IMAGINE: Collaborative Research: Epigenetic potential and range expansion in the house sparrow

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Some species have managed to colonize much of the planet, but others have narrow geographic ranges. Answering why some species can live so many places is interesting to basic biology, namely because it reveals the details of evolutionary processes. However, this form of research also has practical value, as it could help us understand how species come to be pests, causing economic damage and sometimes spreading disease. Our goal here is to ask if the secret to the success of one globally-distributed bird, the house sparrow, has to do with the way it uses its genome to combat parasites. No place on Earth is safe from infection, so when animals colonize new places, they must kill or control new parasites, or the invasion fails. Preliminary data show that house sparrows have an exceptional ability to adjust their immune systems via a process called DNA methylation. We liken this ability to knobs on a radio; more knobs mean more sophisticated control of sound quality. For house sparrows, more successful birds seem to have more knobs in their genomes, which we expect helps them adjust their immune gene expression and thus control especially new parasites well. With this grant, we’ll perform experiments to test directly if more genome control knobs mean better protection from infections, then we’ll compare genome knob number between native and introduced groups of sparrows, expecting more knobs in invading birds. We’ll also study sparrows in museum collections, asking how knob number has changed since introductions first happened in the 1850s.Our plan is to leverage the near-ubiquity of the house sparrow (Passer domesticus) to learn how the CpG (i.e., cytosines proximal to guanines in DNA sequences) content of gene regulatory regions influenced the distribution of this avian species. CpG content, something we term epigenetic potential (EP), might allow genotypes to mask and manifest phenotypic plasticity reversibly within generations, as some CpG sites alter gene expression when methylated. In support, preliminary data reveal that i) introduced sparrow populations have more CpG sites in two immune gene promoters than native populations, and ii) EP in promoters, but not exons, declined since introduction ~170 years ago in four independent populations. We expect that EP represents a form of adaptive potential, providing organisms with a propensity to cope with the novel conditions. In particular, we expect EP to be important to the regulation of Toll-like receptors, major microbial surveillance mechanisms that reside on and in leukocytes. In a series of experiments and descriptive field and museum studies, we will ask how are EP, DNA methylation, and TLR expression related within individual sparrows, whether EP for TLRs protective against gut microbial infections, if EP in TLRs influences gut microbial communities in ongoing range expansions, and finally whether EP for TLRs important to range expansions historically? The term, adaptive potential, connotes a latent ability of organisms to cope with or exploit novel conditions. The core concept of our proposal, EP, could be one measurable form of adaptive potential, applicable to many animal systems.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.