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:

Devonian arthrodire embryos and the origin of internal fertilization in vertebrates

Abstract

Evidence of reproductive biology is extremely rare in the fossil record. Recently the first known embryos were discovered within the Placodermi1, an extinct class of armoured fish, indicating a viviparous mode of reproduction in a vertebrate group outside the crown-group Gnathostomata (Chondrichthyes and Osteichthyes). These embryos were found in ptyctodontids, a small group of placoderms phylogenetically basal to the largest group, the Arthrodira2,3. Here we report the discovery of embryos in the Arthrodira inside specimens of Incisoscutum ritchiei from the Upper Devonian Gogo Formation of Western Australia4 (approximately 380 million years ago), providing the first evidence, to our knowledge, for reproduction using internal fertilization in this diverse group. We show that Incisoscutum and some phyllolepid arthrodires possessed pelvic girdles with long basipterygia that articulated distally with an additional cartilaginous element or series, as in chondrichthyans, indicating that the pelvic fin was used in copulation. As homology between similar pelvic girdle skeletal structures in ptyctodontids, arthrodires and chondrichthyans is difficult to reconcile in the light of current phylogenies of lower gnathostomes2,3,5, we explain these similarities as being most likely due to convergence (homoplasy). These new finds confirm that reproduction by internal fertilization and viviparity was much more widespread in the earliest gnathostomes than had been previously appreciated.

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: Incisoscutum ritchiei specimens showing embryo fossils.
Figure 2: Placoderm and shark pelvic structures.
Figure 3: Lower gnathostome phylogenies showing reproductive strategies.

Similar content being viewed by others

References

  1. Long, J. A., Trinajstic, K., Young, G. C. & Senden, T. Live birth in the Devonian period. Nature 453, 650–652 (2008)

    Article  ADS  CAS  Google Scholar 

  2. Goujet, D. & Young, G. C. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Cloutier, R.) 109–126 (Dr Freiderich Pfeil, 2004)

    Google Scholar 

  3. Brazeau, M. D. The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins. Nature 457, 305–308 (2009)

    Article  ADS  CAS  Google Scholar 

  4. Dennis, K. & Miles, R. S. A pachyosteomorph arthrodire from Gogo, Western Australia. Zool. J. Linn. Soc. 73, 213–258 (1981)

    Article  Google Scholar 

  5. Janvier, P. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E.) 172–186 (Taylor & Francis, 2001)

    Google Scholar 

  6. Wourms, J. Viviparity: The maternal-fetal relationship in fishes. Am. Zool. 21, 473–515 (1981)

    Article  Google Scholar 

  7. Blackburn, D. in Viviparous Fishes (eds Grier, H. & Uribe, M.) 287–301 (New Life Publications, 2005)

    Google Scholar 

  8. López, J. A., Ryburn, J. A., Fedrigo, O. & Naylor, G. J. P. Phylogeny of sharks of the family Triakidae (Carcharhiniformes) and its implications for the evolution of carcharhiniform placental viviparity. Mol. Phyl. Evol. 40, 50–60 (2006)

    Article  Google Scholar 

  9. Mank, J. E. & Avise, J. C. Supertree analyses of the roles of viviparity and habitat in the atherinomorph fishes. Eur. Soc. Evol. Biol 19, 734–740 (2006)

    Article  CAS  Google Scholar 

  10. Webb, S. et al. Molecular phylogeny of the livebearing Goodeidae (Cyprinidontiformes). Mol. Phyl. Evol. 30, 527–544 (2004)

    Article  CAS  Google Scholar 

  11. Lee, M. Y. S. & Shine, R. Reanalysis of the evolution of viviparity and egg-guarding in squamate reptiles. Herpetologica 55, 538–549 (1998)

    Google Scholar 

  12. Davidson, R. & Trewin, N. Unusual preservation of the internal organs of acanthodian and actinopterygian fish in the Middle Devonian of Scotland. Scot. J. Geol. 41, 129–134 (2005)

    Article  Google Scholar 

  13. Long, J. A. Swimming in Stone—The Amazing Gogo Fossils of the Kimberley 320 (Fremantle Arts Centre Press, 2006)

    Google Scholar 

  14. Trewin, N. H. Palaeoecology and sedimentology of the Achanarras fish bed of the Middle Old Red Sandstone, Scotland. Trans. R. Soc. Edinb. Earth Sci. 77, 21–46 (1986)

    Article  Google Scholar 

  15. Maxwell, E. E. & Caldwell, M. W. First record of live birth in Cretaceous ichthyosaurs: closing an 80 million year gap. Proc. R. Soc. Lond. B 270 (suppl.). S104–S107 (2003)

    Article  Google Scholar 

  16. Chiappe, L. M., Cordorniu, L., Greller-Tinner, G. & Rivarola, D. Argentinian unhatched pterosaur fossil. Nature 432, 571–572 (2004)

    Article  ADS  CAS  Google Scholar 

  17. Young, G. C. Antiarchs (placoderm fishes) from the Devonian Aztec Siltstone, southern Victoria Land, Antarctica. Palaeontographica A202, 1–125 (1988)

    Google Scholar 

  18. Upeniece, I. The unique fossil assemblage from the Lode Quarry (Upper Devonian, Latvia). Mitt. Mus. Natkd. Berl. Geowiss 4, 101–119 (2001)

    Google Scholar 

  19. Long, J. A. New phyllolepid placoderms from the Late Devonian of Victoria, Australia and the relationships of the group. Proc. Linn. Soc. NSW 107, 263–308 (1984)

    Google Scholar 

  20. Ritchie, A. Cowralepis, a new genus of phyllolepid fish (Pisces, Placodermi) from the Late Middle Devonian of New South Wales, Australia. Proc. Linn. Soc. NSW 126, 215–259 (2005)

    Google Scholar 

  21. Sewertzoff, A. N. Development of the pelvic fins of Acipenser ruthenus. New data for the theory of the paired fins of fishes. J. Morph. Physiol. 41, 547–579 (1926)

    Article  Google Scholar 

  22. Bürgin, T. Reproduction in the Middle Triassic actinopterygians; complex fin structures and evidence of viviparity in fossil fishes. Zool. J. Linn. Soc. 100, 379–391 (1990)

    Article  Google Scholar 

  23. Schultze, H.-P. Early growth stages in coelacanth fishes. Nat. New Biol. 236, 90–91 (1972)

    Article  CAS  Google Scholar 

  24. Lund, R. Viviparity and interuterine feeding in a new holocephalan fish from the Lower Carboniferous of Montana. Science 209, 697–699 (1980)

    Article  ADS  CAS  Google Scholar 

  25. Miles, R. S. Observations on the ptyctodont fish, Rhamphodopsis Watson. Zool. J. Linn. Soc. 47, 99–120 (1967)

    Article  Google Scholar 

  26. Young, G. C. The relationships of placoderm fishes. Zool. J. Linn. Soc. 88, 1–57 (1986)

    Article  MathSciNet  Google Scholar 

  27. Stensiö, E. A. Anatomical Studies on the Arthrodiran Head. Kungl. Svenska Vetensk. Akad. Handl. 4 (9) 2, 1–419 (1963)

Download references

Acknowledgements

We thank M. Brazeau for access to his manuscript before publication, A. Ritchie for discussions, and G. Young and G. Edgecombe for reviewing the manuscript. We also thank K. Bifield for the photograph of WAM 04.10.02, and the Centre for Microscopy, Characterisation and Analysis, UWA, for microscopy assistance. J.A.L. and K.T. are supported by Australian Research Council Discovery grants.

Author Contributions All three authors contributed equally to the description of the new embryos and arthrodire pelvic structures, and to the general discussion; J.A.L. provided new data on Victorian phyllolepids.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John A. Long.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Supplementary References and Supplementary Figures 1-3 with Legends (PDF 3355 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Long, J., Trinajstic, K. & Johanson, Z. Devonian arthrodire embryos and the origin of internal fertilization in vertebrates. Nature 457, 1124–1127 (2009). https://doi.org/10.1038/nature07732

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature07732

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