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Fossil jawless fish from China foreshadows early jawed vertebrate anatomy

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.

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Figure 1: Shuyu zhejiangensis , Silurian of Zhejiang, China.
Figure 2: The nasohypophyseal complex of Shuyu zhejiangensis.
Figure 3: The nasohypophyseal complex in craniates.

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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.).

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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

Correspondence to Philip C. J. Donoghue or Min Zhu.

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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)

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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

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