Abstract
Early-life social experiences cause lasting changes in behavior and health for a variety of animals including humans, but it is not well understood how social information ‘‘gets under the skin’’ resulting in these effects. Adult honey bees (Apis mellifera) exhibit socially coordinated collective nest defense, providing a model for social modulation of aggressive behavior. Here we report for the first time that a honey bee’s early-life social environment has lasting effects on individual aggression: bees that experienced high-aggression environments during pre-adult stages showed increased aggression when they reached adulthood relative to siblings that experienced low-aggression environments, even though all bees were kept in a common environment during adulthood. Unlike other animals including humans however, high-aggression honey bees were more, rather than less, resilient to immune challenge, assessed as neonicotinoid pesticide susceptibility. Moreover, aggression was negatively correlated with ectoparasitic mite presence. In honey bees, early-life social experience has broad effects, but increased aggression is decoupled from negative health outcomes. Because honey bees and humans share aspects of their physiological response to aggressive social encounters, our findings represent a step towards identifying ways to improve individual resiliency. Pre-adult social experience may be crucial to the health of the ecologically threatened honey bee.
Highlights
Adult honey bees exhibit collective nest defense against mammalian predators and conspecific robber bees from other colonies
The rapid defensive response is socially coordinated by pheromone cues, but aggression is socially modulated over longer time scales allowing colonies to adjust their behavior in response to local ecological conditions[9,10,11]
We evaluated titers of deformed wing virus (DWV), which is the most common virus transmitted by Varroa mites and an indicator of significant mite feeding[25]
Summary
We manipulated honey bee early-life social experience by fostering juvenile individuals in either high or low aggression colonies. We found that colony level variation in aggression is larger than individual variation (Fig. 1A vs B), which could reflect differences in behavioral assays, or indicate that social influences during adulthood ameliorate or accentuate early-life effects. Our results could reflect the opposite relationship, i.e., that mite feeding on bees during development negatively influences aggression, and this effect manifests at both the colony and cross-fostered individual levels. The molecular mechanisms underlying the broad behavioral and physiological effects of worker pre-adult environment are unknown; here we speculate about two possible candidate systems that have previously been implicated in both pesticide response and aggression in honey bees. High-aggression social environments may prime individuals to better withstand an immune challenge like pesticide treatment, e.g., by upregulating NF-kappa B or P450 activity in adult animals, similar to what occurs in humans in response to social stress. Elucidating the shared and unique mechanisms underlying the response to social aggression in animals should improve our understanding of resilience to adversity
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