Vertebral architecture in the earliest stem tetrapods

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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.

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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.

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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.).

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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.

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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)

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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

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