Honey bee neurogenomic responses to affiliative and agonistic social interactions

Hagai Y. Shpigler, Michael C. Saul, Emma E. Murdoch, Frida Corona, Amy C. Cash-Ahmed, Christopher H. Seward, Sriram Chandrasekaran, Lisa J Stubbs, Gene E Robinson

Research output: Contribution to journalArticle

Abstract

Social interactions can be divided into two categories, affiliative and agonistic. How neurogenomic responses reflect these opposing valences is a central question in the biological embedding of experience. To address this question, we exposed honey bees to a queen larva, which evokes nursing, an affiliative alloparenting interaction, and measured the transcriptomic response of the mushroom body brain region at different times after exposure. Hundreds of genes were differentially expressed at distinct time points, revealing a dynamic temporal patterning of the response. Comparing these results to our previously published research on agonistic aggressive interactions, we found both shared and unique transcriptomic responses to each interaction. The commonly responding gene set was enriched for nuclear receptor signaling, the set specific to nursing was enriched for olfaction and neuron differentiation, and the set enriched for aggression was enriched for cytoskeleton, metabolism, and chromosome organization. Whole brain histone profiling after the affiliative interaction revealed few changes in chromatin accessibility, suggesting that the transcriptomic changes derive from already accessible areas of the genome. Although only one stimulus of each type was studied, we suggest that elements of the observed transcriptomic responses reflect molecular encoding of stimulus valence, thus priming individuals for future encounters. This hypothesis is supported by behavioral analyses showing that bees responding to either the affiliative or agonistic stimulus exhibited a higher probability of repeating the same behavior but a lower probability of performing the opposite behavior. These findings add to our understanding of the biological embedding at the molecular level.

Original languageEnglish (US)
Article numbere12509
JournalGenes, Brain and Behavior
Volume18
Issue number1
DOIs
StatePublished - Jan 2019

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Honey
Bees
Interpersonal Relations
Nursing
Mushroom Bodies
Body Regions
Smell
Brain
Cytoplasmic and Nuclear Receptors
Cytoskeleton
Aggression
Histones
Genes
Chromatin
Larva
Chromosomes
Genome
Neurons
Research

Keywords

  • ChIP-seq
  • RNA-seq
  • affiliative behavior
  • alloparental care
  • biological embedding
  • epigenetics
  • honey bee
  • mushroom bodies
  • social behavior
  • transcriptional regulatory network
  • transcriptomic

ASJC Scopus subject areas

  • Genetics
  • Neurology
  • Behavioral Neuroscience

Cite this

Shpigler, H. Y., Saul, M. C., Murdoch, E. E., Corona, F., Cash-Ahmed, A. C., Seward, C. H., ... Robinson, G. E. (2019). Honey bee neurogenomic responses to affiliative and agonistic social interactions. Genes, Brain and Behavior, 18(1), [e12509]. https://doi.org/10.1111/gbb.12509

Honey bee neurogenomic responses to affiliative and agonistic social interactions. / Shpigler, Hagai Y.; Saul, Michael C.; Murdoch, Emma E.; Corona, Frida; Cash-Ahmed, Amy C.; Seward, Christopher H.; Chandrasekaran, Sriram; Stubbs, Lisa J; Robinson, Gene E.

In: Genes, Brain and Behavior, Vol. 18, No. 1, e12509, 01.2019.

Research output: Contribution to journalArticle

Shpigler, HY, Saul, MC, Murdoch, EE, Corona, F, Cash-Ahmed, AC, Seward, CH, Chandrasekaran, S, Stubbs, LJ & Robinson, GE 2019, 'Honey bee neurogenomic responses to affiliative and agonistic social interactions', Genes, Brain and Behavior, vol. 18, no. 1, e12509. https://doi.org/10.1111/gbb.12509
Shpigler HY, Saul MC, Murdoch EE, Corona F, Cash-Ahmed AC, Seward CH et al. Honey bee neurogenomic responses to affiliative and agonistic social interactions. Genes, Brain and Behavior. 2019 Jan;18(1). e12509. https://doi.org/10.1111/gbb.12509
Shpigler, Hagai Y. ; Saul, Michael C. ; Murdoch, Emma E. ; Corona, Frida ; Cash-Ahmed, Amy C. ; Seward, Christopher H. ; Chandrasekaran, Sriram ; Stubbs, Lisa J ; Robinson, Gene E. / Honey bee neurogenomic responses to affiliative and agonistic social interactions. In: Genes, Brain and Behavior. 2019 ; Vol. 18, No. 1.
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