The transcriptomic signature of low aggression in honey bees resembles a response to infection

Clare C. Rittschof, Benjamin E.R. Rubin, Joseph H. Palmer

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Background: Behavior reflects an organism's health status. 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 impacts 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 is similar to the neuromolecular response to acute predator threat, exposure to a high-aggression environment as an adult, or 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 and parasitic feeding. In the fat body, and to some degree the midgut, our data specifically support the hypothesis that low aggression resembles a diseased or parasitized state. However, we find little evidence of active infection in individuals from the low aggression group. We also find little evidence that the brain molecular signature of aggression is enriched for genes modulated by 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. Conclusions: Results support the hypothesis that low aggression resembles a molecular state of infection. This pattern is most robust in the peripheral fat body, an immune responsive tissue in the honey bee. We find no evidence of acute infection in bees from the low aggression group, suggesting the physiological state characterizing low aggression may instead predispose bees to negative health outcomes when they are exposed to additional stressors. 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.

Original languageEnglish
Article number1029
JournalBMC Genomics
Volume20
Issue number1
DOIs
StatePublished - Dec 30 2019

Bibliographical note

Funding Information:
This work was supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture Hatch Program under accession number 1012993, the Kentucky Science and Engineering Foundation (3489-RDE-019), and by the Foundation for Food and Agriculture Research Pollinator Health Fund (Grant ID: 549049). B.E.R.R. was funded by a postdoctoral fellowship grant (2018–67012-28085) from the USDA National Institute of Food and Agriculture. The funding bodies played no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Publisher Copyright:
© 2019 The Author(s).

Keywords

  • Colony collapse disorder
  • Development
  • Nutrition
  • Pollinator declines
  • Social behavior
  • Social immunity
  • Stress
  • Virus

ASJC Scopus subject areas

  • Biotechnology
  • Genetics

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