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

Abstract
Data availability
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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

(2019) Maternal RNA sequencing of Astyanax mexicanus 2-cells eggs
NCBI Bioproject, PRJNA545230.

https://www.ncbi.nlm.nih.gov/sra/PRJNA545230

The following previously published data sets were used

1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO221961 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0AAA23YC10, mRNA sequence
NCBI, accession no: FO221961.

https://www.ncbi.nlm.nih.gov/nuccore/422274646
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO212120 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0AAA18YA07, mRNA sequence
NCBI, accession no: FO212120.

https://www.ncbi.nlm.nih.gov/nuccore/422224244
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO211529 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0AAA19YL19, mRNA sequence
NCBI, accession no: FO211529.

https://www.ncbi.nlm.nih.gov/nuccore/422226109
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO304658 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0ACA35YA23, mRNA sequence
NCBI, accession no: FO304658.

https://www.ncbi.nlm.nih.gov/nuccore/425531810
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO245358 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0AAA95YG16, mRNA sequence
NCBI, accession no: FO245358.

https://www.ncbi.nlm.nih.gov/nuccore/422281476
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO299407 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0ACA49YF15, mRNA sequence
NCBI, accession no: FO299407.

https://www.ncbi.nlm.nih.gov/nuccore/425597731
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO289143 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0ABA99YL22, mRNA sequence
NCBI, accession no: FO289143.

https://www.ncbi.nlm.nih.gov/nuccore/425545401
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO378514 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0AHA13YJ18, mRNA sequence
NCBI, accession no: FO378514.

https://www.ncbi.nlm.nih.gov/nuccore/425608699
1. Hinaux H
2. Poulain J
3. Da Silva C
4. Noirot C
5. Jeffery WR
6. Casane D
7. Retaux S
(2012) FO263072 Astyanax mexicanus whole embryos and larvae neurula to swimming larvae Astyanax mexicanus cDNA clone ARA0ABA37YE05, mRNA sequence
NCBI, accession no: FO263072.

https://www.ncbi.nlm.nih.gov/nucest/FO263072
1. Menuet A1
2. Alunni A
3. Joly JS
4. Jeffery WR
5. Rétaux S
(2007) Astyanax mexicanus LIM/homeobox protein 9 mRNA, complete cds
NCBI, accession no: EF175738.1.

https://www.ncbi.nlm.nih.gov/nuccore/EF175738
(2004) Astyanax mexicanus sonic hedgehog precursor (shh) mRNA, complete cds
NCBI, accession no: EF175738.1.

https://www.ncbi.nlm.nih.gov/nuccore/AY661431
(2004) Astyanax mexicanus distal-less homeobox gene 3b (dlx3b) mRNA, partial cds
NCBI, accession no: AY661432.

https://www.ncbi.nlm.nih.gov/nuccore/AY661432
1. Warren W
2. McCaugh S
(2017) PREDICTED: Astyanax mexicanus hypocretin neuropeptide precursor (hcrt), mRNA
NCBI, accession no: XM_007287820.3.

https://www.ncbi.nlm.nih.gov/nuccore/XM_007287820.3
1. Warren W
2. McCaugh S
(2017) PREDICTED: Astyanax mexicanus LIM homeobox 8 (lhx8), transcript variant X1, mRNA
NCBI, accession no: XM_022678613.1.

https://www.ncbi.nlm.nih.gov/nuccore/XM_022678613

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0002-7277-6348
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.
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.

Copyright

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.