The Evolving Puzzle of AutosomalVersusY-linked Male Determination inMusca domestica

Abstract

Sex determination is one of the most rapidly evolving developmental pathways, but the factors responsible for this fast evolution are not well resolved. The house fly, Musca domestica, is an ideal model for studying sex determination because house fly sex determination is polygenic and varies considerably between populations. Male house flies possess a male-determining locus, the M factor, which can be located on the Y or X chromosome or any of the five autosomes. There can be a single M or multiple M factors present in an individual male, in heterozygous or homozygous condition. Males with multiple copies of M skew the sex ratio toward the production of males. Potentially in response to these male-biased sex ratios, an allele of the gene transformer, Md-traD, promotes female development in the presence of one or multiple M factors. There have been many studies to determine the linkage and frequency of these male determining factors and the frequency of Md-traD chromosomes in populations from around the world. This review provides a summary of the information available to date regarding the patterns of distribution of autosomal, X-linked and Y-linked M factors, the relative frequencies of the linkage of M, the changes in frequencies found in field populations, and the fitness of males with autosomal M factors vs. Y-linked M. We evaluate this natural variation in the house fly sex determination pathway in light of models of the evolution of sex determination.

The house fly Y Chromosome is young and minimally differentiated from its ancient X Chromosome partner

“…We conclude that the house fly X Chromosome has few genes (if any) not found on the Y Chromosome, and there are only a handful of recently acquired Y-specific genes in addition to Mdmd. This is consistent with previous experiments that failed to identify sexlinked markers and found that XX, XO, and YO flies are viable and fertile (Bull 1983;Hediger et al 1998a;Hamm et al 2015). Additionally, XY males have equal or greater expression of X Chromosome genes when compared to XX (III M ) males , providing further evidence that XY males do not have a haploid X Chromosome dose.…”

“…Mdmd has been mapped to the autosomes as well as the Y Chromosome (Sharma et al 2017), suggesting that the house fly Y and the autosomes harboring Mdmd are all recently derived neo-Y Chromosomes. Second, no sex-linked genetic markers have been identified on the house fly X or Y Chromosomes other than Mdmd (Hamm et al 2015), suggesting that there are no X-specific genes or genetic variants that are not found on the Y Chromosome. Third, males with an autosomal Mdmd that do not carry a Y Chromosome (XX males) are fertile (Bull 1983;Hamm et al 2015), suggesting that no essential male fertility genes are unique to the Y Chromosome apart from Mdmd.…”

“…Second, no sex-linked genetic markers have been identified on the house fly X or Y Chromosomes other than Mdmd (Hamm et al 2015), suggesting that there are no X-specific genes or genetic variants that are not found on the Y Chromosome. Third, males with an autosomal Mdmd that do not carry a Y Chromosome (XX males) are fertile (Bull 1983;Hamm et al 2015), suggesting that no essential male fertility genes are unique to the Y Chromosome apart from Mdmd. Fourth, house flies that carry only a single copy of either the X or Y Chromosome (i.e., XO or YO flies) are viable and fertile (Bull 1983;Hediger et al 1998a), indicating that no essential genes are uniquely found on the X and missing from the Y Chromosome and vice versa.…”

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

“…The house fly X and Y chromosomes can be distinguished based on their length in cytological preparations (Denholm et al, 1983;Cakir and Kence, 1996;Hediger et al, 1998b), and close relatives of the house fly (Lucilia blow flies) have the ancestral karyotype with differentiated X and Y chromosomes (Linger et al, 2015;Vicoso and Bachtrog, 2015). In contrast to other flies, the house fly M factor has been mapped to each of the five autosomes in addition to the Y chromosome (Hamm et al, 2015). The autosomes harboring M are expected to be neo-Y chromosomes, but the house fly Y chromosome is often assumed to be the ancestral brachyceran Y that is differentiated from the X Hamm et al, 2015).…”

Sex chromosome evolution in muscid flies

“…In contrast to flesh flies and blow flies, multiple lineages in the family Muscidae seem to have evolved new sex chromosomes in the <40 My since the common ancestor of the family (Ding et al, 2015). 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).…”