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.

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

“…Upregulation of this gene may therefore help III M males tolerate thermal stress at high temperatures. Consistent with this hypothesis, III M males are more tolerant of extreme heat than Y M males, but only if they develop at warm temperatures (Delclos et al, 2021). Our results demonstrate the utility of simultaneously studying the effects of both genotypic and temperature variation to determine how thermal stress affects gene expression (Rivera et al, 2021).…”

“…Moreover, Y M and III M affect thermal tolerance and preference in male house flies in a way that is consistent with their clinal distribution (Delclos et al, 2021). There are at least two nonexclusive ways in which temperature-dependent selection pressures could maintain the III M -Y M polymorphism.…”

High quality genome assembly of the anhydrobiotic midge provides insights on a single chromosome-based emergence of extreme desiccation tolerance

“…( 63 ). Environmental adaptation through genomic evolution on sex chromosomes in insects is rare, as we have found only one study showing thermal adaptation in the house fly Musca domestic linked with Y sex chromosome genes ( 64 ). The P. vanderplanki Chromosome 4 differs from the D. melanogaster sex chromosome as it contains much more genes and is not highly repetitive.…”

Ecology and the evolution of sex chromosomes

“…Temperature override of genetic sex determination in the Australian bearded dragon, Pogona vitticeps (Holleley et al, 2015) Sex chromosome evolution Alleles associated with cold tolerance and climate are enriched on the Drosophila montana X chromosome (Wiberg et al, 2021) Temperature-dependent fitness effects maintain a cline of house fly proto-Y chromosome (Delclos et al, 2021) The best evidence for temperature-dependent fitness effects of Y chromosomes comes from the house fly, Musca domestica (Table 1). House fly has a polygenic sex determination system, and the male-determining gene is frequently found on one of two different proto-Y chromosomes (Hamm et al, 2015;Sharma et al, 2017).…”