Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain

Adam R. Hamilton, Ian M. Traniello, Allyson M. Ray, Arminius S. Caldwell, Samuel A. Wickline, Gene E Robinson

Research output: Contribution to journalArticle

Abstract

Studies in evolutionary and developmental biology show that relationships between transcription factors (TFs) and their target genes can be altered to result in novel regulatory relationships that generate phenotypic plasticity. We hypothesized that context-dependent shifts in the nervous system associated with behavior may also be linked to changes in TF–target relationships over physiological time scales. We tested this hypothesis using honey bee (Apis mellifera) division of labor as a model system by performing bioinformatic analyses of previously published brain transcriptomic profiles together with new RNAi and behavioral experiments. The bioinformatic analyses identified five TFs that exhibited strong signatures of regulatory plasticity as a function of division of labor. RNAi targeting of one of these TFs (broad complex) and a related TF that did not exhibit plasticity (fushi tarazu transcription factor 1) was administered in conjunction with automated analyses of foraging behavior in the field, laboratory assays of aggression and brood care behavior, and endocrine treatments. The results showed that changes in the regulatory relationships of these TFs were associated with behavioral state, social context and endocrine state. These findings provide the first empirical evidence that TF–target relationships in the brain are altered in conjunction with behavior and social context. They also suggest that one mechanism for this plasticity involves pleiotropic TFs high up in regulatory hierarchies producing behavior-specific transcriptional responses by activating different downstream TFs to induce discrete context-dependent transcriptional cascades. These findings provide new insights into the dynamic nature of the transcriptional regulatory architecture underlying behavior in the brain.

Original languageEnglish (US)
Article numberjeb200196
JournalJournal of Experimental Biology
Volume222
Issue number14
DOIs
StatePublished - Jan 1 2019

Fingerprint

Honey
Bees
labor division
honey
bee
honey bees
plasticity
brain
Transcription Factors
transcription factors
Brain
bioinformatics
RNA Interference
Computational Biology
Fushi Tarazu Transcription Factors
developmental biology
evolutionary biology
phenotypic plasticity
nervous system
foraging behavior

Keywords

  • Behavioral endocrinology
  • Gene regulatory networks
  • Social behavior
  • Social insects
  • Transcriptomic plasticity

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Aquatic Science
  • Animal Science and Zoology
  • Molecular Biology
  • Insect Science

Cite this

Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain. / Hamilton, Adam R.; Traniello, Ian M.; Ray, Allyson M.; Caldwell, Arminius S.; Wickline, Samuel A.; Robinson, Gene E.

In: Journal of Experimental Biology, Vol. 222, No. 14, jeb200196, 01.01.2019.

Research output: Contribution to journalArticle

Hamilton, Adam R. ; Traniello, Ian M. ; Ray, Allyson M. ; Caldwell, Arminius S. ; Wickline, Samuel A. ; Robinson, Gene E. / Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain. In: Journal of Experimental Biology. 2019 ; Vol. 222, No. 14.
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