Bumblebee biodiversity. Distinct genome architecture underlies significant, fine-scale population differentiation in two common European bumblebee species (Bombus pascuorum and Bombus lapidarius)

Bumblebees are keystone pollinators which facilitate the reproduction of a wide range of wild and agricultural plants. Bumblebee abundance and diversity are severely reduced by anthropogenic threats such as land-use change and widespread habitat fragmentation, and despite their vulnerability to these threats, we lack a comprehensive understanding of bumblebee population structure and local adaptation in response to human-altered landscapes. Here, we analyse whole genome data of 106 specimens from 7 sites in Northern Europe, and discover surprisingly fine-scaled population structure (e.g. <400km) within two widely occurring bumblebee species, Bombus lapidarius and Bombus pascuorum. Our sites cover a mosaic of land-use types, with varying levels of habitat fragmentation and with varying natural oceanic barriers among them. The observed population structure is largely associated with reduced gene flow across natural barriers, and we detect increased divergence between populations sampled from more fragmented landscapes. Furthermore, we also identify contrasting patterns in population structure between the two species underpinned by distinct, species-specific genomic architecture. Whereas genetic divergence in B. lapidarius is spread relatively evenly across the genome, divergence in B. pascuorum is concentrated in several large genomic regions with significantly elevated differentiation - including a putative chromosomal inversion - which may underlie well-known colour polymorphisms across its range. Our observations reveal unexpected inter- and intraspecific diversity within the bumblebee genus, highlighting the urgent need to increase our understanding of bumblebee population structure and connectivity to design optimal conservation strategies.