The tragedy of the common? A comparative population genomic study of two bumblebee species

Abstract

1. Within the theoretical framework of the small population paradigm, we investigated the population genomics and parasite load of two bumblebee species across the UK and Ireland. Bombus pratorum is widespread and common throughout its range while Bombus monticola is restricted to higher altitudes and shows a more fragmented distribution.2. Bombus monticola showed stronger population structuring, isolation-by-distance, and a deficit of heterozygotes in the most isolated population in the south of its range (Dartmoor). Heterozygosity and inbreeding coefficients (F IS ) were comparable between both species, but the proportion of polymorphic sites was much greater in B. pratorum. Notably, both species have suffered significant declines in Ne over the last 100 generations and estimates and declines for both species were of similar orders of magnitude. No pattern of increased parasite prevalence in populations of lower heterozygosity was observed. Instead, ecological and demographic factors (age, latitude, date, habitat suitability) were the main drivers of parasite prevalence.3. Distinct patterns of selection were observed in both species in regions involved in regulation of transcription and neurotransmission and in particular pathways targeted by neonicotinoid insecticides. 4. Our results highlight the pressing need for monitoring to include common as well as rare species. This should not focus solely on census population counts, but include estimates of Ne. We also highlight the need for further work to establish adaptive shifts in globally important pollinator communities.

Whole genome analyses reveal weak signatures of population structure and environmentally associated local adaptation in an important North American pollinator, the bumble beeBombus vosnesenskii

“…Gene flow appears extensive across the study area and may be a likely explanation for the relatively small amount of genomic variation associated with the environmental variables and homogenous evolutionary histories reflected in genomes from different regions. Although there were relatively few and sparsely distributed environmentally associated outlier SNPs, there were some notable patterns highlighting the potential importance of ion homeostasis and neuromuscular function that is consistent with other bumble bee studies (Heraghty et al, 2022; Huml et al, 2023; Sun et al, 2020). Overall, the results suggest that B. vosnesenskii may be an example of a species with minimal population structure impeding adaptation or with weak selection over gene networks that will require much more extensive sampling to resolve.…”

“…For instance, the gene LOC117231202 ( hemicentin-1 ) was identified as containing outlier SNPs in both species. This gene reflects the shared trend towards genes involved in neuromuscular function (Kania et al, 1993) in outlier sets for both species, which has also been observed in outlier analysis of other bumble bees (Huml et al, 2023). Although elevation and thermal variables were not as associated with outliers in B. vosnesenskii , given correlations among environmental variables discussed above, such processes could nonetheless reflect shared selection pressures on traits such as thermal adaptation and flight.…”

Whole genome analyses reveal weak signatures of population structure and environmentally associated local adaptation in an important North American pollinator, the bumble bee Bombus vosnesenskii

“…Gene flow appears extensive across the study area and may be a likely explanation for the relatively small amount of genomic variation associated with the environmental variables and homogenous evolutionary histories reflected in genomes from different regions. Although evidence for widespread selection was fairly weak and there were relatively few and sparsely distributed environmentally associated outlier SNPs, there were some notable patterns highlighting the potential importance of ion homeostasis and neuromuscular function that is consistent with other bumble bee studies (Heraghty et al, 2022; Huml et al, 2023; Sun et al, 2020). Overall, the results suggest that B. vosnesenskii may be an example of a species with minimal population structure impeding adaptation or with weak selection over gene networks that will require much more extensive sampling to resolve.…”

“…For instance, the gene LOC117231202 ( hemicentin‐1 ) was identified as containing outlier SNPs in both species. This gene reflects the shared trend towards genes involved in neuromuscular function (Kania et al, 1993) in outlier sets for both species, which has also been observed in outlier analysis of other bumble bees (Huml et al, 2023). Although elevation and thermal variables were not as associated with outliers in B. vosnesenskii , given correlations among environmental variables discussed above, such processes could nonetheless reflect shared selection pressures on traits such as thermal adaptation and flight.…”

“…For instance, the gene LOC117231202 (hemicentin-1) was identified as containing outlier SNPs in both species. This gene reflects the shared trend towards genes involved in neuromuscular function (Kania et al, 1993) in outlier sets for both species, which has also been observed in outlier analysis of other bumble bees (Huml et al, 2023). in Bombus (Heinrich, 1975).…”