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

Abstract

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.