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

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.

Metrics

  • 1,822
    Page views
  • 242
    Downloads
  • 6
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. 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

Further reading

    1. Developmental Biology
    Danelle Devenport
    Insight

    Advanced imaging techniques reveal details of the interactions between the two layers of the embryonic midgut that influence its ultimate shape.

    1. Developmental Biology
    2. Evolutionary Biology
    Katelyn Mika et al.
    Research Advance

    Structural and physiological changes in the female reproductive system underlie the origins of pregnancy in multiple vertebrate lineages. In mammals, the glandular portion of the lower reproductive tract has transformed into a structure specialized for supporting fetal development. These specializations range from relatively simple maternal nutrient provisioning in egg-laying monotremes to an elaborate suite of traits that support intimate maternal-fetal interactions in Eutherians. Among these traits are the maternal decidua and fetal component of the placenta, but there is considerable uncertainty about how these structures evolved. Previously we showed that changes in uterine gene expression contributes to several evolutionary innovations during the origins of pregnancy (Marinic, Mika, and Lynch 2021). Here we reconstruct the evolution of entire transcriptomes ('ancestral transcriptome reconstruction') and show that maternal gene expression profiles are correlated with degree of placental invasion. These results indicate that an epitheliochorial-like placenta evolved early in the mammalian stem-lineage and that the ancestor of Eutherians had a hemochorial placenta, and suggest maternal control of placental invasiveness. These data resolve major transitions in the evolution of pregnancy and indicate that ancestral transcriptome reconstruction can be used to study the function of ancestral cell, tissue, and organ systems.