Cross-species systems analysis of evolutionary toolkits of neurogenomic response to social challenge

Michael C. Saul, Charles Blatti, Wei Yang, Syed A. Bukhari, Hagai Y. Shpigler, Joseph M. Troy, Christopher H. Seward, Laura Sloofman, Sriram Chandrasekaran, Alison M. Bell, Lisa Stubbs, Gene E. Robinson, Sihai D. Zhao, Saurabh Sinha

Research output: Contribution to journalArticle

Abstract

Social challenges like territorial intrusions evoke behavioral responses in widely diverging species. Recent work has showed that evolutionary “toolkits”—genes and modules with lineage‐specific variations but deep conservation of function—participate in the behavioral response to social challenge. Here, we develop a multispecies computational‐experimental approach to characterize such a toolkit at a systems level. Brain transcriptomic responses to social challenge was probed via RNA‐seq profiling in three diverged species—honey bees, mice and three‐spined stickleback fish—following a common methodology, allowing fair comparisons across species. Data were collected from multiple brain regions and multiple time points after social challenge exposure, achieving anatomical and temporal resolution substantially greater than previous work. We developed statistically rigorous analyses equipped to find homologous functional groups among these species at the levels of individual genes, functional and coexpressed gene modules, and transcription factor subnetworks. We identified six orthogroups involved in response to social challenge, including groups represented by mouse genes Npas4 and Nr4a1, as well as common modulation of systems such as transcriptional regulators, ion channels, G‐protein‐coupled receptors and synaptic proteins. We also identified conserved coexpression modules enriched for mitochondrial fatty acid metabolism and heat shock that constitute the shared neurogenomic response. Our analysis suggests a toolkit wherein nuclear receptors, interacting with chaperones, induce transcriptional changes in mitochondrial activity, neural cytoarchitecture and synaptic transmission after social challenge. It shows systems‐level mechanisms that have been repeatedly co‐opted during evolution of analogous behaviors, thus advancing the genetic toolkit concept beyond individual genes.
Original languageEnglish (US)
Pages (from-to)e12502
JournalGenes, Brain and Behavior
Early online dateJul 2 2018
DOIs
StatePublished - Jan 2019

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Systems Analysis
Synaptic Transmission
Genetic Phenomena
Genes
Smegmamorpha
Neurotransmitter Receptor
Gene Regulatory Networks
Bees
Brain
Cytoplasmic and Nuclear Receptors
Ion Channels
Shock
Transcription Factors
Fatty Acids
Hot Temperature
Proteins

Keywords

  • animal behavior
  • coexpression
  • comparative genomics
  • honey bee
  • mouse
  • social behavior
  • social challenge
  • systems biology
  • three-spined stickleback

Cite this

Cross-species systems analysis of evolutionary toolkits of neurogenomic response to social challenge. / Saul, Michael C.; Blatti, Charles; Yang, Wei; Bukhari, Syed A.; Shpigler, Hagai Y.; Troy, Joseph M.; Seward, Christopher H.; Sloofman, Laura; Chandrasekaran, Sriram; Bell, Alison M.; Stubbs, Lisa; Robinson, Gene E.; Zhao, Sihai D.; Sinha, Saurabh.

In: Genes, Brain and Behavior, 01.2019, p. e12502.

Research output: Contribution to journalArticle

Saul, Michael C. ; Blatti, Charles ; Yang, Wei ; Bukhari, Syed A. ; Shpigler, Hagai Y. ; Troy, Joseph M. ; Seward, Christopher H. ; Sloofman, Laura ; Chandrasekaran, Sriram ; Bell, Alison M. ; Stubbs, Lisa ; Robinson, Gene E. ; Zhao, Sihai D. ; Sinha, Saurabh. / Cross-species systems analysis of evolutionary toolkits of neurogenomic response to social challenge. In: Genes, Brain and Behavior. 2019 ; pp. e12502.
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AU - Shpigler, Hagai Y.

AU - Troy, Joseph M.

AU - Seward, Christopher H.

AU - Sloofman, Laura

AU - Chandrasekaran, Sriram

AU - Bell, Alison M.

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AU - Robinson, Gene E.

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AU - Sinha, Saurabh

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AB - Social challenges like territorial intrusions evoke behavioral responses in widely diverging species. Recent work has showed that evolutionary “toolkits”—genes and modules with lineage‐specific variations but deep conservation of function—participate in the behavioral response to social challenge. Here, we develop a multispecies computational‐experimental approach to characterize such a toolkit at a systems level. Brain transcriptomic responses to social challenge was probed via RNA‐seq profiling in three diverged species—honey bees, mice and three‐spined stickleback fish—following a common methodology, allowing fair comparisons across species. Data were collected from multiple brain regions and multiple time points after social challenge exposure, achieving anatomical and temporal resolution substantially greater than previous work. We developed statistically rigorous analyses equipped to find homologous functional groups among these species at the levels of individual genes, functional and coexpressed gene modules, and transcription factor subnetworks. We identified six orthogroups involved in response to social challenge, including groups represented by mouse genes Npas4 and Nr4a1, as well as common modulation of systems such as transcriptional regulators, ion channels, G‐protein‐coupled receptors and synaptic proteins. We also identified conserved coexpression modules enriched for mitochondrial fatty acid metabolism and heat shock that constitute the shared neurogenomic response. Our analysis suggests a toolkit wherein nuclear receptors, interacting with chaperones, induce transcriptional changes in mitochondrial activity, neural cytoarchitecture and synaptic transmission after social challenge. It shows systems‐level mechanisms that have been repeatedly co‐opted during evolution of analogous behaviors, thus advancing the genetic toolkit concept beyond individual genes.

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KW - coexpression

KW - comparative genomics

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