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

Abstract

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 dispersal limitation and population structure may also influence patterns of genetic 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. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model-based and model-free clustering methods and identify three geographically distinct genetic clusters. Next, using a composite-likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linked RAD markers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge of Pinus refugia, estimated demographic parameters and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario for N. lecontei. 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, dispersal limitation and ecological divergence all contribute to genomewide differentiation in this species and support the hypothesis that host use is a common driver of population divergence in host-specialized insects.

Repurposing population genetics data to discern genomic architecture: A case study of linkage cohort detection in mountain pine beetle (Dendroctonus ponderosae)

“…A typical study of population structure with SNP data entails the use of three widely applied filtering procedures: (a) minor allele frequency (MAF) cutoffs to reduce the impact of rare alleles or genotyping errors in a population‐level analysis (Bagley, Sousa, Niemiller, & Linnen, ; Malenfant, Coltman, & Davis, ); (b) conformance to Hardy–Weinberg equilibrium (HWE) proportions to detect potential genotyping errors and support the assumption of neutrality in most markers (Hosking et al, ); and (c) linkage disequilibrium (LD) filtering to ensure independence of loci and remove repetitive genetic signal (Baird, ; Barton, ; Lu et al, ; Schilling et al, ). These methods are not consistently applied, however, and filtering is evaluated on a case‐by‐case basis depending on research needs and study species (Arnold, Corbet‐Detig, Hartl, & Bomblies, ; Narum, Buerkle, Davey, Miller, & Hohenlohe, ).…”

Gregariousness does not vary with geography, developmental stage, or group relatedness in feeding redheaded pine sawfly larvae

“…Sawfly larvae used in our experiments were either wild-caught or derived from colonies that we reared for no more than two generations in the laboratory using our standard laboratory protocols (described in more detail in Bagley et al, 2017;Harper, Bagley, Thompson, & Linnen, 2016). Briefly, we transported wild-caught larval colonies to the laboratory in brown paper bags.…”

Evaluating species interactions as a driver of phytophagous insect divergence

“…Alternatively, mutualism could also lead to highly specialized interactions and thereby promote diversification in insects and plants [83,45,46]. Early divergences between species or populations of insects that feed on plants are often associated with exploitation of new host plants, either in sympatry [18,6] or allopatry [53,4,26]. While host races following a switch to a new plant seem to be common, insect co-divergence with a plant species is also an important mechanism generating insect diversity.…”