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. alviin the gut, while precocious foraging resulted in poor G. apicolaestablishment, nutrient deficient gene expression, and increased
oxidative damage. Metabolism associated with oxidative stress and the
immune response is costly. While normal nurse development is a
prerequisite for longevity, the metabolic trajectory of precocious
foragers indicates early senescence. Our results suggest that the
physiological cost of early foraging is extreme, and highlight the
progression of colony dwindling, a common but poorly understood process.