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Original article : anatomy atlas
Skeletogenesis during the late embryonic development of the catshark Scyliorhinus canicula (Chondrichthyes; Neoselachii)
Published online: 2016-04-25
Keywords:
Chondrichthyes; development; mineralization; Scyliorhinus canicula; skeleton
doi: 10.18563/m3.1.4.e2
Cite this article:
Enault S., Adnet S., Debiais-Thibaud M., 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
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Abstract
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
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M3#50_SC6_2_2015_03_20 Mineralized skeleton of a 6,2 cm long embryo of Scyliorhinus canicula Type: "3D_surfaces"
3D view: doi: 10.18563/m3.sf.50
Data citation:
Enault S., Adnet S., Debiais-Thibaud M., 2016. M3#50_SC6_2_2015_03_20. doi: 10.18563/m3.sf.50
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Scyliorhinus canicula SC6_7_2015_03_20
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M3#51_SC6_7_2015_03_20 Mineralized skeleton of a 6,7 cm long embryo of Scyliorhinus canicula Type: "3D_surfaces"
3D view: doi: 10.18563/m3.sf.51
Data citation:
Enault S., Adnet S., Debiais-Thibaud M., 2016. M3#51_SC6_7_2015_03_20. doi: 10.18563/m3.sf.51
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Scyliorhinus canicula SC7_1_2015_04_03
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M3#52_SC7_1_2015_04_03 Mineralized skeleton of a 7,1 cm long embryo of Scyliorhinus canicula Type: "3D_surfaces"
3D view: doi: 10.18563/m3.sf.52
Data citation:
Enault S., Adnet S., Debiais-Thibaud M., 2016. M3#52_SC7_1_2015_04_03. doi: 10.18563/m3.sf.52
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Scyliorhinus canicula SC7_5_2015_03_13
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M3#53_SC7_5_2015_03_13 Mineralized skeleton of a 7,5 cm long embryo of Scyliorhinus canicula
Type: "3D_surfaces"
3D view: doi: 10.18563/m3.sf.53
Data citation:
Enault S., Adnet S., Debiais-Thibaud M., 2016. M3#53_SC7_5_2015_03_13. doi: 10.18563/m3.sf.53
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Scyliorhinus canicula SC8_2015_03_20
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M3#54_SC8_2015_03_20 Mineralized skeleton of a 8 cm long embryo of Scyliorhinus canicula Type: "3D_surfaces"
3D view: doi: 10.18563/m3.sf.54
Data citation:
Enault S., Adnet S., Debiais-Thibaud M., 2016. M3#54_SC8_2015_03_20. doi: 10.18563/m3.sf.54
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Scyliorhinus canicula SC10_2015_02_27
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M3#55_SC10_2015_02_27 Mineralized skeleton of a 10 cm long embryo of Scyliorhinus canicula Type: "3D_surfaces"
3D view: doi: 10.18563/m3.sf.55
Data citation:
Enault S., Adnet S., Debiais-Thibaud M., 2016. M3#55_SC10_2015_02_27. doi: 10.18563/m3.sf.55
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Published in Volume 01, Issue 04 (2016)
Bibliography
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. http://dx.doi.org/10.1002/jez.1402670309
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. http://dx.doi.org/10.1016/j.ydbio.2013.02.022
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. http://dx.doi.org/10.1016/j.ygcen.2013.06.021
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. http://dx.doi.org/10.1038/nature05436
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. http://dx.doi.org/10.1016/j.zool.2006.03.002
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. http://dx.doi.org/10.1186/1471-2148-11-307
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. http://dx.doi.org/10.1007/BF02041246
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. http://dx.doi.org/10.1111/j.1469-7580.2007.00723.x
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. http://dx.doi.org/10.1111/j.1095-8649.1997.tb01672.x
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. http://dx.doi.org/10.3389/fgene.2015.00283
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. http://dx.doi.org/10.1111/j.1469-7580.2012.01552.x
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. http://dx.doi.org/10.1073/pnas.1010335107
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. http://dx.doi.org/10.1038/ncomms7698
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. http://dx.doi.org/10.1007/BF00213858
Reif, W.-E., 1980. Development of dentition and dermal skeleton in embryonic Scyliorhinus canicula. Journal of morphology. 166, 275–88. http://dx.doi.org/10.1002/jmor.1051660303
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. http://dx.doi.org/10.1002/(SICI)1097-4687(200002)243:2<113::AID-JMOR1>3.0.CO;2-A
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