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Evolution of Skeletal Tissues

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Evolutionary Developmental Biology

Abstract

The vertebrate skeletal system is a central subject of research in evolutionary developmental biology. Morphological homologies of vertebrate skeletal elements can be traced in two separate systems: exoskeletons and endoskeletons. This separation is not necessarily linked to differences in histogenesis or to cell lineage origins: homologous bones can be formed through different types of ossification or from cells of different origin. The earliest skeleton that appeared in evolution was an endoskeleton consisting of a notochord and cartilage, likely having evolved through the elaboration of an ancestral developmental mechanism. The exoskeleton consisting of dermal bones first evolved in basal members of the gnathostome lineage, prior to the acquisition of the jaw. From this lineage, a group including jawed vertebrates newly acquired endoskeletal bones. Of the latter group, the chondrichthyans, or “cartilaginous fishes,” underwent a secondary reduction of these bony tissues. Endochondral ossification, in which osteoblasts produce bones inside of a cartilage template, was a new type of ossification and evolved in the osteichthyan lineage. These evolutionary processes based on the fossil record provide a framework for an understanding of the evolutionary developmental biology of vertebrate skeletal tissues based on developmental genetics.

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References

  • Arratia G, Schultze HP, Casciotta J (2001) Vertebral column and associated elements in dipnoans and comparison with other fishes: development and homology. J Morphol 250:101–172

    Article  CAS  Google Scholar 

  • Burke AC, Nowicki JL (2003) A new view of patterning domains in the vertebrate mesoderm. Dev Cell 4:159–165

    Article  CAS  Google Scholar 

  • Cattell M, Lai S, Cerny R, Medeiros DM (2011) A new mechanistic scenario for the origin and evolution of vertebrate cartilage. PLoS One 6:e22474

    Article  CAS  Google Scholar 

  • Chen D, Blom H, Sanchez S, Tafforeau P, Ahlberg PE (2016) The stem osteichthyan Andreolepis and the origin of tooth replacement. Nature 539:237–241

    Article  Google Scholar 

  • Clack JA (2012) Gaining ground: the origin and evolution of tetrapods, 2nd edn. Indiana University Press, Bloomington

    Google Scholar 

  • Debnath S, Yallowitz AR, McCormick J, Lalani S, Zhang T, Xu R, Li N, Liu Y, Yang YS, Eiseman M, Shim JH, Hameed M, Healey JH, Bostrom MP, Landau DA, Greenblatt MB (2018) Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature 562:133–139

    Article  CAS  Google Scholar 

  • Donoghue PCJ, Sansom IJ (2002) Origin and early evolution of vertebrate skeletonization. Microsc Res Tech 59:352–372

    Article  Google Scholar 

  • Giles S, Rücklin M, Donoghue PCJ (2013) Histology of “placoderm” dermal skeletons: implications for the nature of the ancestral gnathostome. J Morphol 274:627–644

    Article  Google Scholar 

  • Haines RW, Mohuiddin A (1968) Metaplastic bone. J Anat 103:527–538

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hall BK (2015) Bones and cartilage: developmental and evolutionary skeletal biology, 2nd edn. Academic, San Diego

    Google Scholar 

  • Hirasawa T, Kuratani S (2015) Evolution of the vertebrate skeleton: morphology, embryology, and development. Zool Lett 1:2

    Article  Google Scholar 

  • Hirasawa T, Kuratani S (2018) Evolution of the muscular system in tetrapod limbs. Zool Lett 4:27

    Article  Google Scholar 

  • Hirasawa T, Nagashima H, Kuratani S (2013) The endoskeletal origin of the turtle carapace. Nat Commun 4:2107

    Article  Google Scholar 

  • Janvier P (2007) Homologies and evolutionary transitions in early vertebrate history. In: Anderson JS, Sues HD (eds) Major transitions in vertebrate evolution. Indiana University Press, Bloomington, pp 57–121

    Google Scholar 

  • Keating JN, Marquart CL, Marone F, Donoghue PCJ (2018) The nature of aspidin and the evolutionary origin of bone. Nat Ecol Evol 2:1501–1506

    Article  Google Scholar 

  • Kuratani S, Oisi Y, Ota KG (2016) Evolution of the vertebrate cranium: viewed from the hagfish developmental studies. Zool Sci 33:229–238

    Article  Google Scholar 

  • Lauri A, Brunet T, Handberg-Thorsager M, Fischer AH, Simakov O, Steinmetz PR, Tomer R, Keller PJ, Arendt D (2014) Development of the annelid axochord: insights into notochord evolution. Science 345:1365–1368

    Article  CAS  Google Scholar 

  • Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, Mackem S, Carmeliet G, Kronenberg HM (2010) Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19:329–344

    Article  CAS  Google Scholar 

  • Ota KG, Fujimoto S, Oisi Y, Kuratani S (2011) Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish. Nat Commun 2:373

    Article  Google Scholar 

  • Pattappa G, Li Z, Peroglio M, Wismer N, Alini M, Grad S (2012) Diversity of intervertebral disc cells: phenotype and function. J Anat 221:480–496

    Article  CAS  Google Scholar 

  • Patterson C (1977) Cartilage bones, dermal bones and membrane bones, or the exoskeleton versus the endoskeleton. In: Andrews SM, Miles RS, Walker AD (eds) Problems in vertebrate evolution. Academic Press, London, pp 77–121

    Google Scholar 

  • Qu Q, Haitina T, Zhu M, Ahlberg PE (2015) New genomic and fossil data illuminate the origin of enamel. Nature 526:108–111

    Article  CAS  Google Scholar 

  • Ryll B, Sanchez S, Haitina T, Tafforeau P, Ahlberg PE (2014) The genome of Callorhinchus and the fossil record: a new perspective on SCPP gene evolution in gnathostomes. Evol Dev 16:123–124

    Article  CAS  Google Scholar 

  • Sire JY, Donoghue PCJ, Vickaryous MK (2009) Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. J Anat 214:409–440

    Article  Google Scholar 

  • Tarazona OA, Slota LA, Lopez DH, Zhang G, Cohn MJ (2016) The genetic program for cartilage development has deep homology within Bilateria. Nature 533:86–89

    Article  CAS  Google Scholar 

  • Trinajstic K, Sanchez S, Dupret V, Tafforeau P, Long J, Young G, Senden T, Boisvert C, Power N, Ahlberg PE (2013) Fossil musculature of the most primitive jawed vertebrates. Science 341:160–164

    Article  CAS  Google Scholar 

  • Wada H (2010) Origin and genetic evolution of the vertebrate skeleton. Zool Sci 27:119–123

    Article  CAS  Google Scholar 

  • Wang NZ, Donoghue PCJ, Smith MM, Sansom IJ (2005) Histology of the galeaspid dermoskeleton and endoskeleton, and the origin and early evolution of the vertebrate cranial endoskeleton. J Vertebr Paleontol 25:745–756

    Article  Google Scholar 

  • Witten PE, Sire JY, Huysseune A (2014) Old, new and new-old concepts about the evolution of teeth. J Appl Ichthyol 30:636–642

    Article  Google Scholar 

  • Wuelling M, Vortkamp A (2019) Stem cells: the fountain of bone growth. Nature 567:178–179

    Article  CAS  Google Scholar 

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Correspondence to Tatsuya Hirasawa .

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Hirasawa, T., Kuratani, S. (2020). Evolution of Skeletal Tissues. In: Nuno de la Rosa, L., Müller, G. (eds) Evolutionary Developmental Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-33038-9_190-1

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  • DOI: https://doi.org/10.1007/978-3-319-33038-9_190-1

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  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-33038-9

  • Online ISBN: 978-3-319-33038-9

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