Collaborative Research: Testing for physiological and genetic independence of rapidly evolving lifecycle components in the apple maggot, a model for seasonal adaptation

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Organisms must time their lifecycles to avoid stressful periods of the year (e.g., winter cold and lack of resources) and to exploit the good times of the year when weather is favorable and resources are abundant. Dormancy responses have evolved in many organisms, from plants and microbes to mammals and insects, to achieve synchrony with local seasonal conditions. Organisms are increasingly challenged by new seasonal regimes caused by 1) contemporary climate change, 2) habitat modifications from human development and urbanization, and 3) movement of species into new areas through managed or accidental introductions. Thus, understanding how dormancy responses rapidly evolve and compensate for shifts in seasonality will be a critical component for understanding the persistence and spread of native and invasive species in our rapidly changing world. This research will characterize the mechanisms that allow rapid adaptation to novel seasonality via changes in dormancy in the apple maggot fly, Rhagoletis pomonella, a major pest of apples and a textbook example of rapid species formation. Within the last 200 years, R. pomonella has shifted from its native host hawthorn (Crataegus mollis) to introduced, domesticated apple (Malus domestica), and in the process has formed new, partially reproductively isolated populations on apples. Seasonal fruiting time differs substantially among plant species in a given region, so adapting to a novel fruit requires adaptation in insect seasonal timing. In R. pomonella, the newly derived apple population has become established on their novel host fruit via evolved differences in timing of the overwintering dormant stage, which results in temporal matching of insect growth and reproduction with earlier seasonal availability of apple compared to hawthorn fruits. Physiological mechanisms that evolve to adjust dormancy timing are poorly understood, and this research will leverage variation among the fly populations to quantify physiological differences in gene and protein expression and differences in the genome that underlie adaptation at key regulatory points across the fly life cycle. Additionally, experiments will address whether common physiological mechanisms underlie adaptation across the three phases of dormancy (dormancy induction, maintenance, and termination) potentially constraining the rate or direction of evolutionary responses to changing seasonality. This fundamental research has implications in numerous contexts from preserving biodiversity to forecasting agricultural production and the spread of invasive species. Beyond identifying important features facilitating rapid responses to seasonal change, the project will also enhance a pre-collegiate education program in evolutionary biology. Host race formation in R. pomonella provides a clear and intuitive example of ecological adaptation and the genesis of new crop pests, making the flies excellent ambassadors for evolution, a subject poorly understood by many students and the general public. The research team previously developed a workshop and outreach program for STEM education to enhance the evolution knowledge of high school teachers and students from Florida and Puerto Rico, providing materials for science curricula. The current grant will expand the high-school teacher training, add freely accessible web-based curricular materials, and most importantly, formally evaluate the impact of the educational program. Survey-based assessments delivered before, during and after the workshop will assess changes in perception of frequently misunderstood concepts in evolutionary biology.