Gene flow and climate-associated genetic variation in a vagile habitat specialist

Previous work in landscape genetics suggests that geographic isolation is of greater importance to genetic divergence than variation in environmental conditions. This is intuitive when configurations of suitable habitat are a dominant factor limiting dispersal and gene flow, but has not been thoroughly examined for habitat specialists with strong dispersal capability. Here, we evaluate the effects of geographic and environmental isolation on genetic divergence for a vagile invertebrate with high habitat specificity and a discrete dispersal life stage: Dod's Old World swallowtail butterfly, Papilio machaon dodi. In Canada, P. m. dodi are generally restricted to eroding habitat along major river valleys where their larval host plant occurs. A series of causal and linear mixed effects models indicate that divergence of genome-wide single nucleotide polymorphisms is best explained by a combination of environmental isolation (variation in summer temperatures) and geographic isolation (Euclidean distance). Interestingly, least-cost path and circuit distances through a resistance surface parameterized as the inverse of habitat suitability were not supported. This suggests that, although habitat associations of many butterflies are specific due to reproductive requirements, habitat suitability and landscape permeability are not equivalent concepts due to considerable adult vagility. We infer that divergent selection related to variation in summer temperatures has produced two genetic clusters within P. m. dodi, differing in voltinism and diapause propensity. Within the next century, temperatures are predicted to rise by amounts greater than the present-day difference between regions of the genetic clusters, potentially affecting the persistence of the northern cluster under continued climate change.