Thermal tolerance and preference are both consistent with the clinal distribution of house fly proto-Y chromosomes

Abstract

Selection pressures can vary within localized areas and across massive geographical scales. Temperature is one of the best studied ecologically variable abiotic factors that can affect selection pressures across multiple spatial scales. Organisms rely on physiological (thermal tolerance) and behavioral (thermal preference) mechanisms to thermoregulate in response to environmental temperature. In addition, spatial heterogeneity in temperatures can select for local adaptation in thermal tolerance, thermal preference, or both. However, the concordance between thermal tolerance and preference across genotypes and sexes within species and across populations is greatly understudied. The house fly, Musca domestica, is a well-suited system to examine how genotype and environment interact to affect thermal tolerance and preference. Across multiple continents, house fly males from higher latitudes tend to carry the male-determining gene on the Y chromosome, whereas those from lower latitudes usually have the male-determiner on the third chromosome. We tested whether these two male-determining chromosomes differentially affect thermal tolerance and preference as predicted by their geographical distributions. We identify effects of genotype and developmental temperature on male thermal tolerance and preference that are concordant with the natural distributions of the chromosomes, suggesting that temperature variation across the species range contributes to the maintenance of the polymorphism. In contrast, female thermal preference is bimodal and largely independent of congener male genotypes. These sexually dimorphic thermal preferences suggest that temperature-dependent mating dynamics within populations could further affect the distribution of the two chromosomes. Together, the differences in thermal tolerance and preference across sexes and male genotypes suggest that different selection pressures may affect the frequencies of the male-determining chromosomes across different spatial scales. Impact StatementGenetic variation within species can be maintained by environmental factors that vary across the species range, creating clinal distributions of alleles responsible for ecologically important traits. Some of the best examples of clinal distributions come from temperature-dependent phenotypes, such as thermal tolerance and preference. Although genotype and developmental temperature strongly affect physiological and behavioral traits in ectotherms, the correlation between these traits across genotypes and sexes within species is greatly understudied. We show that two different male-determining chromosomes found in natural populations of house flies affect both thermal tolerance and preference in a way that is concordant with their clinal distributions across latitudes. This provides strong evidence that temperature variation across the species range contributes to the maintenance of the polymorphism. Furthermore, we find evidence that thermal preference is sexually dimorphic, suggesting that temperature-dependent mating dynamics could further affect the distribution of genetic variation in this system. Therefore, at a macro-geographical scale, the differences in thermal tolerance and preference across male genotypes likely contributes to the maintenance of the cline. Within populations, differences in thermal preference likely affect sexual selection dynamics, which may further affect the frequencies of the chromosomes.