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Three-dimensional limb joint mobility in the early tetrapod Ichthyostega

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.

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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.

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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.

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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.

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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)

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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

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