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PLoS Genet. 2017 Jul 13;13(7):e1006840. doi: 10.1371/journal.pgen.1006840. eCollection 2017 Jul.

Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks.

Author information

1
Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana Champaign, Urbana, IL, United States of America.
2
Illinois Informatics Institute, University of Illinois, Urbana Champaign, Urbana, IL, United States of America.
3
Program in Ecology, Evolution and Conservation Biology, University of Illinois, Urbana Champaign, Urbana, IL, United States of America.
4
Neuroscience Program, University of Illinois, Urbana Champaign, Urbana, IL, United States of America.
5
Department of Statistics, University of Illinois, Urbana Champaign, Urbana, IL United States of America.
6
Harvard Society of Fellows, Harvard University, Cambridge, MA, United States of America.
7
Faculty of Arts and Sciences, Harvard University, Cambridge, MA, United States of America.
8
Broad Institute of MIT and Harvard, Cambridge, MA, United States of America.
9
Department of Cell and Developmental Biology, University of Illinois, Urbana Champaign, Urbana, IL, United States of America.

Abstract

Animals exhibit dramatic immediate behavioral plasticity in response to social interactions, and brief social interactions can shape the future social landscape. However, the molecular mechanisms contributing to behavioral plasticity are unclear. Here, we show that the genome dynamically responds to social interactions with multiple waves of transcription associated with distinct molecular functions in the brain of male threespined sticklebacks, a species famous for its behavioral repertoire and evolution. Some biological functions (e.g., hormone activity) peaked soon after a brief territorial challenge and then declined, while others (e.g., immune response) peaked hours afterwards. We identify transcription factors that are predicted to coordinate waves of transcription associated with different components of behavioral plasticity. Next, using H3K27Ac as a marker of chromatin accessibility, we show that a brief territorial intrusion was sufficient to cause rapid and dramatic changes in the epigenome. Finally, we integrate the time course brain gene expression data with a transcriptional regulatory network, and link gene expression to changes in chromatin accessibility. This study reveals rapid and dramatic epigenomic plasticity in response to a brief, highly consequential social interaction.

PMID:
28704398
PMCID:
PMC5509087
DOI:
10.1371/journal.pgen.1006840
[Indexed for MEDLINE]
Free PMC Article

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