Abstract
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.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 579-591 |
| Number of pages | 13 |
| Journal | Genes, Brain and Behavior |
| Volume | 16 |
| Issue number | 6 |
| DOIs | |
| State | Published - Jul 1 2017 |
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Keywords
- Aggression
- ChIPseq
- RNAseq
- biological embedding
- cis-motif
- epigenetics
- honey bee
- mushroom bodies
- social challenge
- transcriptional regulatory network
- transcriptomics
ASJC Scopus subject areas
- Genetics
- Neurology
- Behavioral Neuroscience
Cite this
Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees. / Shpigler, H. Y.; Saul, M. C.; Murdoch, E. E.; Cash-Ahmed, A. C.; Seward, C. H.; Sloofman, L.; Chandrasekaran, S.; Sinha, S.; Stubbs, L. J.; Robinson, G. E.
In: Genes, Brain and Behavior, Vol. 16, No. 6, 01.07.2017, p. 579-591.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees
AU - Shpigler, H. Y.
AU - Saul, M. C.
AU - Murdoch, E. E.
AU - Cash-Ahmed, A. C.
AU - Seward, C. H.
AU - Sloofman, L.
AU - Chandrasekaran, S.
AU - Sinha, S.
AU - Stubbs, L. J.
AU - Robinson, G. E.
PY - 2017/7/1
Y1 - 2017/7/1
N2 - 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.
AB - 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.
KW - Aggression
KW - ChIPseq
KW - RNAseq
KW - biological embedding
KW - cis-motif
KW - epigenetics
KW - honey bee
KW - mushroom bodies
KW - social challenge
KW - transcriptional regulatory network
KW - transcriptomics
UR - http://www.scopus.com/inward/record.url?scp=85018633813&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85018633813&partnerID=8YFLogxK
U2 - 10.1111/gbb.12379
DO - 10.1111/gbb.12379
M3 - Article
VL - 16
SP - 579
EP - 591
JO - Genes, Brain and Behavior
JF - Genes, Brain and Behavior
SN - 1601-1848
IS - 6
ER -