Social microbiota and social gland gene expression of worker honey bees by age and climate

Winter forage dearth is a major contributor to honey bee colony loss and can influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the social environment on many levels. During winter or forage dearth, colonies produce a long-lived (diutinus) worker phenotype that survives until environmental conditions improve. We used a known-age worker cohort to investigate microbiome integrity and social gene expression of workers in early and late winter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor environments. Our results provide novel evidence that social immune gene expression is associated with worker longevity, and highlight the midgut as a target of opportunistic disease during winter. Host microbial interactions suggest opportunistic disease progression and resistance in long-lived workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and non-core bacterial abundance. The results are consistent with increased social immunity, including host associations with the social microbiota, and a social immune response by long-lived workers to combat microbial opportunism. The cost/benefit ratio associated with limited expression of the diutinus phenotype may be a strong determinant of colony survival during winter forage dearth.