1. Developmental Biology
  2. Evolutionary Biology

Maternally-regulated gastrulation as a source of variation contributing to cavefish forebrain evolution

  1. Jorge Torres-Paz  Is a corresponding author
  2. Julien Leclercq
  3. Sylvie Rétaux  Is a corresponding author
  1. CNRS, Université Paris Sud, Université Paris-Saclay, France
https://doi.org/10.7554/eLife.50160
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  1. Jorge Torres-Paz
  2. Julien Leclercq
  3. Sylvie Rétaux
(2019)
Maternally-regulated gastrulation as a source of variation contributing to cavefish forebrain evolution
eLife 8:e50160.
https://doi.org/10.7554/eLife.50160
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Abstract

Sequential developmental events, starting from the moment of fertilization, are crucial for the acquisition of animal body plan. Subtle modifications in such early events are likely to have major impacts in later morphogenesis, bringing along morphological diversification. Here, comparing the blind cave and the surface morphotypes of Astyanax mexicanus fish, we found heterochronies during gastrulation, producing organizer and axial mesoderm tissues with different properties, including differences in expression of dkk1b, that may have contributed to cavefish brain evolution. These variations observed during gastrulation depend fully on maternal factors. The developmental evolution of retinal morphogenesis and hypothalamic patterning are among those traits that retained significant maternal influence at larval stages. Transcriptomic analysis of fertilized eggs from both morphotypes and reciprocal F1 hybrids showed a strong and specific maternal signature. Our work strongly suggests that maternal effect genes and developmental heterochronies occurring during gastrulation have impacted morphological brain change during cavefish evolution.

Data availability

Raw sequencing data are available through the NCBI Sequence Reads Archive (SRA) under BioProject accession PRJNA545230

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

Article and author information

Author details

  1. Jorge Torres-Paz

    Paris-Saclay Institute of Neuroscience, CNRS, Université Paris Sud, Université Paris-Saclay, Gif-sur-Yvette, France
    For correspondence
    jorge.torres-paz@cnrs.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7277-6348

  2. Julien Leclercq

    Paris-Saclay Institute of Neuroscience, CNRS, Université Paris Sud, Université Paris-Saclay, Gif-sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.

  3. Sylvie Rétaux

    Paris-Saclay Institute of Neuroscience, CNRS, Université Paris Sud, Université Paris-Saclay, Gif-sur-Yvette, France
    For correspondence
    retaux@inaf.cnrs-gif.fr
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (blindtest)

  • Sylvie Rétaux

Fondation pour la Recherche Médicale (DEQ20150331745 RETAUX)

  • Sylvie Rétaux

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

Ethics

Animal experimentation: Animal experimentation: Animals were treated according to the French and European regulationsfor handling of animals in research. SR's authorization for use of animals in research including Astyanax mexicanus is 91-116 and Paris Centre-Sud Ethic Committee authorization numbers are 2012-0052, -0053, and -0054.

Reviewing Editor

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

Publication history

  1. Received: July 12, 2019
  2. Accepted: October 30, 2019
  3. Accepted Manuscript published: October 31, 2019 (version 1)
  4. Version of Record published: November 22, 2019 (version 2)

Copyright

© 2019, Torres-Paz 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. Jorge Torres-Paz
  2. Julien Leclercq
  3. Sylvie Rétaux
(2019)
Maternally-regulated gastrulation as a source of variation contributing to cavefish forebrain evolution
eLife 8:e50160.
https://doi.org/10.7554/eLife.50160

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