Selection despite low genetic diversity and high gene flow in a rapid island invasion of the bumblebee, Bombus terrestris.

Invasive species are predicted to adjust their morphological, physiological and life-history traits to adapt to their non-native environments. Although a loss of genetic variation during invasion may restrict local adaptation, introduced species often thrive in novel environments. Despite being founded by just a few individuals, Bombus terrestris (Hymenoptera: Apidae) has in less than 30 years successfully spread across the island of Tasmania (Australia), becoming abundant and competitive with native pollinators. We use RADseq to investigate what neutral and adaptive genetic processes associated with environmental and morphological variation allow B. terrestris to thrive as an invasive species in Tasmania. Given the widespread abundance of B. terrestris, we expected little genetic structure across Tasmania and weak signatures of environmental and morphological selection. We found high gene flow with low genetic diversity, although with significant isolation-by-distance and spatial variation in effective migration rates. Restricted migration was evident across the mid-central region of Tasmania, corresponding to higher elevations, pastural land, low wind speeds and low precipitation seasonality. Tajima's D indicated a recent population expansion extending from the south to the north of the island. Selection signatures were found for loci in relation to precipitation, wind speed and wing loading. Candidate loci were annotated to genes with functions related to cuticle water retention and insect flight muscle stability. Understanding how a genetically impoverished invasive bumblebee has rapidly adapted to a novel island environment provides further understanding about the evolutionary processes that determine successful insect invasions, and the potential for invasive hymenopteran pollinators to spread globally.

Morphological Variation in Bumblebees (Bombus terrestris) (Hymenoptera: Apidae) After Three Decades of an Island Invasion.

Introduced social insects can be highly invasive outside of their native range. Around the world, the introduction and establishment of the eusocial bumblebee Bombus terrestris (L. 1758) (Hymenoptera: Apidae) has negatively impacted native pollinators and ecosystems. Understanding how morphological variation is linked to environmental variation across invasive ranges can indicate how rapidly species may be diverging or adapting across novel ranges and may assist with predicting future establishment and spread. Here we investigate whether B. terrestris shows morphological variation related to environmental variation across the island of Tasmania (Australia) where it was introduced three decades ago. We collected 169 workers from 16 sites across Tasmania and related relative abundance and morphology to landscape-wide climate, land use, and vegetation structure. We found weak morphological divergence related to environmental conditions across Tasmania. Body size of B. terrestris was positively associated with the percentage of urban land cover, a relationship largely driven by a single site, possibly reflecting high resource availability in urban areas. Proboscis length showed a significant negative relationship with the percentage of pasture. Wing loading and local abundance were not related to the environmental conditions within sites. Our results reflect the highly adaptable nature of B. terrestris and its ability to thrive in different environments, which may have facilitated the bumblebee's successful invasion across Tasmania.

Genomic divergence and a lack of recent introgression between commercial and wild bumblebees (Bombus terrestris).

The global movement of bees for agricultural pollination services can affect local pollinator populations via hybridization. When commercial bumblebees are of the same species but of different geographic origin, intraspecific hybridization may result in beneficial integration of new genetic variation, or alternatively may disrupt locally adapted gene complexes. However, neither the existence nor the extent of genomic introgression and evolutionary divergence between wild and commercial bumblebees is fully understood. We obtained whole-genome sequencing data from wild and commercial Bombus terrestris collected from sites in Southern Sweden with and without long-term use of commercially imported B. terrestris. We search for evidence of introgression, dispersal and genome-wide differentiation in a comparative genomic analysis of wild and commercial bumblebees. Commercial B. terrestris were found in natural environments near sites where commercial bumblebees were used, as well as drifting wild B. terrestris in commercial bumblebee colonies. However, we found no evidence for widespread, recent genomic introgression of commercial B. terrestris into local wild conspecific populations. We found that wild B. terrestris had significantly higher nucleotide diversity (Nei's pi, π), while the number of segregating sites (Watterson's theta, θw) was higher in commercial B. terrestris. A highly divergent region on chromosome 11 was identified in commercial B. terrestris and found to be enriched with structural variants. The genes present in this region are involved in flight muscle contraction and structure and pathogen immune response, providing evidence for differing evolutionary processes operating in wild and commercial B. terrestris. We did not find evidence for recent introgression, suggesting that co-occurring commercial B. terrestris have not disrupted evolutionary processes in wild B. terrestris populations.