Overwintering honey bee colonies: Effect of worker age and climate on the Hindgut Microbiota

Authors: MAES, P. - University Of Arizona; FLOYD, A.S. - University Of Arizona; Mott, Brendon; Anderson, Kirk

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/2/2021
Publication Date: 3/5/2021
Citation: Maes, P., Floyd, A., Mott, B.M., Anderson, K.E. 2021. Overwintering honey bee colonies: Effect of worker age and climate on the Hindgut Microbiota. Insects. 121(3):224. https://doi.org/10.3390/insects12030224.
DOI: https://doi.org/10.3390/insects12030224

Interpretive Summary: In honey bees, three longevity phenotypes can arise from a single genotype. This inherent variability in lifespan provides a unique opportunity to study age-associated microbial changes over time and how they affect the honey bee. Similar to other model organisms, the aging hindgut microbiota of short-lived (worker) honey bees becomes depleted of Firmicutes while the abundance of Proteobacteria increases. Long-lived reproductive phenotypes show the opposite pattern. However, the age-associated microbial changes of intermediate-lived (overwintering) honey bees is unknown. Understanding the host-microbe relationships across these three longevity phenotypes will produce a rich context for understanding age-related microbial changes in general. We sequenced the hindgut bacterial communities of 110 winter honey bees from three locations and two climates. A known age cohort was sampled congruently to act as a control for chronological age. We compared the microbial changes from known age bees to samples sourced from cold and warm winter climates. We found no discernable differences in the hindgut microbiota of aging worker bees based on chronological age or climate. Additionally, there were no major differences in community size across treatment groups considering both bacteria and fungus. These results contribute to the understanding of aging and microbiota across three honey bee longevity phenotypes. The guts of short-lived worker phenotypes are progressively dominated by three major Proteobacteria, long-lived reproductive phenotypes become enriched with probiotic species, while the long-lived worker phenotype maintains a remarkably static hindgut microbiome. Stability of the hindgut bacterial community over extended time periods provides a novel tool to investigate host-microbial interactions. The gut microbial changes documented here highlights the honey bee as a model for understanding the contribution of diet and gut microbes to the aging process.

Technical Abstract: Honey bee overwintering health is essential to meet the demands of spring pollination. Managed honey bee colonies are overwintered in a variety of climates, and increasing rates of winter colony loss have prompted investigations into overwintering management, including indoor climate controlled overwintering. Central to colony health, the worker hindgut gut microbiota has been largely ignored in this context. We sequenced the hindgut microbiota of overwintering workers from both a warm southern climate and controlled indoor cold climate. Congruently, we sampled a cohort of known chronological age to estimate worker longevity in southern climates, and assess age-associated changes in the core hindgut microbiota. We found that worker longevity over winter in southern climates was much lower than that recorded for northern climates. Workers showed decreased bacterial and fungal load with age, but the relative structure of the core hindgut microbiome remained stable. Compared to cold indoor wintering, collective microbiota changes in the southern outdoor climate suggest compromised host physiology. Fungal abundance increased by two orders of magnitude in southern climate hindguts and was positively correlated with non-core, likely opportunistic bacteria. Our results contribute to understanding overwintering honey bee biology and microbial ecology and provide insight into overwintering strategies.