CAREER: The contributions of imperfect transmission and cytoplasmic incompatibility to Wolbachia frequency variation

Over a billion years ago a host cell engulfed a free-living bacterium in a remarkable event that led to the evolution of mitochondria that now provide the chemical energy for animal, plant, and fungal cells. Recent research has revealed that the process of microbes taking up residence inside the cells of other species (known as endosymbiosis) is very common, especially among insects. For example, a single microbe called Wolbachia infects more than half of all insect species on Earth. Unlike mitochondria, Wolbachia are usually not required for their hosts to survive and reproduce. Instead, the proportion of individuals within a host species with Wolbachia at any time varies greatly for unknown reasons, making it hard to predict the consequences for host biology. This project will unravel the causes of variable Wolbachia prevalence as a model for more broadly understanding conditions that favor endosymbiosis. This work will also potentially contribute to improving human health. Wolbachia can block viruses like dengue and Zika in mosquito systems, but increasing the efficacy of this work requires identifying conditions that favor high Wolbachia prevalence. This project will identify such conditions in natural systems. Locally, this project will educate and train first-generation and Native Montana students in cutting-edge laboratory, field, and computational approaches that will improve their competitiveness in STEM-related careers. A new course at the University of Montana focused on host-microbe interactions will be further developed to include outreach activities aimed at exposing individuals in rural Montana to the unique biology of endosymbiosis. Organismal performance and fitness depends on interactions across levels of biological organization. Among all species interactions, those between animals and microbial endosymbionts that live inside their cells are perhaps the most intimate, influencing host behavior, physiology, life history, and fitness. Some endosymbionts may even contribute to reproductive isolation and speciation, highlighting their broad importance for host biology. The evolutionary outcomes of host-endosymbiont interactions ultimately depend on endosymbiont prevalence in host populations, which varies widely for unknown reasons. This project will leverage 50 million years of Wolbachia evolution distributed across divergent host species to determine the causes of Wolbachia frequency variation. The project will specifically dissect how genes in host and endosymbiont genomes interact with each other and with temperature (GxGxE interactions) to influence maternal Wolbachia transmission rates and the strength of Wolbachia-induced reproductive manipulations like cytoplasmic incompatibility. Mathematical models will then be used to evaluate how both genomic and environmental interactions contribute to Wolbachia prevalence in divergent host systems. At each step, this project includes activities that will leverage the unique biology of endosymbiosis to educate and train first-generation and Native students in Montana. 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.