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

Authors: Anderson, Kirk; MAES, P. - University Of Arizona

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/7/2022
Publication Date: 6/23/2022
Citation: Anderson, K.E., Maes, P. 2022. Social microbiota and social gland gene expression of worker honey bees by age and climate. Scientific Reports. 12. Article 10690. https://doi.org/10.1038/s41598-022-14442-0.
DOI: https://doi.org/10.1038/s41598-022-14442-0

Interpretive Summary: Overwintering is a major contributor to honey bee colony loss worldwide and is hypothesized to involve changes in colony physiology and behavior that render individuals more susceptible to disease. Here we DNA sequence the microbes associated with stored food, mouthparts and midguts of honey bees before and after winter from both warm and cold overwintering climates. We hypothesized that fluctuations in temperature and water availability may affect microbial character producing an environment conducive to the growth of opportunists. We detail the change in immune gene expression in the hypopharygeal gland overwinter, a secretory gland that interfaces with the extended social environment on many levels. We found major differences in the microbiome of stored pollen overwinter. The cold, controlled overwintering environment produced the healthiest result based on immune gene expression, and microbiome characteristics. Warm overwintering was associated changes in the midgut and mouthpart microbiota that suggest increased disease susceptibility, including significantly greater abundance of opportunistic bacteria in the worker midgut post-winter. Concurrently, the significant reduction in opportunistic bacteria on the mouthparts of the same bees showing significantly greater immune gene expression in their salivary glands, and increased opportunistic bacteria in their midguts suggests a hygienic response to hive opportunists overwinter. In general, we found many differences in microbiome structure between warm and cold overwintering environments. Our results may reflect selection pressures that shaped the social and hive microbiome with evolution to a perennial life history.

Technical Abstract: 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.