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.

Bterrestris_genotypes_env_vars

Genotypes_all

The multilocus genotypes of all 376 successfully genotyped buff-tailed bumble bee individuals. Data is coded in GenAlEx input data scheme. See the GenAlEx v.6.5 user guide for more information.

Genotypes_Colony

The multilocus genotypes of the 368 buff-tailed bumble bee individuals provided to Colony for sibship and clone detection. Data is coded in GenAlEx scheme, but for haploid individuals the second allele of each locus has already been set to -99. As Colony cannot work with samples whose ploidy level is unclear, two individuals being heterozygous at one and two loci, respectively, are not featured in this data set. See the Colony v.2.0.6.5 user guide for more information on how input data is coded.

Colony_marker_info

The ‘Marker Types and Error rates’ file requested by Colony. The reader is referred to the Colony v.2.0.6.5 user guide.

Complete_data_set

The multilocus genotypes of the 347 buff-tailed bumble bee individuals after having excluded putative clones and full siblings using GenAlEx and Colony. This data set is referred to as ‘cpds’ in the publication. Data is coded in GenAlEx input data scheme.

Mixed_ploidy_data_set

The data set encompassing 338 haploid males/diploid females, and which is referred to as ‘mpds’ in the publication. The two individuals with unclear ploidy levels (see ‘Genotypes_Colony’) are not featured in this data set, nor are the populations ‘Coastra’ and ‘Billed’, which were excluded due to small samples sizes. Data is coded in GenAlEx input data scheme.

Diploid_data_set

The multilocus genotypes of the 304 putative diploid buff-tailed bumble bees, referred to as ‘dpds’ in the publication. Data is coded in GenAlEx input data scheme.

Structure_complete

The multilocus genotypes of the 345 haploid/diploid individuals that were provided to Structure. Data is coded mainly in GenAlEx input data scheme. Yet, the missing data value of Structure is already used. Additionally, as requested by Structure, for each haploid male, the second allele at each locus is coded as -9. This data set is largely congruent to ‘cpds’, with the exception of two missing individuals from the population ‘Valea Pӑdurii’.

Structure_pop10

The Structure_complete data set after excluding the populations ‘Billed’ and ‘Coastra’, which had fewer than 10 individuals.

Env_vars_poplocs

The values of environmental variables which were extracted at population locations, and that were used for generalized dissimilarity modelling (GDM) analyses.

Bterrestris_pop10_raw_results

Raw results from the Structure runs using the ‘Structure_pop10’ data set as input, with either STARTATPOPINFO set to zero or to one, respectively. To inspect the results in Structure most conveniently, go to ‘File’, ‘Open Project …’ and then select the desired ‘.spj’ file.