The pre-adult social environment has lasting impacts on adult behavior and health in the honey bee Apis mellifera

Honey bees, with a single morphological worker caste, rely on behavioral flexibility during adulthood to manage diverse and socially coordinated colony tasks. One such task is nest defense: during an attack from a predator or foreign bee, guard bees release an alarm pheromone into the colony, causing a rapid aggressive response from nestmates. Over a longer timescale, adult bees also adjust their sensitivity to alarm cues depending on nestmate behaviors and colony experience of previous disturbance. Because colony aggression level is socially coordinated across long time scales, there may be inter-colony variation in the aggressive social cues experienced by larval and pupal bees. However, no study has evaluated whether pre-adult social experience has lasting effects on aggressive behavior; such an effect could have consequences for behavioral flexibility later in life. We fostered sibling eggs in relatively high or low aggression colonies until one day prior to adult emergence, and then transferred bees to a common laboratory environment until they were 8-day-old adults. Using a lab-based test that measures aggressive responses to a foreign bee, we found that adult bees reared in high aggression colonies showed higher aggression levels compared to sisters reared in low aggression colonies. This effect was consistent across 3 experimental trials, two study sites, and 18 unique genotypes and foster colony environments. Because high aggression has been positively correlated with foraging activity and survivorship in previous studies, we evaluated whether high aggression pre-adult environments also confer resilience to other health stressors. We found that bees with increased aggression as a function of their social environment had lower mortality following treatment with acetamiprid, a neonicotinoid pesticide. Moreover, high aggression was correlated with lower rates of infestation with Varroa destructor mites. These results suggest for the first time that adult behavioral phenotypes, and thus colony performance, may be affected and even constrained by pre-adult experiences. Furthermore, exposure to a high aggression social environment may confer resilience to health stressors later in life. Improving early-life experiences could be critical to fostering stress resilience in the threatened honey bee.