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:

Vertebral architecture in the earliest stem tetrapods

Subjects

Abstract

The construction of the vertebral column has been used as a key anatomical character in defining and diagnosing early tetrapod groups1. Rhachitomous vertebrae2—in which there is a dorsally placed neural arch and spine, an anteroventrally placed intercentrum and paired, posterodorsally placed pleurocentra—have long been considered the ancestral morphology for tetrapods1,3,4,5,6. Nonetheless, very little is known about vertebral anatomy in the earliest stem tetrapods, because most specimens remain trapped in surrounding matrix, obscuring important anatomical features7,8,9. Here we describe the three-dimensional vertebral architecture of the Late Devonian stem tetrapod Ichthyostega using propagation phase-contrast X-ray synchrotron microtomography. Our scans reveal a diverse array of new morphological, and associated developmental and functional, characteristics, including a possible posterior-to-anterior vertebral ossification sequence and the first evolutionary appearance of ossified sternal elements. One of the most intriguing features relates to the positional relationships between the vertebral elements, with the pleurocentra being unexpectedly sutured or fused to the intercentra that directly succeed them, indicating a ‘reverse’ rhachitomous design10. Comparison of Ichthyostega with two other stem tetrapods, Acanthostega7 and Pederpes8, shows that reverse rhachitomous vertebrae may be the ancestral condition for limbed vertebrates. This study fundamentally revises our current understanding11 of vertebral column evolution in the earliest tetrapods and raises questions about the presumed vertebral architecture of tetrapodomorph fish12,13 and later, more crownward, tetrapods.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Virtual restoration of vertebral elements in the earliest stem tetrapods, depicted in left lateral view.
Figure 2: Thoracic region of Ichthyostega (MGUH VP 6115) rendered from PPC-SRµCT data.
Figure 3: Lumbar region of Ichthyostega (MGUH VP 29017a) rendered from PPC-SRµCT data.

Similar content being viewed by others

References

  1. Romer, A. S. Review of the Labyrinthodontia. Bull. Mus. Comp. Zool. Harv. 99, 368 (1947)

    Google Scholar 

  2. Cope, E. D. Geology and palaeontology. Am. Nat. 5, 324–328 (1878)

    Google Scholar 

  3. Jarvik, E. On the fish-like tail in the ichthyostegid stegocephalians. Medd. Gronl. 114, 1–90 (1952)

    Google Scholar 

  4. Romer, A. S. The skeleton of the lower Carboniferous labyrinthodont Pholidogaster pisciformis. Bull. Mus. Comp. Zoo. Harv. 131, 129–159 (1964)

    Google Scholar 

  5. Panchen, A. L. The homologies of the labyrinthodont centrum. Evolution 21, 24–33 (1967)

    Article  CAS  Google Scholar 

  6. Panchen, A. L. in Problems in Vertebrate Evolution (ed. Andrews, S. & Miles, R. S. ) 289–318 (Academic, 1977)

    Google Scholar 

  7. Coates, M. I. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution. Trans. R. Soc. Edinb. Earth Sci. 87, 363–421 (1996)

    Article  Google Scholar 

  8. Clack, J. A. An early tetrapod from ‘Romer’s Gap’. Nature 418, 72–76 (2002)

    Article  ADS  CAS  Google Scholar 

  9. Ahlberg, P. E., Clack, J. A. & Blom, H. The axial skeleton of the Devonian tetrapod Ichthyostega. Nature 437, 137–140 (2005)

    Article  ADS  CAS  Google Scholar 

  10. Shishkin, M. A. The axial skeleton of early amphibians and the origin of resegmentation in tetrapod vertebrae. Prog. Zool. 35, 180–195 (1989)

    Google Scholar 

  11. Benton, M. J. Vertebrate Palaeontology 3rd edn (Blackwell, 2005)

    Google Scholar 

  12. Andrews, S. M. & Westoll, T. S. The postcranial skeleton of Eusthenopteron foordi Whiteaves. Trans. R. Soc. Edinb. 68, 207–329 (1970)

    Article  Google Scholar 

  13. Vorobyeva, E. I. & 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, 1991)

    Google Scholar 

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

    Google Scholar 

  15. Jarvik, E. The Devonian tetrapod Ichthyostega. Fossils Strata 40, 1–206 (1996)

    Google Scholar 

  16. Pierce, S. E., Clack, J. A. & Hutchinson, J. R. Three-dimensional limb joint mobility in the early tetrapod Ichthyostega. Nature 486, 523–526 (2012)

    Article  ADS  CAS  Google Scholar 

  17. Carlson, K. J. et al. The endocast of MH1, Australopithecus sediba. Science 333, 1402–1407 (2011)

    Article  ADS  CAS  Google Scholar 

  18. Slijper, E. Comparative Biologic-Anatomical Investigations on the Vertebral Column and Spinal Musculature of Mammals (North-Holland, 1946)

    Google Scholar 

  19. Pierce, S. E., Clack, J. A. & Hutchinson, J. R. Comparative axial morphology in pinnipeds and its correlation with aquatic locomotory behaviour. J. Anat. 219, 502–514 (2011)

    Article  CAS  Google Scholar 

  20. Carroll, R. L., Kuntz, A. & Albright, K. Vertebral development and amphibian evolution. Evol. Dev. 1, 36–48 (1999)

    Article  CAS  Google Scholar 

  21. Cote, S., Carroll, R., Cloutier, R. & Bar-Sagi, L. Vertebral development in the Devonian sarcopterygian fish Eusthenopteron foordi and the polarity of vertebral evolution in non-amniote tetrapods. J. Vertebr. Paleontol. 22, 487–502 (2002)

    Article  Google Scholar 

  22. Dequéant, M.-L. & Pourquié, O. Segmental patterning of the vertebrate embryonic axis. Nature Rev. Genet. 9, 370–382 (2008)

    Article  Google Scholar 

  23. Wellik, D. M. Hox patterning of the vertebrate axial skeleton. Dev. Dyn. 236, 2454–2463 (2007)

    Article  CAS  Google Scholar 

  24. Callier, V., Clack, J. A. & Ahlberg, P. E. Contrasting developmental trajectories in the earliest known tetrapod forelimbs. Science 324, 364–367 (2009)

    Article  ADS  CAS  Google Scholar 

  25. Long, J. H., Pabst, D. A., Shepherd, W. R. & McLellan, W. A. Locomotor design of dolphin vertebral columns: bending mechanics and morphology of Delphinus delphis. J. Exp. Biol. 200, 65–81 (1997)

    PubMed  Google Scholar 

  26. Milner, A. R. & Sequeira, S. E. K. The temnospondyl amphibians from the Viséan of East Kirkton, West Lothian, Scotland. Trans. Roy. Soc. Edin. 84, 331–361 (1993)

    Google Scholar 

  27. Hildebrand, M. & Goslow, G. Analysis of Vertebrate Structure 5th edn (John Wiley & Sons, 2001)

    Google Scholar 

  28. Aoyama, H. & Asamoto, K. The developmental fate of rostral/caudal half of a somite for vertebra and rib formation: experimental confirmation of the resegmentation theory using chick-quail chimeras. Mech. Dev. 99, 71–82 (2000)

    Article  CAS  Google Scholar 

  29. Fleming, A., Keynes, R. & Tannahill, D. A central role for the notochord in vertebral patterning. Development 131, 873–880 (2004)

    Article  CAS  Google Scholar 

  30. Morin-Kensicki, E. M., Melancon, E. & Eisen, J. S. Segmental relationship between somites and vertebral column in zebrafish. Development 129, 3851–3860 (2002)

    CAS  PubMed  Google Scholar 

  31. Paganin, D., Mayo, S. C., Gureyev, T. E., Miller, P. R. & Wilkins, S. W. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J. Microsc. 206, 33–40 (2002)

    Article  MathSciNet  CAS  Google Scholar 

  32. Lyckegaard, A., Johnson, G. & Tafforeau, P. Correction of ring artifacts in X-ray tomographic images. Int. J. Tomograph. Stat. 18, 1–9 (2011)

    Google Scholar 

  33. Sanchez, S., Ahlberg, P. E., Trinajstic, K., Mirone, A. & Tafforeau, P. Three dimensional synchrotron virtual paleohistology: a new insight into the world of fossil bone microstructures. Microsc. Microanal. 18, 1095–1105 (2012)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank the European Synchrotron Radiation Facility (ESRF) in Grenoble, France, for access to beamline ID19; S. Schmidt for support using the μCT scanner at Abertay University; J. Liston and the Glasgow Hunterian Museum for access to fossils in their care; and G. Cuny for access to collections housed in the Geological Museum at the University of Copenhagen. This research was supported by NERC grants NE/G005877/1 and NE/G00711X/1 (J.A.C., J.R.H. and S.E.P.) and ERC grant 233111 (P.E.A. and S.S.).

Author information

Authors and Affiliations

Authors

Contributions

The second to fifth authors have been arranged in alphabetical order. S.E.P., P.E.A., J.R.H. and J.A.C. conceived and designed the project. S.E.P., P.E.A. and J.A.C. analysed and interpreted the data. S.E.P. developed the manuscript, including the main text, figures and Supplementary Information. S.S. and P.T. conceived, designed and performed the synchrotron experiments, processed and reconstructed the raw PPC-SRμCT scan data and wrote the PPC-SRμCT methods section. S.E.P. and J.L.M. performed, processed and reconstructed the μCT scan data. J.L.M. segmented all scan data and composed Supplementary Fig. 2. All authors provided a critical review of the manuscript and approved the final draft.

Corresponding author

Correspondence to Stephanie E. Pierce.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

The synchrotron data will be made available through the European Synchrotron Radiation Facility (ESRF) palaeontology database (http://paleo.esrf.eu). To allow exploration of the scan data, reduced and compressed image stack movies have been deposited in the Dryad Digital Repository (http://dx.doi.org/10.5061/dryad.0003s).

Supplementary information

Supplementary Information

This file includes Supplementary Figures 1-5. Supplementary Figure 1 shows vertebral column of Ichthyostega MGUH VP 6115 entombed in ribcage. Supplementary Figure 2 contains PPC-SRµCT slices of Ichthyostega showing micro-anatomical structure of sternabrae. Supplementary Figure 5 shows anatomical and taphonomic details of stenebrae. Supplementary Figure 4 shows alternative positions of pleurocentra/intercentra in Pederpes and Supplementary Figure 5 shows details of the articulation between pleurocentra/intercentra in Ichthyostega, Acanthostega and Pederpes. (PDF 3601 kb)

Thoracic vertebral column and ribcage of Ichthyostega stensioi

This video shows the segmented PPC-SRµCT of Ichthyostega stensioi MGUH VP 6115 spinning in yaw and roll. (MOV 29315 kb)

Lumbar vertebral column of Ichthyostega eigili

This video shows the segmented PPC-SRµCT of Ichthyostega eigili MGUH VP 29017a spinning in yaw and roll. (MOV 31993 kb)

Dorsal vertebral column segment of Acanthostega gunnari

This video shows the segmented PPC-SRµCT of Acanthostega gunnari MGUH f.n. 1227 spinning in yaw. (MOV 18040 kb)

Dorsal vertebral column segment of Pederpes finneyae

This video shows the segmented µCT of Pederpes finneyae GLAHMS 100815 spinning in yaw. (MOV 14340 kb)

Unfused pleurocentra of Ichthyostega stensioi

This video shows the transverse micro-anatomical structure of the third (anterior) thoracic centrum of Ichthyostega stensioi MGUH VP 6115 with unfused pleurocentra. (MOV 5428 kb)

Fused pleurocentra of Ichthyostega stensioi

This video shows the transverse micro-anatomical structure of the seventh (posterior) thoracic centrum of Ichthyostega stensioi MGUH VP 6115 with fused pleurocentra. (MOV 5096 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pierce, S., Ahlberg, P., Hutchinson, J. et al. Vertebral architecture in the earliest stem tetrapods. Nature 494, 226–229 (2013). https://doi.org/10.1038/nature11825

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11825

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