Spatially organized chemical defences shape microbial communities in honey bee colonies

The success of social insects relies on dense colony living, but these conditions also favour pathogen transmission. Colonies mitigate this risk through social immunity, a coordinated system of behavioural, chemical, and immunological defences. Here, we investigate how chemical defences contribute to colony-level immunity using the European honey bee (Apis mellifera) as a model system. Integrating microbiome profiling, antimicrobial assays, and chemical characterization across hive components, we show that antimicrobial activity exhibits clear distance decay across compartments, closely paralleling shifts in microbial communities. This spatial pattern is most pronounced for bacterial communities and hive-associated pathogenic taxa, indicating selective suppression of harmful microbes while permitting neutral or beneficial species. Chemical analyses identify mediators including H₂O₂ in honey, flavonoids in propolis and wax, and polar aliphatics in pollen as drivers of this structured immunity. Variation in antimicrobial activity and chemical composition correlates with environmental and colony-level factors, such as apiary location, hive health, and pest exposure, highlighting the ecological sensitivity of these defences. Collectively, these results demonstrate that chemical social immunity is a coordinated, spatially organized system that shapes microbial communities and supports colony function, offering a framework to link chemical defence, microbiome dynamics, and resilience of social insects under environmental and pathogen pressures.