Systems Biology of the Bumblebee: Sociality, Adaptation, and the Holobiont in the Multi-Omics Era

The genus Bombus occupies an unusual position in modern organismal biology: it is ecologically indispensable and economically central yet historically treated as a non-model taxon. Over the past decade, this status has changed decisively. Two short-read draft genomes published in 2015 have been succeeded by a growing set of chromosome-scale assemblies, population-genomic resequencing panels, methylomes, transcriptomes, venom and hemolymph proteomes, lipidomes, and gut microbiome surveys. This review consists of a combination of literature published between 2010 and 2026 across seven molecular layers and argues that the field is now structured by three asymmetries rather than by a shortage of data. First, the primitively eusocial organization of bumblebees, which consists of annual colonies, reproductively totipotent workers, and a socially reversible reproductive hierarchy, offers experimental access to the molecular basis of sociality that the advanced eusocial honeybee cannot provide; yet much of the mechanistic narrative in the Bombus literature is still imported from Apis mellifera and ants without being flagged as extrapolation. Second, the phenotypic layers rest overwhelmingly on two commercially reared Holarctic species, Bombus terrestris and Bombus impatiens, whereas extinction risk is concentrated in lineages such as Thoracobombus that are almost absent from the omics record. Third, and most consequentially, the rate-limiting step has shifted from data generation to causal inference: no peer-reviewed germline CRISPR knockout and no continuous cell line exist for any Bombus species, and formal statistical fusion of three or more omics layers has not yet been published for the genus. We review each molecular layer in turn, evaluate the holobiont framework as the most productive organizing concept for multi-stressor biology, and close with four concrete benchmarks whose achievement would move bumblebee systems biology from a descriptive to a predictive science.