Tempo and mode of gene expression evolution in the brain across primates

  1. Katherine Rickelton  Is a corresponding author
  2. Trisha M Zintel
  3. Jason Pizzollo
  4. Emily Miller
  5. John J Ely
  6. Mary Ann Raghanti
  7. William D Hopkins
  8. Patrick R Hof
  9. Chet C Sherwood
  10. Amy L Bauernfeind
  11. Courtney C Babbitt  Is a corresponding author
  1. University of Massachusetts Amherst, United States
  2. MAEBIOS, United States
  3. Kent State University, United States
  4. The University of Texas MD Anderson Cancer Center, United States
  5. Icahn School of Medicine at Mount Sinai, United States
  6. George Washington University, United States
  7. Washington University in St. Louis, United States

Abstract

Primate evolution has led to a remarkable diversity of behavioral specializations and pronounced brain size variation among species (Barton, 2012; DeCasien & Higham, 2019; Powell, Isler, & Barton, 2017). Gene expression provides a promising opportunity for studying the molecular basis of brain evolution, but it has been explored in very few primate species to date (e.g. Khaitovich et al., 2005; Khrameeva et al., 2020; Ma et al., 2022; Somel et al., 2009). To understand the landscape of gene expression evolution across the primate lineage, we generated and analyzed RNA-Seq data from four brain regions in an unprecedented eighteen species. Here we show a remarkable level of variation in gene expression among hominid species, including humans and chimpanzees, despite their relatively recent divergence time from other primates. We found that individual genes display a wide range of expression dynamics across evolutionary time reflective of the diverse selection pressures acting on genes within primate brain tissue. Using our samples that represents a 190-fold difference in primate brain size, we identified genes with variation in expression most correlated with brain size. Our study extensively broadens the phylogenetic context of what is known about the molecular evolution of the brain across primates and identifies novel candidate genes for study of genetic regulation of brain evolution.

Data availability

Sequencing data have been deposited in the Short Read Archive: BioProject PRJNA639850

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Katherine Rickelton

    Department of Biology, University of Massachusetts Amherst, Amherst, United States
    For correspondence
    krickelton@umass.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Trisha M Zintel

    Department of Biology, University of Massachusetts Amherst, Amherst, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jason Pizzollo

    Department of Biology, University of Massachusetts Amherst, Amherst, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Emily Miller

    Department of Biology, University of Massachusetts Amherst, Amherst, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. John J Ely

    Epidemiology Unit, MAEBIOS, Alamogordo, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mary Ann Raghanti

    Department of Anthropology, Kent State University, Kent, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. William D Hopkins

    Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center, Bastrop, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Patrick R Hof

    Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Chet C Sherwood

    Department of Anthropology, George Washington University, Washington DC, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Amy L Bauernfeind

    Department of Neuroscience, Washington University in St. Louis, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8518-3819
  11. Courtney C Babbitt

    Department of Biology, University of Massachusetts Amherst, Amherst, United States
    For correspondence
    cbabbitt@bio.umass.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8793-4364

Funding

National Science Foundation (BCS-1750377)

  • Courtney C Babbitt

National Institutes of Health (T32 GM135096)

  • Katherine Rickelton

James S. McDonnell Foundation (220020293)

  • Chet C Sherwood

National Institutes of Health (NS-092988)

  • Chet C Sherwood

National Science Foundation (SMA-1542848)

  • Chet C Sherwood

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2024, Rickelton et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Katherine Rickelton
  2. Trisha M Zintel
  3. Jason Pizzollo
  4. Emily Miller
  5. John J Ely
  6. Mary Ann Raghanti
  7. William D Hopkins
  8. Patrick R Hof
  9. Chet C Sherwood
  10. Amy L Bauernfeind
  11. Courtney C Babbitt
(2024)
Tempo and mode of gene expression evolution in the brain across primates
eLife 13:e70276.
https://doi.org/10.7554/eLife.70276

Share this article

https://doi.org/10.7554/eLife.70276

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