The Evolution of Sex Determination Mechanisms and Sex Chromosomes in House fly, Musca domestica L.



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Sex determination (SD) evolves fast, often due to changes in master regulatory SD genes. SD genes are found on sex chromosomes, and evolution of SD can also drive evolutionary turnover of sex chromosomes. As a consequence, young (proto) sex chromosomes are generated, in which the X and Y are minimally diverged from each other. Multiple young sex chromosomes can coexist in species with multiple (polygenic) SD master regulators. Species with polygenic SD are informative of the factors driving the early evolution of sex chromosomes. The house fly, Musca domestica, is a well-suited model to those ends because natural populations have polygenic SD and young sex chromosomes. Natural selection appears to maintain polygenic SD, but the targets of selection are elusive. To address this, I examined the effects of two house fly proto-Y chromosomes (YM and IIIM) on gene expression. I find that the proto-Y chromosomes have minor effects on gene expression, which is paradoxical given that natural selection likely maintains polygenic SD in house fly. I identified evidence for disproportionate effects of the proto-Y chromosomes on sex-biased expression. These few expression differences could be targets upon which natural selection acts to maintain polygenic SD. The frequencies of YM and IIIM vary along latitudinal clines, and I tested whether temperature could explain these clines by examining the expression of SD pathway genes at different developmental temperatures. I did not find differences in expression of the sex-determining genes between YM and IIIM males consistent with the clines. I also found that one house fly proto-Y chromosome is differentiated from its homologous proto-X in the sequences of many genes, but gene expression divergence between the proto-X and proto-Y is limited to a subset of genes. This suggests that subtle gene expression differentiation constitutes the earliest stages of X-Y differentiation. Lastly, I tried constructing a stable line that has females carrying the dominant female-determining Md-traD allele. In this line, all females and males would carry two copies of IIIM. However, I could not create a stable line because males homozygous for IIIM could have low fitness or deleterious effects.



Polygenic sex determination, Young sex chromosome, RNA-seq, Sexual dimorphic expression, Allele-specific expression, Temperature-dependent selection