Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees.
Understanding how social experiences are represented in the brain and shape future responses is a major challenge in the study of behavior. We addressed this problem by studying behavioral, transcriptomic and epigenetic responses to intrusion in honey bees. Previous research showed that initial exposure to an intruder provokes an immediate attack; we now show that this also leads to longer-term changes in behavior in the response to a second intruder, with increases in the probability of responding aggressively and the intensity of aggression lasting 2 and 1 h, respectively. Previous research also documented the whole-brain transcriptomic response; we now show that in the mushroom bodies (MBs) there are 2 waves of gene expression, the first highlighted by genes related to cytoskeleton remodeling, and the second highlighted by genes related to hormones, stress response and transcription factors (TFs). Overall, 16 of 37 (43%) of the TFs whose cis-motifs were enriched in the promoters of the differentially expressed genes (DEGs) were also predicted from transcriptional regulatory network analysis to regulate the MB transcriptional response, highlighting the strong role played by a relatively small subset of TFs in the MB's transcriptomic response to social challenge. Whole brain histone profiling showed few changes in chromatin accessibility in response to social challenge; most DEGs were 'ready' to be activated. These results show how biological embedding of a social challenge involves temporally dynamic changes in the neurogenomic state of a prominent region of the insect brain that are likely to influence future behavior.
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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0000-0003-1369-4112
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Shpigler
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Saul
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Murdoch
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Cash-Ahmed
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Seward
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Sloofman
Harvard Society of Fellows, Harvard University, Cambridge, MA, USA.|Faculty of Arts and Sciences, Harvard University, Cambridge, MA, USA.|Broad Institute of MIT and Harvard, Cambridge, MA, USA.|Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI, USA.
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Chandrasekaran
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Department of Computer Science, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Department of Entomology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Sinha
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Neuroscience Program, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Stubbs
Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Department of Entomology, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.|Neuroscience Program, University of Illinois at Urbana-Champaign (UIUC), Urbana, IL, USA.
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Robinson
D000818:Animals; D001516:Bees / Q000235:genetics* / Q000502:physiology; D001921:Brain / Q000378:metabolism; D002843:Chromatin / Q000235:genetics / Q000378:metabolism; D003599:Cytoskeleton / Q000378:metabolism; D044127:Epigenesis, Genetic; D053263:Gene Regulatory Networks; D017344:Genes, Insect; D006657:Histones / Q000235:genetics / Q000378:metabolism; D012919:Social Behavior; D059467:Transcriptome
D002843:Chromatin; D006657:Histones
 ChIPseq;  RNAseq;  cis-motif; Aggression; biological embedding; epigenetics; honey bee; mushroom bodies; social challenge; transcriptional regulatory network; transcriptomics