Gut and Colony Microbiota of Honey Bees: Social Immunity and Opportunism Overwinter

Overwintering is a major contributor to honey bee colony loss and involves factors that influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the extended social environment on many levels. With the coming of winter, 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 diutinus workers overwinter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor overwintering environments. Our results provide the first evidence that social immune gene expression is associated with diutinus bees, and highlight the midgut as a target of opportunistic disease overwinter. Host microbial interactions suggest opportunistic disease progression and resistance in diutinus workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and bacterial diversity abundance. The results are consistent with increased social immunity overwinter, including host associations with the colony microbiota, and a social immune response by long-lived diutinus 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 overwinter.