Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and solitary life-cycle phases, and some social parasite species, they are especially interesting models to understand social evolution, behavior, and ecology. Reports of many species in decline point to pathogen transmission, habitat loss, pesticide usage, and global climate change, as interconnected causes. These threats to bumblebee diversity make our reliance on a handful of well-studied species for agricultural pollination particularly precarious. To broadly sample bumblebee genomic and phenotypic diversity, we de novo sequenced and assembled the genomes of 17 species, representing all 15 subgenera, producing the first genus-wide quantification of genetic and genomic variation potentially underlying key ecological and behavioral traits. The species phylogeny resolves subgenera relationships while incomplete lineage sorting likely drives high levels of gene tree discordance. Five chromosome-level assemblies show a stable 18-chromosome karyotype, with major rearrangements creating 25 chromosomes in social parasites. Differential transposable element activity drives changes in genome sizes, with putative domestications of repetitive sequences influencing gene coding and regulatory potential. Dynamically evolving gene families and signatures of positive selection point to genus-wide variation in processes linked to foraging, diet and metabolism, immunity and detoxification, as well as adaptations for life at high altitudes. Our study reveals how bumblebee genes and genomes have evolved across the Bombus phylogeny and identifies variations potentially linked to key ecological and behavioral traits of these important pollinators.

Hosts and their parasites and pathogens are locked in antagonistic co-evolution. The genetic consequence of this can be seen in the rates of adaptive evolution in immunologically important loci in many taxa. As the risk of disease transmission increases we might also expect to see greater rates of adaptive evolution on genes of immune function. The evolution of sociality and its elaborations in insects represent enormous shift in disease transmission risk. Here, we examine whether sociality in the bees corresponds to changes in the rate of adaptive evolution in both classical canonical immune genes, and genes with putative immune functions identified from meta-analyses of honey-bee transcriptomic responses to infection. We find that measures of gene-wide adaptive evolution do not differ among canonical immune, non-canonical candidate immune, and background gene sets, but that branch-site adaptive evolution does increase with sociality regardless of gene category. Solitary species have greater rates of adaptive evolution in canonical immune genes than background genes, supporting the suggestion that social immune mechanisms may instead be the site of host-pathogen co-evolution in social species. We identify three genes with putative roles in immunity that warrant further attention (Vitellogenin Vg, disks large 1 tumour suppressor, and the uncharacterised protein LOC100577972). There are more gene family changes after the origin of sociality across all gene classes, with contractions occurring after the elaboration of sociality to complex eusociality. There are few genes or functions under adaptive selection that appear to be shared outside of specific lineages, suggesting that evolution of the immune system may be specific to individual species and their pathogen interactions.

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Microbiomes are increasingly recognised as critical for the health of an organism. In eusocial insect societies, frequent social interactions allow for high fidelity transmission of microbes across generations, leading to closer host-microbe coevolution. The microbial communities of bees with different social lifestyles are less well studied, and few comparisons have been made between taxa that vary in social structure. To address this gap, we leveraged a cloud-computing resource and publicly available transcriptomic data to conduct a survey of microbial diversity in bee samples from a variety of social lifestyles and taxa. We consistently recover the core microbes of well-studied corbiculates, supporting this method's ability to accurately characterise microbial communities. We find that the bacterial communities of bees are influenced by host location, phylogeny, and social lifestyle, although no clear effect was found for fungal or viral microbial communities. Bee genera with more complex societies tend to harbour more diverse microbes, with Wolbachia detected more commonly in solitary tribes. We present the first description of the microbiota of Euglossine bees and find that they do not share the "corbiculate" core microbiome. Notably, we find that bacteria with known anti-pathogenic properties are present across social bee genera, suggesting that symbioses that enhance host immunity are important with higher sociality. Our approach provides an inexpensive means of exploring microbiomes of a given taxa and identifying avenues for further research. These findings contribute to our understanding of the relationships between bees and their associated microbial communities, highlighting the importance of considering microbiome dynamics in investigations of bee health.