The gnathostome (jawed vertebrate) crown group comprises two extant clades with contrasting character complements. Notably, Chondrichthyes (cartilaginous fish) lack the large dermal bones that characterize Osteichthyes (bony fish and tetrapods). The polarities of these differences, and the morphology of the last common ancestor of crown gnathostomes, are the subject of continuing debate. Here we describe a three-dimensionally preserved 419-million-year-old placoderm fish from the Silurian of China that represents the first stem gnathostome with dermal marginal jaw bones (premaxilla, maxilla and dentary), features previously restricted to Osteichthyes. A phylogenetic analysis places the new form near the top of the gnathostome stem group but does not fully resolve its relationships to other placoderms. The analysis also assigns all acanthodians to the chondrichthyan stem group. These results suggest that the last common ancestor of Chondrichthyes and Osteichthyes had a macromeric dermal skeleton, and provide a new framework for studying crown gnathostome divergence.
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Moy-Thomas, J. A. & Miles, R. S. Palaeozoic Fishes (Chapman & Hall, 1971)
Jarvik, E. Basic Structure and Evolution of Vertebrates Vol. 1 (Academic, 1980)
Goujet, D. F. Placoderm interrelationships: a new interpretation, with a short review of placoderm classifications. Proc. Linn. Soc. N. S. W. 107, 211–243 (1984)
Gardiner, B. G. The relationship of placoderms. J. Vertebr. Paleontol. 4, 379–395 (1984)
Maisey, J. G. Heads and tails: a chordate phylogeny. Cladistics 2, 201–256 (1986)
Schultze, H.-P. in The Skull Vol. 2 (eds Janke, J. & Hall, B. K. ) 189–254 (Univ. Chicago Press, 1993)
Janvier, P. Early Vertebrates (Oxford Univ. Press, 1996)
Young, G. C. Placoderms (armored fish): dominant vertebrates of the Devonian period. Annu. Rev. Earth Planet. Sci. 38, 523–550 (2010)
Long, J. A. The Rise of Fishes: 500 Million Years of Evolution 2nd edn (John Hopkins Univ. Press, 2011)
Gross, W. Peut-on homologuer les os des Arthrodires et des Téléostomes? Colloq. Int. CNRS 104, 69–74 (1962)
Young, G. C. The relationships of placoderm fishes. Zool. J. Linn. Soc. 88, 1–57 (1986)
Schaeffer, B. in Problèmes actuels de Paléontologie-Evolution des Vertébrés Vol. 218 (ed. Lehman, J. P. ) 101–109 (Actes du Colloque International CNRS, 1975)
Goujet, D. F. in Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development (ed. Ahlberg, P. E. ) 209–222 (Taylor & Francis, 2001)
Johanson, Z. Vascularization of the osteostracan and antiarch (Placodermi) pectoral fin: similarities, and implications for placoderm relationships. Lethaia 35, 169–186 (2002)
Brazeau, M. D. The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins. Nature 457, 305–308 (2009)
Davis, S. P., Finarelli, J. A. & Coates, M. I. Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature 486, 247–250 (2012)
Zhu, M. et al. Fossil fishes from China provide first evidence of dermal pelvic girdles in osteichthyans. PLoS ONE 7, e35103 (2012)
Zhu, M., Yu, X.-B. & Janvier, P. A primitive fossil fish sheds light on the origin of bony fishes. Nature 397, 607–610 (1999)
Zhu, M. & Schultze, H.-P. in Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development (ed. Ahlberg, P. ) 289–314 (Taylor & Francis, 2001)
Zhu, M. et al. The oldest articulated osteichthyan reveals mosaic gnathostome characters. Nature 458, 469–474 (2009)
Gardiner, B. G. The relationships of the palaeoniscid fishes, a review based on new specimens of Mimia and Moythomasia from the Upper Devonian of western Australia. Bull. Br. Mus. Nat. Hist. Geol. 7, 173–428 (1984)
Forey, P. L. & Gardiner, B. G. Observations on Ctenurella (Ptyctodontida) and the classification of placoderm fishes. Zool. J. Linn. Soc. 86, 43–74 (1986)
Stensiö, E. A. Anatomical studies on the arthrodiran head. Part 1. Preface, geological and geographical distribution, the organization of the head in the Dolichothoraci, Coccosteomorphi and Pachyosteomorphi. Taxonomic appendix. Kungl. Svenska Vetenskap. Hand. 9, 1–419 (1963)
Zhao, W.-J. & Zhu, M. Siluro-Devonian vertebrate biostratigraphy and biogeography of China. Palaeoworld 19, 4–26 (2010)
Zhu, M., Liu, Y.-H., Jia, L.-T. & Gai, Z.-K. A new genus of eugaleaspidiforms (Agnatha:Galeaspida) from the Ludlow, Silurian of Qujing, Yunnan, southwestern China. Vertebr. PalAsiat. 50, 1–7 (2012)
Denison, R. H. in Handbook of Paleoichthyology Vol. 2 (ed. Schultze, H.-P. ) 1–128 (Gustav Fischer, 1978)
Goujet, D. F. Sigaspis, un nouvel arthrodire du Dévonien inférieur du Spitsberg. Palaeontogr. A 143, 73–88 (1973)
Liu, Y.-H. in Early Vertebrates and Related Problems of Evolutionary Biology (eds Chang, M.-M., Liu, Y.-H. & Zhang, G.-R. ) 139–177 (Science Press, 1991)
Burrow, C. J., Newman, M. J., Davidson, R. G. & den Blaauwen, J. L. Sclerotic plates or circumorbital bones in early jawed fishes? Palaeontology 54, 207–214 (2011)
Goujet, D. F. Les Poissons Placodermes du Spitsberg. Arthrodires Dolichothoraci de la Formation de Wood Bay (Dévonien Inférieur) (CNRS, 1984)
Trinajstic, K., Long, J. A., Johanson, Z., Young, G. & Senden, T. New morphological information on the ptyctodontid fishes (Placodermi, Ptyctodontida) from western Australia. J. Vertebr. Paleontol. 32, 757–780 (2012)
Friedman, M. & Brazeau, M. D. A reappraisal of the origin and basal radiation of the Osteichthyes. J. Vertebr. Paleontol. 30, 36–56 (2010)
Young, G. C. New information on the structure and relationships of Buchanosteus (Placodermi: Euarthrodira) from the Early Devonian of New South Wales. Zool. J. Linn. Soc. 66, 309–352 (1979)
Schultze, H.-P. & Cumbaa, S. L. in Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development (ed. Ahlberg, P. E. ) 315–332 (Taylor & Francis, 2001)
Botella, H., Blom, H., Dorka, M., Ahlberg, P. E. & Janvier, P. Jaws and teeth of the earliest bony fishes. Nature 448, 583–586 (2007)
Maddison, W. P. & Maddison, D. R. Mesquite: A Modular System For Evolutionary Analysis. v. 2.5 (http://mesquiteproject.org, 2008)
Swofford, D. L. PAUP*: Phylogenetic analysis using parsimony (* and other methods), version 4.0b 10 (Sinauer Associates, 2003)
Sorenson, M. D. TreeRot. Program and documentation v. 2 (Boston Univ., 1999)
Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003)
Huelsenbeck, J. P. & Ronquist, F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)
We thank M.-M. Chang, J. Long, G. Young, D. Goujet and J.-Q. Wang for discussions, X.-F. Lu, J. Zhang and C.-H. Xiong for specimen preparation, Y.-M. Hou for X-ray micro-computerized tomography. This work was supported by the Major State Basic Research Projects (2012CB821902) of MST of China, and the National Natural Science Foundation of China (40930208). P.E.A. and Q.Q. were supported by ERC Advanced Investigator Grant 233111 and a Wallenberg Scholarship from the Knut and Alice Wallenberg Foundation, both awarded to P.E.A.
The authors declare no competing financial interests.
The LSIDs urn:lsid:zoobank.org:pub:1CE67C34-52CC-4CEF-B731-DF1A4E85DE4B (article), urn:lsid:zoobank.org:act:D88DD67F-1159-4E7E-AE4C-814249337351(genus), and urn:lsid:zoobank.org:act:77F76728-FBC1-407D-B2C1-1C5D5BF9B59C (species) have been deposited in ZooBank.
This file contains Phylogenetic analyses, Supplementary Table 1, Supplementary Figures 1-27 and Supplementary References (see Table of Contents for full list). (PDF 12048 kb)
This zipped file contains the Nexus file of the dataset with 253 morphological characters for 75 taxa. (ZIP 11 kb)
Digital dynamic restoration of specimen IVPP V18620 (holotype of Entelognathus primordialis gen. et sp. nov.) showing the cheek complex, sclerotic ring, mandible, submandibular and gular series in external and internal views. (MOV 8467 kb)
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Zhu, M., Yu, X., Ahlberg, P. et al. A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502, 188–193 (2013). https://doi.org/10.1038/nature12617
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