A brain-wide analysis maps structural evolution to distinct anatomical module
- Florida Atlantic University, United States
- University of Massachusetts Amherst, United States
- Texas A&M University, United States
- Lehigh University, United States
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.
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Data from: A brain-wide analysis maps structural evolution to distinct anatomical modulesDryad Digital Repository, doi:10.5061/dryad.w9ghx3frw.
Article and author information
Author details
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.
Reviewing Editor
- Marianne E Bronner, California Institute of Technology, United States
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.
Version history
- Preprint posted: March 18, 2022 (view preprint)
- Received: June 3, 2022
- Accepted: July 26, 2023
- Accepted Manuscript published: July 27, 2023 (version 1)
- 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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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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