Genetic structure across urban and agricultural landscapes reveals evidence of resource specialization and philopatry in the Eastern carpenter bee

摘要

Human activity continues to impact global ecosystems, often by altering the habitat suitability, persistence, and movement of native species. It is thus critical to examine the population genetic structure of key ecosystemservice providers across human‐altered landscapes to provide insight into the forces that limit wildlife persistence and movement across multiple spatial scales. While some studies have documented declines of bee pollinators as a result of human‐mediated habitat alteration, others suggest that some bee species may benefit from altered land use due to increased food or nesting resource availability; however, detailed population and dispersal studies have been lacking. We investigated the population genetic structure of the Eastern carpenter bee, Xylocopa virginica, across 14 sites spanning more than 450 km, including dense urban areas and intensive agricultural habitat. X. virginica is a large bee which constructs nests in natural and human‐associated wooden substrates, and is hypothesized to disperse broadly across urbanizing areas. Using 10 microsatellite loci, we detected significant genetic isolation by geographic distance and significant isolation by land use, where urban and cultivated landscapes were most conducive to gene flow. This is one of the first population genetic analyses to provide evidence of enhanced insect dispersal in human‐altered areas as compared to semi‐natural landscapes. We found moderate levels of regional‐scale population structure across the study system (GʹST = 0.146) and substantial co‐ancestry between the sampling regions, where co‐ancestry patterns align with major human transportation corridors, suggesting that human‐mediated movement may be influencing regional dispersal processes. Additionally, we found a signature of strong site‐level philopatry where our analyses revealed significant levels of high genetic relatedness at very fine scales (<1 km), surprising given X. virginica's large body size. These results provide unique genetic evidence that insects can simultaneously exhibit substantial regional dispersal as well as high local nesting fidelity in landscapes dominated by human activity.