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Cited by 38

The DOI matches its Crossref record; 67 of the 67 references it cites were found in a registry or an index.

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·2019·Genes, Brain and Behavior
DOI 10.1111/gbb.12502PMC PMC6314924

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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.

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Metadata

Authors
Saul, M. C., Blatti, C., Yang, W., Bukhari, S. A., Shpigler, H. Y., Troy, J. M., Seward, C. H., Sloofman, L., Chandrasekaran, S., Bell, A. M., Stubbs, L., Robinson, G. E., Zhao, S. D., & Sinha, S.
Affiliations
  • Carl R. Woese Institute for Genomic Biology University of Illinois at Urbana‐Champaign Urbana Illinois
  • Biomedical Engineering University of Michigan Ann Arbor Michigan
ORCID
Shpigler, Hagai Y.
Venue
Genes, Brain and Behavior
Publisher
Wiley
Published
2018-07-16
Volume
18
Issue
1
ISSN
  • 1601-1848
  • 1601-183X
DOI
10.1111/gbb.12502
PMC
PMC6314924
Cited by
38
References
67
Language
en
Licence
Funders
  • Division of Mathematical Sciences (DMS‐1613005)
  • National Institute of General Medical Sciences (1U54GM114838)
  • Simons Foundation (SFLife 291812)

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