Comparative population genomics reveal stark differences in the genomic structure and drivers of isolation for two sky island bumble bees

Abstract Genetic diversity is critical for species’ persistence and for preserving biodiversity. Regions with extreme elevation gradients, including ‘sky island’ systems, are predicted to restrict gene flow owing to dispersal barriers between high-elevation habitat patches (isolation by resistance, IBR) and the sheer distances between patches (isolation by distance, IBD). However, the drivers of genomic structure for sky island species remain poorly characterized. We evaluated the effects of IBR and IBD on the genomic structure of two co-occurring bumblebees, Bombus centralis and Bombus huntii, in the Cordilleran and Madrean sky islands using single-nucleotide polymorphism data. These species share similar sizes and diet breadths, but B. centralis is strongly associated with high-elevation forest and grasslands, representing only a subset of habitats used by B. huntii. We found that both species are experiencing moderate to high levels of inbreeding, but that B. centralis populations are highly differentiated, while B. huntii shows little genomic structure. IBR owing to land cover and elevation was evident for both, with support for IBD found only in B. huntii. Our study highlights the risk of isolation in sky island systems and demonstrates how small differences in ecological niche space can lead to dramatically different genomic structure.