Transcriptomic evidence connecting low aggression to disease risk in honey bees

Abstract Background: Many organisms display a generalized suite of behaviors that indicate infection or predict infection susceptibility. We apply this concept to honey bee aggression, a behavior that has been associated with positive health outcomes in previous studies. We sequenced the transcriptomes of the brain, fat body, and midgut of adult sibling worker bees who developed as pre-adults in relatively high versus low aggression colonies. Previous studies showed that this pre-adult experience impacted both aggressive behavior and resilience to pesticides. We performed enrichment analyses on differentially expressed genes to determine whether variation in aggression resembles the molecular response to infection. We further assessed whether the transcriptomic signature of aggression in the brain overlapped with that observed following acute predator threat, exposure to a high-aggression environment as an adult, or changes associated with adult behavioral maturation. Results: Across all three tissues assessed, genes that are differentially expressed as a function of aggression significantly overlap with genes whose expression is modulated by a variety of pathogens. In the fat body, and to a lesser degree the midgut, we find evidence of directional concordance consistent with the hypothesis that low aggression resembles a diseased or parasitized state. However, we find little evidence of acute infection in low aggression individuals. Furthermore, we find little evidence that the brain molecular signature of aggression in the current study is enriched for genes modulated by either ephemeral or stable social cues that induce aggression in adults. However, we do find evidence that genes associated with adult behavioral maturation are enriched in our brain samples, with no clear directional bias. Conclusions: Results support the hypothesis that low aggression resembles a molecular state associated with infection. This pattern is most robust in the peripheral fat body, an immune responsive tissue in the honey bee. Although these results are correlative, we find no evidence of acute infection in low aggression bees, suggesting the physiological state associated with low aggression may predispose bees to negative health outcomes. The similarity of molecular signatures associated with the seemingly disparate traits of aggression and disease suggests that these characteristics may, in fact, be intimately tied.