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

Abstract

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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“…This type of mutation has been demonstrated as occurring within several Diptera, including mosquitoes (Diptera: Culicidae), and is responsible for the increased receptibility to the repellent N,Ndietyl-3-toluamide (DEET), [72] which would possibly explain why H. illucens is highly sensitive to insecticides. [73] More generally, the varied expression of OBPs has been shown to have downstream effects on mating behavior, [74] including the ability to recognize a wider array of pheromones, including those emitted by microbes. [63,75] Hence, for H. illucens, the transition from aquatic life, to terrestrial rotting vegetation, to rotting animal material could either have been gradual or saltatorial, though not necessarily acted on upon directly by natural selection [76] (i.e., not pre-determined [77] ).…”

“…illucens is highly sensitive to insecticides. [ 73 ] More generally, the varied expression of OBPs has been shown to have downstream effects on mating behavior, [ 74 ] including the ability to recognize a wider array of pheromones, including those emitted by microbes. [ 63,75 ] Hence, for H .…”