Abstract

Using brain transcriptomic profiles from 853 individual honey bees exhibiting 48 distinct behavioral phenotypes in naturalistic contexts, we report that behavior-specific neurogenomic states can be inferred from the coordinated action of transcription factors (TFs) and their predicted target genes. Unsupervised hierarchical clustering of these transcriptomic profiles showed three clusters that correspond to three ecologically important behavioral categories: aggression, maturation, and foraging. To explore the genetic influences potentially regulating these behavior-specific neurogenomic states, we reconstructed a brain transcriptional regulatory network (TRN) model. This brain TRN quantitatively predicts with high accuracy gene expression changes of more than 2,000 genes involved in behavior, even for behavioral phenotypes on which it was not trained, suggesting that there is a core set of TFs that regulates behavior-specific gene expression in the bee brain, and other TFs more specific to particular categories. TFs playing key roles in the TRN include well-known regulators of neural and behavioral plasticity, e.g., Creb, as well as TFs better known in other biological contexts, e.g., NF-κB (immunity). Our results reveal three insights concerning the relationship between genes and behavior. First, distinct behaviors are subserved by distinct neurogenomic states in the brain. Second, the neurogenomic states underlying different behaviors rely upon both shared and distinct transcriptional modules. Third, despite the complexity of the brain, simple linear relationships between TFs and their putative target genes are a surprisingly prominent feature of the networks underlying behavior.

Original languageEnglish (US)
Pages (from-to)18020-18025
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number44
DOIs
StatePublished - Nov 1 2011

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Transcription Factors
Gene Regulatory Networks
Brain
Bees
Genes
Phenotype
Gene Expression
Neuronal Plasticity
Honey
Aggression
Cluster Analysis
Immunity

Keywords

  • Apis mellifera
  • Gene regulation
  • Social behavior
  • Systems biology

ASJC Scopus subject areas

  • General

Cite this

Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. / Chandrasekaran, Sriram; Ament, Seth A.; Eddy, James A.; Rodriguez-Zas, Sandra L.; Schatz, Bruce R.; Price, Nathan D.; Robinson, Gene E.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 44, 01.11.2011, p. 18020-18025.

Research output: Contribution to journalArticle

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