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.

Three-dimensional limb joint mobility in the early tetrapod Ichthyostega

Nature volume 486, pages 523–526 (2012)Cite this article

Subjects

Abstract

The origin of tetrapods and the transition from swimming to walking was a pivotal step in the evolution and diversification of terrestrial vertebrates. During this time, modifications of the limbs—particularly the specialization of joints and the structures that guide their motions—fundamentally changed the ways in which early tetrapods could move1,2,3,4. Nonetheless, little is known about the functional consequences of limb anatomy in early tetrapods and how that anatomy influenced locomotion capabilities at this very critical stage in vertebrate evolution. Here we present a three-dimensional reconstruction of the iconic Devonian tetrapod Ichthyostega and a quantitative and comparative analysis of limb mobility in this early tetrapod. We show that Ichthyostega could not have employed typical tetrapod locomotory behaviours, such as lateral sequence walking. In particular, it lacked the necessary rotary motions in its limbs to push the body off the ground and move the limbs in an alternating sequence. Given that long-axis rotation was present in the fins of tetrapodomorph fishes5,6,7, it seems that either early tetrapods evolved through an initial stage of restricted shoulder8,9 and hip joint mobility or that Ichthyostega was unique in this respect. We conclude that early tetrapods with the skeletal morphology and limb mobility of Ichthyostega were unlikely to have made some of the recently described Middle Devonian trackways10.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Three-dimensional reconstruction of Ichthyostega from μCT scan data.
Figure 2: Maximum ranges of mobility in the limb joints of Ichthyostega and five modern tetrapod analogues.
Figure 3: Partitioned range of mobility in the hip joint and shoulder joint of Ichthyostega.

References

  1. Coates, M. I. & Clack, J. A. Polydactyly in the earliest known tetrapod limbs. Nature 347, 66–69 (1990)

    Article  ADS  Google Scholar 

  2. 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 

  3. Clack, J. A. Devonian tetrapod trackways and trackmakers: a review of the fossils and footprints. Palaeogeogr. Palaeoclimatol. Palaeoecol. 130, 227–250 (1997)

    Article  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  6. Shubin, N. H., Daeschler, E. B. & Jenkins, F. A., Jr The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb. Nature 440, 764–771 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Boisvert, C. A., Mark-Kurik, E. & Ahlberg, P. E. The pectoral fin of Panderichthys and the origin of digits. Nature 456, 636–638 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Shubin, N. H., Daeschler, E. B. & Coates, M. I. The evolution of the tetrapod humerus. Science 304, 90–93 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Ahlberg, P. E. Humeral homology and the origin of the tetrapod elbow: a reinterpretation of the enigmatic specimens ANSP 21350 and GSM 104536. Spec. Pap. Palaeontol. 86, 17–29 (2011)

    Google Scholar 

  10. Niedzwiedzki, G., Szrek, P., Narkiewicz, K., Narkiewicz, M. & Ahlberg, P. E. Tetrapod trackways from the early Middle Devonian period of Poland. Nature 463, 43–48 (2010)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Gregory, W. K. & Raven, H. C. Origin of paired fins and limbs. Ann. NY Acad. Sci. 42, 273–360 (1941)

    Article  ADS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  14. King, H. M., Shubin, N. H., Coates, M. I. & Hale, M. E. Behavioural evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes. Proc. Natl Acad. Sci. USA 108, 21146–21151 (2011)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. Edwards, J. L. in Major Patterns of Vertebrate Evolution (eds Hecht, M. K., Goody, P. C. & Hecht, B. M. ) 553–577 (Plenum, 1977)

    Book  Google Scholar 

  16. Rewcastle, S. C. Stance and gait in tetrapods: an evolutionary scenario. Symp. Zool. Soc. Lond. 48, 239–267 (1981)

    Google Scholar 

  17. O’Gorman, F. Observations on terrestrial locomotion in Antarctic seals. Proc. Zool. Soc. Lond. 141, 837–850 (1962)

    Article  Google Scholar 

  18. Ashley-Ross, M. A. Hindlimb kinematics during terrestrial locomotion in a salamander (Dicamptodon tenebrosus). J. Exp. Biol. 193, 255–283 (1994)

    CAS  PubMed  Google Scholar 

  19. Reilly, S. M. & Elias, J. A. Locomotion in Alligator mississippiensis: kinematic effects of speed and posture and their relevance to the sprawling-to-erect paradigm. J. Exp. Biol. 201, 2559–2574 (1998)

    PubMed  Google Scholar 

  20. Jayne, B. C. & Irschick, D. J. Effects of incline and speed on the three-dimensional hindlimb kinematics of a generalized iguanian lizard (Dipsosaurus dorsalis). J. Exp. Biol. 202, 143–159 (1998)

    Google Scholar 

  21. Ashley-Ross, M. A., Lundin, R. & Johnson, K. L. Kinematics of level terrestrial and underwater walking in the California newt, Taricha torosa . J. Exp. Zool. 311A, 240–257 (2009)

    Article  Google Scholar 

  22. Jenkins, F. A., Jr & Goslow, G. E., Jr The functional anatomy of the shoulder of the savannah monitor lizard (Varanus exanthematicus). J. Morphol. 175, 195–216 (1983)

    Article  PubMed  Google Scholar 

  23. Pridmore, P. A. Submerged walking in the epaulette shark Hemiscyllium ocellatum (Hemischyllidae) and its implications for locomotion in rhipidistian fishes and early tetrapods. Zoology 98, 278–297 (1994)

    Google Scholar 

  24. Pace, C. M. & Gibb, A. C. Mudskipper pectoral fin kinematics in aquatic and terrestrial environments. J. Exp. Biol. 212, 2279–2286 (2009)

    Article  CAS  PubMed  Google Scholar 

  25. Markey, M. J. & Marshall, C. R. Terrestrial-style feeding in a very early aquatic tetrapod is supported by evidence from experimental analysis of suture morphology. Proc. Natl Acad. Sci. USA 104, 7134–7138 (2007)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Daeschler, E. B., Shubin, N. H., Thomson, K. S. & Amaral, W. W. A Devonian tetrapod from North America. Science 265, 639–642 (1994)

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Neyt, C. et al. Evolutionary origins of the vertebrate appendicular muscle. Nature 408, 82–88 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Cole, N. J. et al. Development and evolution of the muscles of the pelvic fin. PLoS Biol. 9, e1001168 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Delp, S. L. & Loan, J. P. A graphics-based software system to develop and analyze models of musculoskeletal structures. Comput. Biol. Med. 25, 21–34 (1995)

    Article  CAS  PubMed  Google Scholar 

  30. Barnett, C. H., Davies, D. V. & MacConaill, M. A. Synovial Joints: Their Structure and Mechanics (Longmans, Green & Co., 1961)

    Google Scholar 

Download references

Acknowledgements

We thank J. Molnar for assistance with segmentation, model construction, and movie generation; L. Witmer for access to platypus scan data; Digimorph for access to salamander scan data (National Science Foundation grant IIS-9874781 and IIS-0208675 to T. Rowe); M. Lowe for collections support at the University Museum of Zoology, Cambridge; G. Cuny for access to collections housed in the Geological Museum at the University of Copenhagen; J. Rankin for musculoskeletal modelling support; and P. Ahlberg for commenting on an earlier draft of this manuscript. For access to μCT scanning equipment in their care, we also acknowledge R. Abel, C. Martin and A. Heaver. This research was supported by Natural Environment Research Council grants NE/G005877/1 and NE/G00711X/1.

Author information

Authors and Affiliations

  1. Department of Veterinary Basic Sciences and Structure and Motion Laboratory, The Royal Veterinary College, Hawkshead Lane, Hatfield AL9 7TA, UK,

    Stephanie E. Pierce & John R. Hutchinson

  2. Department of Zoology, University Museum of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK,

    Stephanie E. Pierce & Jennifer A. Clack

Authors
  1. Stephanie E. Pierce
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer A. Clack
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John R. Hutchinson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to project concept and design. S.E.P. collected and analysed the data and wrote the manuscript, including main text, figures and Supplementary Information. J.A.C. and J.R.H. provided a critical review of all aspects of manuscript development. All authors approved the final draft.

Corresponding author

Correspondence to Stephanie E. Pierce.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This proof contains Supplementary Text, which includes details of how the 3D model of Ichthyostega was constructed, Supplementary References, Supplementary Figures 1-6 and Supplementary Tables 1-6. (PDF 1908 kb)

Supplementary Movie 1

This movie shows the 3D whole body reconstruction of Ichthyostega spinning 360 degrees in yaw and roll. (MOV 17633 kb)

Supplementary Movie 2

This movie shows maximum range of motion in the shoulder joint of Ichthyostega during flexion/extension, adduction/abduction and pronation/supination. (MOV 8567 kb)

Supplementary Movie 3

This movie shows maximum range of motion in the hip joint of Ichthyostega during flexion/extension, adduction/abduction and pronation/supination. (MOV 7864 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pierce, S., Clack, J. & Hutchinson, J. Three-dimensional limb joint mobility in the early tetrapod Ichthyostega. Nature 486, 523–526 (2012). https://doi.org/10.1038/nature11124

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11124

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