Molecular mechanisms for signal-receptor functional coupling in pheromonal systems

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Successful mating is essential for the survival of most animal species. For many species, the decision with whom to mate depends on information communicated via the release of 'pheromones', a complex blend of chemicals that are released by one animal to be sensed by another. Therefore, understanding how pheromones affect mating behaviors has broad implications for animal behavior and evolutionary biology. Because pheromones communicate precise information, the links between pheromone production and perception are expected to be relatively stable within species. However, previous studies suggest that pheromones are remarkably flexible, and can change rapidly as new species evolve. One possible explanation for this apparent puzzle is that some shared genes co-regulate the independent processes responsible for pheromone production and perception. These shared genes could provide a path for the evolution of pheromone signals without losing the link between pheromone production and perception. This hypothesis will be tested by taking advantage of the fruit fly courtship ritual as a model. Studies will focus on genes that encode proteins that function as pheromone receptors in the nervous system, as well as regulators of pheromone cuticular production, and their possible role in pheromonal differences between males and females and across related fruit fly species. In addition to training opportunities for high school and undergraduate students, the broader impacts of this project will include genetics and neuroscience outreach and education activities associated with the public education system in the St. Louis region. Mating pheromones are essential for the maintenance of species boundaries in diverse animal taxa. However, it is puzzling how, as closely related species diversify, pheromones could evolve without fitness costs associated with their decoupling from related mate choice behaviors. The goal of this project is to test the hypothesis that mating pheromone production and perception are genetically linked via the action of pleiotropic genes. Specifically, the project will test the hypothesis that members of the Gustatory receptor protein family in Drosophila play a role in the sensory perception of specific cuticular pheromones as well as in the regulation of their synthesis by acting as regulatory autoreceptors in the pheromone-producing oenocytes. Approaches will include a combination of behavioral, chemo-analytical, and state-of-the-art CRISPR/Cas9-dependent genome editing approaches to establish a genetic linkage between the perception and production of pheromones, to investigate the role of pleiotropic chemoreceptors in regulating the female pre-to-post-mating phenotypic switch from attractive to repulsive pheromonal profile, and the role of pheromone receptor evolution in promoting assortative mating and speciation in the genus Drosophila. Findings will provide novel mechanistic insights into the regulation of mating behaviors by pheromones in particular, and the evolution of mating signals in general. In addition to diverse genetics and neuroscience outreach activities in the St. Louis region, the investigator and co-workers will use studies of mating behaviors as training opportunities for high school and undergraduate students in experimental design, behavioral and genetic data collection and analyses, and scientific presentations.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.