Distinct genome architecture underlies fine-scale population differentiation in two common European bumblebees (Bombus pascuorumandBombus lapidarius)

Abstract

Bumblebees are keystone pollinators which facilitate the reproduction of a wide range of wild and agricultural plants. Their abundance and diversity have been severely reduced by anthropogenic stressors such as land-use change and widespread habitat fragmentation. However, we lack a comprehensive understanding of bumblebee population structure and local adaptation in response to human-altered landscapes. We here discover surprisingly fine-scaled population structure (e.g. ~300km) within two widely occurring bumblebee species, Bombus lapidarius and Bombus pascuorum, by analysing whole genome data of 106 specimens from 7 sites in Northern Europe. Our sample range encompasses a mosaic of land-use types with varying levels of habitat fragmentation and natural oceanic barriers. While the observed population structure is largely associated with reduced gene flow across natural barriers, we also detect significant divergence between populations sampled from more fragmented, agricultural landscapes. Furthermore, we identify species-specific patterns of population structure which are underpinned by distinct genomic architecture. Whereas genetic divergence in B. lapidarius is spread relatively evenly across the genome, divergence in B. pascuorum is concentrated within several megabase-sized genomic regions with significantly elevated differentiation, including a putative chromosomal inversion, which may underlie well-known colour polymorphisms across its range. Our observations reveal unexpectedly high levels of inter- and intraspecific genomic diversity within the bumblebee genus, and highlight the necessity of increasing our understanding of bumblebee population structure and connectivity to design optimal bumblebee conservation strategies.