Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Lamprey-like gills in a gnathostome-related Devonian jawless vertebrate

Abstract

So far, the Palaeozoic fossil jawless vertebrates have not provided any direct evidence for the organization of the gills, apart from vague impressions—supposedly left by gill filaments—on the bony surface of the gill chamber in certain armoured forms or ‘ostracoderms’ (for example, osteostracans and heterostracans)1. The latter are currently regarded as more closely related to the living jawed vertebrates (crown gnathostomes) than to the living jawless vertebrates (hagfish and lampreys, or cyclostomes)2,3. Here we report the first direct evidence for the position of the gill filaments—possibly supported by gill rays—enclosed by gill pouches in a 370-million year (Myr)-old jawless vertebrate, Endeiolepis, from the Late Devonian fossil fish site of Miguasha, Quebec, Canada. This extinct jawless fish has much the same gill organization as living lampreys, although it possesses an unusually large number of gill pouches—a condition unlike that in any extant vertebrates and that raises questions about gill development4. Endeiolepis is currently regarded as a close relative of anaspids3, a group of 410–430-Myr-old ‘ostracoderms’. Assuming that current vertebrate phylogeny is correct, this discovery demonstrates that pouches enclosing the gills are primitive for vertebrates, but have been subsequently lost in jawed vertebrates.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Purchase on Springer Link

Instant access to full article PDF

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The two ‘naked anaspids’ from the Upper Devonian of Miguasha, Quebec, Canada.
Figure 2: Endeiolepis aneri (MHNM 01-154).

Similar content being viewed by others

References

  1. Janvier, P. Early Vertebrates (Oxford Univ. Press, Oxford, 1996)

    Google Scholar 

  2. Donoghue, P. C. J., Forey, P. L. & Aldridge, R. J. Conodont affinity and chordate phylogeny. Biol. Rev. 75, 191–251 (2000)

    Article  CAS  PubMed  Google Scholar 

  3. 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)

    Article  Google Scholar 

  4. Janvier, P. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Cloutier, R. & Wilson, M. V. H.) 29–52 (Dr Friedrich Pfeil, Munich, 2004)

    Google Scholar 

  5. Arsenault, M., Desbiens, S., Janvier, P. & Kerr, J. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Cloutier, R. & Wilson, M. V. H.) 439–454 (Dr Friedrich Pfeil, Munich, 2004)

    Google Scholar 

  6. Stensiö, E. A. A new anaspid from the Upper Devonian of Scaumenac Bay in Canada, with remarks on the other anaspids. K. Svenska Vetensk. Akad. Handl. 18, 1–25 (1939)

    Google Scholar 

  7. Arsenault, M. & Janvier, P. in Early Vertebrates and Related Problems of Evolutionary Biology (eds Chang, M.-M., Liu, Y.-H. & Zhang, G.-R.) 19–37 (Science Press, Beijing, 1991)

    Google Scholar 

  8. Janvier, P. in Devonian Fishes and Plants of Miguasha, Québec, Canada (eds Schultze, H. P. & Cloutier, R.) 134–140 (Dr Friedrich Pfeil, Munich, 1996)

    Google Scholar 

  9. Janvier, P. & Arsenault, M. Calcification of early vertebrate cartilage. Nature 417, 609 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Marinelli, W. & Strenger, A. Vergleichende Anatomie und Morphologie der Wirbeltiere. 1. Lampetra fluviatilis (L.) (Franz Deuticke, Vienna, 1954)

    Google Scholar 

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

    Google Scholar 

  12. Maisey, J. G. Visceral skeleton and musculature of a Late Devonian shark. J. Vert. Paleont. 9, 174–190 (1989)

    Article  Google Scholar 

  13. Hou, H. G., Aldridge, R. J., Siveter, D. J., Siveter, D. J. & Feng, X.-H. New evidence on the anatomy and phylogeny of the earliest vertebrates. Proc. R. Soc. Lond. B 269, 1865–1869 (2002)

    Article  Google Scholar 

  14. Mallatt, J. & Chen, J. Fossil sister-group of craniates: predicted and found. J. Morphol. 258, 1–31 (2003)

    Article  PubMed  Google Scholar 

  15. Watson, D. M. S. A consideration of ostracoderms. Phil. Trans. R. Soc. Lond. B 238, 1–15 (1954)

    Article  ADS  Google Scholar 

  16. Stensiö, E. Traité de Paléontologie Vol. 4 (Masson, Paris, 1964)

    Google Scholar 

  17. Mallatt, J. Ventilation and the origin of jawed vertebrates: a new mouth. Zool. J. Linn. Soc. 117, 329–404 (1996)

    Article  Google Scholar 

  18. Massabuau, J. C. From low arterial- to low tissue-oxygenation strategy. An evolutionary theory. Respir. Physiol. 128, 299–315 (2001)

    Article  PubMed  Google Scholar 

  19. Prichonnet, G., Di Vergilio, M. & Chidiac, Y. in Devonian Fishes and Plants of Miguasha, Québec, Canada (eds Schultze, H. P. & Cloutier, R.) 23–36 (Dr Friedrich Pfeil, Munich, 1996)

    Google Scholar 

  20. Graham, A. & Smith, A. Patterning the pharyngeal arches. Bioessays 23, 54–61 (2001)

    Article  CAS  PubMed  Google Scholar 

  21. Quinlan, R., Martin, P. & Graham, A. The role of actin cables in directing the morphogenesis of the pharyngeal pouches. Development 131, 593–599 (2004)

    Article  CAS  PubMed  Google Scholar 

  22. Donoghue, P. C. J. & Purnell, M. A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312–319 (2005)

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Author Contributions J.A.W. discovered the specimen MHNM 01-154 described herein; the other authors have contributed equally to the article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philippe Janvier.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains a discussion on synonymy, taphonomy and interpretation of the gill pouches of Euphanerops and Endeiolepis. (DOC 23 kb)

Supplementary Figure 1

This illustrates the organization and orientation of the gill pouch natural casts in Endeiolepis. (PDF 90 kb)

Supplementary Figure 2

A simplified phylogenetic tree of euchordates, showing the nodes where gill pouches and gill rays may have appeared and then disappeared. (PDF 134 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Janvier, P., Desbiens, S., Willett, J. et al. Lamprey-like gills in a gnathostome-related Devonian jawless vertebrate. Nature 440, 1183–1185 (2006). https://doi.org/10.1038/nature04471

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04471

This article is cited by

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

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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