The Honey Bee Superorganism: Social Insect Life History and the Microbiome

Abstract

Honey bee colonies are a complex society of individuals functioning to serve the collective group, colloquially known as a ‘superorganism.’ Their life history is intimately linked with their ability to separate reproduction, resource provisioning, defense, and offspring across thousands of individuals. Similarly, their gut microbiota also greatly influences their physiology and health. Here we explore the honey bee gut microbiota at pivotal moments during the honey bee life history. First we explore gut microbial succession and gene expression in freshly mated queens placed in colonies (high metabolic demand) or queen banks (low metabolic demand). We found differences in gut microbiota abundance between the two environments; colony queens were less diverse, while queen bank queens had microbiota similar to older queens who produce less eggs. We also found gene expression was similar between the two environments, suggesting post-mating had a stronger effect on gut gene expression. Our findings suggest that the queen gut microbiota experiences an extended period of microbial succession associated with post-mating development and colony assimilation. Next, we looked at the gut microbiota’s role in precocious forager midguts and ileums by determining if aging of the microbiota precedes or succeeds physiological aging. We found that social structure greatly influenced the absolute and relative abundance of midgut and ileum microbiota. We also performed immune and oxidative stress gene expression and found genes were explained by an interaction of both age and behavioral task. Our findings suggest that the physiological cost of early foraging is early senescence to the individual which can progress to population dwindling at the colony level. Finally, we conducted the first metaanalysis of the honey bee gut microbiota. We resolve the core microbiota and rare biosphere from over 3000 16S rRNA gene sequence libraries. We also highlight strain diversity and niche partitioning of the core microbiota. Collectively, we present the honey bee microbiota as a functional component of honey bee health from the novel perspectives of nascent queens, precocious foragers, and through a macro lens meta-analysis.