Background The environment is a strong driver of genetic structure in many natural populations, yet often neglected in population genetic studies. This may be a particular problem in vagile species, where subtle structure cannot be explained by limitations to dispersal. Consequently, these species might falsely be considered quasi-panmictic and hence potentially mismanaged. A species this might apply to, is the buff-tailed bumble bee (Bombus terrestris), an economically important and widespread pollinator, which is considered to be quasi-panmictic at mainland continental scales. Here we aimed to (i) quantify genetic structure in 21+ populations of the buff-tailed bumble bee, sampled throughout two Eastern European countries, and (ii) analyse the degree to which structure is explained by environmental differences, habitat permeability and geographic distance. Using 12 microsatellite loci, we characterised populations of this species with Fst analyses, complemented by discriminant analysis of principal components and Bayesian clustering approaches. We then applied generalized dissimilarity modelling to simultaneously assess the informativeness of geographic distance, habitat permeability and environmental differences among populations in explaining divergence. Results Genetic structure of the buff-tailed bumble bee quantified by means of Fst was subtle and not detected by Bayesian clustering. Discriminant analysis of principal components suggested insignificant but still noticeable structure that slightly exceeded estimates obtained through Fst analyses. As expected, geographic distance and habitat permeability were not informative in explaining the spatial pattern of genetic divergence. Yet, environmental variables related to temperature, vegetation and topography were highly informative, explaining between 33 and 39% of the genetic variation observed. Conclusions In contrast to previous studies reporting quasi-panmixia in continental populations of this species, we demonstrated the presence of subtle population structure related to environmental heterogeneity. Environmental data proved to be highly useful in unravelling the drivers of genetic structure in this vagile and opportunistic species. We highlight the potential of including these data to obtain a better understanding of population structure and the processes driving it in species considered to be quasi-panmictic.

BackgroundThe environment is a strong driver of genetic structure in many natural populations, yet often neglected in population genetic studies. This may be a particular problem in vagile species, where subtle structure cannot be explained by limitations to dispersal. These species might falsely be considered panmictic and hence potentially mismanaged. Here we analysed the genetic structure in an economically important and widespread pollinator, the buff-tailed bumble bee (Bombus terrestris), which is considered to be quasi-panmictic at mainland continental scales. We first quantified population structure in Romania and Bulgaria with spatially implicit Fst and Bayesian clustering analyses. We then incorporated environmental information to infer the influence of the permeability of the habitat matrix between populations (resistance distances) as well as environmental differences among sites in explaining population divergence.ResultsGenetic structure of the buff-tailed bumble bee was subtle and not detected by Bayesian clustering. As expected, geographic distance and habitat permeability were not informative in explaining the spatial pattern of genetic divergence. Yet, environmental variables related to temperature, vegetation and topography were highly informative, explaining between 33 and 39% of the genetic variation observed.ConclusionsWhere in the past spatially implicit approaches had repeatedly failed, incorporating environmental data proved to be highly beneficial in detecting and unravelling the drivers of genetic structure in this vagile and opportunistic species. Indeed, structure followed a pattern of isolation by environment, where the establishment of dispersers is limited by environmental differences among populations, resulting in the disruption of genetic connectivity and the divergence of populations through genetic drift and divergent natural selection. With this work, we highlight the potential of incorporating environmental differences among population locations to complement the more traditional approach of isolation by geographic distance, in order to obtain a holistic understanding of the processes driving structure in natural populations.