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Developmental paleobiology of the vertebrate skeleton

  • Martin Rücklin (a1) (a2), Philip C. J. Donoghue (a1), John A. Cunningham (a1), Federica Marone (a3) and Marco Stampanoni (a3) (a4)...
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.

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Brazeau M. D. 2009. The braincase and jaws of a Devonian ‘acanthodian' and modern gnathostome origins. Nature, 457:305308.
Burrow C. J. 2003. Comment on “Separate evolutionary origins of teeth from evidence in fossil jawed vertebrates.” Science, 300:1661.
Chinsamy-Turan A. 2012. Forerunners of Mammals: Radiation, Histology, Biology. Indiana University Press, Bloomington, U.S.A., 352p.
Cloutier R. 2010. The fossil record of fish ontogenies: Insights into developmental patterns and processes. Seminars in Cell and Developmental Biology, 21:400413.
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, 8:833837.
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, 32:939955.
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, 486:247250.
de Pinna M. C. C. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics, 7:415–394.
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, 467:436439.
Donoghue P. C. J. and Aldridge R. J. 2001. Origin of a mineralised skeleton, p. 85105. InAhlberg P. E.(ed.), Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development. Taylor and Francis, London.
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, 442:680683.
Donoghue P. C. J. and Sansom I. J. 2002. Origin and early evolution of vertebrate skeletonization. Microscopy Research and Technique, 59:352372.
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:278294.
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, 270:13641380.
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, 274:627644.
Goodrich E. S. 1909. Vertebrata craniata. Volume IX, 518 p. InLankester E. R.(ed.), Treatise on Zoology. Adam and Charles Black, London.
Hall B. K. 2003a. Descent with modification: The unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biological Reviews, 78:409433.
Hall B. K. 2003b. Evo-Devo: Evolutionary developmental mechanisms. The International Journal of Developmental Biology, 47:491495.
Hall B. K. 2012. Evolutionary developmental biology (Evo-Devo): Past, present, and future. Evolution: Education and Outreach, 5:184193.
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, 4:115213.
Hertwig O. 1874a. Ueber Bau und Entwickelung der Placoidschuppen und der Zähne der Selachier. Jenaische Zeitschrift für Naturwissenschaft, 8:221404.
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.
Hertwig O. 1876. Ueber das Hautskelet der Fische. Morphologisches Jahrbuch, 2:328395.
Hertwig O. 1879. Ueber das Hautskelet der Fische. 2: Das Hautskelet der Ganoiden (Lepidosteus und Polypterus). Morphologisches Jahrbuch, 5:121.
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, 7:142.
Janvier P. 1996. Early Vertebrates. Oxford Monographs on Geology and Geophysics 33. Clarendon Press, Oxford, 393p.
Johanson Z. and Smith M. M. 2003. Placoderm fishes, pharyngeal denticles, and the vertebrate dentition. Journal of Morphology, 257:289307.
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, 80:303345.
Klein N. and Sander P. M. 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology, 34:247263.
Marone F. and Stampanoni M. 2012. Regridding reconstruction algorithm for real time tomographic imaging. Journal of Synchrotron Radiation, 19:19.
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, 2:321454.
Ørvig T. 1968. The dermal skeleton: general considerations, p. 374397. InØrvig T.(ed.), Current Problems of Lower Vertebrate Phylogeny. Almquist and Wiksell, Stockholm.
Ørvig T. 1977. A survey of odontodes (‘dermal teeth') from developmental, structural, functional, and phyletic points of view, p. 5375. InAndrews S. M., Miles R. S., and Walker A. D.(eds.), Problems in Vertebrate Evolution: Linnean Society Symposium Series 4. Academic Press, London.
Ørvig T. 1980. Histologic studies of ostracoderms, placoderms and fossil elasmobranchs 3. Structure and growth of gnathalia of certain arthrodires. Zoologica Scripta, 9:141159.
Padian K. and Lamm E.-T. 2013. Bone histology of fossil tetrapods. University of California Press, Berkeley, 298p.
Patterson C. 1982. Morphological characters and homology, p. 2174. InJoysey K. A. and Friday A. E.(eds.), Problems of Phylogenetic Reconstruction. Systematics Association Special Volume 21. Academic Press, London.
Reif W.-E. 1976. Morphogenesis, pattern formation and function of the dentition of Heterodontus (Selachii). Zoomorphologie, 83:147.
Reif W.-E. 1978a. Shark dentitions: Morphogenetic processes and evolution. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 157:107115.
Reif W.-E. 1978b. Types of morphogenesis of the dermal skeleton in fossil sharks. Paläontologische Zeitschrift, 52:110128.
Reif W.-E. 1980. Development of dentition and dermal skeleton in embryonic Scyliorhinus canicula. Journal of Morphology, 166:275288.
Reif W.-E. 1982. Evolution of dermal skeleton and dentition in vertebrates: The odontode regulation theory. Evolutionary Biology, 15:287368.
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, 13:523532.
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, 491:748751.
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, 18:10951105.
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.
Sánchez-Villagra M. R. 2012. Embryos in Deep Time. University of California Press, 265p.
Sander P. M. and Klein N. 2005. Developmental plasticity in the life history of a prosauropod dinosaur. Science, 310:18001802.
Sander P. M., Mateus O., Laven T., and Knötschke N. 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature, 441:739741.
Scheyer T. M., Klein N., and Sander P. M. 2010. Developmental palaeontology of Reptilia as revealed by histological studies, p. 462470. InSánchez-Villagra M. R.(ed.), Developmental Vertebrate Palaeontology. Seminars in Cell and Developmental Biology, 21.
Smith M. M. 2003. Vertebrate dentitions at the origin of jaws: When and how pattern evolved. Evolution and Development, 5:394413.
Smith M. M. and Johanson Z. 2003 . Separate evolutionary origin of teeth from evidence in fossil jawed vertebrates. Science, 299:12351236.
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, 2012:116.
Sollas W. J. 1903. A method for the investigation of fossils by serial sections. Philosophical Transactions of the Royal Society, B, 196:259265.
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, 204:201225.
Stensiö E. A. 1927. The Downtonian and Devonian vertebrates of Spitsbergen. Part I. Family Cephalaspidae. Skrifter Svalbard Nordishavet 12, 391p.
Stein K. and Prondvai E. 2013. Rethinking the nature of fibrolamellar bone: An integrative biological revision of sauropod plexiform bone formation. Biological Reviews, 89:2447.
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.
Sutton M. 2008 . Tomographic techniques for the study of exceptionally preserved fossils. Proceedings of the Royal Society, B, 275:15871593.
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, 83:195202.
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, 6180:523526.
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, 288:9598.
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:14.
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, 139:435475.
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, 141:643702.
Young G. C. 2003. Did placoderm fish have teeth? Journal of Vertebrate Paleontology, 23:987990.
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