Abstract
Most living vertebrates are jawed vertebrates (gnathostomes), and the living jawless vertebrates (cyclostomes), hagfishes and lampreys, provide scarce information about the profound reorganization of the vertebrate skull during the evolutionary origin of jaws1,2,3,4,5,6,7,8,9. The extinct bony jawless vertebrates, or ‘ostracoderms’, are regarded as precursors of jawed vertebrates and provide insight into this formative episode in vertebrate evolution8,9,10,11,12,13,14. Here, using synchrotron radiation X-ray tomography15,16, we describe the cranial anatomy of galeaspids, a 435–370-million-year-old ‘ostracoderm’ group from China and Vietnam17. The paired nasal sacs of galeaspids are located anterolaterally in the braincase, and the hypophyseal duct opens anteriorly towards the oral cavity. These three structures (the paired nasal sacs and the hypophyseal duct) were thus already independent of each other, like in gnathostomes and unlike in cyclostomes and osteostracans (another ‘ostracoderm’ group), and therefore have the condition that current developmental models regard as prerequisites for the development of jaws1,2,3. This indicates that the reorganization of vertebrate cranial anatomy was not driven deterministically by the evolutionary origin of jaws but occurred stepwise, ultimately allowing the rostral growth of ectomesenchyme that now characterizes gnathostome head development1,2,3.
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
Kuratani, S. & Ota, K. G. Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies. J. Exp. Zool. 310B, 294–314 (2008)
Kuratani, S., Nobusada, Y., Horigome, N. & Shigetani, Y. Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Phil. Trans. R. Soc. B 356, 1615–1632 (2001)
Uchida, K., Murakami, Y., Kuraku, S., Hirano, S. & Kuratani, S. Development of the adenohypophysis in the lamprey: evolution of epigenetic patterning programs in organogenesis. J. Exp. Zool. 300B, 32–47 (2003)
Shigetani, Y. et al. Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science 296, 1316–1319 (2002)
Khonsari, R. H., Li, B., Vernier, P., Northcutt, R. G. & Janvier, P. Agnathan brain anatomy and craniate phylogeny. Acta Zool. 90, 52–68 (2009)
Smeets, W. J. A. in The Central Nervous System of Vertebrates (eds Nieuwenhuys, R., ten Donlelaar, H. J. & Nicholson, C.) 551–654 (Springer, 1998)
Janvier, P. Early Vertebrates (Clarendon, 1996)
Janvier, P. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 172–186 (Taylor and Francis, 2001)
Janvier, P. in Major Transitions in Vertebrate Evolution (eds Anderson, J. S. & Sues, H.-D.) 57–121 (Indiana Univ. Press, 2007)
Janvier, P. The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Palaeontology 39, 259–287 (1996)
Forey, P. L. & Janvier, P. Agnathans and the origin of jawed vertebrates. Nature 361, 129–134 (1993)
Forey, P. L. Agnathans recent and fossil, and the origin of jawed vertebrates. Rev. Fish Biol. Fish. 5, 267–303 (1995)
Donoghue, P. C. J. & Smith, M. P. The anatomy of Turinia pagei (Powrie) and the phylogenetic status of the Thelodonti. Trans. R. Soc. Edinb. Earth Sci. 92, 15–37 (2001)
Donoghue, P. C. J. & Purnell, M. A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312–319 (2005)
Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006)
Tafforeau, P. et al. Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl. Phys. A 83, 195–202 (2006)
Zhu, M. & Gai, Z.-K. Phylogenetic relationships of galeaspids (Agnatha). Vertebr . PalAsiat. 44, 1–27 (2006)
Stensiö, E. A. The Downtonian and Devonian Vertebrates of Spitsbergen. Part 1: Family Cephalaspidae. (Arno, 1927)
Mazan, S., Jaillard, D., Baratte, B. & Janvier, P. Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics. Evol. Dev. 2, 186–193 (2000)
Halstead, L. B. Internal anatomy of the polybranchiaspids (Agnatha, Galeaspida). Nature 282, 833–836 (1979)
Halstead, L. B. & Liu, Y.-H. &. P’an, K. Agnathans from the Devonian of China. Nature 282, 831–833 (1979)
Wang, N.-Z. in Early Vertebrates and Related Problems in Evolutionary Biology (eds Chang, M.-M., Liu, Y.-H. & Zhang, G.-R.) 41–65 (Science Press, 1991)
Gai, Z.-K., Zhu, M. & Zhao, W.-J. New material of eugaleaspids from the Silurian of Changxing, Zhejiang, China, with a discussion on the eugaleaspid phylogeny. Vertebr . PalAsiat. 43, 61–75 (2005)
Pan, J. in Professional Papers Presented to Professor Yoh Sen-shing 67–75 (Geological Publishing House, 1986)
Heimberg, A. M. Cowper-Sal·lari, R. Sémon, M., Donoghue, P. C. J. & 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)
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)
von Kupffer, C. Studien zur Vergleichenden Entwicklungsgeschichte des Kopfes der Kranioten. Heft 4: Zur Kopfentwicklung von Bdellostoma (Lehmann, 1900)
Gans, C. & Northcutt, R. G. Neural crest and the origin of the vertebrates: a new head. Science 220, 268–273 (1983)
Baker, C. V. H. & Schlosser, G. The evolutionary origin of neural crest and placodes. J. Exp. Zool. 304B, 269–273 (2005)
Stampanoni, M. et al. TOMCAT: a beamline for tomographic microscopy and coherent radiology experiments. Synchr. Radiat. Instrum. 879, 848–851 (2007)
Acknowledgements
We thank F. Marone, S. Bengtson, E.-M. Friis, N. J. Gostling, T. Huldtgren, M. Pawlowska and C.-W. Thomas for assistance in retrieving synchrotron radiation X-ray tomographic microscopy data; Q.-S. Chen and W.-J. Zhao for field work; and S. Powell, F.-X. Wu, B. Choo and R.-D. Zhao for illustrations. This work was supported by the Chinese Academy of Sciences (KZCX2-YW-156), the Chinese Foundation of Natural Sciences (40872020, 40930208), the Major Basic Research Projects (2006CB806400) of MST of China, the Paul Scherrer Institut (P.C.J.D.), European Union FP6 (P.C.J.D.), the Leverhulme Trust (P.C.J.D.), the Natural Environmental Research Council (P.C.J.D.), the SYNTHESYS Project (Z.G.) and a Dorothy Hodgkin studentship from the Royal Society (Z.G.).
Author information
Authors and Affiliations
Contributions
P.C.J.D. and M.Z. designed the project. Z.G. performed the research and led the writing of the manuscript. P.C.J.D., M.S. and Z.G. conducted the synchrotron radiation X-ray tomographic microscopy. All authors discussed the results and wrote the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
The file contains Supplementary Text, Supplementary References and Supplementary Figures 1-9 with legends. (PDF 9377 kb)
Supplementary Movie 1
The movie shows the virtual endocast of specimen V 14334.3, showing the brain and cranial nerves (dark blue), arterial canals (red), nasal sacs and oralobranchial chamber (orange), orbital cavity and dorsal jugular vein (light blue) and inner ear (yellow). (MOV 3056 kb)
Supplementary Movie 2
The movie shows the synchrotron-based X-ray tomographic slice data of specimen V14334.3, horizontal section. (MOV 1573 kb)
Rights and permissions
About this article
Cite this article
Gai, Z., Donoghue, P., Zhu, M. et al. Fossil jawless fish from China foreshadows early jawed vertebrate anatomy. Nature 476, 324–327 (2011). https://doi.org/10.1038/nature10276
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature10276
This article is cited by
-
Getting inside the oldest known vertebrate skull
Nature (2023)
-
The oldest three-dimensionally preserved vertebrate neurocranium
Nature (2023)
-
How did Jawed Vertebrates Originate and Rise?
Journal of Earth Science (2023)
-
Galeaspid anatomy and the origin of vertebrate paired appendages
Nature (2022)
-
Fossils reveal the deep roots of jawed vertebrates
Nature (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.