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.
Highlights
By measuring the time course of gene expression in response to a territorial challenge in two brain regions, we show that a single brief territorial intrusion provoked waves of gene expression that persisted for hours afterwards, with waves of transcription associated with distinct biological processes
Changes in chromatin accessibility corresponded to changes in gene expression, and to the activity of transcription factors operating within gene regulatory networks
This study reveals rapid and dramatic epigenomic plasticity in response to a brief, highly consequential social interaction
Summary
Social interactions in particular can provoke moment-to-moment changes in behavior. These changes are coordinated at the neural level, but social interactions elicit transcriptional changes within the brains of behaving animals [1]. We know little about the temporal and spatial dynamics of neurogenomic plasticity in response to social interactions. It is likely that there are waves of transcription associated with perceiving social information, responding to social information, maintaining a behavioral response, recovering from the social interaction and modifying future behavior [14, 15]. Static experiments that measure gene expression at a single time point can only catch a glimpse of what is probably a very dynamic and coordinated process
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