Collaborative Research: Molecular and evolutionary mechanisms underlying the rapid gain and loss of an insect pheromone

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Insects make critical decisions about reproduction and survival based on the perception of pheromones, specialized chemical signals exchanged between members of the same species that indicate whether an individual is male or female and its mating status. The chemical structures of pheromones can differ between closely related species, implying rapid evolution. However, unlike visual signals like wing patterns or auditory signals like mating songs, little is known about how new chemical signals arise and diversify. This collaborative project will investigate the genetic and biochemical processes that underlie the evolution of an anti-aphrodisiac pheromone produced by Drosophila fruit fly species. The findings will deepen our understanding of how evolution at the chemical and molecular level can lead to organismal-scale changes in social behaviors such as mate choice. The research outcomes will have direct application to the design of pheromone-based strategies to disrupt the reproduction of agricultural pests and insects that transmit disease. Training opportunities will be provided to undergraduate students from underrepresented minority backgrounds through laboratory- and literature-based research experiences. In collaboration with Hawaiian language scholars, students will investigate the history of entomological science in Hawai‘i from a Native Hawaiian perspective by researching and translating archival materials that document endemic insects, their habitats, and their role in Hawaiian culture. That work will be disseminated through exchanges between the two participating institutions, University of Hawai‘i Manoa and Michigan State University, and at local public outreach events. Insects represent 80% of the world’s species and use a wide variety of chemosensory signals to make critical decisions about reproduction and survival. However, little is known about the biochemical and genetic processes that shape the diversification of chemosensory traits. The overall goal of this project is to understand how pheromones originate and evolve. The study will identify the metabolic and genetic mechanisms that control the synthesis and evolution of CH503, a male anti-aphrodisiac pheromone produced in the ejaculatory bulb, which is present in some species of Drosophila, but not others. The central hypothesis is that the evolution of the lipid pheromone CH503 is driven by diversification of secondary metabolites and changes in the tissue-specific activation of lipid biosynthesis genes. To uncover mechanisms underlying the rapid evolution of this pheromone, mass spectrometry, transcriptomic analysis, and genetic manipulation will be used to: 1) identify and trace the evolution of the metabolome of the ejaculatory bulb in CH503-producers and non-producers, including D. melanogaster, six other members of the same subgroup, and two distantly related species; 2) identify and trace the evolution of the genetic components underlying the biosynthesis of CH503; and 3) determine how introduction of a novel biosynthetic pathway to species that do not produce CH503 changes the chemical profile of the ejaculatory bulb. The high-sensitivity mass spectrometry-based methods for lipid analysis to be developed, as well as the metabolomic data generated, will be made available to other researchers. This award will also contribute to the training of at least two post-doctoral scholars and six undergraduate researchers, and the results have potential applications in agriculture for the development of methods to control insect populations.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.