Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-17T19:37:43.995Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental paleobiology of the vertebrate skeleton

Published online by Cambridge University Press:  14 July 2015

Martin Rücklin ,
Philip C. J. Donoghue ,
John A. Cunningham ,
Federica Marone  and
Marco Stampanoni
Martin Rücklin
Affiliation:
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol BS8 1RJ, UK, ; ; Naturalis Biodiversity Center, Postbus 9517, 2300 RA Leiden, Netherlands,
Philip C. J. Donoghue
Affiliation:
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol BS8 1RJ, UK, ; ;
John A. Cunningham
Affiliation:
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol BS8 1RJ, UK, ; ;
Federica Marone
Affiliation:
Swiss Light Source, Paul Scherrer Institut, Villigen, Switzerland; ;
Marco Stampanoni
Affiliation:
Swiss Light Source, Paul Scherrer Institut, Villigen, Switzerland; ; Institute for Biomedical Engineering, University and ETH Zürich, Zürich, Switzerland
Get access Rights & Permissions [Opens in a new window]

Abstract

Studies of the development of organisms can reveal crucial information on homology of structures. Developmental data are not peculiar to living organisms, and they are routinely preserved in the mineralized tissues that comprise the vertebrate skeleton, allowing us to obtain direct insight into the developmental evolution of this most formative of vertebrate innovations. The pattern of developmental processes is recorded in fossils as successive stages inferred from the gross morphology of multiple specimens and, more reliably and routinely, through the ontogenetic stages of development seen in the skeletal histology of individuals. Traditional techniques are destructive and restricted to a 2-D plane with the third dimension inferred. Effective non-invasive methods of visualizing paleohistology to reconstruct developmental stages of the skeleton are necessary.

In a brief survey of paleohistological techniques we discuss the pros and cons of these methods. The use of tomographic methods to reconstruct development of organs is exemplified by the study of the placoderm dentition. Testing evidence for the presence of teeth in placoderms, the first jawed vertebrates, we compare the methods that have been used. These include inferring development from morphology, and using serial sectioning, microCT or synchrotron X-ray tomographic microscopy (SRXTM), to reconstruct growth stages and directions of growth. The ensuing developmental interpretations are biased by the methods and degree of inference. The most direct and reliable method is using SRXTM data to trace sclerochronology. The resulting developmental data can be used to resolve homology and test hypotheses on the origin of evolutionary novelties.

Type
Research Article
Information
Journal of Paleontology , Volume 88 , Issue 4 , July 2014 , pp. 676 - 683
Copyright
Copyright © The Paleontological Society 

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

Brazeau, M. D. 2009. The braincase and jaws of a Devonian ‘acanthodian' and modern gnathostome origins. Nature, 457:305–308.CrossRefGoogle ScholarPubMed
Burrow, C. J. 2003. Comment on “Separate evolutionary origins of teeth from evidence in fossil jawed vertebrates.” Science, 300:1661.CrossRefGoogle Scholar
Chinsamy-Turan, A. 2012. Forerunners of Mammals: Radiation, Histology, Biology. Indiana University Press, Bloomington, U.S.A., 352p.Google Scholar
Cloutier, R. 2010. The fossil record of fish ontogenies: Insights into developmental patterns and processes. Seminars in Cell and Developmental Biology, 21:400–413.CrossRefGoogle ScholarPubMed
Cunningham, J. A., Rücklin, M., Blom, H., Botella, H., and Donoghue, P. C. J. 2012. Testing models of dental development in the earliest bony vertebrates, Andreolepis and Lophosteus. Biology Letters, 8:833–837.CrossRefGoogle ScholarPubMed
Curtin, A. J., Macdowell, A. A., Schaible, E. G., and Roth, V. L. 2012. Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation X-ray microtomography. Journal of Vertebrate Paleontology, 32:939–955.CrossRefGoogle Scholar
Davis, S. P., Finarelli, J. A., and Coates, M. I. 2012. Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature, 486:247–250.CrossRefGoogle ScholarPubMed
de Pinna, M. C. C. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics, 7:415–394.CrossRefGoogle Scholar
Dierolf, M., Menzel, A., Thibault, P., Schneider, P., Kewish, C. M., Wepf, P., Bunk, O., and Pfeiffer, F. 2010. Ptychograpic X-ray computed tomography at the nanoscale. Nature, 467:436–439.CrossRefGoogle ScholarPubMed
Donoghue, P. C. J. and Aldridge, R. J. 2001. Origin of a mineralised skeleton, p. 85–105. InAhlberg, P. E.(ed.), Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development. Taylor and Francis, London.Google Scholar
Donoghue, P. C. J., Bengtson, S., Dong, X.-P., Gostling, N. J., Huldtgren, T., Cunningham, J. A., Yin, C., Yue, Z., Peng, F., and Stampanoni, M. 2006. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature, 442:680–683.CrossRefGoogle ScholarPubMed
Donoghue, P. C. J. and Sansom, I. J. 2002. Origin and early evolution of vertebrate skeletonization. Microscopy Research and Technique, 59:352–372.CrossRefGoogle ScholarPubMed
Donoghue, P. C. J., Sansom, I. J., and Downs, J. P. 2006. Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. Journal of Experimental Zoology, Part B, Molecular and Developmental Evolution, 306B:278–294.CrossRefGoogle Scholar
Downs, J. P. and Donoghue, P. C. J. 2009 . Skeletal histology of Bothriolepis canadensis (Placodermi, Antiarchi) and evolution of the skeleton at the origin of jawed vertebrates. Journal of Morphology, 270:1364–1380.CrossRefGoogle ScholarPubMed
Giles, S., Rücklin, M., and Donoghue, P. C. J. 2013. Histology of “placoderm” dermal skeletons: Implications for the nature of the ancestral gnathostome. Journal of Morphology, 274:627–644.CrossRefGoogle ScholarPubMed
Goodrich, E. S. 1909. Vertebrata craniata. Volume IX, 518 p. InLankester, E. R.(ed.), Treatise on Zoology. Adam and Charles Black, London.Google Scholar
Hall, B. K. 2003a. Descent with modification: The unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biological Reviews, 78:409–433.CrossRefGoogle ScholarPubMed
Hall, B. K. 2003b. Evo-Devo: Evolutionary developmental mechanisms. The International Journal of Developmental Biology, 47:491–495.Google ScholarPubMed
Hall, B. K. 2012. Evolutionary developmental biology (Evo-Devo): Past, present, and future. Evolution: Education and Outreach, 5:184–193.Google Scholar
Heintz, A. 1932. The structure of Dinichthys: A contribution to our knowledge of the Arthrodira. In Archaic fishes. American Museum of Natural History, New York, 4:115–213.Google Scholar
Hertwig, O. 1874a. Ueber Bau und Entwickelung der Placoidschuppen und der Zähne der Selachier. Jenaische Zeitschrift für Naturwissenschaft, 8:221–404.Google Scholar
Hertwig, O. 1874b. Ueber das Zahnsystem der Amphibien und seine Bedeutung für die Genese des Skelets der Mundhöhle. Eine vergleichend anatomische, entwickelungsgeschichtliche Untersuchung. Archiv für mikroskopische Anatomie, 11 supplement.CrossRefGoogle Scholar
Hertwig, O. 1876. Ueber das Hautskelet der Fische. Morphologisches Jahrbuch, 2:328–395.Google Scholar
Hertwig, O. 1879. Ueber das Hautskelet der Fische. 2: Das Hautskelet der Ganoiden (Lepidosteus und Polypterus). Morphologisches Jahrbuch, 5:1–21.Google Scholar
Hertwig, O. 1882. Ueber das Hautskelet der Fische. 3: Das Hautskelet der Pediculati, der Discoboli, der Gattung Diana, der Centriscidae, einiger Gattungen aus der Familie der Triglidae und der Plectognathen. Morphologisches Jahrbuch, 7:1–42.Google Scholar
Janvier, P. 1996. Early Vertebrates. Oxford Monographs on Geology and Geophysics 33. Clarendon Press, Oxford, 393p.Google Scholar
Johanson, Z. and Smith, M. M. 2003. Placoderm fishes, pharyngeal denticles, and the vertebrate dentition. Journal of Morphology, 257:289–307.CrossRefGoogle ScholarPubMed
Johanson, Z. and Smith, M. M. 2005. Origin and evolution of gnathostome dentitions: A question of teeth and pharyngeal denticles in placoderms. Biological Reviews of the Cambridge Philosophical Society, 80:303–345.CrossRefGoogle Scholar
Klein, N. and Sander, P. M. 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology, 34:247–263.CrossRefGoogle Scholar
Marone, F. and Stampanoni, M. 2012. Regridding reconstruction algorithm for real time tomographic imaging. Journal of Synchrotron Radiation, 19:1–9.CrossRefGoogle ScholarPubMed
Ørvig, T. 1951. Histologic studies of ostracoderms, placoderms and fossil elasmobranchs 1. The endoskeleton, with remarks on the hard tissues of lower vertebrates in general. Arkiv för Zoologi, 2:321–454.Google Scholar
Ørvig, T. 1968. The dermal skeleton: general considerations, p. 374–397. InØrvig, T.(ed.), Current Problems of Lower Vertebrate Phylogeny. Almquist and Wiksell, Stockholm.Google Scholar
Ørvig, T. 1977. A survey of odontodes (‘dermal teeth') from developmental, structural, functional, and phyletic points of view, p. 53–75. InAndrews, S. M., Miles, R. S., and Walker, A. D.(eds.), Problems in Vertebrate Evolution: Linnean Society Symposium Series 4. Academic Press, London.Google Scholar
Ørvig, T. 1980. Histologic studies of ostracoderms, placoderms and fossil elasmobranchs 3. Structure and growth of gnathalia of certain arthrodires. Zoologica Scripta, 9:141–159.CrossRefGoogle Scholar
Padian, K. and Lamm, E.-T. 2013. Bone histology of fossil tetrapods. University of California Press, Berkeley, 298p.Google Scholar
Patterson, C. 1982. Morphological characters and homology, p. 21–74. InJoysey, K. A. and Friday, A. E.(eds.), Problems of Phylogenetic Reconstruction. Systematics Association Special Volume 21. Academic Press, London.Google Scholar
Reif, W.-E. 1976. Morphogenesis, pattern formation and function of the dentition of Heterodontus (Selachii). Zoomorphologie, 83:1–47.CrossRefGoogle Scholar
Reif, W.-E. 1978a. Shark dentitions: Morphogenetic processes and evolution. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 157:107–115.Google Scholar
Reif, W.-E. 1978b. Types of morphogenesis of the dermal skeleton in fossil sharks. Paläontologische Zeitschrift, 52:110–128.CrossRefGoogle Scholar
Reif, W.-E. 1980. Development of dentition and dermal skeleton in embryonic Scyliorhinus canicula. Journal of Morphology, 166:275–288.CrossRefGoogle ScholarPubMed
Reif, W.-E. 1982. Evolution of dermal skeleton and dentition in vertebrates: The odontode regulation theory. Evolutionary Biology, 15:287–368.CrossRefGoogle Scholar
Rücklin, M., Giles, S., Janvier, P., and Donoghue, P. C. J. 2011. Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica. Evolution and Development, 13:523–532.CrossRefGoogle ScholarPubMed
Rücklin, M., Donoghue, P. C. J., Johanson, Z., Trinajstic, K., Marone, F., and Stampanoni, M. 2012. Development of teeth and jaws in the earliest jawed vertebrates. Nature, 491:748–751.CrossRefGoogle ScholarPubMed
Sanchez, S., Ahlberg, P. E., Trinajstic, K., Mirone, A., and Tafforeau, P. 2012 . Three-dimensional synchrotron virtual paleohistology: A new insight into the world of fossil bone microstructures. Microscopy and Microanalysis, 18:1095–1105.CrossRefGoogle ScholarPubMed
Sanchez, S., Dupret, V., Tafforeau, P., Trinajstc, K. M., Ryll, B., Gouttenoire, P.-J., Wretman, L., Zylberberg, L., Peyrin, F., and Ahlberg, P. E. 2013. 3D microstructural architecture of muscle attachments in extant and fossil vertebrates revealed by synchrotron microtomography. PloS ONE, 8:e56992.CrossRefGoogle ScholarPubMed
Sánchez-Villagra, M. R. 2012. Embryos in Deep Time. University of California Press, 265p.CrossRefGoogle Scholar
Sander, P. M. and Klein, N. 2005. Developmental plasticity in the life history of a prosauropod dinosaur. Science, 310:1800–1802.CrossRefGoogle ScholarPubMed
Sander, P. M., Mateus, O., Laven, T., and Knötschke, N. 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature, 441:739–741.CrossRefGoogle Scholar
Scheyer, T. M., Klein, N., and Sander, P. M. 2010. Developmental palaeontology of Reptilia as revealed by histological studies, p. 462–470. InSánchez-Villagra, M. R.(ed.), Developmental Vertebrate Palaeontology. Seminars in Cell and Developmental Biology, 21.Google ScholarPubMed
Smith, M. M. 2003. Vertebrate dentitions at the origin of jaws: When and how pattern evolved. Evolution and Development, 5:394–413.CrossRefGoogle ScholarPubMed
Smith, M. M. and Johanson, Z. 2003 . Separate evolutionary origin of teeth from evidence in fossil jawed vertebrates. Science, 299:1235–1236.CrossRefGoogle ScholarPubMed
Smith, M. M., Johanson, Z., Underwood, C., and Diekwisch, T. G. H. 2012. Pattern formation in development of chondrichthyan dentitions: a review of an evolutionary model. Historical Biology, 2012:1–16.Google Scholar
Sollas, W. J. 1903. A method for the investigation of fossils by serial sections. Philosophical Transactions of the Royal Society, B, 196:259–265.Google Scholar
Sollas, I. B. and Sollas, W. J. 1913. A study of a Dicynodon by means of serial sections. Philosophical Transactions of the Royal Society, B, 204:201–225.Google Scholar
Stensiö, E. A. 1927. The Downtonian and Devonian vertebrates of Spitsbergen. Part I. Family Cephalaspidae. Skrifter Svalbard Nordishavet 12, 391p.Google Scholar
Stein, K. and Prondvai, E. 2013. Rethinking the nature of fibrolamellar bone: An integrative biological revision of sauropod plexiform bone formation. Biological Reviews, 89:24–47.CrossRefGoogle Scholar
Straehl, F. R., Scheyer, T. M., Forasiepi, A. M., MacPhee, R. D., and Sánchez-Villagra, M. R. 2013. Evolutionary patterns of bone histology and bone compactness in xenarthran mammal long bones. PLoS ONE, 8: e69275.CrossRefGoogle ScholarPubMed
Sutton, M. 2008 . Tomographic techniques for the study of exceptionally preserved fossils. Proceedings of the Royal Society, B, 275:1587–1593.CrossRefGoogle Scholar
Tafforeau, P., Boistel, R., Boller, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J.-J., Kay, R. F., Lazzari, V., Marivaux, L., Neil, A., Nemoz, C., Thibault, X., Vignaud, P., and Zabler, S. 2006. Applications of X-ray synchrotron microtomography for nondestructive 3D studies of paleontological specimens. Applied Physics A, Materials Science and Processing, 83:195–202.CrossRefGoogle Scholar
Teshima, Y., Matsuoka, A., Fujiyoshi, M., Ikegami, Y., Keneko, T., Oouchi, S., Watanabe, Y., and Yamazawa, K. 2010. Enlarged skeleton models of plankton for tactile teaching. Lecture Notes in Computer Science, 6180:523–526.CrossRefGoogle Scholar
Wagner, G. P. 2000. What is the promise of developmental evolution? Part I: Why is developmental biology necessary to explain evolutionary innovations? Journal of Experimental Zoology, Molecular and Developmental Evolution, 288:95–98.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Wagner, G. P. and Larsson, H. C. E. 2003. What is the promise of developmental evolution? Part III: The crucible of developmental evolution. Journal of Experimental Zoology, 300B:1–4.CrossRefGoogle Scholar
Williamson, W. C. 1849. On the microscopic structure of the scales and dermal teeth of some ganoid and placoid fish. Philosophical Transactions of the Royal Society of London, 139:435–475.Google Scholar
Williamson, W. C. 1851. Investigations into the structure and development of the scales and bones of fishes. Philosophical Transactions of the Royal Society of London, 141:643–702.Google Scholar
Young, G. C. 2003. Did placoderm fish have teeth? Journal of Vertebrate Paleontology, 23:987–990.CrossRefGoogle Scholar