The oldest articulated osteichthyan reveals mosaic gnathostome characters

Abstract

The evolutionary history of osteichthyans (bony fishes plus tetrapods) extends back to the Ludlow epoch of the Silurian period. However, these Silurian forms have been documented exclusively by fragmentary fossils. Here we report the discovery of an exceptionally preserved primitive fish from the Ludlow of Yunnan, China, that represents the oldest near-complete gnathostome (jawed vertebrate). The postcranial skeleton of this fish includes a primitive pectoral girdle and median fin spine as in non-osteichthyan gnathostomes, but a derived macromeric squamation as in crown osteichthyans, and substantiates the unexpected mix of postcranial features in basal sarcopterygians, previously restored from the disarticulated remains of Psarolepis. As the oldest articulated sarcopterygian, the new taxon offers insights into the origin and early divergence of osteichthyans, and indicates that the minimum date for the actinopterygian–sarcopterygian split was no later than 419 million years ago.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Summary Silurian sequence in Qujing (Yunnan, China), showing the stratigraphic positions of Guiyu oneiros gen. et sp. nov. and other bony fishes.
Figure 2: Guiyu oneiros gen. et sp. nov., holotype V15541.
Figure 3: Guiyu oneiros gen. et sp. nov.
Figure 4: Guiyu oneiros gen. et sp. nov.
Figure 5: Timing of earliest evolution of the Osteichthyes.

References

  1. 1

    Nelson, J. S. Fishes of the World (Wiley, 2006)

    Google Scholar 

  2. 2

    Janvier, P. Early Vertebrates (Clarendon Press, 1996)

    Google Scholar 

  3. 3

    Yu, X.-B. A new porolepiform-like fish Psarolepis romeri gen. et sp. nov. (Sarcopterygii, Osteichthyes) from the Lower Devonian of Yunnan, China. J. Vert. Paleontol. 18, 261–274 (1998)

    Article  Google Scholar 

  4. 4

    Zhu, M., Yu, X.-B. & Janvier, P. A primitive fossil fish sheds light on the origin of bony fishes. Nature 397, 607–610 (1999)

    ADS  CAS  Article  Google Scholar 

  5. 5

    Zhu, M. & Schultze, H.-P. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 289–314 (Taylor & Francis, 2001)

    Google Scholar 

  6. 6

    Basden, A. M., Young, G. C., Coates, M. I. & Ritchie, A. The most primitive osteichthyan braincase? Nature 403, 185–188 (2000)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Basden, A. M. & Young, G. C. A primitive actinopterygian neurocranium from the Early Devonian of southeastern Australia. J. Vert. Paleontol. 21, 754–766 (2001)

    Article  Google Scholar 

  8. 8

    Schultze, H.-P. & Cumbaa, S. L. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 315–332 (Taylor & Francis, 2001)

    Google Scholar 

  9. 9

    Zhu, M., Yu, X.-B., Wang, W., Zhao, W.-J. & Jia, L.-T. A primitive fish provides key characters bearing on deep osteichthyan phylogeny. Nature 441, 77–80 (2006)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Friedman, M. Styloichthys as the oldest coelacanth: implications for early osteichthyan interrelationships. J. Syst. Palaeontol. 5, 289–343 (2007)

    Article  Google Scholar 

  11. 11

    Botella, H., Blom, H., Dorka, M., Ahlberg, P. E. & Janvier, P. Jaws and teeth of the earliest bony fishes. Nature 448, 583–586 (2007)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Gross, W. Fragliche Actinopterygier-Schuppen aus dem Silur Gotlands. Lethaia 1, 184–218 (1968)

    Article  Google Scholar 

  13. 13

    Gross, W. Lophosteus superbus Pander, ein Teleostome aus dem Silur Oesels. Lethaia 2, 15–47 (1969)

    Article  Google Scholar 

  14. 14

    Janvier, P. On the oldest known teleostome fish Andreolepis heder Gross (Ludlow of Gotland), and the systematic position of the lophosteids. Eesti NSV Teaduste Akad. Toimetised Geol. 27, 88–95 (1978)

    Google Scholar 

  15. 15

    Gagnier, P. Y., Jahnke, H. & Shi, Y. A fish fauna of the Lower Yulongsi Formation (Upper Silurian) of Qujing (E. Yunnan, S. W. China) and its depositional environment. Cour. Forsch.-Inst. Senckenberg 110, 123–135 (1989)

    Google Scholar 

  16. 16

    Wang, N.-Z. & Dong, Z.-Z. Discovery of Late Silurian microfossils of Agnatha and fishes from Yunnan, China. Acta Palaeont. Sin. 28, 192–206 (1989)

    Google Scholar 

  17. 17

    Zhu, M. & Schultze, H.-P. The oldest sarcopterygian fish. Lethaia 30, 293–304 (1997)

    Google Scholar 

  18. 18

    Cumbaa, S. L. & Schultze, H.-P. An Early Devonian (Emsian) acanthodian from the Bear Rock Formation, Anderson River, Northwest Territories, Canada. Can. J. Earth Sci. 39, 1457–1465 (2002)

    ADS  Article  Google Scholar 

  19. 19

    Schultze, H.-P. in Fossil Fishes as Living Animals (ed. Mark-Kurik, E.) 233–242 (Academy of Sciences of Estonia, 1992)

    Google Scholar 

  20. 20

    Jarvik, E. Middle and Upper Devonian Porolepiformes from East Greenland with special reference to Glyptolepis groenlandica n. sp. Meddr . Grønland 187, 1–307 (1972)

    ADS  Google Scholar 

  21. 21

    Denison, R. H. Early Devonian lungfishes from Wyoming, Utah, and Idaho. Fieldiana Geol. 17, 353–413 (1968)

    Google Scholar 

  22. 22

    Janvier, P. & Phuong, T. H. Les vertébrés (Placodermi, Galeaspida) du Dévonien inférieur de la coupe de Lung Cô-Mia Lé, province de Hà Giang, Viêt Nam, avec des données complémentaires sur les gisements à vertébrés du Dévonian du Bac Bo oriental. Geodiversitas 21, 33–67 (1999)

    Google Scholar 

  23. 23

    Wang, C.-Y. Age of the Guandi Formation in Qujing District, E. Yunnan. J. Stratigr. 25, 125–127 (2001)

    Google Scholar 

  24. 24

    Ting, V.-K. & Wang, Y.-L. Cambrian and Silurian Formations of Malung and Chutsing Districts, Yunnan. Bull. Geol. Soc. China 16, 1–28 (1937)

    Article  Google Scholar 

  25. 25

    Fang, R.-S. et al. The Middle Silurian and Early Devonian Stratigraphy and Palaeontology in Qujing District, Yunnan (Yunnan People’s Publishing House, 1985)

    Google Scholar 

  26. 26

    Rong, J.-Y. et al. Some problems concerning the correlation of the Silurian rocks in South China. J. Stratigr. 14, 161–177 (1990)

    Google Scholar 

  27. 27

    Walliser, O. H. & Wang, C.-Y. Upper Silurian stratigraphy and conodonts from the Qujing District, East Yunnan, China. Cour. Forsch.-Inst. Senckenberg 110, 111–121 (1989)

    Google Scholar 

  28. 28

    Pan, J. Notes on Silurian vertebrates of China. Bull. Chinese Acad. Geol. Sci. 15, 227–249 (1986)

    Google Scholar 

  29. 29

    Zhu, M., Yu, X.-B. & Ahlberg, P. E. A primitive sarcopterygian fish with an eyestalk. Nature 410, 81–84 (2001)

    ADS  CAS  Article  Google Scholar 

  30. 30

    Zhu, M. & Yu, X.-B. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Cloutier, R.) 271–286 (Verlag Dr. Friedrich Pfeil, 2004)

    Google Scholar 

  31. 31

    Pearson, D. M. & Westoll, T. S. The Devonian actinopterygian Cheirolepis Agassiz. Trans. R. Soc. Edinb. 70, 337–399 (1979)

    Article  Google Scholar 

  32. 32

    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. 37, 173–428 (1984)

    Google Scholar 

  33. 33

    Long, J. A. New palaeoniscoid fishes from the Late Devonian and Early Carboniferous of Victoria. Mem. Ass. Australas. Palaeontols 7, 1–64 (1988)

    Google Scholar 

  34. 34

    Friedman, M. & Blom, H. A new actinopterygian from the Famennian of East Greenland and the interrelationships of Devonian ray-finned fishes. J. Paleontol. 80, 1186–1204 (2006)

    Article  Google Scholar 

  35. 35

    Schultze, H.-P. Palaeoniscoiden-Schuppen aus dem Unterdevon Australiens und Kanadas und aus dem Mitteldevon Spitzbergens. Bull. Br. Mus. Nat. Hist. 16, 341–368 (1968)

    Google Scholar 

  36. 36

    Richter, M. & Smith, M. M. A microstructural study of the ganoine tissue of selected lower vertebrates. Zool. J. Linn. Soc. 114, 173–212 (1995)

    Article  Google Scholar 

  37. 37

    Andrews, S. M., Long, J., Ahlberg, P. E., Barwick, R. & Campbell, K. S. W. The structure of the sarcopterygian Onychodus jandemarrai n. sp. from Gogo, Western Australia: with a functional interpretation of the skeleton. Trans. R. Soc. Edinb. Earth Sci. 96, 197–307 (2006)

    Article  Google Scholar 

  38. 38

    Jarvik, E. Basic Structure and Evolution of Vertebrates Vol. 1 (Academic Press, 1980)

    Google Scholar 

  39. 39

    Miller, R. F., Cloutier, R. & Turner, S. The oldest articulated chondrichthyan from the Early Devonian Period. Nature 425, 501–504 (2003)

    ADS  CAS  Article  Google Scholar 

  40. 40

    Denison, R. H. Placodermi. Handbook of Paleoichthyology Vol. 2 (ed. Schultze, H.-P.) 1–128 (Gustav Fischer Verlag, 1978)

    Google Scholar 

  41. 41

    Grande, L. & Bemis, W. E. Osteology and phylogenetic relationships of fossil and recent paddlefishes (Polyodontidae) with comments on the interrelationships of Acipenseriformes. J. Vert. Paleontol. 11 (Suppl. 1). 1–121 (1991)

    Article  Google Scholar 

  42. 42

    Bemis, W. E., Findeis, E. K. & Grande, L. An overview of Acipenseriformes. Environ. Biol. Fishes 48, 25–71 (1997)

    Article  Google Scholar 

  43. 43

    Zhu, M. & Yu, X.-B. A primitive fish close to the common ancestor of tetrapods and lungfish. Nature 418, 767–770 (2002)

    ADS  CAS  Article  Google Scholar 

  44. 44

    Müller, J. & Reisz, R. R. Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. Bioessays 27, 1069–1075 (2005)

    Article  Google Scholar 

  45. 45

    Benton, M. J. & Donoghue, P. C. J. Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26–53 (2007)

    CAS  Article  Google Scholar 

  46. 46

    Sansom, I. J., Smith, M. M. & Smith, M. P. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 156–171 (Taylor & Francis, 2001)

    Google Scholar 

  47. 47

    Burrow, C. J. & Young, G. C. An articulated teleostome fish from the Late Silurian (Ludlow) of Victoria, Australia. Rec. West. Austr. Mus. 57 (Suppl.). 1–14 (1999)

    Google Scholar 

  48. 48

    Zhang, G.-R., Wang, J.-Q. & Wang, N.-Z. The structure of pectoral fin and tail of Yunnanolepidoidei, with a discussion of the pectoral fin of chuchinolepids. Vertebr. PalAsiat. 39, 1–13 (2001)

    Google Scholar 

  49. 49

    Swofford, D. L. PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods), Version 4.0b 10 (Sinauer Associates, 2003)

    Google Scholar 

  50. 50

    Gradstein, F. M. et al. A Geologic Time Scale 2004 (Cambridge Univ. Press, 2004)

    Google Scholar 

Download references

Acknowledgements

We thank M.-M. Chang, P. Janvier, J. Long, P. Ahlberg, X.-B. Yu and B. Choo for discussions, X.-B. Yu and B. Choo for improving the manuscript, J. Zhang and C.-H. Xiong for field work, X.-F. Lu and C.-H. Xiong for specimen preparation, W.-D. Zhang and W. Wang for making thin sections, B. Choo for life restoration, J.-L. Huang for illustrations, and J. Zhang for photography. This work was supported by the Major State Basic Research Projects (2006CB806400) of MST of China, the Chinese Academy of Sciences, the National Natural Science Foundation of China, and the CAS/SAFEA International Partnership Program for Creative Research Teams. M.Z., J.L. and T.Q. thank G. Young and J. Long for the examination of Australian specimens with the support of an Australian Research Council Discovery Grant (DP0772138).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Min Zhu.

Supplementary information

Supplementary Information 1

This file contains Supplementary Methods, Supplementary Results, Supplementary Tables 1-7, Supplementary Figures 1-9 with Legends, Supplementary Notes, Supplementary Data and Supplementary References. (PDF 541 kb)

Supplementary Information 2

This file contains photographs to show morphological details of Guiya. (PDF 2054 kb)

Supplementary Information 3

Life reconstruction was drawn by B. Choo (Victoria Museum) through communication with M.Z. (PDF 270 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zhu, M., Zhao, W., Jia, L. et al. The oldest articulated osteichthyan reveals mosaic gnathostome characters. Nature 458, 469–474 (2009). https://doi.org/10.1038/nature07855

Download citation

Further reading

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.

Search

Nature Briefing

Sign up for the Nature Briefing newsletter for a daily update on COVID-19 science.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing