Temperature‐dependent effects of house fly proto‐Y chromosomes on gene expression could be responsible for fitness differences that maintain polygenic sex determination

Abstract

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 cis regulatory variants that affect the expression of genes on the proto‐sex chromosomes, or trans 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‐wide cis‐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 have trans effects on the expression of genes on other chromosomes.

Strong variation in frequencies of male and female determiners between neighboring housefly populations

“…In the Spanish populations, it seems that the invasion of tra D leads to fixation of a quasi-female heterogametic system, whereas absence of tra D or loss of tra D results in the establishment (or maintenance) of a male heterogametic system. A complicating factor may be the fitness differences of the various M-carrying chromosomes (proto-Y chromosomes, because they are male-determining), as was reported by Adhikari et al (2021). This may cause an ongoing competition of proto-Y among themselves and presence of tra D as the condition for the invasion of multiple proto-Y in the population.…”

Ecology and the evolution of sex chromosomes

“…Moreover, the northern proto-Y chromosome confers greater cold tolerance and preference for colder temperatures, while the southern proto-Y confers heat tolerance and preference (Delclos et al, 2021). Transcriptome-wide gene expression analysis has identified candidate genes whose temperature-dependent expression may be responsible for the phenotypes under selection (Adhikari et al, 2021). These patterns suggest that the polymorphism is maintained by temperature-dependent fitness effects of the proto-Y chromosomes, but it is not yet resolved if these effects are sex-specific.…”

“…In other cases, temperature affects the sex determination pathway in a way that over-rides an existing genetic or chromosomal sex determination system (Holleley et al, 2015). However, temperature can affect the evolution of sex chromosomes independently of the sex determination pathway by, for example, maintaining polymorphisms in which different sex chromosomes have temperature-dependent effects on fitness (Adhikari et al, 2021;Wiberg et al, 2021). Each of these phenomena is illustrated by a small number of examples (Tables 1 and 2), and future work should examine the generalities of these patterns.…”

Divergent evolution of genetic sex determination mechanisms along environmental gradients

“…The geographical transition between these two SD systems is gradual, so that clines exist in the frequencies of Y-chromosomal Mdmd (decreasing towards lower latitudes), autosomal Mdmd and tra D (both increasing towards lower latitudes). Temperature likely plays a causal role in maintaining these gradients by affecting the SD process [41][42][43][44] . Temperature effects on housefly SD have been reported in the form of biased sex ratios produced in wildtype crosses 42 as well as in females carrying the masculinizer (man) mutation, another variant of tra 21,37 .…”