History, geography, and host use shape genome-wide patterns of genetic variation in the redheaded pine sawfly (Neodiprion lecontei)

Divergent host use has long been suspected to drive population differentiation and speciation in plant-feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as isolation-by-distance and population structure may also influence neutral variation. In this study, we use double-digest restriction-associated DNA (ddRAD) sequencing  to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiple Pinus hosts throughout its range in eastern North America. Due to this species’ broad range and strict specialization with host plants known to have changed range during the Pleistocene, we first assess overall genetic structure using model-based clustering and principle components analyses, and identify three distinct genetic clusters. Next, using a composite-likelihood approach based on the site frequency spectrum, we infer the population topology and date divergence to the late Pleistocene. Based on existing knowledge of Pinus refugia and patterns of diversity among Neodiprion populations, we infer locations of glacial refugia and post-glacial colonization routes. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters; and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, isolation-by-distance, and ecological divergence all contribute to neutral genetic variation in this species, and support the hypothesis that host use is a common driver of population divergence in host-specialized insects.