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

Abstract

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.

Signatures of Adaptation, Constraints, and Potential Redundancy in the Canonical Immune Genes of a Key Pollinator

“…Declines in pollinator populations, including bumblebees ( Fitzpatrick et al 2007 ; Kosior et al 2007 ; Cameron et al 2011 ), have led to concern about the sustainability of pollination services provided by insects which greatly contribute to global economies, food security, and ecosystem functioning ( Aizen et al 2009 ; Stout et al 2019 ). Our understanding of the capacity of wild bee populations to respond to ongoing environmental threats has been greatly informed by recent studies using population genomics, which have highlighted the genetic variation harbored in a population, as well as the targets of recent positive selection acting throughout the genome ( Harpur and Rehan 2021 ; Colgan et al 2022 ; Heraghty et al 2022 ; Kardum Hjort et al 2022 ), including immune genes ( Kent et al 2018 ). However, despite the importance of hymenopteran insects such as bees, wasps, and ants, focused population genetic studies on their immune genes are limited.…”

Limited introgression from non‐native commercial strains and signatures of adaptation in the key pollinator Bombus terrestris

“…The geographic location of Broadway in the central region of the United Kingdom means that at the time of sampling there were farms using both non‐native and native commercial colonies close to, or within foraging distance of the sampling location (Natural England), which could facilitate the different scenarios of introgression or escape. Indeed escapees from commercial colonies have been detected in other studies of B. terrestris in the Iberian peninsula and southern Sweden (Kardum Hjort et al, 2022; Seabra et al, 2019), and B. impatiens in New England, USA (Suni et al, 2017). The finding that individuals from the commercial native subspecies are genetically assigned in similar proportions to the wild individuals cluster and the commercial non‐native bees cluster (at K = 2) may be due to the use of B. terrestris queens from several different origins in commercial breeding programs (Velthuis & van Doorn, 2006), and/or interbreeding in breeding facilities.…”

“…Where introgression was detected was between the commercial subspecies and wild populations close to agricultural regions where greenhouses utilize commercial colonies. These wild populations include those in the regions of Bognor Regis, Broadway, Brockholes Sweden (Kardum Hjort et al, 2022;Seabra et al, 2019), and B. impatiens in New England, USA (Suni et al, 2017). The finding that individuals from the commercial native subspecies are genetically assigned in similar proportions to the wild individuals cluster and the commercial non-native bees cluster (at K = 2) may be due to the use of B. terrestris queens from several different origins in commercial breeding programs (Velthuis & van Doorn, 2006), and/or interbreeding in breeding facilities.…”

“…Furthermore, if invasion leads to the establishment of populations of commercially bred bumblebee subspecies, and/or hybridization between these bees and native subspecies occurs, a multitude of key biological traits in native populations may be affected, with impacts on their genetic diversity, ecological adaptation, as well as key plant–pollinator interactions. However, the effects of commercially bred subspecies on native pollinator genetic integrity and evolution have been the focus of few studies to date (Cejas et al, 2021; Kardum Hjort et al, 2022; Seabra et al, 2019).…”

“…However, it has been suggested that warmer temperatures due to climate change may enable winter activity, and facilitate the successful establishment of commercial B. t. dalmatinus colonies in the south of the UK (Owen et al, 2016). On the other hand, introgression was not detected between commercial B. t. dalmatinus and wild B. t. audax in the UK (Hart et al, 2021), or between commercial and wild B. impatiens in New England, USA (Suni et al, 2017), and no evidence was found for recent introgression of commercial B. terrestris into local wild conspecific populations in southern Sweden (Kardum Hjort et al, 2022). It may simply be the case that the behaviour is plastic, and that B. t. audax can express winter‐active behaviour under the right environmental conditions, such as can be seen with the facultative expression of social behaviour in Halictus sweat bees (Field et al, 2010).…”