Sex determination, the developmental process by which sexually dimorphic phenotypes are established, evolves fast. Evolutionary turnover in a sex determination pathway may occur via selection on alleles that are genetically linked to a new master sex determining locus on a newly formed proto‐sex chromosome. Species with polygenic sex determination, in which master regulatory genes are found on multiple different proto‐sex chromosomes, are informative models to study the evolution of sex determination and sex chromosomes. House flies are such a model system, with male determining loci possible on all six chromosomes and a female‐determiner on one of the chromosomes as well. The two most common male‐determining proto‐Y chromosomes form latitudinal clines on multiple continents, suggesting that temperature variation is an important selection pressure responsible for maintaining polygenic sex determination in this species. Temperature‐dependent fitness effects could be manifested through temperature‐dependent gene expression differences across proto‐Y chromosome genotypes. These gene expression differences may be the result of
- Award ID(s):
- 1845686
- PAR ID:
- 10304351
- Date Published:
- Journal Name:
- bioRxiv
- ISSN:
- 2692-8205
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract cis regulatory variants that affect the expression of genes on the proto‐sex chromosomes, ortrans effects of the proto‐Y chromosomes on genes elswhere in the genome. We used RNA‐seq to identify genes whose expression depends on proto‐Y chromosome genotype and temperature in adult male house flies. We found no evidence for ecologically meaningful temperature‐dependent expression differences of sex determining genes between male genotypes, but we were probably not sampling an appropriate developmental time‐point to identify such effects. In contrast, we identified many other genes whose expression depends on the interaction between proto‐Y chromosome genotype and temperature, including genes that encode proteins involved in reproduction, metabolism, lifespan, stress response, and immunity. Notably, genes with genotype‐by‐temperature interactions on expression were not enriched on the proto‐sex chromosomes. Moreover, there was no evidence that temperature‐dependent expression is driven by chromosome‐widecis ‐regulatory divergence between the proto‐Y and proto‐X alleles. Therefore, if temperature‐dependent gene expression is responsible for differences in phenotypes and fitness of proto‐Y genotypes across house fly populations, these effects are driven by a small number of temperature‐dependent alleles on the proto‐Y chromosomes that may havetrans effects on the expression of genes on other chromosomes. -
Abstract Sex chromosomes often differ between closely related species and can even be polymorphic within populations. Species with multifactorial sex determination segregate for multiple different sex-determining loci within populations, making them uniquely informative of the selection pressures that drive the evolution of sex chromosomes. The house fly (Musca domestica) is a model species for studying multifactorial sex determination because male-determining genes have been identified on all six of the chromosomes, which means that any chromosome can be a “proto-Y.” Natural populations of house flies also segregate for a recently derived female-determining locus, meaning house flies also have a proto-W chromosome. The different proto-Y chromosomes are distributed along latitudinal clines on multiple continents, their distributions can be explained by seasonality in temperature, and they have temperature-dependent effects on physiological and behavioral traits. It is not clear, however, how the clinal distributions interact with the effect of seasonality on the frequencies of house fly proto-Y and proto-W chromosomes across populations. To address this question, we measured the frequencies of house fly proto-Y and proto-W chromosomes across nine populations in the United States of America. We confirmed the clinal distribution along the eastern coast of North America, but it is limited to the eastern coast. In contrast, the annual mean daily temperature range predicts proto-Y chromosome frequencies across the entire continent. Our results therefore suggest that temperature heterogeneity can explain the distributions of house fly proto-Y chromosomes in a way that does not depend on the cline.
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