Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates

Maxence Lanoizelet, Léo Michel, Ronan Lagadec, Hélène Mayeur, Lucile Guichard, Valentin Logeux, Dany Séverac, Kyle Martin, Christophe Klopp, Sylvain Marcellini, Héctor Castillo, Nicolas Pollet, Eva Candal, Mélanie Debiais-Thibaud, Catherine Boisvert, Bernard Billoud, Michael Schubert, Patrick Blader and Sylvie Mazan ()
Additional contact information
Maxence Lanoizelet: Observatoire Océanologique
Léo Michel: Observatoire Océanologique
Ronan Lagadec: Observatoire Océanologique
Hélène Mayeur: Observatoire Océanologique
Lucile Guichard: Observatoire Océanologique
Valentin Logeux: UMS 2348
Dany Séverac: INSERM
Kyle Martin: Biotechnology and Biological Sciences Research Council
Christophe Klopp: INRAE
Sylvain Marcellini: University of Concepcion
Héctor Castillo: University of Concepcion
Nicolas Pollet: Université Paris-Saclay
Eva Candal: Universidade de Santiago de Compostela
Mélanie Debiais-Thibaud: EPHE
Catherine Boisvert: Curtin University
Bernard Billoud: Station Biologique
Michael Schubert: CNRS
Patrick Blader: UPS
Sylvie Mazan: Observatoire Océanologique

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-54042-2

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