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
Share this article
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
  2. Download BibTeX
  3. Download .RIS

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.

Reviewing Editor

  1. 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

  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.

Metrics

  • 857
    views
  • 113
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.80777

Categories and tags

Further reading

    1. Evolutionary Biology

    CLOCK evolved in cnidaria to synchronize internal rhythms with diel environmental cues

    Raphael Aguillon, Mieka Rinsky ... Oren Levy
    Research Article

    The circadian clock enables anticipation of the day/night cycle in animals ranging from cnidarians to mammals. Circadian rhythms are generated through a transcription-translation feedback loop (TTFL or pacemaker) with CLOCK as a conserved positive factor in animals. However, CLOCK’s functional evolutionary origin and mechanism of action in basal animals are unknown. In the cnidarian Nematostella vectensis, pacemaker gene transcript levels, including NvClk (the Clock ortholog), appear arrhythmic under constant darkness, questioning the role of NvCLK. Utilizing CRISPR/Cas9, we generated a NvClk allele mutant (NvClkΔ), revealing circadian behavior loss under constant dark (DD) or light (LL), while maintaining a 24 hr rhythm under light-dark condition (LD). Transcriptomics analysis revealed distinct rhythmic genes in wild-type (WT) polypsunder LD compared to DD conditions. In LD, NvClkΔ/Δ polyps exhibited comparable numbers of rhythmic genes, but were reduced in DD. Furthermore, under LD, the NvClkΔ/Δ polyps showed alterations in temporal pacemaker gene expression, impacting their potential interactions. Additionally, differential expression of non-rhythmic genes associated with cell division and neuronal differentiation was observed. These findings revealed that a light-responsive pathway can partially compensate for circadian clock disruption, and that the Clock gene has evolved in cnidarians to synchronize rhythmic physiology and behavior with the diel rhythm of the earth’s biosphere.

    1. Computational and Systems Biology
    2. Evolutionary Biology

    CoCoNuTs are a diverse subclass of Type IV restriction systems predicted to target RNA

    Ryan T Bell, Harutyun Sahakyan ... Eugene V Koonin
    Research Article

    A comprehensive census of McrBC systems, among the most common forms of prokaryotic Type IV restriction systems, followed by phylogenetic analysis, reveals their enormous abundance in diverse prokaryotes and a plethora of genomic associations. We focus on a previously uncharacterized branch, which we denote coiled-coil nuclease tandems (CoCoNuTs) for their salient features: the presence of extensive coiled-coil structures and tandem nucleases. The CoCoNuTs alone show extraordinary variety, with three distinct types and multiple subtypes. All CoCoNuTs contain domains predicted to interact with translation system components, such as OB-folds resembling the SmpB protein that binds bacterial transfer-messenger RNA (tmRNA), YTH-like domains that might recognize methylated tmRNA, tRNA, or rRNA, and RNA-binding Hsp70 chaperone homologs, along with RNases, such as HEPN domains, all suggesting that the CoCoNuTs target RNA. Many CoCoNuTs might additionally target DNA, via McrC nuclease homologs. Additional restriction systems, such as Type I RM, BREX, and Druantia Type III, are frequently encoded in the same predicted superoperons. In many of these superoperons, CoCoNuTs are likely regulated by cyclic nucleotides, possibly, RNA fragments with cyclic termini, that bind associated CARF (CRISPR-Associated Rossmann Fold) domains. We hypothesize that the CoCoNuTs, together with the ancillary restriction factors, employ an echeloned defense strategy analogous to that of Type III CRISPR-Cas systems, in which an immune response eliminating virus DNA and/or RNA is launched first, but then, if it fails, an abortive infection response leading to PCD/dormancy via host RNA cleavage takes over.

    1. Evolutionary Biology
    2. Neuroscience

    Large-scale deorphanization of Nematostella vectensis neuropeptide G protein-coupled receptors supports the independent expansion of bilaterian and cnidarian peptidergic systems

    Daniel Thiel, Luis Alfonso Yañez Guerra ... Gáspár Jékely
    Research Article

    Neuropeptides are ancient signaling molecules in animals but only few peptide receptors are known outside bilaterians. Cnidarians possess a large number of G protein-coupled receptors (GPCRs) – the most common receptors of bilaterian neuropeptides – but most of these remain orphan with no known ligands. We searched for neuropeptides in the sea anemone Nematostella vectensis and created a library of 64 peptides derived from 33 precursors. In a large-scale pharmacological screen with these peptides and 161 N. vectensis GPCRs, we identified 31 receptors specifically activated by 1 to 3 of 14 peptides. Mapping GPCR and neuropeptide expression to single-cell sequencing data revealed how cnidarian tissues are extensively connected by multilayer peptidergic networks. Phylogenetic analysis identified no direct orthology to bilaterian peptidergic systems and supports the independent expansion of neuropeptide signaling in cnidarians from a few ancestral peptide-receptor pairs.