Role of Genotype-by-Temperature Interactions in the Maintenance of Polygenic Sex Determination in the House Fly

Sex determination is the process by which sexually dimorphic developmental pathways are established. In genetic sex determination systems, a single master regulatory locus determines the sex of an individual. However, some organisms have multiple master sex determining loci in their genome that segregate independently, resulting in polygenic sex determination. Most population genetics models predict that polygenic sex determination will be an unstable intermediate between monogenic systems, and the factors responsible for maintaining polygenic sex determination are poorly understood. House fly (Musca domestica) has a stable polygenic sex determination system with multiple male and female determiners segregating in natural populations. The male determining gene is commonly found on two different proto-Y chromosomes (YM and IIIM). YM is found in colder, northern latitudes, whereas IIIM is found in southern, warmer latitudes. This suggests that selection operating on a genotype-by-temperature (G×T) interaction maintains this polymorphism. To test this hypothesis, I raised IIIM and YM males with otherwise common genetic backgrounds at high and low temperatures, and I studied the resulting G×T effects on multiple phenotypes. YM males raised at low temperature are more cold tolerant, and IIIM males raised at high temperatures are more heat tolerant, consistent with their distribution in nature. Next, using RNA-seq, I identified 247 genes whose expression in testis and 50 genes whose expression in head depends on GxT interactions. I found G×T effects on the expression of genes on the proto-Y chromosomes other than those in the sex determination pathway. Chemosensory, metabolic, immune, reproductive, and lifespan related genes are differentially expressed because of G×T interactions. Further, using inter-strain and intra-strain mating assays, I found IIIM males have a mating advantage over YM males and males from lower temperatures have a mating advantage over males from higher temperatures. Using a survival assay, I found some differences in lifespan between YM and IIIM males. My results suggest that G×T effects of genes on the proto-Y chromosomes other than the male-determiner are the targets of selection responsible for maintaining polygenic sex determination in house fly, which could be mediated through effects of the proto-Y chromosomes on gene expression. This provides an ecological mechanism to maintain polygenic sex determination.Biology and Biochemistry, Department o