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-limited (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 can arise if an existing sex chromosome fuses to an autosome or an autosome acquires a new sex-determining locus/allele. Sex chromosomes often differ between closely related species and can even be polymorphic within species, suggesting that nascent sex chromosomes arise frequently over the course of evolution. 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 yr ago; therefore, the 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 the house fly has retained the ancient X Chromosome, but the ancestral Y was replaced by an X Chromosome carrying a new male determining gene. Our proposed hypothesis provides a mechanism for how one member of a sex chromosome pair can experience evolutionary turnover while the other member remains unaffected.

Sex chromosome evolution in muscid flies

“…We hypothesize that stable fly has young, cryptic sex chromosomes (Fig 1). Nascent sex chromosomes can be identified based on elevated heterozygosity in the heterogametic sex (i.e., XY males) because the X and Y have begun to differentiate in the sequences of genes, but the Y still retains most of the genes in common with the X chromosome (Meisel et al, 2017;Vicoso and Bachtrog, 2015). The stable fly genome was sequenced from male DNA (Olafson et al, 2019), allowing us to identify the sex-linked element(s) by testing for elevated heterozygosity in the genome sequencing reads.…”

“…The small number of annotated element F genes in stable fly likely limit our ability to detect significant masculinization of stable fly element F (Fig 4). There is no significant difference in log 2 M F between genes on horn fly element A (the new portion of the sex (Meisel et al, 2017). There is no evidence for a difference in log 2 M F between genes on element F and the autosomes in house fly.…”

“…Our approach to identifying sex chromosomes involves testing for Muller elements with increased heterozygosity in males, which is the expectation for young, undifferentiated X-Y chromosome pairs (Meisel et al, 2017;Vicoso and Bachtrog, 2015). To those ends, we used the Genome Analysis Toolkit (GATK) version 3.4-0 to identify heterozygous single nucleotide polymorphisms generations (Olafson et al, 2019).…”

“…We used a modified GATK pipeline to identify SNPs in stable fly and horn fly RNA-seq 6 "bioRxiv-2019˙09" -2019/9/20 -15:08 -page 7 -#7 (Meisel et al, 2017). First, RNA-seq reads were aligned to the reference genomes of the appropriate species using STAR version 2.4.0.1 (Dobin et al, 2013).…”

“…The iconic example of sex chromosome evolution in Muscidae is the house fly (Musca domestica), which has a well-characterized polygenic sex determination system (Hamm et al, 2015). House fly appears to have the ancestral brachyceran karyotype (i.e., 5 pairs of euchromatic chromosomes and a heterochromatic sex chromosome pair), but the X and Y chromosomes are not differentiated (Meisel et al, 2017). This is because the house fly maledetermining locus (Mdmd ) is a recently derived duplicated gene that can be found on at least 5 of the 6 chromosomes (Sharma et al, 2017).…”