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7 - Plasticity and Variation of Skeletal Cells and Tissues and the Evolutionary Development of Actinopterygian Fishes

Published online by Cambridge University Press:  31 December 2018

By
Brian K. Hall  and
P. Eckhard Witten
Edited by
Zerina Johanson ,
Charlie Underwood  and
Martha Richter
Zerina Johanson
Affiliation:
Natural History Museum, London
Charlie Underwood
Affiliation:
Birkbeck, University of London
Martha Richter
Affiliation:
Natural History Museum, London
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Summary

Plasticity of skeletal cells, tissues and organs is a general vertebrate character and rampant among teleost fishes. Plasticity is not restricted to early ontogeny but is evident throughout the entire life history. Epigenetic factors during development influence skeletal anatomy, mechanical properties of skeletal tissues and numbers of meristic characters such as vertebrae. Adult teleost skeletons demonstrate plasticity in functional adaptation, especially to mechanical forces and mechanical loading and to physiological factors such as temperature or the availability of minerals. Plasticity influences the character of skeletal tissues that can range from cartilage to acellular bone, as well as numbers of serial elements such as vertebrae, scales or fin rays. Variable numbers of vertebrae and the existence of vestiges, rudiments, atavisms and hyperostotic bones are discussed as examples of skeletal variation. Plasticity at the cellular level is best understood by recognising features of fish skeletal cells not seen in mammals, two of which are the absence of osteocytes in the acellular bone of most species of teleosts and the resorption of bone by mononucleated rather than multinucleated osteoclasts. A third is that mineral resorption in teleosts is phosphorous rather than calcium-based. The fourth is the variety of skeletal tissues that share features of bone and cartilage (chondroid bone, secondary cartilage) or between cartilage and notochord (chondroid) or of bone and dentine. Phenotypic plasticity of skeletal tissues is affected at the cellular level by modulation, transdifferentiation, metaplasia and remodelling. Plasticity of skeletal cells, tissues and organs has important consequences for skeletal development and evolution.

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Evolution and Development of Fishes , pp. 126 - 143
Publisher: Cambridge University Press
Print publication year: 2019

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References

Abzhanov, A, Protas, M, Grant, BR, Tabin, CR. 2004. Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305:1462–1465.Google Scholar
Adriaens, D, Devaere, S, Teugels, GG, Dekegel, B, Verraes, W. 2002. Intraspecific variation in limblessness in vertebrates: A unique example of microevolution. Biol J Linn Soc 75:367–377.Google Scholar
Albertson, RC, Streelman, JT, Kocher, TD. 2003. Genetic basis of adaptive shape differences in the cichlid head. J Hered 94:291–301.Google Scholar
Albertson, RC, Streelman, JT, Kocher, TD, Yelick, PC. 2005. Integration and evolution of the cichlid mandible: The molecular basis of alternate feeding strategies. Proc Natl Acad Sci USA 102:16287–16292.Google Scholar
Allard, B, Magloire, H, Couble, ML, Maurin, JC, Bleicher, F. 2006. Voltage-gated sodium channels confer excitability to human odontoblasts. Possible role in tooth pain transmission. J Biol Chem 281:29002–29010.Google Scholar
Amling, M, Takeda, S, Karsenty, G. 2000. A neuro (endo)crine regulation of bone remodeling. BioEssays 22:970–975.Google Scholar
Ando, D, Mano, S-I, Koide, N, Nakajima, M. 2008. Estimation of heritability and genetic correlation of number of abdominal and caudal vertebrae in masu salmon. Fish Sci 74:293–298.Google Scholar
Arratia, G, Schultze, H-P. 1992. Reevaluation of the caudal skeleton of certain actinopterygian fishes. III. Salmonidae. Homologization of caudal skeletal structures. J Morph 214:187–249.Google Scholar
Arratia, G, Schultze, H-P, Casciotta, J. 2001. Vertebral column and associated elements in dipnoans and comparison with other Fishes: Development and homology. J Morph 250:101–172.Google Scholar
Benjamin, M. 1986. The oral sucker of Gyrinocheilus aymonieri (Teleostei: Cypriniformes). J Zool London Ser B 1:211–254.Google Scholar
Benjamin, M. 1989a. Hyaline-cell cartilage (chondroid) in the heads of teleosts. Anat Embryol 179:285–303.Google Scholar
Benjamin, M. 1989b. The development of hyaline-cell cartilage in the head of the black molly, ‘Poecilia sphenops’. Evidence for secondary cartilage in a teleost. J Anat 164:145–154.Google Scholar
Benjamin, M. 1990. The cranial cartilages of teleosts and their classification. J Anat 169:153–172.Google Scholar
Benjamin, M., Rufai, A, Ralphs, JR. 2000. The mechanism of formation of bony spurs (enthesophytes) in the Achilles tendon. Arthr Rheum 43:576–583.Google Scholar
Bensimon-Brito, A, Cancela, ML, Huysseune, A, Witten, PE. 2012a. Vestiges, rudiments and fusion events: The zebrafish caudal fin endoskeleton in an evo-devo perspective. Evo Dev 14:116–127.Google Scholar
Bensimon-Brito, A, Cardeira, J, Cancela, ML, Huysseune, A, Witten, PE. 2012b. Distinct patterns of notochord mineralization in zebrafish coincide with the localization of Osteocalcin isoform 1 during early vertebral centra formation. BMC Dev Biol 12, 28:1–14.Google Scholar
Beresford, WA. 1981. Chondroid bone, Secondary Cartilage and Metaplasia. Baltimore-München: Urban and Schwarzenberg.Google Scholar
Beresford, WA. 1993. Cranial skeletal tissues: Diversity and evolutionary trends. In: Hanken, J, Hall, BK, editors. The Skull. Volume 2, Patterns of Structural and Systematic Diversity. Chicago: University of Chicago Press. pp. 69–130.Google Scholar
Bertram, JEA, Swartz, SM. 1991. The ‘Law of bone transformation’: A case of crying Wolff? Biol Rev Camb Phil Soc 66:245–273.CrossRefGoogle ScholarPubMed
Bird, NC, Mabee, PM. 2003. Developmental morphology of the axial skeleton of the zebrafish Danio rerio (Ostariophysi: Cyprinidae). Dev Dyn 228: 337–357.Google Scholar
Bonewald, LF 2004. Osteocyte biology: Its implications for osteoporosis. J Musculoskel Neuron Inter 4:101–104.Google Scholar
Bonucci, E. 2009. The osteocyte: The underestimated conductor of the bone orchestra. Rend Fis Acc Lincei 20: 237–254.Google Scholar
Boot-Handford, RP, Tuckwell, DS. 2003. Fibrillar collagen: The key to vertebrate evolution? BioEssays 25: 142–151.Google Scholar
Boyce, BF, Yao, Z, Xing, L. 2009. Osteoclasts have multiple roles in bone in addition to bone resorption. Crit Rev Eukar Gene 19: 171–180.Google Scholar
Brakefield, PM, Wijngaarden, PJ. 2003. Phenotypic Plasticity. In: Hall, BK, Olson, WM, editors. Keywords and Concepts in Evolutionary Developmental Biology. Cambridge, MA: Harvard University Press. pp. 288–297.Google Scholar
Brooks, S, Johnston, IA. 1994. Temperature and somitogenesis in embryos of the plaice (Pleuronectes platessa). J Fish Biol 45:699–702.Google Scholar
Burger, EH, Klein-Mullend, J, Van Der Plas, A. 1995. Function of osteocytes in bone – Their role in mechanotransduction. J Nutrit 125 Suppl:202S–2023S.Google Scholar
Burger, EH, Klein-Mullend, J, Smith, TH. 2003. Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon – A proposal. J Biomech 36:1453–1459.Google Scholar
Carroll, RL. 1988. Vertebrate Paleontology and Evolution. New York: W. H. Freeman and Company.Google Scholar
Cole, AG. 2011. A review of diversity in the evolution and development of cartilage: The search for the origin of chondrocytes. Eur Cells Mat 21:122–129.Google Scholar
Cole, AG, Hall, BK. 2004a. Cartilage is a metazoan tissue: Integrating data from non-vertebrate sources. Acta Zool 85:65–80.Google Scholar
Cole, AG, Hall, BK. 2004b. The nature and significance of invertebrate cartilages revisited: Distribution and histology of cartilage and cartilage-like tissues within the Metazoa. Zoology 107: 261–274.Google Scholar
Cole, NJ, Tanaka, M, Prescott, A, Tickle, C. 2003. Expression of limb initiation genes and clues to the morphological diversification of threespine sticklebacks. Curr Biol 13:R951–R952.Google Scholar
Connolly, MH, Hall, BK. 2008. Embryonic heat shock reveals latent hsp90 translation in zebrafish (Danio rerio). Int J Dev Biol 52: 71–77.Google Scholar
Currey, JD. 2010. Mechanical properties and adaptations of some less familiar bony tissues. J Mech Behav Biomed Mat 3:357–372.Google Scholar
Currey, JD, Shahar, R. 2013. Cavities in the compact bone in tetrapods and fish and their effect on mechanical properties. J Struct Biol 183:107–122.Google Scholar
Danos, N, Staab, KL. 2010. Can mechanical forces be responsible for novel bone development and evolution in fishes? J Appl Ichthyol 26:156–161.Google Scholar
Darwin, C. 1859. The Origin of Species. The Harvard Classics. Reprint of the 6th edition from 1872. New York: P. F. Collier and Son 1909.Google Scholar
Dean, MN, Ekstrom, L, Monsonego-Ornan, E, Ballantyne, J, Witten, PE, et al. 2015. Mineral homeostasis and regulation of mineralization processes in the skeletons of sharks, rays and relatives (Elasmobranchii). Sem Cell Dev Biol 46:51–67.Google Scholar
De Schepper, N, Adriaens, D, Teugels, GG, Devaere, S, Verraes, W. 2004. Intraspecific variation in the postcranial skeleton morphology in African clariids: A case study of extreme phenotypic plasticity. Zool J Linn Soc 140: 437–446.Google Scholar
Deschamps, MH, Labbe, L, Baloche, S, Fouchereau-Peron, M, Dufour, S, Sire, JY. 2009. Sustained exercise improves vertebral histomorphometry and modulates hormonal levels in rainbow trout. Aquaculture 296: 337–346.Google Scholar
Dewit, J, Witten, PE, Huysseune, A. 2011. The mechanism of cartilage subdivision in the reorganization of the zebrafish pectoral fin endoskeleton. J Exp Zool B Mol Dev Evol 316:584–597.Google Scholar
Don, EK, Currie, PD, Cole, NJ. 2013. The evolutionary history of the development of the pelvic fin/hindlimb. J Anat 222:114–133.Google Scholar
Don, EK, Hall, TE, Currie, PD, Cole, NJ. 2011. Morphology of pelvic fin loss in a zebrafish strain (Danio rerio). J Morph 272: 583–589.Google Scholar
Eastman, JT. 1979. The caudal skeletons of catostomid fishes. Am Midl Nat 103:133–148.Google Scholar
Ekanayake, S, Hall, BK. 1987. The development of acellularity of the vertebral bone of the Japanese medaka, Oryzias latipes (Teleostei; Cyprinidontidae). J Morph 193:253–261.Google Scholar
Ekanayake, S, Hall, BK. 1988. Ultrastructure of the osteogenesis of acellular vertebral bone in the Japanese medaka, Oryzias latipes (Teleostei, Cyprinidontidae). Am J Anat 182:241–249.CrossRefGoogle ScholarPubMed
Estêvão, MD, Silva, N, Redruello, B, Costa, R, Gregorio, S, Canario, AVM, Power, DM. 2011. Cellular morphology and markers of cartilage and bone in the marine teleost Sparus auratus. Cell Tissue Res 343: 619–635.Google Scholar
Favaloro, E, Mazzola, A. 2003. Meristic variation and skeletal anomalies of wild and reared sharpsnout seabream juveniles (Diplodus puntazzo, Cetti 1777) off coastal Sicily, Mediterranean Sea. Aquacult Res 34:575–579.Google Scholar
Ferreri, F, Nicolais, C, Boglione, C, Bertolini, B. 2000. Skeletal characterization of wild and reared zebrafish: Anomalies and meristic characters. J Fish Biol 56:1115–1128.Google Scholar
Fiaz, AW, Léon-Kloosterziel, KM, Gort, G, Schulte-Merke, S, van Leeuwen, JL, Kranenbarg, S. 2012. Swim-training changes the spatio-temporal dynamics of skeletogenesis in zebrafish larvae (Danio rerio). PLoS ONE 7(4):e34072.Google Scholar
Fiaz, AW, van Leeuwen, JL, Kranenbar, S. 2010. Phenotypic plasticity and mechano-transduction in the teleost skeleton. J Appl Ichthyol 26: 289–293.Google Scholar
Fidler, AL, Vanacore, RM, Chetyrkib, SV, Bhave, G, Yin, VP, et al. 2013. A unique covalent bond in basement membrane is a primordial innovation for tissue evolution. Proc Natl Acad Sci USA. 111:331–336.Google Scholar
Fjelldal, PG, Grotmol, S, Kryvi, H, Gjerdet, NR, Taranger, GL, et al. 2004. Pinealectomy induces malformation of the spine and reduces the mechanical strength of the vertebrae in Atlantic salmon, Salmo salar. J Pineal Res 36:132–139.Google Scholar
Forsman, A. 2015. Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115:276–284.Google Scholar
Fowler, JA. 1970. Control of vertebral number in teleosts – An embryological problem. Quart Rev Biol 45:148–167.Google Scholar
Franz-Odendaal, T, Hall, BK, Witten, PE. 2006. Buried alive: How did osteoblasts become osteocytes Dev Dyn 235:176–190.Google Scholar
Galea, GL, Lanyon, LE, Price, JS. 2017. Sclerostin’s role in bone’s adaptive response to mechanical loading. Bone 96:38–44.Google Scholar
Gatesy, J, Amato, G, Norell, M, DeSalle, R, Hayashi, C. 2003. Combined support for wholesale taxic atavism in gavialine crocodylians. Syst Biol 52:403–422.Google Scholar
Geurtzen, K, Knopf, F, Wehner, D, Huitema, LF, Schulte-Merker, S, Weidinger, G 2014. Mature osteoblasts dedifferentiate in response to traumatic bone injury in the zebrafish fin and skull. Development 141: 2225–2234.Google Scholar
GiarratanaF, RA, Muscolino, D, Marino, F, Gallo, M, Panebianco, A. 2012. Occurrence of hyperostotic pterygiophores in the silver scabbardfish, Lepidopus caudatus (Actinopterygii: Perciformes: Trichiuridae). Acta Ichthyol Piscata 42:233–237.Google Scholar
Gillis, JA, Witten, PE, Hall, BK, 2006. Chondroid Bone and secondary cartilage contribute to apical dentary growth in juvenile Atlantic salmon, Salmo salar Linnaeus (1758). J Fish Biol 68:1133–1143.Google Scholar
Gomez, C, Özbudak, EM, Wunderlich, J, Baumann, D, Lewis, J, Pourquié, O. 2008. Control of segment number in vertebrate embryos. Nature 454:335–339.Google Scholar
Gorodilov, YN. 2004. Studies of temporal and spatial peculiarities of somitogenesis in fish embryos. Russ J Dev Biol 35:92–105.Google Scholar
Gosline, WA. 1961. The perciform caudal skeleton. Copeia 1961:265–270.Google Scholar
Greenwood, PH. 1965. Environmental effects on the pharyngeal mill of a cichlid fish, Astatoreochromis alluaudi, and their taxonomic implications. Proc Linn Soc Lond 176:1–10.Google Scholar
Grünbaum, T, Cloutier, R. 2010. Ontogeny, variation, and homology in Salvelinus alpinus caudal skeleton (Teleostei: Salmonidae). J Morph 271:12–24.Google Scholar
Grünbaum, T, Cloutier, R, Vincent, B 2012. Dynamic skeletogenesis in fishes: Insight of exercise training on developmental plasticity. Dev Dyn 241:1507–1524.Google Scholar
Gunter, H, Meyer, A. 2014. Molecular investigation of mechanical strain-induced phenotypic plasticity in the ecologically important pharyngeal jaws of cichlid fish. J Appl Ichthyol 30:630–635.Google Scholar
Gunter, HM, Xiong, F, Franchini, P, Fruciano, C, Meyer, A. 2013. Shaping development through mechanical strain: The transcriptional basis of diet-induced phenotypic plasticity in a cichlid fish. Mol Ecol 22:4516–4531.Google Scholar
Hall, BK. 1970. Cellular differentiation in skeletal tissues. Biol Rev Camb Philos Soc 45: 455–484.Google Scholar
Hall, BK. 1983. Epigenetic control in development and evolution. In: Goodwin, BC, Holder, N, Wylie, CC, editors. Development and Evolution. Cambridge: Cambridge University Press. pp. 353–379.Google Scholar
Hall, BK. 1984. Developmental mechanisms underlying the formation of atavisms. Biol Rev Camb Philos Soc 59:89–124.Google Scholar
Hall, BK. 1990. Genetic and epigenetic control of vertebrate embryonic development. Nether J Zool 40:352–361.Google Scholar
Hall, BK. 2000. The evolution of the neural crest in vertebrates. In: Olsson, L, Jacobson, CO, editors. Regulatory Processes in Development. Wenner-Gren International Series, Volume 76. London: The Portland Press. pp. 101–113.Google Scholar
Hall, BK. 2003. Descent with modification: The unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol Rev Camb Philos Soc 78: 409–43.Google Scholar
Hall, BK. 2004. Evolution as the Control of Development by Ecology. In: Hall, BK, Pearson, R, Müller, GB, editors. Environment, Evolution and Development: Towards a Synthesis. Cambridge: Mit Press. pp. ix–xxiii.Google Scholar
Hall, BK. 2005. Bones and Cartilage. Developmental and Evolutionary Skeletal Biology. San Diego: Elsevier Academic Press.Google Scholar
Hall, BK. 2007a. Homoplasy and homology: Dichotomy or continuum? J Human Evol 52:473–479.Google Scholar
Hall, BK. 2007b. Homology and Homoplasy. In: Matthen, M, Stephens, C, editors. Handbook of the Philosophy of Science. London: Elsevier. pp. 429–453.Google Scholar
Hall, BK. 2009. The Neural Crest and Neural Crest Cells in Vertebrate Development and Evolution. New York: Springer.Google Scholar
Hall, BK. 2010. Charles Darwin, embryology, evolution and skeletal plasticity. J Appl Ichthyol 26:148–151.Google Scholar
Hall, BK. 2011 . A Brief History of the Term and Concept Epigenetics. In: Hallgrîmsson, B, Hall, BK, editors. Epigenetics: Linking Genotype and Phenotype in Development and Evolution. Berkeley: University of California Press. pp. 9–13.Google Scholar
Hall, BK. 2014. Endoskeleton/exo (dermal) skeleton – Mesoderm/neural Crest: Two pair of problems and a shifting paradigm. J Appl Ichthyol 30: 608–615.Google Scholar
Hall, BK. 2015. Bones and Cartilage. Developmental and Evolutionary Skeletal Biology. 2nd edition. San Diego: Elsevier Academic Press.Google Scholar
Hall, BK, Kerney, R. 2012. Levels of biological organization and the origin of novelty. J Exp Zool Mol Dev Evol 318B:428–437.Google Scholar
Hall, BK, Witten, PE. 2007. Plasticity of and Transitions between Skeletal Tissues in Vertebrate Evolution and Development. In: Anderson, JS, Sues, HD, editors. Major Transitions in Vertebrate Evolution. Bloomington: Indiana University Press. pp. 13–56.Google Scholar
Hanken, J, Wake, DB 1993 Adaptation of bone growth to miniaturisation of body size. In: Hall, BK, editor, Bone, vol. 7. Boca Raton: CRC Press. pp. 79–104.Google Scholar
Harris, MP, Henke, K, Hawkins, MB, Witten, PE. 2014. Fish is fish: The use of experimental model species to reveal causes of skeletal diversity in evolution and disease. J Appl Ichthyol 30:616–629.Google Scholar
Harris, MP, Rohner, N, Schwarz, H, Perathoner, S, Konstantinidis, P, Nüsslein-Volhard, C. 2008. Zebrafish eda and edar mutants reveal conserved and ancestral roles of ectodysplasin signaling in vertebrates. PLoS Genet 410: e1000206.Google Scholar
Hegrenes, S. 2010. Diet-induced phenotypic plasticity of feeding morphology in the orange spotted sunfish, Lepomis humilis. Ecol Freshwater Fish 10:35–42.Google Scholar
Hollander, J, Snell-Rood, E, Foster, S. 2015. Editorial. New frontiers in phenotypic plasticity and evolution. Heredity 115:273–275.Google Scholar
Hunt von Herbing, I. Miyake, T, Hall, BK, Boutilier, RG 1996a. The ontogeny of feeding and respiration in larval Atlantic cod, Gadus morhua (Teleostei; Gadiformes): (1) Morphology. J Morph 227:15–35.Google Scholar
Hunt von Herbing, I. Miyake, T, Hall, BK, Boutilier, RG. 1996b. The ontogeny of feeding and respiration in larval Atlantic cod, Gadus morhua (Teleostei; Gadiformes): (2) Function. J Morph 227:37–50.Google Scholar
Huxley, TH. 1859. Observations on the development of some parts of the skeleton of fishes. Q J Microsc Sci 7:33–46.Google Scholar
Huysseune, A. 1986. Late skeletal development at the articulation between upper pharyngeal jaws and neurocranial base in the fish, Astatotilapia elegans, with the participation of a chondroid form of bone. Am J Anat 177:119–137.Google Scholar
Huysseune, A. 2000. Skeletal system. In: Ostrander, GK, editor. The Laboratory Fish. Part 4, Microscopic Functional Anatomy. San Diego: Academic Press. pp. 307–317.Google Scholar
Huysseune, A, Sire, JY. 1990. Ultrastructural observations on chondroid bone in the teleost fish Hemichromis bimaculatus. Tissue Cell 22:371–383.Google Scholar
Huysseune, A, Sire, JY, Meunier, FJ. 1994. Comparative study of lower pharyngeal jaw structure in two phenotypes of Astatoreochromis alluaudi (Teleostei: Cichlidae). J Morph 221:25–43.Google Scholar
Huysseune, A, Takle, H, Soenens, M, Taerwe, K, Witten, PE. 2008. Unique and shared gene expression patterns in Atlantic salmon (Salmo salar) tooth development. Dev Genes Evol 218:427–437.Google Scholar
Huysseune, A, Verraes, W. 1986. Chondroid bone on the upper pharyngeal jaws and neurocranial base in the adult fish Astatotilapia elegans. Am J Anat 177:527–535.Google Scholar
Huysseune, A, Verraes, W. 1990. Carbohydrate histochemistry of mature chondroid bone in Astatotilapia elegans. (Teleostei: Cichlidae) with a compassion to acellular bone and cartilage. Ann Sci Nat Zool Paris 13 (11):29–43.Google Scholar
Janvier, P. 2015. Facts and fancies about early fossil chordates and vertebrates. Nature 520:483–489.Google Scholar
Jawad, LA. 2013. Hyperostosis in three fish species collected from the Sea of Oman. Anat Record 296:1145–1147.Google Scholar
Johnston, JA, Wilson, RS. 2002. Temperature-induced developmental plasticity in ectotherms. In Warburton, SJ, Burggren, WW, Pelster, B, Reiberand, CL, Spicer, J, editors. Comparative Developmental Physiology. Oxford: Oxford University Press, pp. 124–138.Google Scholar
Jordan, DS. 1982. Relations of temperature to vertebrae among fishes. Proc U S Natl Mus 14:231–253.Google Scholar
Karsenty, G, Ferron, M. 2012. The contribution of bone to whole-organism physiology. Nature 481:314–320.Google Scholar
Karsenty, G, Oury, F. 2012. Biology without walls: the novel endocrinology of bone. Annu Rev Physiol 74: 87–110.CrossRefGoogle ScholarPubMed
Kimmel, CB. 2014. Skull developmental modularity: A view from a single bone – or two. J Appl Ichthyol 30:600–607.Google Scholar
Kimmel, CB, Ballard, WW, Kimmel, SR, Ullmann, B, Schilling, TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310.Google Scholar
Knecht, AK, Hosemann, KE, Kingsley, DM. 2007. Constraints on utilization of the EDA-signaling pathway in threespine stickleback evolution. Evol Dev 9:141–154.Google Scholar
Knopf, F, Hammond, C, Chekuru, A, Kurth, T, Hans, S, et al. 2011. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev Cell 20:713–724.Google Scholar
Kölliker, A. 1859. On the different types in the microstructure of the skeletons of osseous fish. Proc R Soc Lond 9:656–668.Google Scholar
Kranenbarg, S, van Cleynenbreugel, T, Schipper, H, van Leeuwen, J. 2005. Adaptive bone formation in acellular vertebrae of sea bass (Dicentrarchus labrax L.). J Exp Biol 208:3494–3502.Google Scholar
Laerm, J. 1976. The development, function, and design of amphicoelous vertebrae in teleost fishes. Zool J Linn Soc 58:237–254.Google Scholar
Lauder, GV. 1983. Functional design and evolution of the pharyngeal jaw apparatus in euteleostean fishes. Zool J Linn Soc 77:1–33.Google Scholar
Liem, KF. 1973. Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws. Syst Zool 22:425–441.Google Scholar
Magloire, H, Couble, ML, Romeas, A, Bleicher, F 2004. Odontoblast primary cilia: Facts and hypotheses. Cell Biol Intern 28:93–99.Google Scholar
Maisey, JG. 1988. Phylogeny of early vertebrate skeletal induction and ossification patterns. Evol Biol 23:1–36.Google Scholar
Maisey, JG. 2000. Discovering Fossil Fishes. Boulder: Westview Press.Google Scholar
McDowall, RM. 2003. Variation in vertebral number in galaxiid fishes (Teleostei: Galaxiidae): A legacy of life history, latitude and length. Envir Biol Fishes 66:361–381.Google Scholar
Metscher, BD, Ahlberg, PE. 2001. Origin of teleost tail: Phylogenetic frameworks for developmental studies. In Ahlberg, PE, editor. Major Events in Early Vertebrate Evolution – Paleontology, Phylogeny, Genetics and Development. London: Taylor and Francis, pp. 333–349.Google Scholar
Meunier, FJ. 2002. Skeleton. In Panfili, J, de Pontual, H, Troadec, H, Wright, PJ, editors, Manual of Fish Sclerochronology. Brest: Ifremer-IRD Co-edition, pp. 65–88.Google Scholar
Meunier, FJ. 2011. The Osteichthyes, from the Paleozoic to the extant time, through histology and palaeohistology of bony tissues. Comp Rend Palevol 1:347–355.Google Scholar
Meunier, FJ, Desse, G. 1986. Les hyperostoses chez les téleosténs: Description, histologie et problèmes étiologiques. Ichthyophys Acta 10:130–142.Google Scholar
Meunier, FJ, Huysseune, A 1992. The concept of bone tissue in Osteichthyes. Nether J Zool 42:445–458.Google Scholar
Meyer, A. 1987a. Phenotypic plasticity and heterochrony in Cichlasoma manganese (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41:1357–1369.Google Scholar
Meyer, A. 1987b. Morphologic measurements from specimens and their X-rays: Test of a method for the study of allometry and phenotypic plasticity in fishes. Nether J Zool 37:315–321.Google Scholar
Meyer, A. 1999. Homology and homoplasy: The retention of genetic programmes. In Bock, GR, Cardew, G, editors. Homology. Chichester: John Wiley and Sons, pp. 141–157.Google Scholar
Meyer, A, Ritchie, PA, Witte, KE. 1995. Predicting developmental processes from phylogenetic patterns: A molecular phylogeny of the zebrafish (Danio rerio) and its relatives. Phil Trans Ther Soc Biol 349:103–111.Google Scholar
Mitton, JB, Koehn, RK. 1976. Morphological adaptation to thermal stress in a marine fish, Fundulus heteroclitus. Biol Bull 151:540–559.Google Scholar
Moczek, A P. 2015. Developmental plasticity and evolution – Quo vadis? Heredity 215:302–305.Google Scholar
Morin-Kensicki, EM, Melancon, E, Eisen, JS. 2002. Segmental relationship between somites and vertebral column in zebrafish. Development 129: 3851–3860.Google Scholar
Moriyama, Y, Kawanishi, T, Nakamura, R, Tsukahara, T, Sumiyama, K, et al. 2012. The Medaka zic1/zic4 mutant provides molecular insights into teleost caudal fin evolution. Curr Biol 22:601–607.Google Scholar
Moss, ML. 1961a. Studies of the acellular bone of teleost fish. I. Morphological and systematic variations. Acta Anat 46:343–462.Google Scholar
Moss, ML. 1961b. Osteogenesis of acellular teleost fish bone. Am J Anat 108:99–110.Google Scholar
Moss, ML. 1962. Studies of the acellular bone of teleost fish. II. Response to fracture under normal and acalcemic variations. Acta Anat 48:46–60.Google Scholar
Moss, ML. 1963. The biology of acellular teleost bone. Ann NY Acad Sci 109:337–350.Google Scholar
Murray, CB, Beacham, TD. 1989. Responses of meristic characters in chum salmon (Oncorhynchus keta) to temperature changes during development. Can J Zool 67:596–600.Google Scholar
Nelson, JS. 1989–1990. Analysis of the multiple occurrence of pelvic fin absence in extant fishes. Matsya 15–16:21–38.Google Scholar
Nordvik, K, Kryvi, H, Totland, GK, Grotmol, S. 2005. The salmon vertebral body develops through mineralization of two preformed tissues that are encompassed by two layers of bone. J Anat 206:103–114.Google Scholar
Parenti, LR. 1986. The phylogenetic significance of bone types in the euteleost fishes. Zool J Linn Soc 87:37–51.Google Scholar
Parsons, KJ, Marquez, E, Albertson, RC. 2012. Constraint and opportunity: The genetic basis and evolution of modularity in the cichlid mandible. Amer Nat 179:1–15.Google Scholar
Pigliucci, M, Murren, C, Schlichting, CD. 2006. Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209: 2362–2367.Google Scholar
Pourquié, O. 2011. Vertebrate segmentation: From cyclic gene networks to scoliosis. Cell 145:650–663.Google Scholar
Raikow, RJ, Borecky, SR, Berman, SL. 1979. The evolutionary re-establishment of a lost ancestral muscle in the bowerbird assemblage. Condor 81:203–206.Google Scholar
Reif, WE. 1982. Evolution of dermal skeleton and dentition in vertebrates. The odontode regulation theory. Evol Biol 304:287–368.Google Scholar
Resende, TP, Andrade, RP, Ferreira, M, Teillet, MA, Palmeirim, I. 2009. Sonic hedgehog: A new player in temporal control of somite formation. Mech Dev 126:S48–S49.Google Scholar
Ridewood, WG. 1921. On the calcification of the vertebral centra in sharks and rays. Phil Trans R Soc London Ser B Biol Sci 210:312–407.Google Scholar
Rolvien, T, Nagel, F, Milovanovic, P, Wuertz, S, Marshall, PR et al. How the European eel (Anguilla anguilla) loses its skeletal framework across lifetime. Proc R Soc Lond B Biol Sci 283:20161550.Google Scholar
Roux, W. 1881. Der züchtende Kampf der Teile, oder die “Tei-lauslee” im Organismus (Theorie der “funktionellen Anpassung”). Leipzig: Wilhelm Engelmann.Google Scholar
Ruff, C, Holt, B, Trinkaus, E. 2006. Who’s afraid of the big bad Wolff? “Wolff’s Law” and bone functional adaptation. Amer J Phys Anthrop 129:484–498.Google Scholar
Sambraus, F, Glover, KA, Hansen, T, Fraser, TWK, Solberg, MF, Fjelldal, PG. 2014. Vertebra deformities in wild Atlantic salmon caught in the Figgjo River, southwest Norway. J Appl Ichthyol 30:777–782.Google Scholar
Sanger, TJ, McCune, AR. 2002. Comparative osteology of the Danio (Cyprinidae: Ostariophysi) axial skeleton with comments on Danio relationships based on molecules and morphology. Zool J Linn Soc. 135:529–546.Google Scholar
Schaffer, J. 1930. Die Stutzbeweße. In: von Mallendorff, W, editor. Handbuch der Mikroskopischen Anatomie des Mensche, Volume 2, Part 2. Berlin: Springer-Verlag. pp. 338–350.Google Scholar
Schultze, HP, Arratia, G. 2013. The caudal skeleton of basal teleosts, its conventions, and some of its major evolutionary novelties in a temporal dimension. In: Arratia, G, Schultze, HP, Wilson, MVH, editors. Mesozoic Fishes. Volume 5, Global Diversity and Evolution. München: Verlag Dr. Friedrich Pfeil. pp. 187–246.Google Scholar
Scott, A, Stemple, DL. 2004. Zebrafish notochordal basement membrane: Signaling and structure. Curr Top Devel Biol 65:229–253.Google Scholar
Sfakianakis, DG, Leris, I, Laggis, A, Kentouri, M. 2011. The effect of rearing temperature on body shape and meristic characters in zebrafish (Danio rerio) juveniles. Env Biol Fishes 92:197–205.Google Scholar
Shkil, FN, Kapitanova, DV, Borisov, VB, Abdissa, B, Smirnov, SV. 2012. Thyroid hormone in skeletal development of cyprinids: Effects and morphological consequences. J Appl Ichthyol 28:398–405.Google Scholar
Shkil, FN, Levin, BA, Abdissa, B, Smirnov, SV. 2010. Variability in the number of tooth rows in the pharyngeal dentition of Barbus intermedius (Teleostei; Cyprinidae): genetic, hormonal and environmental factors. J Appl Ichthyol 26:315–319.Google Scholar
Sire, JY, Huysseune, A. 2003. Formation of dermal skeletal and dental tissues in fish: A comparative and evolutionary approach. Biol Rev Camb Philos Soc 78:219–249.Google Scholar
Sire, JY, Huysseune, A, Meunier, FJ. 1990. Osteoclasts in teleost fish: Light and electron-microscopical observations. Cell Tissue Res 260:85–94.Google Scholar
Smirnov, SV, Dzerzhinskii, KF, Levin, BA. 2006. On the relationship between the scale number in the lateral line in the African barbel Barbus intermedius and the rate of ontogeny (by experimental data). J Ichthyol 46:129–132.Google Scholar
Smirnov, SV, Levin, BA. 2007. Reduced number of serial elements in the african barb Barbus intermedius with accelerated ontogeny: a new type of paedomorphosis. Dokl Biol Sci 413:140–142.Google Scholar
Smith, MM, Hall, BK. 1990. Developmental and evolutionary origins of vertebrate skeletogenic odontogenic tissues. Biol Rev Camb Philos Soc 65:277–374.Google Scholar
Smith, MM, Hall, BK. 1993. A developmental model for evolution of the vertebrate exoskeleton and teeth: The role of cranial and trunk neural crest. Evol Biol 27: 387–448.Google Scholar
Smith-Vaniz, WF, Carpenter, KE. 2007. Review of the crevalle jacks, Caranx hippos complex (Teleostei: Carangidae), with a description of a new species from West Africa. Fishery Bull 105:207–233.Google Scholar
Smith-Vaniz, WF, Kaufman, LS, Glowacki, J. 1995. Species-specific patterns of hyperostosis in marine teleost fishes. Mar Biol 121:573–580.Google Scholar
Sousa, S, Afonso, N, Bensimon-Brito, A, Fonseca, M, Simões, M, et al. 2011. Differentiated skeletal cells contribute to blastema formation during zebrafish fin regeneration. Development 138:3897–3905Google Scholar
Staab, KL, Hernandez, LP. 2010. Development of the cypriniform protrusible jaw complex: Constructional insights for evolution. J Morph 271:814–825.Google Scholar
Staab, KL, Holzman, R, Hernandez, LP, Wainwright, PC. 2012. Independently evolved upper jaw protrusion mechanisms show convergent hydrodynamic function in teleost fishes. J Exp Biol 215:1456–1463.Google Scholar
Standen, EM, Du, TY, Larsson, HCE. 2014. Developmental plasticity and the origin of tetrapods. Nature 513:54–58.Google Scholar
Stewart, TA, Hale, ME. 2013. First description of a musculoskeletal linkage in an adipose fin: Innovations for active control in a primitively passive appendage. Proc R Soc Lond B 280:2012–2159.Google Scholar
Stiassny, MLJ. 1992. Atavisms, phylogenetic character reversals, and the origin of evolutionary novelties. Nether J Zool 42:260–276.CrossRefGoogle Scholar
Stiassny, MLJ. 2003. Atavism. In: Hall, BK, Olson, WM, editors. Keywords and Concepts in Evolutionary and Developmental Biology. Cambridge, MA: Harvard University Press. pp. 10–14.Google Scholar
Swain, DP. 1992. The functional basis of natural selection for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. Evolution 46:987–997.Google Scholar
Swain, DP, Lindsey, CC. 1984. Selective predation for vertebral number of young sticklebacks, Gasterosteus aculeatus. Can J Fish Aquat Sci 41:1231–1233.Google Scholar
Tanaka, M, Hale, LA, Amores, A, Yan, YL, Cresko, WA, Suzuki, T, Postlethwait, JH. 2005. Developmental genetic basis for the evolution of pelvic fin loss in the pufferfish Takifugu rubripes. Dev Biol 281: 227–239.Google Scholar
Taylor, LH, Hall, BK, Cone, DK. 1993. Experimental infections of yellow perch (Perca flavescens) with Apophallus brevis (Digenia, Heterophyidae): Parasite invasion, encystment and bony ossicle development. Can J Zool 71:1886–1894.Google Scholar
Taylor, LH, Hall, BK, Miyake, T, Cone, DK. 1994. Ectopic ossicles associated with metacercaria of Apophallus brevis (Trematoda) in yellow perch, Perca flavescens (Teleostei): Development and identification of bone and chondroid bone. Anat Embryol 190:29–46.Google Scholar
To, TT, Witten, PE, Renn, J, Bhattacharya, D, Huysseune, A: Winkler, C. 2012. Rankl induced osteoclastogenesis leads to loss of mineralization in a medaka osteoporosis model. Development 139:141–150.Google Scholar
Totland, GK, Fjelldal, PG, Kryvi, H, Løkka, G, Wargelius, A, et al. 2011. Sustained swimming increases the mineral content and osteocyte density of salmon vertebral bone. J Anat 219:490–501.Google Scholar
van der Meulen, T. 2005. Epigenetics of the locomotory system in zebrafish. PhD thesis, Wageningen University, Wageningen, Netherlands.Google Scholar
Van Eeden, FJ, Granato, M, Schach, U, Brand, M, Furutani-Seiki, M, et al. 1996. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123:153–164.Google Scholar
Vatsa, A, Mizuno, D, Smit, TH, Schmidt, CF, Mackintosh, FC, Klein-Nulend, J. 2006. Bio imaging of intracellular NO production in single bone cells after mechanical stimulation. J Bone Min Res 21:1722–1728.Google Scholar
Vilizzi, L, Kovác, V. 2014. Alternate ontogenies and developmental plasticity: Implications for ecological and evolutionary studies on species complexes. Fish Fisheries 15:523–531.Google Scholar
Wada, H, Okuyama, M, Satoh, N, Zhang, S. 2006. Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny. Evol Dev 8:370–377.Google Scholar
Wainwright, SA. 2000. The animal axis. Amer Zool 40:19–27.Google Scholar
Wake, DB. 1979. The endoskeleton: the comparative anatomy of the vertebral column and ribs. In: Wake, MH, editor. Hyman’s Comparative Vertebrate Anatomy. 3rd edition. Chicago: University of Cicago Press. pp. 192–237.Google Scholar
Wang, S, Kryvi, H, Grotmol, S, Wargelius, A, Krossøy, K, et al. 2013. Mineralization of the vertebral bodies in Atlantic salmon (Salmo salar L.) is initiated segmentally in the form of hydroxyapatite crystal accretions in the notochord sheath. J Anat 223:159–170.Google Scholar
West-Eberhard, M J. 2003. Developmental Plasticity and Evolution. New York: Oxford University Press.Google Scholar
West-Eberhard, MJ. 2005a. Developmental plasticity and the origin of species differences. Proc Natl Acad Sci USA 102 (Suppl. 1): 6543–6549.Google Scholar
West-Eberhard, MJ 2005b. Phenotypic accommodation: Adaptive innovation due to developmental plasticity. J Exp Zool Mol Dev Evol 304B:610–618.Google Scholar
Wiley, EO, Fuiten, AM, Doosey, MH, Lohman, BK, Merkes, C, Azuma, M. 2015. The caudal skeleton of the zebrafish: Danio rerio, from a phylogenetic perspective: A polyural interpretation of homologous structures. Copeia 103:740–750.Google Scholar
Witmer, LM. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason, JJ, editor. Functional Morphology in Vertebrate Paleontology. Cambridge: Cambridge University Press. pp. 19–33.Google Scholar
Witten, PE. 1997. Enzyme histochemical characteristics of osteoblasts and mononucleated osteoclasts in a teleost fish with acellular bone (Oreochromis niloticus, Cichlidae). Cell Tissue Res 287:591–599.Google Scholar
Witten, PE, Hall, BK. 2002. Differentiation and growth of kype skeletal tissues in anadromous male Atlantic Salmon (Salmo salar). Int J Dev Biol 46:719–730.Google Scholar
Witten, PE, Hall, BK. 2003. Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): Remodelling and regression of the kype after spawning. J Anat 203:435–450.Google Scholar
Witten, PE, Hall, BK. 2015. Teleost skeletal plasticity: Modulation, adaptation and remodelling. Copeia 103:727–739.Google Scholar
Witten, PE, Hall, BK. in preparation. Evolution of the Notochord and Notochordal Cells. Boca Raton: CRC Press.Google Scholar
Witten, PE, Hall, BK, Huysseune, A. 2005. Are breeding teeth in Atlantic salmon a component of the drastic alterations of the oral facial skeleton? Arch Oral Biol 50: 213–217.Google Scholar
Witten, PE, Hansen, A, Hall, BK. 2001. Features of mono and multinucleated bone resorbing cells of the zebrafish Danio rerio and their contribution to skeletal development, remodeling and growth. J Morph 250:197–207.Google Scholar
Witten, PE, Huysseune, A. 2007. Mechanisms of Chondrogenesis and Osteogenesis in Fins. In: Hall, BK, editor. Fins into Limbs: Evolution, Development, and Transformation. Chicago: University of Chicago Press. pp. 79–92.Google Scholar
Witten, PE, Huysseune, A. 2009. A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev Camb Philos Soc 84:315–346.Google Scholar
Witten, PE, Huysseune, A, Franz-Odendaal, T, Fedak, T, Vickaryous, M, et al. 2004. Acellular teleost bone: Primitive or derived, dead or alive? Palaeo Assoc Newslett 55:37–41.Google Scholar
Witten, PE, Huysseune, A, Hall, BK. 2010. A practical approach for the identification of the many cartilaginous tissues in teleost fish. J Appl Ichthyol 26:257–262.Google Scholar
Witten, PE, Obach, A, Huysseune, A, Baeverfjord, G. 2006. Vertebrae fusion in Atlantic salmon (Salmo salar): Development, aggravation and pathways of containment. Aquaculture 258:164–172.Google Scholar
Witten, PE, Owen, MAG, Fontanillas, R, Soenens, M, McGurk, C, Obach, A. 2016. Primary phosphorous-deficiency in juvenile Atlantic salmon: The uncoupling of bone formation and mineralisation. J Fish Biol 88 690–708.Google Scholar
Witten, PE, Harris, MP, Huysseune, A, Winkler, C. 2017 Small Teleost Fish Provide New Insights into Human Skeletal Diseases. Meth Cell Biol 138:321–344.Google Scholar
Wolff, J. 1892. Das Gesetz der Transformation der Knochen. Berlin: Hirschwald A. Translation available as: Wolff, J. (1986) The Law of Bone Remodelling. Translated by Maquet, P. and Furlong, R.. Berlin: Springer Verlag.Google Scholar
Wund, MA. 2012. Assessing the impacts of phenotypic plasticity on evolution. Integ Comp Biol 52:5–15.Google Scholar
Wund, MA, Valena, S, Wood, S, Baker, JA. 2012. Ancestral plasticity and allometry in threespine stickleback reveal phenotypes associated with derived freshwater ecotypes. Biol J Linn Soc 105:573–583.Google Scholar
Yamanoue, Y, Setiamarga, DHE, Matsuura, K. 2010. Pelvic fins in teleosts: Structure, function and evolution. J Fish Biol 77:1173–1208.Google Scholar
Ytteborg, E, Torgersen, J, Baeverfjord, G, Tackle, H. 2010. Morphological and molecular characterization of developing vertebral fusions using a teleost model. BMC Physiol 10:13.Google Scholar
Ytteborg, E, Torgersen, J, Baeverfjord, G, Tackle, H. 2012. Four stages characterizing vertebral fusions in Atlantic salmon. J Appl Ichthyol 28:3–459.Google Scholar
Yu, T, Graf, M, Renn, J, Schartl, M, Larionova, D, et al. 2017. A vertebrate specific and essential role for sp7/osterix in osteogenesis revealed by gene knock-out in the teleost medaka. Development 144: 265–271.Google Scholar
Yurtseva, A, Lajus, D, Makhrov, A, Artamono, V. 2014. Atlantic salmon (Salmo salar L.) in the border of distribution range: Patterns of osteological variation. J Appl Ichthyol 30:721–727.Google Scholar

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