Antibiotic exposure retracts the behavioral caste transition of honeybees from nurse to foragers

The behavioral transition from nurse bees to foragers of worker bees is under sophisticated regulations and is essential for the survival and reproduction of populations. An increasing number of evidence showed that honeybee workers taking the two behavioral tasks varied in gut microbiota. Gut microbiota plays essential roles in the modulation of host behavior, as do honeybees. However, the impacts of gut microbiota variance on the transition of behavioral castes of honeybees remain obscure. Here, by constructing single cohort colonies, we validated that the gut microbiota varied in composition but not in size and richness between the two behaviors of age-matched bees. Then, a low dose of antibiotic treatment was leveraged to perturb the gut microbiota, and the behavior development was monitored in the field. Results showed that despite a low amount of antibiotic treatment, the gut bacterial community continuously diverged from the control group, even after the cessation of antibiotic treatment, suggesting a displacement of gut homeostasis. The transition to forager was retracted in the antibiotic treatment group. Decreased gut metabolic gene repertoires, reduced tyramine and dopamine titers in the brain, and the down-regulated brain immune genes contributed to the behavioral interference. This work highlights the importance of investigating the impact of gut microbiota on honeybee behavior regulation, marking the need to focus on antibiotic pollution threatening honeybee population health.