The Role of Hybridization in Generating Biodiversity: Insights from Genomics of Madagascar's True Lemurs (Eulemur)

PROJECT SUMMARY: Overview Hybridization is common across the Tree of Life, but scientists have only recently started to appreciate the creative role that hybridization can play in generating new biological diversity. One particularly surprising finding in recent studies has been that the most rapid and prolific radiations often experience the highest amounts of hybridization. This begs a fundamental question in evolutionary biology: How do radiations proliferate in the face of hybridization and gene flow? To fully answer this question, we must investigate the role of hybridization at multiple levels: how it shapes the genome, how it shapes species limits, and how it shapes the evolutionary trajectory of an entire radiation. The goals of the proposed work are to understand how new species form in the face of gene flow and to expose the genomic signatures of these processes across a diversifying radiation. Our first objective will be to characterize patterns of gene flow, selection, and genome architecture in a case of homoploid hybrid speciation (Eulemur rufifrons x E. cinereiceps), and in doing so, develop a genomic perspective on how species boundaries evolve in systems featuring high levels of inter-lineage gene flow. We will then assess how hybridization and introgression have shaped the evolutionary history of all of Madagascar’s true lemurs and will ask whether the patterns of gene flow, selection, and genome architecture are repeatable and predictable across the clade. Finally, we will bring together data on geographic range, diet, and social behavior to construct a model aimed at understanding which extrinsic factors facilitate hybridization in true lemurs. As a whole, this study will yield insights into the origins of species in a hyperdiverse region of the world and will provide useful information to systematists contending with signatures of gene flow in phylogenetic and demographic analyses. Intellectual Merit The first deliverables from this research will be a genomic assessment of species boundaries in a putatively unique case of primate hybrid speciation, and a robust estimation of the species tree for young radiation of lemurs historically challenging to resolve. Using these as tools, and coupled with whole- genome sequence data, we will be able to address several important and emerging questions in systematics and evolution: What do patterns of gene flow, selection, and genomic structural change look like across the genome as species boundaries take form? What is the relationship between the strength of selection and the degree of hybrid introgression, taken from a genome-wide and clade-wide perspective? Further, how are signatures of gene flow spatially arrayed across chromosomes, and are these predictable/repeatable across different hybrid events? Finally, by leveraging the wealth of available data on geographic range, diet, and social behavior, we will be able to test for factors most likely associated with hybrid introgression. In sum, this project represents an exciting opportunity to address fundamental questions about the role of hybridization in generating biodiversity in a hyperdiverse region of the world. Broader Impacts The extensive field, lab, and bioinformatic work proposed here will afford opportunities to integrate Malagasy students, American students from underrepresented groups, and conservation practitioners. We plan to conduct a sequencing workshop for Malagasy graduate students. As our lab is located at the University of Kentucky (UK), our research will also integrate undergraduate researchers from diverse backgrounds in the U.S., including rural Appalachia through course-based research experiences and summer independent research funding. Finally, our research will support lemur conservation, with significant implications for E. cinereiceps, a Critically Endangered species on the verge of extinction. We will share all ecological and genetic assessments with three non-governmental organization with whom we have already established partnerships, and with Madagascar National Parks, to enable more efficient conservation planning. Overall, this research will have value to all stakeholders, leading to synergistic relationships with local actors while helping save Madagascar’s unparalleled biodiversity.