Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates
The mode of evolution of left-right asymmetries in the vertebrate habenulae remains largely unknown. Using a transcriptomic approach, we show that in a cartilaginous fish, the catshark Scyliorhinus canicula, habenulae exhibit marked asymmetries, in both their medial and lateral components. Comparisons across vertebrates suggest that those identified in lateral habenulae reflect an ancestral gnathostome trait, partially conserved in lampreys, and independently lost in tetrapods and neopterygians. Asymmetry formation involves distinct mechanisms in the catshark lateral and medial habenulae. Medial habenulae are submitted to a marked, asymmetric temporal regulation of neurogenesis, undetectable in their lateral counterparts. Conversely, asymmetry formation in lateral habenulae results from asymmetric choices of neuronal identity in post-mitotic progenitors, a regulation dependent on the repression of Wnt signaling by Nodal on the left. Based on comparisons with the mouse and the zebrafish, we propose that habenular asymmetry formation involves a recurrent developmental logic across vertebrates, which relies on conserved, temporally regulated genetic programs sequentially shaping choices of neuronal identity on both sides and asymmetrically modified by Wnt activity.
Authors
- Léo Michel (ORCID: https://orcid.org/0000-0002-6688-5708)
- Catherine Boisvert (ORCID: https://orcid.org/0000-0002-0618-7270)
- Ronan Lagadec
- Maxence Lanoizelet (ORCID: https://orcid.org/0000-0002-6622-1645)
- Eva Candal (ORCID: https://orcid.org/0000-0001-6136-7605)
- Sylvain Marcellini (ORCID: https://orcid.org/0000-0001-9986-2054)
- Patrick Blader (ORCID: https://orcid.org/0000-0003-3299-6108)
- Mélanie Debiais‐Thibaud (ORCID: https://orcid.org/0000-0002-1377-2515)
- Michael Schubert (ORCID: https://orcid.org/0000-0002-2341-712X)
- Bernard Billoud (ORCID: https://orcid.org/0000-0002-5140-8087)
- Sylvie Mazan (ORCID: https://orcid.org/0000-0003-4657-8097)
- Héctor Castillo (ORCID: https://orcid.org/0000-0001-9260-4298)
- Kyle J. Martin (ORCID: https://orcid.org/0000-0002-4081-6835)
- Valentin Logeux
- Christophe Klopp (ORCID: https://orcid.org/0000-0001-7126-5477)
- Nicolas Pollet (ORCID: https://orcid.org/0000-0002-9975-9644)
- Lucile Guichard (ORCID: https://orcid.org/0009-0003-9142-6364)
- Hélène Mayeur
- Dany Séverac
Institutions
- Centre National de la Recherche Scientifique (FR)
- Université Toulouse III - Paul Sabatier (FR)
- Inserm (FR)
- École Pratique des Hautes Études (FR)
- University of Concepción (CL)
- Université Fédérale de Toulouse Midi-Pyrénées (FR)
- Université de Montpellier (FR)
- Universidade de Santiago de Compostela (ES)
- Curtin University (AU)
- Université Paris-Saclay (FR)
- Biotechnology and Biological Sciences Research Council (GB)
- Station Biologique de Roscoff (FR)
- Sorbonne Université (FR)
- Laboratoire de Biologie Intégrative des Modèles Marins (FR)
- UK Research and Innovation (GB)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Institut des Sciences de l'Evolution de Montpellier (FR)
- Biologie Intégrative des Organismes Marins (FR)
- Observatoire Océanologique de Banyuls-sur-Mer (FR)
- Laboratoire de Biologie du Développement de Villefranche-sur-Mer (FR)
- Institut de Recherche pour le Développement (FR)
- Institut de la Mer de Villefranche (FR)
Publication Details
- Journal
- Nature Communications
- Published
- 2024-11-25
- DOI
- https://doi.org/10.1038/s41467-024-54042-2
- Citations
- 1
- Primary Topic
- Hemispheric Asymmetry in Neuroscience
- Type
- article
- Field-Weighted Citation Impact
- 0.34
Funders
- Agence Nationale de la Recherche