Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development.

The stratigraphically earliest and the most primitive examples of vertebrate skeletal mineralization belong to lineages that are entirely extinct. Therefore, palaeontology offers a singular opportunity to address the patterns and mechanisms of evolution in the vertebrate mineralized skeleton. We test the two leading hypotheses for the emergence of the four skeletal tissue types (bone, dentine, enamel, cartilage) that define the present state of skeletal tissue diversity in vertebrates. Although primitive vertebrate skeletons demonstrate a broad range of tissues that are difficult to classify, the first hypothesis maintains that the four skeletal tissue types emerged early in vertebrate phylogeny and that the full spectrum of vertebrate skeletal tissue diversity is explained by the traditional classification system. The opposing hypothesis suggests that the early evolution of the mineralized vertebrate skeleton was a time of plasticity and that the four tissue types did not emerge until later. On the basis of a considerable, and expanding, palaeontological dataset, we track the stratigraphic and phylogenetic histories of vertebrate skeletal tissues. With a cladistic perspective, we present findings that differ substantially from long-standing models of tissue evolution. Despite a greater diversity of skeletal tissues early in vertebrate phylogeny, our synthesis finds that bone, dentine, enamel and cartilage do appear to account for the full extent of this variation and do appear to be fundamentally distinct from their first inceptions, although why a higher diversity of tissue structural grades exists within these types early in vertebrate phylogeny is a question that remains to be addressed. Citing recent evidence that presents a correlation between duplication events in secretory calcium-binding phosphoproteins (SCPPs) and the structural complexity of mineralized tissues, we suggest that the high diversity of skeletal tissues early in vertebrate phylogeny may result from a low diversity of SCPPs and a corresponding lack of constraints on the mineralization of these tissues.

[1]  G. Nelson Gill arches and the phylogeny of fishes : with notes on the classification of vertebrates. Bulletin of the AMNH ; v. 141, article 4 , 1969 .

[2]  Philip C J Donoghue,et al.  Genome duplication, extinction and vertebrate evolution. , 2005, Trends in ecology & evolution.

[3]  M. M. Smith,et al.  Development, Function and Evolution of Teeth: Evolutionary origins of dentine in the fossil record of early vertebrates: diversity, development and function , 2000 .

[4]  B. Hall,et al.  The neural crest as a fourth germ layer and vertebrates as quadroblastic not triploblastic , 2000, Evolution & development.

[5]  W. Ellenberger,et al.  Handbuch der Vergleichenden Anatomie der Haustiere , 1896 .

[6]  P. Donoghue,et al.  Origin and early evolution of vertebrate skeletonization , 2002, Microscopy research and technique.

[7]  P. Forey,et al.  Evolution of the Early Vertebrates , 1994 .

[8]  B. Hall,et al.  Calcification of cartilage from the lamprey Petromyzon marinus (L.) in vitro , 1993 .

[9]  P. Janvier,et al.  Complete mitochondrial DNA of the hagfish, Eptatretus burgeri: the comparative analysis of mitochondrial DNA sequences strongly supports the cyclostome monophyly. , 2002, Molecular phylogenetics and evolution.

[10]  R. Denison,et al.  Early Devonian fishes from Utah , 1952 .

[11]  E. Cope On the Phylogeny of the Vertebrata , 1892 .

[12]  V. Talimaa,et al.  Teslepis, a new mongolepid elasmobranchian fish from the Lower Silurian of Mongolia , 1992 .

[13]  Pcj Donoghue,et al.  The origin and early evolution of chordates: molecular clocks and the fossil record , 2003 .

[14]  E. Stensiö The cephalaspids of Great Britain , 1932 .

[15]  P. Donoghue,et al.  The anatomy of Turinia pagei (Powrie), and the phylogenetic status of the Thelodonti , 2001, Transactions of the Royal Society of Edinburgh: Earth Sciences.

[16]  T. S. Westoll Radotina and other tesserate fishes , 1967 .

[17]  R. Denison The exoskeleton of Tremataspis , 1947 .

[18]  M. Coates,et al.  The evolution of vertebrate dentitions: phylogenetic pattern and developmental models , 2001 .

[19]  M. M. Smith,et al.  Presence of the earliest vertebrate hard tissue in conodonts. , 1992, Science.

[20]  K. Weiss,et al.  Mineralized tissue and vertebrate evolution: The secretory calcium-binding phosphoprotein gene cluster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[21]  P. Janvier,et al.  Palaeobiology: Calcification of early vertebrate cartilage , 2002, Nature.

[22]  I. Sasagawa Fine structure of the cap enameloid and of the dental epithelial cells during enameloid mineralisation and early maturation stages in the tilapia, a teleost , 1997, Journal of anatomy.

[23]  V. Smith,et al.  Implications of resource-ratio theory for oral microbial ecology. , 1998, European journal of oral sciences.

[24]  B. Erdtmann,et al.  A POSSIBLE AGNATHAN PLATE FROM THE LOWER ARENIG (LOWER ORDOVICIAN) OF SOUTH BOLIVIA , 2000 .

[25]  J. Sire Light and TEM study of nonregenerated and experimentally regenerated scales of Lepisosteus oculatus (holostei) with particular attention to ganoine formation , 1994, The Anatomical record.

[26]  W. Reif Evolution of Dermal Skeleton and Dentition in Vertebrates , 1982 .

[27]  P. Janvier The relationships of the Osteostraci and Galeaspida , 1984 .

[28]  B. Hall,et al.  A Developmental Model for Evolution of the Vertebrate Exoskeleton and Teeth , 1993 .

[29]  M. P. Smith,et al.  Dentine in conodonts , 1994, Nature.

[30]  P. Donoghue Microstructural variation in conodont enamel is a functional adaptation , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  B. Hall Germ Layers and the Germ-Layer Theory Revisited , 1998 .

[32]  R. Denison Ordovician vertebrates from Western United States / Robert H. Denison -- , 1967 .

[33]  M. M. Smith,et al.  Development, Function and Evolution of Teeth: Evolutionary origins of teeth and jaws: developmental models and phylogenetic patterns , 2000 .

[34]  P. Janvier The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies [Palaeontological Association 1995 annual address] , 1996 .

[35]  P. Holland,et al.  Bayesian Phylogenetic Analysis Supports Monophyly of Ambulacraria and of Cyclostomes , 2002, Zoological science.

[36]  B. Hall,et al.  DEVELOPMENT AND EVOLUTIONARY ORIGINS OF VERTEBRATE SKELETOGENIC AND ODONTOGENIC TISSUES , 1990, Biological reviews of the Cambridge Philosophical Society.

[37]  I. Sasagawa The fine structure of initial mineralisation during tooth development in the gummy shark, Mustelus manazo, Elasmobranchia. , 1989, Journal of anatomy.

[38]  P. Donoghue Growth and patterning in the conodont skeleton , 1998 .

[39]  M. Moss The Phylogeny of Mineralized Tissues , 1964 .

[40]  R. Denison The Early History of the Vertebrate Calcified Skeleton , 1963, Clinical orthopaedics and related research.

[41]  P. Donoghue,et al.  HISTOLOGY OF THE GALEASPID DERMOSKELETON AND ENDOSKELETON, AND THE ORIGIN AND EARLY EVOLUTION OF THE VERTEBRATE CRANIAL ENDOSKELETON , 2005 .

[42]  P. Holland,et al.  Were vertebrates octoploid? , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  P. Forey Agnathans recent and fossil, and the origin of jawed vertebrates , 1995, Reviews in Fish Biology and Fisheries.

[44]  R. Shellis Structural organization of calcospherites in normal and rachitic human dentine. , 1983, Archives of oral biology.

[45]  J. Sire,et al.  Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach , 2003, Biological reviews of the Cambridge Philosophical Society.

[46]  P. Donoghue,et al.  Histology and affinity of the earliest armoured vertebrate , 2005, Biology Letters.

[47]  J. Maisey Phylogeny of early vertebrate skeletal induction and ossification patterns , 1988 .

[48]  E. Stensiö The Downtonian and Devonian vertebrates of Spitsbergen. I, Family Cephalaspidae , 1927 .

[49]  H. Blom,et al.  Silurian and earliest Devonian birkeniid anaspids from the Northern Hemisphere , 2001, Transactions of the Royal Society of Edinburgh: Earth Sciences.

[50]  K. Weiss,et al.  Genetic basis for the evolution of vertebrate mineralized tissue. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  P. Janvier The phylogeny of the Craniata, with particular reference to the significance of fossil “agnathans” , 1981 .

[52]  W. Gross Anaspiden-Schuppen aus dem Ludlow des Ostseegebiets , 1958 .

[53]  W. Gross Histologische Studien am Außenskelett fossiler Agnathen und Fische , 1935 .

[54]  M. M. Smith,et al.  Evolutionary origins of the vertebrate dentition: phylogenetic patterns and developmental evolution. , 1998, European journal of oral sciences.

[55]  R. Palmer,et al.  Development of periodontal ligament and alveolar bone in homografted recombinations of enamel organs and papillary, pulpal and follicular mesenchyme in the mouse. , 1987, Archives of oral biology.

[56]  J. Appleton Formation and structure of dentine in the rat incisor after chronic exposure to sodium fluoride. , 1994, Scanning microscopy.

[57]  I. Sansom Pseudooneotodus: a histological study of an Ordovician to Devonian vertebrate lineage , 1996 .

[58]  L. Tarlo Aspidin : The Precursor of Bone , 1963, Nature.

[59]  P. Holland,et al.  Polyploidy in vertebrate ancestry: Ohno and beyond , 2004 .

[60]  Moya M. Smith Distribution and variation in enamel structure in the oral teeth of sarcopterygians: Its significance for the evolution of a protoprismatic enamel , 1989 .

[61]  P. Donoghue Saving the stem group—a contradiction in terms? , 2005, Paleobiology.

[62]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[63]  W. Gross Porenschuppen und Sinneslinien des ThelodontiersPhlebolepis elegansPander , 1968 .

[64]  M. Moss Skeletal Tissues in Sharks , 1977 .

[65]  P. Forey YET MORE REFLECTIONS ON AGNATHAN-GNATHOSTOME RELATIONSHIPS , 1984 .

[66]  M. P. Smith,et al.  Histology of the first fish , 1996, Nature.

[67]  S. E. Bendix-Almgreen,et al.  Carcharodon megalodon from the Upper Miocene of Denmark, with comments on elasmobranch tooth enameloid: coronoi:n , 2008 .

[68]  J. Sire,et al.  On the origin of ganoine: histological and ultrastructural data on the experimental regeneration of the scales of Calamoichthys calabaricus (Osteichthyes, Brachyopterygii, Polypteridae). , 1987, The American journal of anatomy.

[69]  Moya M. Smith,et al.  A microvertebrate fauna from the Llandovery of South China , 1999, Transactions of the Royal Society of Edinburgh: Earth Sciences.

[70]  P. Janvier,et al.  CALCIFIED CARTILAGE IN THE PAIRED FINS OF THE OSTEOSTRACAN ESCUMINASPIS LATICEPS (TRAQUAIR 1880), FROM THE LATE DEVONIAN OF MIGUASHA (QUÉBEC, CANADA), WITH A CONSIDERATION OF THE EARLY EVOLUTION OF THE PECTORAL FIN ENDOSKELETON IN VERTEBRATES , 2004 .

[71]  T. Ubukata Architectural constraints on the morphogenesis of prismatic structure in Bivalvia , 1994 .

[72]  Gustav Wängsjö The Downtonian and Devonian vertebrates of Spitsbergen. IX, Morphologic and systematic studies of the Spitsbergen Cephalaspids , 1952 .

[73]  Paramvir S. Dehal,et al.  Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate , 2005, PLoS biology.

[74]  Sudhir Kumar,et al.  Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[75]  I. Sasagawa Mineralization patterns in elasmobranch fish , 2002, Microscopy research and technique.

[76]  P. Donoghue Evolution of development of the vertebrate dermal and oral skeletons: unraveling concepts, regulatory theories, and homologies , 2002, Paleobiology.

[77]  F. Meunier,et al.  The Concept of Bone Tissue in Osteichthyes , 1991 .

[78]  P. Forey,et al.  Agnathans and the origin of jawed vertebrates , 1993, Nature.

[79]  P. Forey,et al.  Conodont affinity and chordate phylogeny , 2000, Biological reviews of the Cambridge Philosophical Society.

[80]  P. Donoghue,et al.  BASAL TISSUE STRUCTURE IN THE EARLIEST EUCONODONTS: TESTING HYPOTHESES OF DEVELOPMENTAL PLASTICITY IN EUCONODONT PHYLOGENY , 2005 .

[81]  A. Miles,et al.  Autoradiographic study of the formation of enameloid and dentine matrices in teleost fishes using tritiated amino acids , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[82]  J. W. Osborn,et al.  An Autoradiographic Study of Periodontal Development in the Mouse , 1988, Journal of dental research.

[83]  L. B. Halstead Vertebrate hard tissues , 1974 .

[84]  E. Saiff The vertebrate skull , 1994 .

[85]  F. Sedláček,et al.  Disturbed enamel formation in wild boars (Sus scrofa L.) from fluoride polluted areas in central Europe , 2000, The Anatomical record.

[86]  Moya M. Smith,et al.  The histology and affinities of sinacanthid fishes: primitive gnathostomes from the Silurian of China , 2005 .

[87]  Putative Skeletal Neural Crest Cells in Early Late Ordovician Vertebrates from Colorado , 1991, Science.

[88]  A. Poustka,et al.  Timing and mechanism of ancient vertebrate genome duplications -- the adventure of a hypothesis. , 2005, Trends in genetics : TIG.

[89]  J. Maisey HEADS AND TAILS: A CHORDATE PHYLOGENY , 1986, Cladistics : the international journal of the Willi Hennig Society.

[90]  L. Sc Calcified tissues in the earliest vertebrates , 2005, Calcified Tissue Research.

[91]  Moya M. Smith,et al.  Response to Comment on "Separate Evolutionary Origins of Teeth from Evidence in Fossil Jawed Vertebrates" , 2003, Science.

[92]  P. Robson,et al.  The unusual cartilaginous tissues of jawless craniates, cephalochordates and invertebrates , 2001, Cell and Tissue Research.

[93]  P. Janvier Les vertébrés avant le Silurien , 1997 .