Transcriptome Differences between Alternative Sex Determining Genotypes in the House Fly,Musca domestica

Abstract

Sex determination evolves rapidly, often because of turnover of the genes at the top of the pathway. The house fly, Musca domestica, has a multifactorial sex determination system, allowing us to identify the selective forces responsible for the evolutionary turnover of sex determination in action. There is a male determining factor, M, on the Y chromosome (YM), which is probably the ancestral state. An M factor on the third chromosome (IIIM) has reached high frequencies in multiple populations across the world, but the evolutionary forces responsible for the invasion of IIIM are not resolved. To test whether the IIIM chromosome invaded because of sex-specific selection pressures, we used mRNA sequencing to determine whether isogenic males that differ only in the presence of the YM or IIIM chromosome have different gene expression profiles. We find that more genes are differentially expressed between YM and IIIM males in testis than head, and that genes with male-biased expression are most likely to be differentially expressed between YM and IIIM males. We additionally find that IIIM males have a “masculinized” gene expression profile, suggesting that the IIIM chromosome has accumulated an excess of male-beneficial alleles because of its male-limited transmission. These results are consistent with the hypothesis that sex-specific selection acts on alleles linked to the male-determining locus driving evolutionary turnover in the sex determination pathway.

Repeated Duplication of Argonaute2 Is Associated with Strong Selection and Testis Specialization in Drosophila

“…The expression of Ago2 paralogs has previously been characterized in P. monodon and shows that one paralog has indeed specialized to the germline of both males and females, but not the testis alone ( Leebonoi et al 2015 ). Publicly available RNA-seq data from the head, gonad, and carcass of male and female M. domestica (GSE67065, Meisel et al 2015 ) suggest that neither M. domestica Ago2 paralog has specialized to the testis ( Figure S8 ). However, public data from the head, thorax, and abdomen of male and female D. willistoni (GSE31723, Meisel et al 2012 ) show that one D. willistoni Ago2 paralog (FBgn0212615) is expressed ubiquitously, while the other (FBgn0226485) is expressed only in the male abdomen ( Figure S8 ), consistent with the evolution of testis specificity after duplication.…”

Minimal Effects of Proto-YChromosomes on House Fly Gene Expression in Spite of Evidence that Selection Maintains Stable Polygenic Sex Determination

“…We examined gene expression in four house fly strains that each have a different naturally occurring proto-Y chromosome (either Y M or III M ) on a common genetic background ( Figure 1). We used a previously described backcrossing method to move each proto-Y chromosome onto the Cornell Susceptible (CS) genetic background (Meisel et al 2015). CS is an inbred III M strain produced by mixing strains collected from throughout the United States (Scott et al 1996).…”

“…We used RNA-seq to measure gene expression in heads and abdomens from individual males of the four strains carrying either the Y M or III M proto-Y chromosomes (Figure 1). The larvae were raised at 25°on a standard diet of wheat bran, calf manna, yeast, reptile litter, and water, as described previously (Hamm et al 2009;Meisel et al 2015). Unmated adult males and females were sorted within 8 hr of emergence, kept separately at 22°, and provided with water, sugar, and powdered milk ad libitum.…”

The Guppy Sex Chromosome System and the Sexually Antagonistic Polymorphism Hypothesis for Y Chromosome Recombination Suppression

“…In African cichlids, at least nien autosomes have become sex chromosomes, apparently in the last 15 million years, and large regions (≥19 Mb) with clear footprints of complete XY-linkage were found on different chromosomes in three species [ 76 ]. Some fish sex-determining loci could be similar to the apparently moveable housefly M factor (male-determining factor) [ 84 , 85 , 86 ], but, as mentioned above, there is no evidence that the guppy male-determiner is ever carried on a chromosome other than 12. However, a chromosome 12 location has not yet been verified in many families or populations.…”