chromosome are differentiated from the copies on the proto-X
Summary
In many organisms with two separate sexes, a gene on a sex chromosome determines whether an individual develops into a male or female. In XX/XY sex chromosome systems, males are the heterogametic sex (XY genotype), and females are homogametic with the XX genotype Most X and Y chromosomes are derived from a pair of ancestral autosomes. One copy of the autosome can obtain a male-determining gene and become a proto-Y chromosome, and the homologous chromosome without the male-determiner becomes a proto-X. As the proto-X and proto-Y chromosomes diverge from each other over time, they become differentiated X and Y chromosomes (Bull 1983; Charlesworth et al 2005). Sex chromosomes have originated and diverged from each other in multiple independent evolutionary lineages (Bachtrog et al 2014; Beukeboom and Perrin 2014)
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