The Sensory Shark: High-quality Morphological, Genomic and Transcriptomic Data for the Small-spotted Catshark <i>Scyliorhinus Canicula</i> Reveal the Molecular Bases of Sensory Organ Evolution in Jawed Vertebrates
Cartilaginous fishes (chondrichthyans: chimeras and elasmobranchs -sharks, skates, and rays) hold a key phylogenetic position to explore the origin and diversifications of jawed vertebrates. Here, we report and integrate reference genomic, transcriptomic, and morphological data in the small-spotted catshark Scyliorhinus canicula to shed light on the evolution of sensory organs. We first characterize general aspects of the catshark genome, confirming the high conservation of genome organization across cartilaginous fishes, and investigate population genomic signatures. Taking advantage of a dense sampling of transcriptomic data, we also identify gene signatures for all major organs, including chondrichthyan specializations, and evaluate expression diversifications between paralogs within major gene families involved in sensory functions. Finally, we combine these data with 3D synchrotron imaging and in situ gene expression analyses to explore chondrichthyan-specific traits and more general evolutionary trends of sensory systems. This approach brings to light, among others, novel markers of the ampullae of Lorenzini electrosensory cells, a duplication hotspot for crystallin genes conserved in jawed vertebrates, and a new metazoan clade of the transient-receptor potential (TRP) family. These resources and results, obtained in an experimentally tractable chondrichthyan model, open new avenues to integrate multiomics analyses for the study of elasmobranchs and jawed vertebrates.
Authors
- Camille Martinand‐Mari (ORCID: https://orcid.org/0000-0002-9909-0071)
- Erez Lieberman Aiden (ORCID: https://orcid.org/0000-0003-0634-6486)
- Ronan Lagadec
- Craig Corton (ORCID: https://orcid.org/0000-0001-7942-2246)
- Tatjana Haitina (ORCID: https://orcid.org/0000-0002-8754-5534)
- Olga Dudchenko (ORCID: https://orcid.org/0000-0001-9163-9544)
- Julie Poulain (ORCID: https://orcid.org/0000-0002-8744-3116)
- Mélanie Debiais‐Thibaud (ORCID: https://orcid.org/0000-0002-1377-2515)
- Jake Leyhr (ORCID: https://orcid.org/0000-0003-1815-7818)
- Sigrun I. Korsching (ORCID: https://orcid.org/0000-0002-5450-172X)
- Arina D. Omer (ORCID: https://orcid.org/0000-0003-1336-2505)
- Kenneth P. Olive (ORCID: https://orcid.org/0000-0002-3392-8994)
- Sophie Sanchez (ORCID: https://orcid.org/0000-0002-3611-6836)
- Shane McCarthy (ORCID: https://orcid.org/0000-0002-2715-4187)
- David A. Mead (ORCID: https://orcid.org/0000-0003-1982-9356)
- Owen G. Osborne (ORCID: https://orcid.org/0000-0002-1213-1169)
- Donald J. Weisz
- Alan Tracey (ORCID: https://orcid.org/0000-0002-4805-9058)
- Sylvie Mazan (ORCID: https://orcid.org/0000-0003-4657-8097)
- Kerstin Howe (ORCID: https://orcid.org/0000-0003-2237-513X)
- Nicolas Leurs
- Alexander Hayward (ORCID: https://orcid.org/0000-0001-7413-718X)
- John F. Mulley (ORCID: https://orcid.org/0000-0002-1537-7316)
- Jason Skelton
- Tobias Baril (ORCID: https://orcid.org/0000-0002-5936-7531)
- Martin Korňan (ORCID: https://orcid.org/0000-0002-0280-6636)
- James Torrance (ORCID: https://orcid.org/0000-0002-6117-8190)
- Jale Dolucan (ORCID: https://orcid.org/0000-0002-3551-1770)
- Jean‐Marc Aury (ORCID: https://orcid.org/0000-0003-1718-3010)
- Michelle Smith (ORCID: https://orcid.org/0000-0001-5288-0001)
- Laurent Michel (ORCID: https://orcid.org/0000-0001-7230-7130)
- Peter O. Mulhair (ORCID: https://orcid.org/0000-0003-3311-4883)
- Ying Sims (ORCID: https://orcid.org/0000-0003-4765-4872)
- K. K. Sharma (ORCID: https://orcid.org/0000-0002-9896-5286)
- Sophie Mangenot
- Hélène Mayeur
- Emma Betteridge
Institutions
- TH Köln - University of Applied Sciences (DE)
- Broad Institute (US)
- Uppsala University (SE)
- Centre National de la Recherche Scientifique (FR)
- Natural History Museum (GB)
- École Pratique des Hautes Études (FR)
- Bangor University (GB)
- University of Cologne (DE)
- Baylor College of Medicine (US)
- Université de Montpellier (FR)
- University of Exeter (GB)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Université Paris-Saclay (FR)
- European Synchrotron Radiation Facility (FR)
- Wellcome Sanger Institute (GB)
- Sorbonne Université (FR)
- University of Oxford (GB)
- Institut des Sciences de l'Evolution de Montpellier (FR)
- Genoscope (FR)
- CEA Paris-Saclay (FR)
- Biologie Intégrative des Organismes Marins (FR)
- Institute of Genetics (CA)
- Center for Theoretical Biological Physics (US)
- Baylor Genetics (US)
- Institut de Recherche pour le Développement (FR)
- Rice University (US)
Publication Details
- Journal
- Molecular Biology and Evolution
- Published
- 2024-12-01
- DOI
- https://doi.org/10.1093/molbev/msae246
- Citations
- 10
- Primary Topic
- Ichthyology and Marine Biology
- Type
- article
- Field-Weighted Citation Impact
- 6.91
Funders
- National Science Foundation
- Infrastructures en Biologie Santé et Agronomie
- Agence Nationale de la Recherche
- Institut National de la Santé et de la Recherche Médicale
- Ligue Contre le Cancer
- Vetenskapsrådet
- Centre National de la Recherche Scientifique
- University of Haifa
- Institut National Du Cancer
- Direction Générale de l’offre de Soins
- Région Occitanie Pyrénées-Méditerranée
- National Institutes of Health
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council
- Division of Biological Infrastructure