1. Evolutionary Biology
  2. Neuroscience

A brain-wide analysis maps structural evolution to distinct anatomical module

  1. Robert A Kozol  Is a corresponding author
  2. Andrew J Conith
  3. Anders Yuiska
  4. Alexia Cree-Newman
  5. Bernadeth Tolentino
  6. Kasey Banesh
  7. Alexandra Paz
  8. Evan Lloyd
  9. Johanna E Kowalko
  10. Alex C Keene
  11. Craig Albertson
  12. Erik R Duboue  Is a corresponding author
  1. Florida Atlantic University, United States
  2. University of Massachusetts Amherst, United States
  3. Texas A&M University, United States
  4. Lehigh University, United States
https://doi.org/10.7554/eLife.80777
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Cite this article
  1. Robert A Kozol
  2. Andrew J Conith
  3. Anders Yuiska
  4. Alexia Cree-Newman
  5. Bernadeth Tolentino
  6. Kasey Banesh
  7. Alexandra Paz
  8. Evan Lloyd
  9. Johanna E Kowalko
  10. Alex C Keene
  11. Craig Albertson
  12. Erik R Duboue
(2023)
A brain-wide analysis maps structural evolution to distinct anatomical module
eLife 12:e80777.
https://doi.org/10.7554/eLife.80777
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Abstract

The vertebrate brain is highly conserved topologically, but less is known about neuroanatomical variation between individual brain regions. Neuroanatomical variation at the regional level is hypothesized to provide functional expansion, building upon ancestral anatomy needed for basic functions. Classically, animal models used to study evolution have lacked tools for detailed anatomical analysis that are widely used in zebrafish and mice, presenting a barrier to studying brain evolution at fine scale. In this study, we sought to investigate the evolution of brain anatomy using a single species of fish consisting of divergent surface and cave morphs, that permits functional genetic testing of regional volume and shape across the entire brain. We generated a high-resolution brain atlas for the blind Mexican cavefish Astyanax mexicanus and coupled the atlas with automated computational tools to directly assess variability in brain region shape and volume across all populations. We measured the volume and shape of every grossly defined neuroanatomical region of the brain and assessed correlations between anatomical regions in surface fish, cavefish, and surface x cave F2 hybrids, whose phenotypes span the range of surface to cave. We find that dorsal regions of the brain are contracted, while ventral regions have expanded, with F2 hybrid data providing support for developmental constraint along the dorsal-ventral axis. Furthermore, these dorsal-ventral relationships in anatomical variation show similar patterns for both volume and shape, suggesting that the anatomical evolution captured by these two parameters, could be driven by similar developmental mechanisms. Together, these data demonstrate that Astyanax mexicanus is a powerful system for functionally determining basic principles of brain evolution and will permit testing how genes influence early patterning events to drive brain-wide anatomical evolution.

Data availability

All raw and analyzed data, custom code and adapted tools have been uploaded into a Dryad repository, doi:10.5061/dryad.w9ghx3frw. Custom code and adaptive tools are also included in the supplemental material.

The following data sets were generated

Article and author information

Author details

  1. Robert A Kozol

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    For correspondence
    rkozol@fau.edu
    Competing interests
    The authors declare that no competing interests exist.

  2. Andrew J Conith

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

  3. Anders Yuiska

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Alexia Cree-Newman

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Bernadeth Tolentino

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Kasey Banesh

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Alexandra Paz

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Evan Lloyd

    Department of Biology, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.

  9. Johanna E Kowalko

    Department of Biological Sciences, Lehigh University, Bethlehem, United States
    Competing interests
    The authors declare that no competing interests exist.

  10. Alex C Keene

    Department of Biology, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.

  11. Craig Albertson

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

  12. Erik R Duboue

    Jupiter Life Science Initiative, Florida Atlantic University, Jupiter, United States
    For correspondence
    eduboue@fau.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3303-5149

Funding

National Institutes of Health (R15MH118625)

  • Erik R Duboue

National Institutes of Health (R01GM127872)

  • Alex C Keene

National Institutes of Health (R35GM138345)

  • Johanna E Kowalko

National Institutes of Health (R15HD099022)

  • Johanna E Kowalko

National Institutes of Health (R21NS122166)

  • Johanna E Kowalko
  • Alex C Keene

National Science Foundation (1923372)

  • Johanna E Kowalko
  • Alex C Keene
  • Erik R Duboue

National Science Foundation (2202359)

  • Johanna E Kowalko

Human Frontier Science Program (RGP0062)

  • Alex C Keene

National Institutes of Health (DE026446)

  • Craig Albertson

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

Ethics

Animal experimentation: Mexican tetras were cared for in accordance with NIH guidelines and all experiments were approved by the Florida Atlantic University Institutional Care and Use Committee protocol #A1929.

Reviewing Editor

  1. Marianne E Bronner, California Institute of Technology, United States

Version history

  1. Preprint posted: March 18, 2022 (view preprint)
  2. Received: June 3, 2022
  3. Accepted: July 26, 2023
  4. Accepted Manuscript published: July 27, 2023 (version 1)
  5. Version of Record published: August 17, 2023 (version 2)

Copyright

© 2023, Kozol 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. Robert A Kozol
  2. Andrew J Conith
  3. Anders Yuiska
  4. Alexia Cree-Newman
  5. Bernadeth Tolentino
  6. Kasey Banesh
  7. Alexandra Paz
  8. Evan Lloyd
  9. Johanna E Kowalko
  10. Alex C Keene
  11. Craig Albertson
  12. Erik R Duboue
(2023)
A brain-wide analysis maps structural evolution to distinct anatomical module
eLife 12:e80777.
https://doi.org/10.7554/eLife.80777

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