Temperature-dependent effects of house fly proto-Y chromosomes on gene expression

Adhikari, Kiran; Son, Jae Hak; Rensink, Anna H.; Jaweria, Jaweria; Bopp, Daniel; Beukeboom, Leo W.; Meisel, Richard P.

doi:10.1101/2020.08.05.238378

Cited by 2 publications

(4 citation statements)

References 101 publications

(207 reference statements)

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“…However, the effects of the house fly proto‐Y chromosomes on thermal tolerance and preference likely act independently of the sex‐determination pathway because there are not differences in the expression of sex‐determination genes across house fly male genotypes raised at different temperatures in a way that is consistent with their clinal distribution (Adhikari et al. 2020 ). This suggests that the effects of the Y M and III M chromosomes on thermal phenotypes are a result of alleles on proto‐Y chromosomes that are genetically linked to the male‐determining locus, as opposed to the male‐determiner itself.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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“…To do so, we followed methods as in previous studies (Meisel et al 2017; Son and Meisel 2021), which use the Genome Analysis Toolkit (GATK) best practices workflow for single nucleotide polymorphism (SNP) calling to identify sequence variants in our RNA-Seq data (McKenna et al2010). We focused our analysis on libraries that were sequenced from head tissue of male house flies that comprise a CS genetic background (Meisel et al 2015; Son et al 2019; Adhikari et al2021). We used STAR (Dobin et al 2013) to align reads from a total of 30 head libraries (15 III M and 15 Y M libraries) to the house fly reference genome (Musca_domestica-2.0.2).…”

Section: Methodsmentioning

confidence: 99%

“…These two strains have a common genetic background (CS), and only differ in which proto-Y chromosome they carry. Both strains are represented in the RNA-seq data we analyzed (Meisel et al 2015;Son et al 2019) , and IsoCS was also included in a previous RNA-seq study comparing the effects of proto-Y chromosome and temperature on gene expression (Adhikari et al 2021) . Our experiment differed from previous work because we reared larvae from each strain at either 18°C and 29°C, whereas Hamm et al (2009) worked with flies raised at 28°C.…”

Section: Competitive Mating Assaysmentioning

confidence: 99%

“…To those ends, we tested for genotype-by-temperature interactions affecting differences in male mating behavior between Y M and III M males. We also used RNA-seq data to investigate the genetic basis of differences in mating performance between Y M and III M males (Meisel et al 2015; Son et al 2019; Adhikari et al 2021). Our results implicate genes encoding odorant binding proteins (Obps) in an evolutionarily conserved trans regulatory loop involving a chromosome that independently became sex-linked in both house fly and Drosophila .…”

Section: Introductionmentioning

confidence: 99%

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Transregulation of an odorant binding protein by a proto-Y chromosome affects male courtship in house fly

Adhikari

Hassan

et al. 2021

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A major goal in evolutionary biology is to understand how natural variation is maintained in sexually selected and sexually dimorphic traits. Hypotheses to explain genetic variation in sexually selected traits include context-dependent fitness effects, epistatic interactions, and pleiotropic constraints. The house fly, Musca domestica, is a promising system to investigate how these factors affect polymorphism in sexually selected traits. Two common Y chromosomes (YM and IIIM) segregate as stable polymorphisms in natural house fly populations, appear to be locally adapted to different thermal habitats, and differentially affect male mating success. Here, we perform a meta-analysis of RNA-seq data which identifies genes encoding odorant binding proteins (in the Obp56h family) as differentially expressed between the heads of males carrying YM and IIIM. Differential expression of Obp56h has been associated with variation in male mating behavior in Drosophila melanogaster. We find differences in male mating behavior between house flies carrying the Y chromosomes that are consistent with the relationship between male mating behavior and expression of Obp56h in D. melanogaster. We also find that male mating behaviors in house fly are affected by temperature, and the same temperature differentials further affect the expression of Obp56h genes. However, we show that temperature-dependent effects cannot explain the maintenance of genetic variation for male mating behavior in house fly. Using a network analysis and allele-specific expression measurements, we find evidence that the house fly IIIM chromosome is a trans regulator of Obp56h gene expression. Moreover, we find that Obp56h disproportionately affects the expression of genes on the D. melanogaster chromosome that is homologous to the house fly IIIM chromosome. This provides evidence for a conserved trans regulatory loop involving Obp56h expression that affects male mating behavior in flies. The complex regulatory architecture controlling Obp56h expression suggests that variation in male mating behavior could be maintained by epistasis or pleiotropic constraints.

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Temperature-dependent effects of house fly proto-Y chromosomes on gene expression

Cited by 2 publications

References 101 publications

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

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

Transregulation of an odorant binding protein by a proto-Y chromosome affects male courtship in house fly

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