Skip to main content Accessibility help
×
Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-28T17:58:57.025Z Has data issue: false hasContentIssue false

6 - The Evolution of Endoskeletal Mineralisation in Chondrichthyan Fish

Development, Cells and Molecules

Published online by Cambridge University Press:  31 December 2018

Zerina Johanson
Affiliation:
Natural History Museum, London
Charlie Underwood
Affiliation:
Birkbeck, University of London
Martha Richter
Affiliation:
Natural History Museum, London
Get access

Summary

Chondrichthyan fishes possess an endoskeleton made exclusively of cartilage. Their cartilaginous tissue is very similar in terms of cell types, the extracellular matrix and embryonic origins to the cartilage of other jawed vertebrates. In bony fish however, most of the embryonic cartilaginous endoskeleton degrades and is replaced by a skeleton made of endochondral bone often associated with dermal bone. Paleontological data support the view that the chondrichthyan cartilaginous skeleton is evolutionarily associated with a secondary loss of dermal bone (ancestral to jawed vertebrates), while endochondral bone has evolved within the bony fish lineage. A synapomorphy of the chondrichthyan skeleton is the development of a superficial layer of small, mineralised cartilage units covering the endoskeleton, known as ‘tesserae’. Less well described are two other sites of skeletal mineralisation, namely the vertebral centrum that is composed of a mineralised layer surrounding the notochord (herein described as fibrous mineralisation) and only found in selachians, and a mineralised layer surrounding the neural arches (herein described as lamellar mineralisation) that is only well known in Carchariniformes. Embryonic series of histologically stained sections of the skeleton of two selachians (a shark Scyliorhinus canicula, a skate Raja clavata) and new comparable data from an holocephalan Hydrolagus sp. allows cell and extracellular matrix comparisons of developing skeletons in Chondrichthyes. Various cell types might be involved in this developmental process. A review is provided of molecular data already published and the new genomic and transcriptomic tools that highlight current trends in the study of skeletal evolution of cartilaginous fish. These new techniques point to the presence of genetic networks that led to the evolution of various cell populations involved in skeletal mineralisation and chondrichthyan diversification.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adachi, N, Kuratani, S. 2012. Development of head and trunk mesoderm in the dogfish, Scyliorhinus torazame: I. Embryology and morphology of the head. Evol Dev 256:234256.CrossRefGoogle Scholar
Adachi, N, Takechi, M, Hirai, T, Kuratani, S. 2012. Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head. Evol Dev 14:257276.Google Scholar
Applegate, S. 1967. A survey of shark hard parts. In: Gilbert, P, Mathewson, R, Rall, D, editors. Shark, Skates and Rays. Baltimore, Maryland: The Johns Hopkins Press. pp. 3767.Google Scholar
Arratia, G, Schultze, HP, Casciotta, J. 2001. Vertebral column and associated elements in dipnoans and comparison with other fishes: Development and homology. J Morph 250:101172.Google Scholar
Balfour, FM. 1878. A monograph of elasmobranch fishes. Cambridge.Google Scholar
Ballard, WW, Mellinger, J, Lechenault, H. 1993. A series of stages for development of Scyliorhinus canicula the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:143.Google Scholar
Bensimon-Brito, A, Cardeira, J, Cancela, ML, Huysseune, A, Witten, PE. 2012. Distinct patterns of notochord mineralisation in zebrafish coincide with the localization of Osteocalcin isoform 1 during early vertebral centra formation. BMC Dev Biol 12:1.CrossRefGoogle ScholarPubMed
Boisvert, CA, Martins, CL, Edmunds, AG, Cocks, J, Currie, P. 2014. Capture, transport, and husbandry of elephant sharks (Callorhinchus milii) adults, eggs, and hatchlings for research and display. Zoo Biol 5:15.Google Scholar
Brazeau, MD, de Winter, V. 2015. The hyoid arch and braincase anatomy of Acanthodes support chondrichthyan affinity of ‘acanthodians’. Proc R Soc B Biol Sci 282:20152210.Google Scholar
Cervantes-Diaz, F, Contreras, P, Marcellini, S. 2016. Evolutionary origin of endochondral ossification: The transdifferentiation hypothesis. Dev Genes Evol 227:121127.Google Scholar
Chevallier, A. 1975. Rôle du mésoderme somitique dans le développement de la cage thoracique de l’embryon d’oiseau. I. Origine du segment sternal et mécanismes de la différenciation des côtes. J Embryol Exp Morph 33:291311.Google Scholar
Christ, B, Huang, R, Wilting, J. 2000. The development of the avian vertebral column. Anat Embryol (Berl) 202:179194.Google Scholar
Claeson, KM. 2011. The synarcual cartilage of batoids with emphasis on the synarcual of Rajidae. J Morph 272:14441463.Google Scholar
Compagnucci, C, Debiais-Thibaud, M, Coolen, M, Fish, J, Griffin, JN, Bertocchini, F, Minoux, M, Rijli, FM, Borday-Birraux, V, Casane, D, Mazan, S, Depew, MJ. 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. Dev Biol 377:428448.Google Scholar
Coolen, M, Menuet, A, Chassoux, D, Compagnucci, C, Henry, S, Lévèque, L, Da Silva, C, Gavory, F, Samain, S, Wincker, P, Thermes, C, D’Aubenton-Carafa, Y, Rodriguez-Moldes, I, Naylor, G, Depew, M, Sourdaine, P, Mazan, S. 2008. The Dogfish Scyliorhinus canicula: A Reference in Jawed Vertebrates. Cold Spring Harb Protoc.CrossRefGoogle Scholar
Dean, MN, Ekstrom, L, Monsonego-Ornan, E, Ballantyne, J, Witten, PE, Riley, C, Habraken, W, Omelon, S. 2015. Mineral homeostasis and regulation of mineralisation processes in the skeletons of sharks, rays and relatives (Elasmobranchii). Semin Cell Dev Biol 46:5167.Google Scholar
Dean, MN, Mull, CG, Gorb, SN, Summers, AP. 2009. Ontogeny of the tessellated skeleton: Insight from the skeletal growth of the round stingray Urobatis halleri. J Anat 215:227239.CrossRefGoogle ScholarPubMed
Dean, MN, Socha, JJ, Hall, BK, Summers, AP. 2010. Canaliculi in the tessellated skeleton of cartilaginous fishes. J Appl Ichthyol 26:263267.Google Scholar
Dean, MN, Summers, AP. 2006. Mineralised cartilage in the skeleton of chondrichthyan fishes. Zoology 109:164168.Google Scholar
Didier, DA, LeClair, EE, Vanbuskirk, DR. 1998. Embryonic staging and external features of development of the Chimaeroid fish, Callorhinchus milii (Holocephali, Callorhinchidae). J Morph 236:2547.Google Scholar
Eames, BF, Allen, N, Young, J, Kaplan, A, Helms, J, Schneider, R. 2007. Skeletogenesis in the swell shark Cephaloscyllium ventriosum. J Anat 210:542554.Google Scholar
Eames, BF, Helms, J a. 2004. Conserved molecular program regulating cranial and appendicular skeletogenesis. Dev Dyn 231:413.Google Scholar
Eames, BF, Sharpe, PT, Helms, JA. 2004. Hierarchy revealed in the specification of three skeletal fates by Sox9 and Runx2. Dev Biol 274:188200.Google Scholar
Egerbacher, M, Helmreich, M, Mayrhofer, E, Böck, P. 2006. Mineralisation of the hyaline cartilage in the small-spotted dogfish Scyliorhinus canicula L. Scr Medica 79:199212.Google Scholar
Enault, S, Adnet, S, Debiais-Thibaud, M. 2016. Skeletogenesis during the late embryonic development of the catshark Scyliorhinus canicula (Chondrichthyes; Neoselachii). Morphomuseum J 1:17.Google Scholar
Enault, S, Muñoz, DN, Silva, WTAF, 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. Front Genet 6:114.CrossRefGoogle ScholarPubMed
Fleming, A, Kishida, MG, Kimmel, CB, Keynes, RJ. 2015. Building the backbone: The development and evolution of vertebral patterning. Development 142:17331744.Google Scholar
Freitas, R, Zhang, G, Cohn, MJ. 2006. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442:10331037.Google Scholar
Gadow, H, Abbott, EC. 1895. On the Evolution of the Vertebral Column. Phil Trans R Soc London B 186:163221.Google Scholar
Giles, S, Rücklin, M, Donoghue, PCJ. 2013. Histology of ‘placoderm’ dermal skeletons: Implications for the nature of the ancestral gnathostome. J Morph 274:627644.Google Scholar
Gillis, JA, Dahn, RD, Shubin, NH. 2009. Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. Proc Natl Acad Sci USA 106:57205724.Google Scholar
Gillis, JA, Modrell, MS, Baker, CVH. 2013. Developmental evidence for serial homology of the vertebrate jaw and gill arch skeleton. Nat Comm 4:1436.Google Scholar
Gómez-Picos, P, Eames, BF. 2015. On the evolutionary relationship between chondrocytes and osteoblasts. Front Genet 6:115.Google Scholar
Goodrich, ES. 1930. Studies on the Structure and Development of Vertebrates. London: Macmillan.Google Scholar
Hall, BK. 2015. Bones and Cartilage. 2nd edition. Amsterdam: Elsevier-Academic Press.Google Scholar
Hall, BK, Gillis, JA. 2013. Incremental evolution of the neural crest, neural crest cells and neural crest-derived skeletal tissues. J Anat 222:1931.CrossRefGoogle ScholarPubMed
Hall, BK, Miyake, T. 2000. All for one and one for all: Condensations and the initiation of skeletal development. BioEssays 22:138147.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Hasse, C. 1879. Das natürliche System der Elasmobranchier auf Grundlage des Baues und der Entwicklung ihrer Wirbelsäule. Eine morphologische und paläontologische Studie. Jena. https://doi.org/10.5962/bhl.title.8431Google Scholar
Hecht, J, Stricker, S, Wiecha, U, Stiege, A, Panopoulou, G, Podsiadlowski, L, Poustka, AJ, Dieterich, C, Ehrich, S, Suvorova, J, Mundlos, S, Seitz, V. 2008. Evolution of a core gene network for skeletogenesis in chordates. PLoS Genet 4:e1000025.CrossRefGoogle ScholarPubMed
Hoenig, JM, Walsh, AH. 1982. The occurrence of cartilage canals in shark vertebrae. Can J Zool Can Zool 60(3): 483485.Google Scholar
Huang, R, Zhi, Q, Brand-Saberi, B, Christ, B. 2000. New experimental evidence for somite resegmentation. Anat Embryol (Berl) 202:195200.Google Scholar
Hunziker, EB, Kapfinger, E, Geiss, J. 2007. The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthr Cartil 15:403413.Google Scholar
Jandzik, D, Garnett, AT, Square, T, Cattell, MV, Yu, J-K, Medeiros, DM, Yu -Kai, , Medeiros, DM. 2014. Evolution of the new vertebrate head by co-option of an ancient chordate skeletal tissue. Nature 518:534537.Google Scholar
Janvier, P. 1996. Early Vertebrates. New York: Oxford University Press Inc.Google Scholar
Janvier, P, Arsenault, M, Desbiens, S. 2004. Calcified Cartilage in the Paired Fins of the Osteostracan Escuminaspis laticeps (Traquair 1880), from the Late Devonian of Miguasha (Québec, Canada), with a consideration of the early evolution of the pectoral fin endoskeleton in vertebrates. J Vert Paleo 24:773779.Google Scholar
Janvier, P, Pradel, A. 2015. Elasmobranchs and their extinct relatives: Diversity, relationships, and adaptations through time. In: Shadwick, RE, Farell, AP, Brauner, CJ, editors. Physiology of Elasmobranch Fishes: Structure and Interaction with Environment. London: Academic Press. pp.117.Google Scholar
Johanson, Z, Boisvert, CA, Maksimenko, A, Currie, P, Trinajstic, K. 2015. Development of the Synarcual in the Elephant Sharks (Holocephali; Chondrichthyes): Implications for Vertebral Formation and Fusion. PLoS ONE 10:e0135138.CrossRefGoogle ScholarPubMed
Kemp, NE, Westrin, SK. 1979. Ultrastructure of calcified cartilage in the endoskeletal tesserae of sharks. J Morph 160:75109.Google Scholar
Kuratani, S, Horigome, N. 2000. Developmental morphology of branchiomeric nerves in a cat shark, Scyliorhinus torazame, with special reference to rhombomeres, cephalic mesoderm, and distribution patterns of cephalic crest cells. Zool Sci 17:893909.CrossRefGoogle Scholar
Leprévost, A, Sire, J-Y. 2014. Architecture, mineralisation and development of the axial skeleton in Acipenseriformes, and occurrences of axial anomalies in rearing conditions; can current knowledge in teleost fish help? J Appl Ichthyol 30:767776.Google Scholar
Luer, CA, Walsh, CJ, Bodine, AB, Wyffels, JT. 2007. Normal embryonic development in the clearnose skate, Raja eglanteria, with experimental observations on artificial insemination. Environ Biol Fishes 80:239255.Google Scholar
Maisey, JG. 1988. Phylogeny of early vertebrate skeletal induction and ossification patterns. In: Hecht, MK,Wallace, B, Prance, GT, editors. Evolutionary Biology. Springer US pp. 1–36.Google Scholar
Maisey, JG. 2013. The diversity of tessellated calcification in modern and extinct chondrichthyans. Rev Paleobiol 32:355371.Google Scholar
Meulemans, D, Bronner-Fraser, M. 2007. Insights from amphioxus into the evolution of vertebrate cartilage. PLoS ONE 2(8): e787.Google Scholar
Morin-Kensicki, EM, Melancon, E, Eisen, JS. 2002. Segmental relationship between somites and vertebral column in zebrafish. Development 129:38513860.Google Scholar
Moss, ML. 1977. Skeletal Tissues in Sharks. Am Zool 17:335342.Google Scholar
Omelon, S, Dean, MN, Masic, A, Georgiou, J, Fratzl, P. 2012. Evidence of polyphosphates and their distribution in active biological apatite mineralisation sites of stingray jaws. Bone 50:S99S100.Google Scholar
Onimaru, K, Marcon, L, Musy, M, Tanaka, M, Sharpe, J. 2016. The fin-to-limb transition as the re-organization of a Turing pattern. Nat Comm 7:11582.Google Scholar
Ortiz-Delgado, JB, Simes, DC, Viegas, CSB, Schaff, BJ, Sarasquete, C, Cancela, ML. 2006. Cloning of matrix Gla protein in a marine cartilaginous fish, Prionace glauca: Preferential protein accumulation in skeletal and vascular systems. Histochem Cell Biol 126:89101.CrossRefGoogle Scholar
Ørvig, T. 1951. Histologic studies of Placoderms and fossil Elasmobranchs. I: The endoskeleton, with remarks on the hard tissues of lower vertebrates in general. Ark för Zool 2:322.Google Scholar
O’Shaughnessy, KL, Dahn, RD, Cohn, MJ. 2015. Molecular development of chondrichthyan claspers and the evolution of copulatory organs. Nat Comm 6:6698.Google Scholar
Oulion, S, Borday-Birraux, V, Debiais-Thibaud, M, Mazan, S, Laurenti, P, Casane, D. 2011. Evolution of repeated structures along the body axis of jawed vertebrates, insights from the Scyliorhinus canicula Hox code. Evol Dev 13:247259.Google Scholar
Park, J, Gebhardt, M, Golovchenko, S, Perez-Branguli, F, Hattori, T, Hartmann, C, Zhou, X, deCrombrugghe, B, Stock, M, Schneider, H, von der Mark, K. 2015. Dual pathways to endochondral osteoblasts: A novel chondrocyte-derived osteoprogenitor cell identified in hypertrophic cartilage. Biol Open 4:608621.CrossRefGoogle ScholarPubMed
Peignoux-Deville, J, Bordat, C, Vidal, B, Bordatt, C, Vidal, B. 1989. Demonstration of bone cells in elasmobranchs: With osteoclasts resorbing. Bone 21:925933.Google Scholar
Peignoux-Deville, J, Lallier, F, Vidal, B. 1982. Evidence for the presence of osseous tissue in dogfish vertebrae. Cell Tissue Res 222:605614.Google Scholar
Porter, ME, Beltrán, JL, Koob, TJ, Summers, AP. 2006. Material properties and biochemical composition of mineralised vertebral cartilage in seven elasmobranch species (Chondrichthyes). J Exp Biol 209:29202928.Google Scholar
Restović, I, Vukojević, K, Paladin, A, Saraga-Babić, M, Bočina, I. 2015. Immunohistochemical studies of cytoskeletal and extracellular matrix components in dogfish Scyliorhinus canicula L. Notochordal cells. Anat Rec 298:17001709.Google Scholar
Ridewood, W. 1899. Some observations on the caudal diplospondyly of sharks. J Linn Soc London, Zool 27:4659.Google Scholar
Ridewood, WG. 1921. On the calcification of the vertebral centra in sharks and rays. Philos Trans R Soc Londonca 210:311407.Google Scholar
Roughley, P, Martens, D, Rantakokko, J, Alini, M, Mwale, F, Antoniou, J. 2006. The involvement of aggrecan polymorphism in degeneration of human intervertebral disc and articular cartilage. Eur Cells Mater 11:17.CrossRefGoogle ScholarPubMed
Rychell, AL, Swalla, BJ. 2007. Development and evolution of chordate cartilage. J Exp Zool B Mol Dev Evol 308B:325335.Google Scholar
Seidel, R, Lyons, K, Blumer, M, Zaslansky, P, Fratzl, P, Weaver, JC, Dean, MN. 2016. Ultrastructural and developmental features of the tessellated endoskeleton of elasmobranchs (sharks and rays). J Anat 229:681702.CrossRefGoogle ScholarPubMed
Smith, MM, Hall, BK. 1990. Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev 65:277373.Google Scholar
St-Jacques, B, Hammerschmidt, M, McMahon, AP. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13:20722086.Google Scholar
Summers, AP. 2000. Stiffening the stingray skeleton – An investigation of durophagy in myliobatid stingrays (Chondrichthyes, batoidea, myliobatidae). J Morph 243:113126.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Tarazona, OA, Slota, LA, Lopez, DH, Zhang, G, Cohn, MJ. 2016. The genetic program for cartilage development has deep homology within Bilateria. Nature 533:115.Google Scholar
Van der Kraan, PM, Van den Berg, WB. 2012. Chondrocyte hypertrophy and osteoarthritis: Role in initiation and progression of cartilage degeneration? Osteoarthr Cartil 20:223232.Google Scholar
Venkatesh, B, Kirkness, EF, Loh, Y-H, Halpern, AL, Lee, AP, Johnson, J, Dandona, N, Viswanathan, D, Tay, A, Venter, JC, Strausberg, RL, Brenner, S. 2007. Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol 5:e101.Google Scholar
Venkatesh, B, Lee, AP, Ravi, V, Maurya, AK, Lian, MM, Swann, JB, Ohta, Y, Flajnik, MF, Sutoh, Y, Kasahara, M, Hoon, S, Gangu, V, Roy, SW, Irimia, M, Korzh, V, Kondrychyn, I, Lim, ZW, Tay, B-H, Tohari, S, Kong, KW, Ho, S, Lorente-Galdos, B, Quilez, J, Marques-Bonet, T, Raney, BJ, Ingham, PW, Tay, A, Hillier, LW, Minx, P, Boehm, T, Wilson, RK, Brenner, S, Warren, WC. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174179.Google Scholar
Vonk, LA, Kroeze, RJ, Doulabi, BZ, Hoogendoorn, RJ, Huang, CL, Helder, MN, Everts, V, Bank, RA. 2010. Caprine articular, meniscus and intervertebral disc cartilage: An integral analysis of collagen network and chondrocytes. Matrix Biol 29:209218.CrossRefGoogle ScholarPubMed
Wang, N-Z, Donoghue, PCJ, Smith, MM, Sansom, I. 2005. Histology of the galeaspid dermoskeleton and endoskeleton, and the origin and early evolution of the vertebrate cranial endoskeleton. J Vert Paleo 25:745756.Google Scholar
Wurmbach, H. 1932. Das wachstum des selachierwirbels und seiner gewebe. Zool Jahrb (Abt Anat Ont Tiere) 55:1136.Google Scholar
Wyffels, J, King, BL, Vincent, J, Chen, C, Wu, CH, Polson, SW. 2014. SkateBase, an elasmobranch genome project and collection of molecular resources for chondrichthyan fishes. F1000Research 3:191.Google Scholar
Yang, G, Zhu, L, Hou, N, Lan, Y, Wu, X-M, Zhou, B, Teng, Y, Yang, X. 2014. Osteogenic fate of hypertrophic chondrocytes. Cell Res 24:12661269.CrossRefGoogle ScholarPubMed
Yang, L, Tsang, KY, Tang, HC, Chan, D, Cheah, KSE. 2014. Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation. Proc Nat Acad Sci 111:1209712102.Google Scholar
Zhang, G, Cohn, MJ. 2006. Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates. Proc Natl Acad Sci U S A 103:1682916833.Google Scholar
Zhou, X, von der Mark, K, Henry, S, Norton, W, Adams, H, de Crombrugghe, B. 2014. Chondrocytes transdifferentiate into osteoblasts in endochondral bone during development, postnatal growth and fracture healing in mice. PLoS Genet 10 0(12): e1004820.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×