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Development of teeth and jaws in the earliest jawed vertebrates

Nature volume 491, pages 748–751 (2012)Cite this article

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Abstract

Teeth and jaws constitute a model of the evolutionary developmental biology concept of modularity1 and they have been considered the key innovations underpinning a classic example of adaptive radiation2. However, their evolutionary origins are much debated. Placoderms comprise an extinct sister clade3 or grade4,5 to the clade containing chondrichthyans and osteichthyans, and although they clearly possess jaws, previous studies have suggested that they lack teeth6,7,8, that they possess convergently evolved tooth-like structures9,10,11 or that they possess true teeth12. Here we use synchrotron radiation X-ray tomographic microscopy (SRXTM)13 of a developmental series of Compagopiscis croucheri (Arthrodira) to show that placoderm jaws are composed of distinct cartilages and gnathal ossifications in both jaws, and a dermal element in the lower jaw. The gnathal ossification is a composite of distinct teeth that developed in succession, polarized along three distinct vectors, comparable to tooth families. The teeth are composed of dentine and bone, and show a distinct pulp cavity that is infilled centripetally as development proceeds. This pattern is repeated in other placoderms, but differs from the structure and development of tooth-like structures in the postbranchial lamina and dermal skeleton of Compagopiscis and other placoderms. We interpret this evidence to indicate that Compagopiscis and other arthrodires possessed teeth, but that tooth and jaw development was not developmentally or structurally integrated in placoderms. Teeth did not evolve convergently among the extant and extinct classes of early jawed vertebrates but, rather, successional teeth evolved within the gnathostome stem-lineage soon after the origin of jaws. The chimaeric developmental origin of this model of modularity reflects the distinct evolutionary origins of teeth and of component elements of the jaws.

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Figure 1: Evolutionary relationships of principal groups of vertebrates.
Figure 2: Lower-jaw element of Compagopiscis croucheri , Late Devonian period, Australia.
Figure 3: Virtual development of a Compagopiscis croucheri lower jaw, Late Devonian period, Australia.
Figure 4: Histological comparison of the Compagopiscis croucheri cusps on jaws, dermal bone and postbranchial lamina, with the jaws and pectoral fins of the antiarch Bothriolepis species, both Late Devonian, Australia, and the jaw of a buchanosteid arthrodire, Early Devonian, Saudi Arabia.

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References

  1. Atchley, W. R. & Hall, B. K. A model for development and evolution of complex morphological structures and its application to the mammalian mandible. Biol. Rev. Camb. Philos. Soc. 66, 101–157 (1991)

    Article  CAS  Google Scholar 

  2. Gans, C. & Northcutt, R. G. Neural crest and the origin of the vertebrates: a new head. Science 220, 268–273 (1983)

    Article  ADS  CAS  Google Scholar 

  3. Young, G. C. Placoderms (armored fish): dominant vertebrates of the Devonian Period. Annu. Rev. Earth Planet. Sci. 38, 523–550 (2010)

    Article  ADS  CAS  Google Scholar 

  4. Brazeau, M. D. The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins. Nature 457, 305–308 (2009)

    Article  ADS  CAS  Google Scholar 

  5. Davis, S. P. et al. Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature 486, 247–250 (2012)

    Article  ADS  CAS  Google Scholar 

  6. Reif, W.-E. Evolution of dermal skeleton and dentition in vertebrates: The odontode regulation theory. Evol. Biol. 15, 287–368 (1982)

    Article  Google Scholar 

  7. Burrow, C. J. Comment on “Separate evolutionary origins of teeth from evidence in fossil jawed vertebrates”. Science 300, 1661 (2003)

    Article  CAS  Google Scholar 

  8. Young, G. C. Did placoderm fish have teeth? J. Vertebr. Paleontol. 23, 987–990 (2003)

    Article  Google Scholar 

  9. Johanson, Z. & Smith, M. M. Placoderm fishes, pharyngeal denticles, and the vertebrate dentition. J. Morphol. 257, 289–307 (2003)

    Article  Google Scholar 

  10. Johanson, Z. & Smith, M. M. Origin and evolution of gnathostome dentitions: a question of teeth and pharyngeal denticles in placoderms. Biol. Rev. Camb. Philos. Soc. 80, 303–345 (2005)

    Article  Google Scholar 

  11. Smith, M. M. & Johanson, Z. Separate evolutionary origin of teeth from evidence in fossil jawed vertebrates. Science 299, 1235–1236 (2003)

    Article  ADS  CAS  Google Scholar 

  12. Ørvig, T. Histologic studies of ostracoderms, placoderms and fossil elasmobranchs 3. Structure and growth of gnathalia of certain arthrodires. Zool. Scr. 9, 141–159 (1980)

    Article  Google Scholar 

  13. Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006)

    Article  ADS  CAS  Google Scholar 

  14. Lelièvre, H. Description of Maideria falipoui n.g., n.sp., a long snouted brachythoracid (Vertebrata, Placodermi, Arthrodira) from the Givetian of Maider (South Morocco), with a phylogenetic analysis of primitive brachythoracids. Bulletin du Muséum National d'Histoire Naturelle, Paris 17, 163–207 (1995)

    Google Scholar 

  15. Young, G. C. The relationships of placoderm fishes. Zool. J. Linn. Soc. 88, 1–57 (1986)

    Article  MathSciNet  Google Scholar 

  16. Downs, J. P. & Donoghue, P. C. J. Skeletal histology of Bothriolepis canadensis (Placodermi, Antiarchi) and evolution of the skeleton at the origin of jawed vertebrates. J. Morphol. 270, 1364–1380 (2009)

    Article  Google Scholar 

  17. Huysseune, A. et al. Evolutionary and developmental origins of the vertebrate dentition. J. Anat. 214 465–476 (2009) Medline

    Article  Google Scholar 

  18. Huysseune, A. et al. Unique and shared gene expression patterns in Atlantic salmon (Salmo salar) tooth development. Dev. Genes Evol. 218, 427–437 (2008)

    Article  CAS  Google Scholar 

  19. Fraser, G. J. et al. Developmental and evolutionary origins of the vertebrate dentition: Molecular controls for spatio-temporal organisation of tooth sites in osteichthyans. J. Exp. Zool. B Mol. Dev. Evol. 306, 183–203 (2006)

    Article  Google Scholar 

  20. Ørvig, T. Acanthodian dentition and its bearing on the relationships of the group. Palaeontographica (Abt. A) 143, 119–150 (1973)

    Google Scholar 

  21. Finarelli, J. A. & Coates, M. I. First tooth-set outside the jaws in a vertebrate. Proc. R. Soc. B 279, 775–779 (2012)

    Article  Google Scholar 

  22. Smith, M. M. The pattern of histogenesis and growth of tooth plates in larval stages of extant lungfish. J. Anat. 140, 627–643 (1985)

    PubMed  PubMed Central  Google Scholar 

  23. Fraser, G. J. et al. The odontode explosion: the origin of tooth-like structures in vertebrates. Bioessays 32, 808–817 (2010)

    Article  CAS  Google Scholar 

  24. Rücklin, M. et al. Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica. Evol. Dev. 13, 523–532 (2011)

    Article  Google Scholar 

  25. Soukup, V. et al. Dual epithelial origin of vertebrate oral teeth. Nature 455, 795–798 (2008)

    Article  ADS  CAS  Google Scholar 

  26. Stampanoni, M. et al. TOMCAT: A beamline for TOmographic Microscopy and Coherent rAdiology experimenTs. Synchrotron Radiation Instrumentation, Pts 1 and 2 879 848–851 http://www.osti.gov/energycitations/product.biblio.jsp?osti_id=21052651 (2007)

    ADS  CAS  Google Scholar 

  27. Goujet, D. & Young, G. C. Interrelationships of placoderms revisited. Geobios 19, 89–95 (1995)

    Article  Google Scholar 

  28. Goujet, D. & Young, G. C. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Cloutier, R. ) 109–126 (Pfeil, 2004)

    Google Scholar 

  29. Marone, F. & Stampanoni, M. Regridding reconstruction algorithm for real time tomographic imaging. J. Synchrotron Radiat. 19, 1–9 (2012)

    Article  Google Scholar 

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Acknowledgements

We thank S. Bengtson, J. Cunningham, D. Murdock, S. Giles and A. Hetherington for help at the TOMCAT beamline; K. Robson-Brown for help at the Micro-CT, and H. Lélièvre and G. Clément for loan of specimens. The study was funded by EU grant FP7 MC-IEF (to M.R. and P.C.J.D.), Australian Research Council Grant DP 110101127 (to Z.J. and K.T.), Natural Environment Research Council grant NE/G016623/1 (to P.C.J.D.) and the Paul Scherrer Institut (P.C.J.D.).

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Authors and Affiliations

  1. School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS8 1RJ, UK,

    Martin Rücklin & Philip C. J. Donoghue

  2. Earth Sciences, The Natural History Museum, Cromwell Road, South Kensington, London SW7 5BD, UK,

    Zerina Johanson

  3. Department of Chemistry, Curtin University, Kent St, 6102, Bentley, Australia

    Kate Trinajstic

  4. Department of Earth and Planetary Sciences, Western Australian Museum, Kew Street, 6106, Welshpool, Australia

    Kate Trinajstic

  5. Swiss Light Source, Paul Scherrer Institut, Villigen, CH-5232, Switzerland

    Federica Marone & Marco Stampanoni

  6. Institute for Biomedical Engineering, University and ETH Zürich, Zürich, CH-8092, Switzerland

    Marco Stampanoni

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  1. Martin Rücklin
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Contributions

M.R., P.C.J.D. and Z.J. conceived the project. K.T. acid-prepared WAM specimens. M.R., P.C.J.D., F.M. and M.S. collected the data. M.R. analysed the data. All authors contributed to the interpretation of the data and the writing of the manuscript.

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Correspondence to Martin Rücklin or Philip C. J. Donoghue.

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The authors declare no competing financial interests.

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Rücklin, M., Donoghue, P., Johanson, Z. et al. Development of teeth and jaws in the earliest jawed vertebrates. Nature 491, 748–751 (2012). https://doi.org/10.1038/nature11555

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