Volume 01, Issue 04
<< prev. next >>
ISSN: 2274-0422

Article Management

You must log in to submit or manage articles.

You do not have an account yet ? Sign up.

MorphoMuseuM Volume 01, Issue 04
<< prev. article next article >>

Original article : anatomy atlas

Skeletogenesis during the late embryonic development of the catshark Scyliorhinus canicula (Chondrichthyes; Neoselachii)
Sébastien Enault, Sylvain Adnet Logo and Mélanie Debiais-Thibaud Logo
Published online: 25/04/2016

Keywords: Chondrichthyes; development; mineralization; Scyliorhinus canicula; skeleton

References: 31
Cited by: 7

Cite this article: Sébastien Enault, Sylvain Adnet and Mélanie Debiais-Thibaud, 2016. Skeletogenesis during the late embryonic development of the catshark Scyliorhinus canicula (Chondrichthyes; Neoselachii). MorphoMuseuM 1 (4)-e2. doi: 10.18563/m3.1.4.e2

Export citation


Current knowledge on the skeletogenesis of Chondrichthyes is scarce compared with their extant sister group, the bony fishes. Most of the previously described developmental tables in Chondrichthyes have focused on embryonic external morphology only. Due to its small body size and relative simplicity to raise eggs in laboratory conditions, the small-spotted catshark Scyliorhinus canicula has emerged as a reference species to describe developmental mechanisms in the Chondrichthyes lineage. Here we investigate the dynamic of mineralization in a set of six embryonic specimens using X-ray microtomography and describe the developing units of both the dermal skeleton (teeth and dermal scales) and endoskeleton (vertebral axis). This preliminary data on skeletogenesis in the catshark sets the first bases to a more complete investigation of the skeletal developmental in Chondrichthyes. It should provide comparison points with data known in osteichthyans and could thus be used in the broader context of gnathostome skeletal evolution. 

Specimens and 3D Data

Scyliorhinus canicula SC6_2_2015_03_20 View specimen


Mineralized skeleton of a 6,2 cm long embryo of Scyliorhinus canicula

Type: "3D_surfaces"

doi: 10.18563/m3.sf.50   state:published

Download 3D surface file

Scyliorhinus canicula SC6_7_2015_03_20 View specimen


Mineralized skeleton of a 6,7 cm long embryo of Scyliorhinus canicula

Type: "3D_surfaces"

doi: 10.18563/m3.sf.51   state:published

Download 3D surface file

Scyliorhinus canicula SC7_1_2015_04_03 View specimen


Mineralized skeleton of a 7,1 cm long embryo of Scyliorhinus canicula

Type: "3D_surfaces"

doi: 10.18563/m3.sf.52   state:published

Download 3D surface file

Scyliorhinus canicula SC7_5_2015_03_13 View specimen


Mineralized skeleton of a 7,5 cm long embryo of Scyliorhinus canicula

Type: "3D_surfaces"

doi: 10.18563/m3.sf.53   state:published

Download 3D surface file

Scyliorhinus canicula SC8_2015_03_20 View specimen


Mineralized skeleton of a 8 cm long embryo of Scyliorhinus canicula

Type: "3D_surfaces"

doi: 10.18563/m3.sf.54   state:published

Download 3D surface file

Scyliorhinus canicula SC10_2015_02_27 View specimen


Mineralized skeleton of a 10 cm long embryo of Scyliorhinus canicula

Type: "3D_surfaces"

doi: 10.18563/m3.sf.55   state:published

Download 3D surface file


Published in Volume 01, Issue 04 (2016)


Applegate, S., 1967. A survey of shark hard parts. In: Gilbert, P., Mathewson, R., Rall, D. (Eds.), Shark, Skates and Rays. The Johns Hopkins Press, Baltimore, Maryland, pp. 37–67.

Ballard, W.W., Mellinger, J., Lechenault, H., 1993. A series of stages for development of Scyliorhinus canicula the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). Journal of Experimental Zoology. 267, 1–43.

Cappetta, H., 2012. Handbook of Paleoichthyology, Vol. 3E: Chondrichthyes · Mesozoic and Cenozoic Elasmobranchii: Teeth. Verlag Dr. Friedrich Pfeil.

Cignoni, P., Cignoni, P., Callieri, M., Callieri, M., Corsini, M., Corsini, M., Dellepiane, M., Dellepiane, M., Ganovelli, F., Ganovelli, F., Ranzuglia, G., Ranzuglia, G., 2008. MeshLab: an Open-Source Mesh Processing Tool. Sixth Eurographics Italian Chapter Conference. 129–136.

Compagno, L.J. V., 1988. Sharks of the order Carcharhiniformes. Princeton University Press, New Jersey.

Compagno, L.J. V., 1999. Endoskeleton. In: Hamlett, W.C. (Ed.), Sharks, Skates and Rays. The Biology of Elasmobranch Fishes.

Compagnucci, C., Debiais-Thibaud, M., Coolen, M., Fish, J., Griffin, J.N., Bertocchini, F., Minoux, M., Rijli, F.M., Borday-Birraux, V., Casane, D., Mazan, S., Depew, M.J., 2013. Pattern and polarity in the development and evolution of the gnathostome jaw: both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Developmental biology. 377, 428–48. 

D’Souza, D.G., Rana, K., Milley, K.M., Maclean, H.E., Zajac, J.D., Bell, J., Brenner, S., Venkatesh, B., Richardson, S.J., Danks, J. a, 2013. Expression of Wnt signaling skeletal development genes in the cartilaginous fish, elephant shark (Callorhinchus milii). General and comparative endocrinology. 1–9.

Dahn, R.D., Davis, M.C., Pappano, W.N., Shubin, N.H., 2007. Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning. Nature. 445, 311–314.

de Beer, G.R., 1931. The development of the skull of Scyllium (Scyliorhinus) canicula L. Quarterly Journal of Microscopical Science. 74, 591–652.

Dean, M.N., Summers, A.P., 2006. Mineralized cartilage in the skeleton of chondrichthyan fishes. Zoology (Jena, Germany). 109, 164–8.

Debiais-Thibaud, M., Oulion, S., Bourrat, F., Laurenti, P., Casane, D., Borday-Birraux, V., 2011. The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula. BMC Evolutionary Biology. 11, 307.

Dingerkus, G., Seret, B., Guilbert, E., 1991. Multiple prismatic calcium phosphate layers in the jaws of present-day sharks (Chondrichthyes; Selachii). Experientia. 47, 38–40.

Eames, B.F., Allen, N., Young, J., Kaplan, A., Helms, J. a, Schneider, R. a, 2007. Skeletogenesis in the swell shark Cephaloscyllium ventriosum. Journal of anatomy. 210, 542–54.

Ellis, J.R., Shackley, S.E., 1997. The reproductive biology of Scyliorhinus canicula in the Bristol Channel, U.K. Journal of Fish Biology. 51, 361–372.

Enault, S., Muñoz, D.N., Silva, W.T.A.F., Borday-birraux, V., Bonade, M., Oulion, S., Ventéo, S., Marcellini, S., Debiais-Thibaud, M., 2015. Molecular footprinting of skeletal tissues in the catshark Scyliorhinus canicula and the clawed frog Xenopus tropicalis identifies conserved and derived features of vertebrate calcification. Frontiers in genetics. 6, 1–14.

Gegenbaur, C., 1872. Untersuchungen zur vergleichenden anatomie der wirbelthiere. Drittes heft. Das kopfskelet der selachier, ein beitrag Zur erkenntniss der genese des kopfskelete der wirbelthiere. Leipzig.

Godard, B.G., Mazan, S., 2012. Early patterning in a chondrichthyan model, the small spotted dogfish: towards the gnathostome ancestral state. Journal of anatomy. 222, 56–66.

Hasse, C., 1879. Das natürliche System der Elasmobranchier auf Grundlage des Baues und der Entwicklung ihrer Wirbelsäule. Eine morphologische und paläontologische Studie. I Allgemei, 1–76.

Hasse, C., 1882a. Das natürliche System der Elasmobranchier auf Grundlage des Baues und der Entwicklung ihrer Wirbelsäule. Eine morphologische und paläontologische Studie. II Besonde, 96–179.

Hasse, C., 1882b. Das natürliche System der Elasmobranchier auf Grundlage des Baues und der Entwicklung ihrer Wirbelsäule. Eine morphologische und paläontologische Studie. III, 181–285.

Hautier, L., Weisbecker, V., Sánchez-Villagra, M.R., Goswami, A., Asher, R.J., 2010. Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences of the United States of America. 107, 18903–8.

Holmgren, N., 1940. Studies of the head in fishes. Part 1. Development of the skull in sharks and rays. Acta Zoologica. 21, 51–257.

Lebrun, R., 2014. ISE-MeshTools, a 3D interactive fossil reconstruction freeware. In: 12th Annual Meeting of EAVP, Torino, Italy.

Mellinger, J., Wrisez, F., 1993. Etude des écailles primaires de l’embryon de la roussette Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) au microscope électronique à balayage. Annales des Sciences Naturelles, Zoologie, Paris, 13e série. 14, 13–22.

O’Shaughnessy, K.L., Dahn, R.D., Cohn, M.J., 2015. Molecular development of chondrichthyan claspers and the evolution of copulatory organs. Nature Communications. 6, 6698.

Peignoux-Deville, J., Lallier, F., Vidal, B., 1982. Evidence for the presence of osseous tissue in dogfish vertebrae. Cell and tissue research. 222, 605–614. 

Reif, W.-E., 1980. Development of dentition and dermal skeleton in embryonic Scyliorhinus canicula. Journal of morphology. 166, 275–88.

Reif, W.-E., 1985. Squamation and ecology of sharks. Cour Forsch Inst Senckenberg. 78, 1–255.

Ridewood, W.G., 1899. Some Observations on the Caudal Diplospondyly of Sharks. Journal of the Linnean Society of London, Zoology. 27, 46–59.

Summers, A., 2000. Stiffening the stingray skeleton- an investigation of durophagy in myliobatid stingrays (Chondrichthyes, batoidea, myliobatidae). Journal of morphology. 243, 113–26.<113::AID-JMOR1>3.0.CO;2-A 

Cited by:

Raphaël Scherrer, Andrés Hurtado, Erik Garcia Machado and Mélanie Debiais-Thibaud (2017). MicroCT survey of larval skeletal mineralization in the Cuban gar Atractosteus tristoechus (Actinopterygii; Lepisosteiformes). MorphoMuseuM.

Giuseppe Marramà, Kerin M. Claeson, Giorgio Carnevale and Jürgen Kriwet (2018). Revision of Eocene electric rays (Torpediniformes, Batomorphii) from the Bolca Konservat-Lagerstätte, Italy, reveals the first fossil embryoin situin marine batoids and provides new insights into the origin of trophic novelties in coral reef fishes. Journal of Systematic Palaeontology.

Jacob B. Pears, Zerina Johanson, Kate Trinajstic, Mason N. Dean and Catherine A. Boisvert (2020). Mineralization of the Callorhinchus Vertebral Column (Holocephali; Chondrichthyes). Frontiers in Genetics.

Nicolas Leurs, Camille Martinand-Mari, Stéphanie Ventéo, Tatjana Haitina and Mélanie Debiais-Thibaud (2021). Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates. Frontiers in Genetics.

Fidji Berio, Morgane Broyon, Sébastien Enault, Nelly Pirot, Faviel A. López-Romero and Mélanie Debiais-Thibaud (2021). Diversity and Evolution of Mineralized Skeletal Tissues in Chondrichthyans. Frontiers in Ecology and Evolution.

Rory L. Cooper, Ella F. Nicklin, Liam J. Rasch and Gareth J. Fraser (2023). Teeth outside the mouth: The evolution and development of shark denticles. Evolution & Development.

Jamie L. Knaub, Michelle Passerotti, Lisa J. Natanson, Tricia Meredith and Marianne Porter (2024). Vertebral morphology in the tail-whipping common thresher shark, Alopias vulpinus . Royal Society Open Science.