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:

Tetrapod-like middle ear architecture in a Devonian fish

Nature volume 439, pages 318–321 (2006)Cite this article

Abstract

Few fossils show the incipient stages of complex morphological transformations1. For example, the earliest stages in the remodelling of the spiracular tract and suspensorium (jaw suspension) of osteolepiform fishes2,3,4 into the middle ear of tetrapods have remained elusive3. The most primitive known tetrapods show a middle ear architecture that is very different from osteolepiforms such as Eusthenopteron3, with little indication of how this transformation took place. Here we present an analysis of tetrapod middle ear origins that is based on a detailed study of Panderichthys, the immediate sister taxon of tetrapods. We show that the spiracular region is radically transformed from osteolepiforms and represents the earliest stages in the origin of the tetrapod middle ear architecture. The posterior palatoquadrate of Panderichthys is completely tetrapod-like and defines a similarly tetrapod-like spiracular tract. The hyomandibula has lost its distal portion, representing a previously unrecognized advance towards a stapes-like morphology. This spiracular specialization suggests that the middle ear of early tetrapods evolved initially as part of a spiracular breathing apparatus5,6.

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
Buy now

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

Figure 1: Hyomandibula and subdivisions of the palatoquadrate of Eusthenopteron foordi.
Figure 2: Suspensorium of Panderichthys LDM 60/123 (Middle to Late Devonian).
Figure 3: Palatoquadrates.
Figure 4: Early evolution of the tetrapod middle ear space.

Similar content being viewed by others

References

  1. Carroll, R. L. Patterns and Processes of Vertebrate Evolution (Cambridge Univ. Press, Cambridge, 1997)

    Google Scholar 

  2. Carroll, R. L. in The Terrestrial Environment and the Origin of Land Vertebrates (ed. Panchen, A. L.) 293–317 (Academic, London, 1980)

    Google Scholar 

  3. Clack, J. A. Patterns and processes in the early evolution of the tetrapod ear. J. Neurobiol. 53, 251–264 (2002)

    Article  Google Scholar 

  4. Clack, J. A. Earliest known tetrapod braincase and the evolution of the stapes and fenestra ovalis. Nature 369, 392–394 (1994)

    Article  ADS  Google Scholar 

  5. Panchen, A. L. On the amphibian Crassigyrinus scoticus Watson from the Carboniferous of Scotland. Phil. Trans. R. Soc. Lond. B 309, 505–568 (1985)

    Article  ADS  Google Scholar 

  6. Clack, J. A. Discovery of the earliest-known tetrapod stapes. Nature 342, 425–427 (1989)

    Article  CAS  ADS  Google Scholar 

  7. Ahlberg, P. E. & Johanson, Z. Osteolepiforms and the ancestry of tetrapods. Nature 395, 792–794 (1998)

    Article  ADS  Google Scholar 

  8. Ahlberg, P. E. A re-examination of sarcopterygian interrelationships, with special reference to the Porolepiformes. Zool. J. Linn. Soc. 103, 241–287 (1991)

    Article  Google Scholar 

  9. Jarvik, E. On the visceral skeleton in Eusthenopteron with a discussion of the parasphenoid and palatoquadrate in fishes. Kungl. Svenska Vetenskakad. Handl. 5, 1–104 (1954)

    Google Scholar 

  10. Long, J. A., Barwick, R. E. & Campbell, K. S. W. Osteology and functional morphology of the osteolepiform fish Gogonasus andrewsae Long, 1985, from the Upper Devonian Gogo Formation, Western Australia. Rec. West. Aust. Mus. 53 (suppl.), 1–89 (1997)

    Google Scholar 

  11. Lebedev, O. A. Morphology of a new osteolepidid fish from Russia. Bull. Mus. Natl Hist. Nat. C 17, 287–341 (1995)

    Google Scholar 

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

    ADS  Google Scholar 

  13. Gardiner, B. G. The relationships of the palaeoniscoid fishes, a review based on new specimens of Mimia and Moythomasia from the Upper Devonian of Western Australia. Bull. Brit. Mus. (Nat. Hist.) Geol. 37, 173–428 (1984)

    Google Scholar 

  14. Clack, J. A. Acanthostega gunnari, a Devonian tetrapod from Greenland; the snout, palate and ventral parts of the braincase, with a discussion of their significance. Meddelelser Grønland Geosci. 31, 1–24 (1994)

    Google Scholar 

  15. Westoll, T. S. The origin of the tetrapods. Biol. Rev. 18, 78–98 (1943)

    Article  Google Scholar 

  16. Rosen, D. E., Forey, P. L., Gardiner, B. G. & Patterson, C. Lungfishes, tetrapods, paleontology, and plesiomorphy. Bull. Am. Mus. Nat. Hist. 167, 159–276 (1981)

    Google Scholar 

  17. Vorobyeva, E. & Schultze, H.-P. in Origins of the Higher Groups of Tetrapods: Controversy and Consensus (eds Schultze, H.-P. & Trueb, L.) 68–109 (Cornell Univ. Press (Canstock), Ithaca, NY, 1991)

    Google Scholar 

  18. Ahlberg, P. E., Clack, J. A. & Luksevics, E. Rapid braincase evolution between Panderichthys and the earliest tetrapods. Nature 381, 61–64 (1996)

    Article  CAS  ADS  Google Scholar 

  19. Clack, J. A. The neurocranium of Acanthostega gunnari Jarvik and the evolution of the otic region in tetrapods. Zool. J. Linn. Soc. 122, 61–97 (1998)

    Article  Google Scholar 

  20. Ahlberg, P. E., Luksevics, E. & Lebedev, O. The first tetrapod finds from the Devonian (Upper Famennian) of Latvia. Phil. Trans. R. Soc. Lond. B 343, 303–328 (1994)

    Article  ADS  Google Scholar 

  21. Smithson, T. R. & Thomson, K. S. The hyomandibula of Eusthenopteron foordi Whiteaves (Pisces: Crossopterygii) and the early evolution of the tetrapod stapes. Zool. J. Linn. Soc. 74, 93–103 (1982)

    Article  Google Scholar 

  22. Clack, J. A. Gaining Ground: The Origin and Evolution of Tetrapods (ed. Farlow, J. O.) (Indiana Univ. Press, Bloomington, IN, 2002)

    Google Scholar 

  23. Rand, H. W. The functions of the spiracle of the skate. Am. Nat. 41, 287–302 (1907)

    Article  Google Scholar 

  24. Summers, A. P. & Ferry-Graham, L. A. Ventilatory modes and mechanics of the hedgehog skate (Leucoraja erinacea): testing the continuous flow model. J. Exp. Biol. 204, 1577–1587 (2001)

    CAS  PubMed  Google Scholar 

  25. Clack, J. A. et al. A uniquely specialized ear in a very early tetrapod. Nature 425, 65–69 (2003)

    Article  CAS  ADS  Google Scholar 

  26. Jarvik, E. Basic Structure and Evolution of Vertebrates (Academic, London, 1980)

    Google Scholar 

Download references

Acknowledgements

We thank E. Luksevics and I. Zupins for access to specimens; T. Rowe for computed tomography scan work; M. Arsenault and S. Desbiens for providing the Eusthenopteron specimen and, together with T. Rowe, for allowing us to publish these early results. M.D.B is supported by a Fonds québecois de la recherche sur la nature et les technologies (FQRNT) bourse de maîtrise (graduate scholarship). P.E.A. is supported by a professorship and research grant from Vetenskapsrådet.

Author information

Authors and Affiliations

  1. Subdepartment of Evolutionary Organismal Biology, Department of Physiology and Developmental Biology, Evolutionary Biology Centre, Uppsala University, Norbyv 18A, SE-752 36, Uppsala, Sweden

    Martin D. Brazeau & Per E. Ahlberg

Authors
  1. Martin D. Brazeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Per E. Ahlberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin D. Brazeau.

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 contains an additional description of the Panderichthys specimen from this work. (DOC 22 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brazeau, M., Ahlberg, P. Tetrapod-like middle ear architecture in a Devonian fish. Nature 439, 318–321 (2006). https://doi.org/10.1038/nature04196

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04196

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

Advanced 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