Head and backbone of the Early Cambrian vertebrate Haikouichthys

Abstract

Agnathan fish hold a key position in vertebrate evolution, especially regarding the origin of the head and neural-crest-derived tissue1. In contrast to amphioxus2, lampreys and other vertebrates possess a complex brain and placodes that contribute to well-developed eyes, as well as auditory and olfactory systems3. These sensory sytems were arguably a trigger to subsequent vertebrate diversifications. However, although they are known from skeletal impressions in younger Palaeozoic agnathans4, information about the earliest records of these systems has been largely wanting. Here we report numerous specimens of the Lower Cambrian vertebrate Haikouichthys ercaicunensis, until now only known from the holotype5. Haikouichthys shows significant differences from other fossil agnathans: key features include a small lobate extension to the head, with eyes and possible nasal sacs, as well as what may be otic capsules. A notochord with separate vertebral elements is also identifiable. Phylogenetic analysis indicates that this fish lies within the stem-group craniates. Although Haikouichthys somewhat resembles the ammocoete larva of modern lampreys, this is because of shared general craniate characters; adult lampreys and hagfishes (the cyclostomes if monophyletic6,7) are probably derived in many respects.

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: Haikouichthys ercaicunensis from Haikou, Kunming, Yunnan.
Figure 2: Phylogenetic analysis.

References

  1. 1

    Northcutt, R. G. The origin of craniates: neural crest, neurogenic placodes, and homeobox genes. Isr. J. Zool. 42, S273–S313 (1996)

    Google Scholar 

  2. 2

    Holland, L. Z. & Holland, N. D. Evolution of neural crest and placodes: amphioxus as a model for the ancestral vertebrate? J. Anat. 199, 85–98 (2001)

    CAS  Article  Google Scholar 

  3. 3

    Kleerekoper, H. The Biology of Lampreys Vol. 2 (eds Hardisty, M. W. & Potter, I. C.) 373–404 (Academic, London, 1972)

    Google Scholar 

  4. 4

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

    Google Scholar 

  5. 5

    Shu, D.-G. et al. Lower Cambrian vertebrates from south China. Nature 402, 42–46 (1999)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Mallatt, J. & Sullivan, J. 28S and 18S rDNA sequences support the monophyly of lampreys and hagfishes. Mol. Biol. Evol. 15, 1706–1718 (1998)

    CAS  Article  Google Scholar 

  7. 7

    Kuraku, S. et al. Monophyly of lampreys and hagfishes supported by nuclear DNA-coded genes. J. Mol. Evol. 49, 729–735 (1999)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Zhang, X.-l. et al. New sites of Chengjiang fossils: crucial windows on the Cambrian explosion. J. Geol. Soc. Lond. 158, 211–218 (2001)

    Article  Google Scholar 

  9. 9

    Janvier, P. Catching the first fish. Nature 402, 21–22 (1999)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Shimeld, S. M. & Holland, P. W. H. Vertebrate innovations. Proc. Natl Acad. Sci. USA 97, 4449–4452 (2000)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Holland, H. D. & Chen, J.-y. Origin and early evolution of the vertebrates: new insights from advances in molecular biology, anatomy, and palaeontology. BioEssays 23, 142–151 (2001)

    CAS  Article  Google Scholar 

  12. 12

    Cole, W. C. & Youson, J. H. Morphology of the pineal complex of the anadromous sea lamprey, Petromyzon marinus L. Am. J. Anat. 165, 131–163 (1982)

    CAS  Article  Google Scholar 

  13. 13

    Bardack, D. & Zangerl, R. The Biology of Lampreys Vol. 1 (eds Hardisty, M. W. & Potter, I. C.) 67–84 (Academic, London, 1971)

    Google Scholar 

  14. 14

    Gabbott, S. E., Aldridge, R. J. & Theron, J. N. A giant conodont with preserved muscle tissue from the Upper Ordovician of South Africa. Nature 374, 800–803 (1995)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Gagnier, P.-Y. Sacabambaspis janvieri, vertébré Ordovicien de Bolivie: I: Analyse morphologique. Ann. Paléontol. 79, 19–51 (1993)

    Google Scholar 

  16. 16

    Gagnier, P.-Y. Sacabambaspis janvieri, vertébré Ordovicien de Bolivie 2: Analyse phylogénétique. Ann. Paléontol. 79, 119–166 (1993)

    Google Scholar 

  17. 17

    Ritchie, A. New evidence on Jamoytius kerwoodi White, an important ostracoderm from the Silurian of Lanarkshire, Scotland. Palaeontology 11, 21–39 (1968)

    Google Scholar 

  18. 18

    Lacalli, T. C. Frontal eye circuitry, rostral sensory pathways and brain organization in amphioxus larvae: evidence from 3D reconstructions. Phil. Trans. R. Soc. Lond. B 351, 243–263 (1996)

    ADS  Article  Google Scholar 

  19. 19

    Lacalli, T. C. New perspectives on the evolution of protochordate sensory and locomotory systems, and the origin of brains and heads. Phil. Trans. R. Soc. Lond. B 356, 1565–1572 (2001)

    CAS  Article  Google Scholar 

  20. 20

    Fritzsch, B. Evolution of the vestibulo-ocular system. Otolaryngology Head Neck Surg. 119, 182–192 (1998)

    CAS  Article  Google Scholar 

  21. 21

    Kuratani, S. et al. Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Phil. Trans. R. Soc. Lond. B 356, 1615–1632 (2001)

    CAS  Article  Google Scholar 

  22. 22

    Cohn, M. J. Lamprey Hox genes and the origin of jaws. Nature 416, 386–387 (2002)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Shigetani, Y. et al. Heterotopic shifts of epithelial–mesenchymal interactions in vertebrate jaw evolution. Science 296, 1316–1319 (2002)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Shu, D.-G. et al. Primitive deuterostomes from the Chengjiang Lagerstätte (Lower Cambrian, China). Nature 414, 419–424 (2001)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Shu, D.-G. et al. An early Cambrian tunicate from China. Nature 411, 472–473 (2001)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Shu, D.-G., Conway Morris, S. & Zhang, X.-L. A Pikaia-like chordate from the Lower Cambrian of China. Nature 384, 157–158 (1996)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Janvier, P. The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Palaeontology 39, 259–287 (1996)

    Google Scholar 

  28. 28

    Farris, J. S. HENNIG86, version 1.5. Program and user's manual (published by the author, Port Jefferson Station, New York, 1988).

  29. 29

    Courrol Ramos, T. TREE GARDENER, version 1.0. 〈http://www.icn.unal.edu.co/extensio/servicio/servicio.html〉 (1996).

Download references

Acknowledgements

This work was supported by the Ministry of Sciences and Technology of China, the Natural Science Foundation of China, the Ministry of Education of China, the National Geographic Society (USA), The Royal Society, and St John's College, Cambridge. We thank K. Kardong and B. J. Swalla. L. Guo, X. Cheng, M. Cheng and S. Last are thanked for technical assistance, and Y. Ji and H. Guo for fieldwork help.

Author information

Affiliations

Authors

Corresponding author

Correspondence to D.-G. Shu.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shu, D., Morris, S., Han, J. et al. Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature 421, 526–529 (2003). https://doi.org/10.1038/nature01264

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

Quick links

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