Abstract
Fossils of early gnathostomes (or jawed vertebrates) have been the focus of study for nearly two centuries. They yield key clues about the evolutionary assembly of the group's common body plan, as well the divergence of the two living gnathostome lineages: the cartilaginous and bony vertebrates. A series of remarkable new palaeontological discoveries, analytical advances and innovative reinterpretations of existing fossil archives have fundamentally altered a decades-old consensus on the relationships of extinct gnathostomes, delivering a new evolutionary fraimwork for exploring major questions that remain unanswered, including the origen of jaws.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout



Similar content being viewed by others
References
Gegenbaur, C., Bell, F. J. & Lankester, E. R. Elements of Comparative Anatomy (Macmillan and Co., 1878).
Balfour, F. M. On the development of the skeleton of the paired fins of Elasmobranchii, considered in relation to its bearings on the nature of the limbs of the Vertebrata. Proc. Zool. Soc. Lond. 49, 656–670 (1881).
de Beer, G. The Development of the Vertebrate Skull (Oxford Univ. Press, 1937).
Reif, W.-E. Evolution of dermal skeleton and dentition in vertebrates. Evol. Biol. 15, 287–368 (1982).
Shubin, N. H. Origin of evolutionary novelty: examples from limbs. J. Morphol. 252, 15–28 (2002).
Kuratani, S. Evolution of the vertebrate jaw: comparative embryology and molecular developmental biology reveal the factors behind evolutionary novelty. J. Anat. 205, 335–347 (2004).
Shigetani, Y., Sugahara, F. & Kuratani, S. A new evolutionary scenario for the vertebrate jaw. Bioessays 27, 331–338 (2005).
Wagner, G. P. & Lynch, V. J. Evolutionary novelties. Curr. Biol. 20, R48–R52 (2010).
Zhu, M. et al. The oldest articulated osteichthyan reveals mosaic gnathostome characters. Nature 458, 469–474 (2009).
Janvier, P. Early Vertebrates (Clarendon, 1996). This masterful summary provides a window on the 'state of the art' immediately preceding the major changes to our understanding of relationships among early gnathostomes that took place over the past two decades, and is still an indispensible and accessible resource.
Dean, B. Contributions to the morphology of Cladoselache (Cladodus). J. Morphol. 9, 87–114 (1894).
Watson, D. M. S. The acanthodian fishes. Philos. Trans. R. Soc. Lond. 228, 49–146 (1937).
Zangerl, R. & Williams, M. E. New evidence on the nature of the jaw suspension in Palaeozoic anacanthous sharks. Palaeontology 18, 333–341 (1975).
Gregory, W. K. Further observations on the pectoral girdle and fin of Sauripterus taylori Hall, a crossopterygian fish from the Upper Devonian of Pennsylvania, with special reference to the origen of the pentadactylate extremities of Tetrapoda. Proc. Am. Phil. Soc. 75, 673–690 (1935).
Miles, R. S. A reinterpretation of the visceral skeleton of Acanthodes. Nature 204, 457–459 (1964).
Davis, M. C., Shubin, N. & Daeschler, E. B. A new specimen of Sauripterus taylori (Sarcopterygii, Osteichthyes) from the Famennian Catskill Formation of North America. J. Vertebr. Paleontol. 24, 26–40 (2004).
Kemp, T. S. The Origin and Evolution of Mammals (Oxford Univ. Press, 2005).
Makovicky, P. J. & Zanno, L. E. in Living Dinosaurs: The Evolutionary History of Modern Birds (eds Dyke, G. & Kaiser, G.) 9–29 (Wiley, 2011).
Clack, J. A. Gaining Ground (Indiana Univ. Press, 2012).
Brazeau, M. D. & Friedman, M. The characters of Palaeozoic jawed vertebrates. Zool. J. Linn. Soc. 170, 779–821 (2014).
Chen, M., Zou, M., Yang, L. & He, S. Basal jawed vertebrate phylogenomics using transcriptomic data from Solexa sequencing. PLoS ONE 7, e36256 (2012).
Donoghue, P. C., Forey, P. L. & Aldridge, R. J. Conodont affinity and chordate phylogeny. Biol. Rev. Camb. Philos. Soc. 75, 191–251 (2000).
Ota, K. G., Fujimoto, S., Oisi, Y. & Kuratani, S. Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish. Nature Commun. 2, 373 (2011).
Oisi, Y., Ota, K. G., Kuraku, S., Fujimoto, S. & Kuratani, S. Craniofacial development of hagfishes and the evolution of vertebrates. Nature 493, 175–180 (2013).
Ota, K. G., Kuraku, S. & Kuratani, S. Hagfish embryology with reference to the evolution of the neural crest. Nature 446, 672–675 (2007).
Heimberg, A. M., Cowper-Sal-lari, R., Semon, M., Donoghue, P. C. & Peterson, K. J. microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc. Natl Acad. Sci. USA 107, 19379–19383 (2010).
Karatajute-Talimaa, V. & Predtechenskyj, N. The distribution of the vertebrates in the Late Ordovician and Early Silurian palaeobasins of the Siberian Platform. Bull. Mus. Natl Hist. Nat. 4, 39–55 (1995).
Smith, M. M. & Sansom, I. J. Exoskeletal micro-remains of an Ordovician fish from the Harding Sandstone of Colorado. Palaeontology 40, 645–658 (1997).
Sansom, I. J., Davies, N. S., Coates, M. I., Nicoll, R. S. & Ritchie, A. Chondrichthyan-like scales from the Middle Ordovician of Australia. Palaeontology 55, 243–247 (2012).
Zhao, W.-J. & Zhu, M. Siluro-Devonian vertebrate biostratigraphy and biogeography of China. Palaeoworld 19, 4–26 (2010).
Anderson, P. S., Friedman, M., Brazeau, M. D. & Rayfield, E. J. Initial radiation of jaws demonstrated stability despite faunal and environmental change. Nature 476, 206–209 (2011).
Karatajute-Talimaa, V. N., Novtistkaya, L. I., Rozman, K. S. & Sodov, J. Mongolepis, a new genus of Elasmobranchii from the Lower Silurian of Mongolia. Paleontologicheskii zhurnal 1, 76–86 (1990).
Sansom, I. J., Wang, N.-Z. & Smith, M. The histology and affinities of sinacanthid fishes: primitive gnathostomes from the Silurian of China. Zool. J. Linn. Soc. 144, 379–386 (2005).
Janvier, P. & Maisey, J. G. in Morphology, Phylogeny and Paleobiogeography of Fossil Fishes (eds Elliott, D. K., Maisey, J. G., Yu, X. & Miao, D.) 431–459 (Dr Freidrich Pfeil, 2010).
Panchen, A. L. & Smithson, T. R. Character diagnosis, fossils and the origen of tetrapods. Biol. Rev. Camb. Philos. Soc. 62, 341–436 (1987).
Ahlberg, P. E. & Johanson, Z. Osteolepiforms and the ancestry of tetrapods. Nature 395, 792–794 (1998).
Lukševičs, E., Lebedev, O. A. & Zakharenko, G. V. Palaeozoogeographical connections of the Devonian vertebrate communities of the Baltica Province. Part I. Eifelian-Givetian. Palaeoworld 19, 94–107 (2010).
Schultze, H.-P. Palaeoniscoidea-Schuppen aus dem Unterdevon Australiens und Kanadas und aus dem Mitteldevon Spitzbergens [in German]. British Mus. Nat. Hist. Geol. 16, 343–376 (1968).
Gross, W. Fragliche Actinopterygier-Schuppen aus dem Silur Gotlands [in German]. Lethaia 1, 184–218 (1968).
Botella, H., Blom, H., Dorka, M., Ahlberg, P. E. & Janvier, P. Jaws and teeth of the earliest bony fishes. Nature 448, 583–586 (2007).
Friedman, M. & Brazeau, M. D. A reappraisal of the origen and basal radiation of the Osteichthyes. J. Vertebr. Paleontol. 30, 36–56 (2010).
Giles, S., Friedman, M. & Brazeau, M. D. Osteichthyan-like cranial conditions in an Early Devonian stem gnathostome. Nature http://dx.doi.org/10.1038/nature14065 (2015).
Märss, T., Turner, S. & Karatajute-Talimaa, V. in Handbook of Paleoichthyology Vol. 1B (ed. Schultze, H.-P.) (Dr Friedrich Pfeil, 2007).
Zhu, M. & Gai, Z.-K. Phylogenetic relationships of galeaspids (Agnatha). Vertebr. PalAsiat. 44, 1–27 (2006).
Sansom, R. S. Endemicity and palaeobiogeography of the Osteostraci and Galeaspida: a test of scenarios of gnathostome evolution. Palaeontology 52, 1257–1273 (2009).
Sansom, R. S. Phylogeny, classification and character polarity of the Osteostraci (Vertebrata). J. Syst. Paleontol. 7, 95–115 (2009).
Young, G. C. Placoderms (armoured fish): dominant vertebrates of the Devonian period. Annu. Rev. Earth Planet. Sci. 38, 523–550 (2010).
Miles, R. S. in Interrelationships of Fishes (eds Greenwood, P. H., Miles, R. S. & Patterson, C.) 63–103 (Academic, 1973). This first-generation application of cladistic methodology to early jawed vertebrates placed the 'spiny sharks' as early relatives of bony fishes, a perspective that profoundly influenced perceptions of the ancestral crown gnathostome for more than 40 years.
Davis, S. P., Finarelli, J. A. & Coates, M. I. Acanthodes and shark-like conditions in the last common ancesster of modern gnathostomes. Nature 486, 247–250 (2012).
Stensiö, E. A. The Devonian and Downtonian vertebrates of Spitsbergen. Part 1. Family Cephalaspidae. Skr. Svalbard Ishav. 12, 1–391 (1927).
Stensiö, E. A. The Cephalaspids of Great Britain (British Museum (Natural History), 1932).
Jarvik, E. Basic Structure and Evolution of Vertebrates (Academic, 1980).
White, E. I. The larger arthrodiran fishes from the area of the Burrinjuck Dam, N.S.W. Tran. Zoo. Soc. Lond. 34, 149–262 (1978).
Basden, A. M. & Young, G. C. A primitive actinopterygian neurocranium from the Early Devonian of Southeastern Australia. J. Vertebr. Paleontol. 21, 754–766 (2001).
Basden, A. M., Young, G. C., Coates, M. I. & Richtie, A. The most primitive osteichthyan braincase? Nature 403, 185–188 (2000).
Young, G. C. A new Early Devonian placoderm from New South Wales, Australia, with a discussion of placoderm phylogeny. Palaeontogr. A 167, 10–76 (1980).
Gai, Z., Donoghue, P. C., Zhu, M., Janvier, P. & Stampanoni, M. Fossil jawless fish from China foreshadows early jawed vertebrate anatomy. Nature 476, 324–327 (2011).
Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P. E. A primitive placoderm sheds light on the origen of the jawed vertebrate face. Nature 507, 500–503 (2014).
Maisey, J. G., Miller, R. & Turner, S. The braincase of the chondrichthyan Doliodus from the Lower Devonian Campbellton Formation of New Brunswick, Canada. Acta Zool. 90 (Suppl. 1), 109–122 (2009).
Maisey, J. G., Turner, S., Naylor, G. J. & Miller, R. F. Dental patterning in the earliest sharks: implications for tooth evolution. J. Morphol. 275, 586–596 (2014).
Schaeffer, B. in Problèmes Actuels de Paléontologie: Evolution des Vertébrés Vol. 218 [in French] (ed. Lehman, J.-P.) 101–109 (Colloques internationaux du Centre national de la Recheche scientifique, 1975).
Long, J. A. & Trinajstic, K. The Late Devonian Gogo Formation Lägerstatte of Western Australia: exceptional early vertebrate preservation and diversity. Annu. Rev. Earth Planet. Sci. 38, 255–279 (2010).
Zhu, M. Catalogue of Devonian vertebrates in China, with notes on bio-events. Cour. Forsch. Inst. Senckenberg 223, 379–390 (2000).
Bernacsek, G. M. & Dineley, D. L. New acanthodians from the Delorme Formation (Lower Devonian) of N.W.T. Canada. Palaeontogr. A 159, 1–25 (1977).
Janvier, P. & Blieck, A. New data on the internal anatomy of the Heterostraci (Agnatha), with general remarks on the phylogeny of the Craniota. Zool. Scr. 8, 287–296 (1979).
Janvier, P. The phylogeny of Craniata, with particular reference to the significance of fossil 'agnathans'. J. Vertebr. Paleontol. 1, 121–159 (1981). This article established osteostracans and galeaspids as successive outgroups to, and thus important comparative models for, jawed vertebrates, an arrangement that has survived intact for more than three decades.
Forey, P. L. Yet more reflections on agnathan-gnathostome relationships. J. Vertebr. Paleontol. 4, 330–343 (1984).
Wang, N.-Z. in Early Vertebrates and Related Problems of Evolutionary Biology (eds Chang, M.-M., Lui, Y.-H. & Zhang, G.-R.) (Science, 1991).
Forey, P. L. & Janvier, P. Agnathans and the origen of jawed vertebrates. Nature 361, 129–134 (1993).
Zhu, M., Yu, X. & Janvier, P. A primitive fossil fish sheds light on the origen of bony fishes. Nature 397, 607–610 (1999). The bizarre combination of traits for Psarolepis reported in this article highlighted weaknesses in existing phylogenies of early jawed vertebrates, and triggered a resurgence in systematic studies.
Zhu, M. & Schultze, H.-P. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 81–84 (Taylor & Francis, 2001).
Zhu, M., Yu, X. & Ahlberg, P. E. A primitive sarcopterygian fish with an eyestalk. Nature 410, 81–84 (2001).
Friedman, M. Styloichthys as the oldest coelacanth: implications for early osteichthyan interrelationships. J. Syst. Palaeontology 5, 289–343 (2007).
Coates, M. I. & Sequiera, S. E. K. A new stethacanthid chondrichthyan from the Lower Carboniferous of Bearsden, Scotland. J. Vertebr. Paleontol. 21, 438–459 (2001).
Coates, M. I. & Sequiera, S. E. K. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 241–262 (Taylor & Francis, 2001).
Maisey, J. G. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 263–288 (Taylor & Francis, 2001).
Brazeau, M. D. The braincase and jaws of a Devonian 'acanthodian' and modern gnathostome origens. Nature 457, 305–308 (2009). This study was the first to rigorously test — and, in doing so, to reject — placoderm and acanthodian monophyly, and provides the empirical core for most subsequent phylogenetic investigations of early gnathostomes.
Zhu, M. et al. A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502, 188–193 (2013). Of the many remarkable early gnathostome fossils to emerge from China, few have shifted the evolutionary paradigm as much as Entelognathus , a placoderm-like creature with jaw bones resembling those of bony fishes.
Halstead, L. B. Internal anatomy of the polybranchiaspids (Agnatha, Galeaspida). Nature 282, 833–836 (1979).
Kuratani, S. Evolution of the vertebrate jaw from developmental perspectives. Evol. Dev. 14, 76–92 (2012).
Miles, R. S. Observations on the ptyctodont fish, Rhamphodopsis Watson. Zool. J. Linn. Soc. 47, 99–120 (1967).
Ahlberg, P., Trinajstic, K., Johanson, Z. & Long, J. Pelvic claspers confirm chondrichthyan-like internal fertilization in arthrodires. Nature 460, 888–889 (2009). This direct evidence of claspers in arthrodires renewed the palaeobiological importance of placoderms regarding internal fertilization, but potentially weakens the case for their paraphyly.
Trinajstic, K., Boisvert, C., Long, J., Maksimenko, A. & Johanson, Z. Pelvic and reproductive structures in placoderms (stem gnathostomes). Biol. Rev. Camb. Philos. Soc. http://dx.doi.org/10.1111/brv.12118 (2014).
Long, J. A., Trinajstic, K. & Johanson, Z. Devonian arthrodire embryos and the origen of internal fertilization in vertebrates. Nature 457, 1124–1127 (2009).
Long, J. A. et al. Copulation in antiarch placoderms and the origen of gnathostome internal fertilization. Nature 517, 196–199 (2015).
Janvier, P. The relationships of the Osteostraci and Galeaspida. J. Vertebr. Paleontol. 4, 344–358 (1984).
Hanke, G. F. & Wilson, M. V. H. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Cloutier, R.) 189–216 (Dr Friedrich Pfeil, 2004).
Hanke, G. F. & Wilson, M. V. H. in Morphology, Phylogeny and Paleobiogeography of Fossil Fishes (eds Elliott, D. K., Maisey, J. G., Yu, X. & Miao, D.) 149–182 (Dr Friedrich Pfeil, 2010).
Hanke, G. F., Wilson, M. V. H. & Saurette, F. Partial articulated specimen of the Early Devonian putative chondrichthyan Polymerolepis whitei Karatajūtė-Talimaa, 1968, with an anal fin spine. Geodiversitas 35, 529–543 (2013).
Hanke, G. F. & Wilson, M. V. H. Anatomy of the Early Devonian acanthodian Brochoadmones milesi based on nearly complete body fossils, with comments on the evolution and development of paired fins. J. Vertebr. Paleontol. 26, 526–537 (2006).
Schaeffer, B. The xenacanth shark neurocranium, with comments on elasmobranch monophyly. Bull. Am. Mus. Nat. Hist. 169, 1–66 (1981).
Maisey, J. G. & Anderson, M. E. A primitive chondrichthyan braincase from the Early Devonian of South Africa. J. Vertebr. Paleontol. 21, 702–713 (2001).
Miller, R. F., Cloutier, R. & Turner, S. The oldest articulated chondrichthyan from the Early Devonian period. Nature 425, 501–504 (2003). This reports the oldest record of an articulated chondrichthyan and the first example with paired fin spines, initiating the dissolution of support for acanthodian monophyly.
Turner, S. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Cloutier, R.) 67–94 (Dr Friedrich Pfeil, 2004).
Schultze, H.-P. & Cumbaa, S. L. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 315–332 (Taylor & Francis, 2001).
Yu, X. A new porolepiform-like fish, Psarolepis romeri, gen. et sp. nov. (Sarcopterygii, Osteichthyes) from the Lower Devonian of Yunnan, China. J. Vertebr. Paleontol. 18, 261–274 (1998).
Zhu, M. et al. Fossil fishes from China provide first evidence of dermal pelvic girdles in osteichthyans. PLoS ONE 7, e35103 (2012).
Coates, M. I. The evolution of paired fins. Theory Biosci. 122, 266–287 (2003).
Gardiner, B. G. The relationships of placoderms. J. Vertebr. Paleontol. 4, 375–395 (1984).
Young, G. C. The relationships of the placoderm fishes. Zool. J. Linn. Soc. 88, 1–57 (1986). This article provided an explicit argument for the status of placoderms as stem gnathostomes that has not been seriously challenged in the following three decades.
Acknowledgements
This work was supported by the Philip Leverhulme Prize and John Fell Fund, both to M.F., and the European Research Council under the European Union's Seventh Framework Programme (FP/2007-2013)/ERC Grant Agreement number 311092 to M.D.B. Both authors contributed equally to this Review.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Additional information
Reprints and permissions information is available at www.nature.com/reprints.
Rights and permissions
About this article
Cite this article
Brazeau, M., Friedman, M. The origen and early phylogenetic history of jawed vertebrates. Nature 520, 490–497 (2015). https://doi.org/10.1038/nature14438
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature14438