The evolving puzzle of autosomal versus Y-linked male determination in Musca 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-tra(D), 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-tra(D) 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.

Keywords: Md-traD; autosomal male; genetics of sex; house fly; sex determination.

Figure 1

Sex-determination pathways. The (A) male and (B) female Drosophila sex-determination pathways are shown, along with the house fly (C) male-determining pathway, (D) canonical female-determining pathway, and (E) female-determining pathway via the action of Md-tra^D. The core of the pathway that is conserved across brachyceran flies is contained within the dashed box. Abbreviations are described in the main text.

Figure 2

Schematic representation of the evolution of changes in the linkage of M and frequency of F (Md-tra^D) in the house fly, M. domestica. Autosomes III and IV are used for illustration purposes but could be any of the autosomes (see Table 1). Genotype is given only for the male unless otherwise specified. Females are assumed to be III⁺/III⁺ ; IV⁺/IV⁺; XX unless otherwise specified. (A) Changes possible from the ancestral state (XY^M, with no autosomomal males). (B) Continued from (A). Schematic representation of the evolution of males and females homozygous for M. (C) Continued from (A). Schematic representation of the evolution of males with copies of M on different autosomes. The A^M factors are assumed to be derived from the M factor on Y (Hiroyoshi 1964), and the M factors are thought to incorporate into a specific site on each autosome (Inoue et al. 1983).

Figure 3

The relative percentage of males with M on each of the chromosomes. Results were calculated from the data in Table 1. Values represent relative percentages, as different reports used in Table 1 accounted for males with multiple M factors using different calculations. Studies failing to find a linkage of M to an autosome called these strains Y^M, although in the absence of karyotype information these strains could also be X^M.