Delclos, P. J. | bioRxiv Science

bioRxiv2021

A conserved trans regulatory loop involving an odorant binding protein controls male mating behavior in flies

Y chromosomes have male-limited inheritance, which favors the fixation of alleles that affect spermatogenesis, courtship, and other male-specific traits. Y-linked male-beneficial alleles can also have female-deleterious (sexually antagonistic) effects because they never experience direct selection in females. However, determining the mechanisms underlying these male-beneficial effects is challenging because it can require studying Y-linked alleles while they still segregate as polymorphism. We used a Y chromosome polymorphism in the house fly, Musca domestica, to address this challenge. Two common male-determining Y chromosomes (YM and IIIM) segregate as stable polymorphisms in natural house fly populations, and they differentially affect multiple traits, including male courtship performance. We performed a meta-analysis of RNA-seq data and identified differentially expressed genes encoding odorant binding proteins (in the Obp56h family) as candidate causal agents in the courtship differences. The Obp56h genes are not found on either the YM or IIIM chromosomes, suggesting that they must be regulated in trans by one of the house fly sex chromosomes. Using a network analysis and allele-specific expression measurements, we identified multiple genes on the house fly IIIM chromosome that could serve as trans inhibitors of Obp56h gene expression. One of those genes is homologous to D. melanogaster CG2120, which encodes a transcription factor that binds both up- and down-stream of Obp56h. We found that up-regulation of CG2120 in D. melanogaster nervous tissues reduces copulation latency, consistent with this transcription factor acting as a negative regulator of Obp56h expression. We propose the name speed date (spdt) for CG2120, with the house fly homolog named Md-spdt. The expression of spdt across D. melanogaster development and tissues suggests that evolution of higher expression in neurons may be constrained by pleiotropic or sexual antagonistic effects. We hypothesize that a cis-regulatory allele that increases expression of Md-spdt on the IIIM chromosome exists because Y-linkage of this allele releases it from those constraints. This provides evidence for a molecular mechanism by which a Y-linked gene can evolve a male-beneficial function regardless of the negative effects on females.

evolutionary biology↗

bioRxiv2021

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

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.

evolutionary biology↗