Conserved, yet disruption-prone, gut microbiomes in neotropical bumblebees

Abstract

Bumblebees are important pollinators in natural ecosystems and agriculture, but many species are declining. Temperate-zone bumblebees have host-specific and beneficial gut microbiomes, which may have a role in mediating the effects of stressors. However, there is almost no published information on the gut microbiomes of tropical bumblebees. As temperate and tropical bumblebees encounter different floral resources and environmental conditions, their microbiomes could differ. Here, we characterized the gut microbiomes of four neotropical Bombus species and, for comparison, co-occurring solitary bees (genus Thygater ). We collected wild-foraging bees from multiple sites in central Colombia and used 16S rRNA gene sequencing to characterize their gut microbiomes. DNA barcoding and morphology were used to identify bumblebee species. We found that the microbiomes of neotropical bumblebees cluster with those of closely related temperate-zone species, in agreement with a model of bumblebee-symbiont codiversification. There was no evidence of geographic differences in microbiome composition between neotropical and temperate-zone bumblebees. These results suggest that the microbiome was conserved during bumblebee dispersal from North America, despite major shifts in ecology and life history. As previously observed in temperate-zone species, some neotropical bumblebees have highly disrupted microbiomes, in which conserved gut bacterial symbionts are replaced by environmental microbes. In these individuals, the gut microbial profile is more like that of solitary bees than of conspecifics. The gut parasites Nosema and Crithidia are also prevalent and associated with microbiome disruption. Our findings provide insights into the biogeography of bee microbiomes and a foundation for studying bee-microbe-stressor interactions in the neotropics. IMPORTANCE Social bees are an important model for the ecology and evolution of gut microbiomes. These bees harbor ancient, specific, and beneficial gut microbiomes and are crucial pollinators. However, most of the research has concentrated on managed honeybees and bumblebees in the temperate zone. Here we used 16S rRNA gene sequencing to characterize gut microbiomes in wild neotropical bumblebee communities from Colombia. We also analyzed drivers of microbiome structure across our data and previously published data from temperate bumblebees. Our results show that lineages of neotropical bumblebees not only retained their ancient gut bacterial symbionts during dispersal from North America but also are prone to major disruption, a shift that is strongly associated with parasite infection. Finally, we also found that microbiomes are much more strongly structured by host phylogeny than by geography, despite the very different environmental conditions and plant communities in the two regions.

Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

“…When moving colonies of B. terrestris outdoors, the microbiota can shift towards an increase in Enterobacteriaceae ( Parmentier et al., 2016 ). Such a shift in wild bumble bee microbiota is often considered as a ‘disrupted’ microbiome and associated with higher pathogen load ( Villabona et al., 2023 ). Overall, the influence of environmental microbes differs a lot between different studies, and it remains unclear what causes such community shifts.…”

Gut microbiome diversity and biogeography for Chinese bumblebee Bombus pyrosoma

“…The reasons underlying this predominance of pathogenic bacteria may be environmental pollution and the spread of disease caused by the dominant animal husbandry in this region, which highlights the urgent need to create a favorable habitat for bumblebees. The disruption of gut microbiota in some individuals from different sites may also be linked to bee colony age, as studies have shown that highest prevalence in B. atratus sampled later in the colony cycle ( 44 , 45 ).…”