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02 06, 2018;7

Developmental evolution of the forebrain in cavefish, from natural variations in neuropeptides to behavior.

Alexandre Alié, Lucie Devos, Jorge Torres-Paz, Lise Prunier, Fanny Boulet, Maryline Blin, Yannick Elipot, Sylvie Retaux
Author Information
  1. Alexandre Alié: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  2. Lucie Devos: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  3. Jorge Torres-Paz: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  4. Lise Prunier: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  5. Fanny Boulet: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  6. Maryline Blin: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  7. Yannick Elipot: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France.
  8. Sylvie Retaux: Paris-Saclay Institute of Neuroscience, Université Paris Sud, CNRS UMR9197, Université Paris-Saclay, Avenue de la terrasse, Gif-sur-Yvette, France. ORCID
PMID: 29405116 DOI: 10.7554/eLife.32808

Abstract

The fish comes in two forms: the normal surface-dwelling and the blind depigmented cave-adapted morphs. Comparing the development of their basal forebrain, we found quantitative differences in numbers of cells in specific clusters for six out of nine studied neuropeptidergic cell types. Investigating the origins of these differences, we showed that early Shh and Fgf signaling impact on the development of NPY and Hypocretin clusters, via effect on Lhx7 and Lhx9 transcription factors, respectively. Finally, we demonstrated that such neurodevelopmental evolution underlies behavioral evolution, linking a higher number of Hypocretin cells with hyperactivity in cavefish. Early embryonic modifications in signaling/patterning at neural plate stage therefore impact neuronal development and later larval behavior, bridging developmental evolution of a neuronal system and the adaptive behavior it governs. This work uncovers novel variations underlying the evolution and adaptation of cavefish to their extreme environment.

Keywords

behavior cavefish developmental biology hypothalamus stem cells

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MeSH Term

Adaptation, Biological
Animals
Behavior, Animal
Biological Evolution
Characidae
Neuropeptides
Prosencephalon

Chemicals

Neuropeptides
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 67

Word Cloud

Created with Highcharts 10.0.0evolutioncavefishbehaviordevelopmentcellsforebraindifferencesclustersimpactHypocretinneuronaldevelopmentalvariationsfishcomestwoforms:normalsurface-dwellingblinddepigmentedcave-adaptedmorphsComparingbasalfoundquantitativenumbersspecificsixninestudiedneuropeptidergiccelltypesInvestigatingoriginsshowedearlyShhFgfsignalingNPYviaeffectLhx7Lhx9transcriptionfactorsrespectivelyFinallydemonstratedneurodevelopmentalunderliesbehaviorallinkinghighernumberhyperactivityEarlyembryonicmodificationssignaling/patterningneuralplatestagethereforelaterlarvalbridgingsystemadaptivegovernsworkuncoversnovelunderlyingadaptationextremeenvironmentDevelopmentalnaturalneuropeptidesbiologyhypothalamusstem

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