Abstract

Honey bees exhibit an elaborate social structure that corresponds with worker aging and division of labor. Young workers perform tasks inside the hive, while older workers forage outside the hive. Critical to colony fitness, the work force can respond rapidly to changes in the environment or colony demography and assume emergency tasks, resulting in young foragers or old nurses. We hypothesized that social structure affects the microbiome, more specifically, that behavioral task independent of age would generate differences in gut microbiota and host physiology. We used high throughput sequencing to track gut microbial succession, and measured gene expression and oxidative protein damage associated with behavioral task and age. We found that both age and behavioral task could explain differences in midgut and ileum microbiota, but host gene expression was best explained by an interaction of task and age. An extended nursing role in early life stabilized the ratio abundance of G. apicola and S. alvi in the ileum, while precocious foraging resulted in poor G. apicola establishment, nutrient deficient gene expression, and increased oxidative damage. Our results suggest that the physiological cost of early foraging is extreme, and highlight the progression of colony dwindling, a common but misunderstood process.