Stem caecilian from the Triassic of Colorado sheds light on the origins of Lissamphibia

Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved May 18, 2017 (received for review April 26, 2017)
June 19, 2017
114 (27) E5389-E5395

Significance

Research into modern amphibian origins is increasingly focusing on the limbless caecilians, a poorly studied group whose pre-Cenozoic fossils are limited to two species. We describe tiny fossils from the Triassic of Colorado with a mixture of traits found in caecilians and extinct Permian–Triassic temnospondyls: Stereospondyli. Computed 3D tomography shows how skull bones organized around internal structures, and we suggest how these may have become fused or simplified in caecilians. The fossils’ association with burrows highlights ecological diversity of Triassic amphibians as well as when and how burrowing evolved in the stereospondyl ancestors of caecilians. Our narrative for research on amphibian origins highlights the importance of stereospondyls, the most numerous and anatomically diverse amphibian group of the Triassic.

Abstract

The origin of the limbless caecilians remains a lasting question in vertebrate evolution. Molecular phylogenies and morphology support that caecilians are the sister taxon of batrachians (frogs and salamanders), from which they diverged no later than the early Permian. Although recent efforts have discovered new, early members of the batrachian lineage, the record of pre-Cretaceous caecilians is limited to a single species, Eocaecilia micropodia. The position of Eocaecilia within tetrapod phylogeny is controversial, as it already acquired the specialized morphology that characterizes modern caecilians by the Jurassic. Here, we report on a small amphibian from the Upper Triassic of Colorado, United States, with a mélange of caecilian synapomorphies and general lissamphibian plesiomorphies. We evaluated its relationships by designing an inclusive phylogenetic analysis that broadly incorporates definitive members of the modern lissamphibian orders and a diversity of extinct temnospondyl amphibians, including stereospondyls. Our results place the taxon confidently within lissamphibians but demonstrate that the diversity of Permian and Triassic stereospondyls also falls within this group. This hypothesis of caecilian origins closes a substantial morphologic and temporal gap and explains the appeal of morphology-based polyphyly hypotheses for the origins of Lissamphibia while reconciling molecular support for the group’s monophyly. Stem caecilian morphology reveals a previously unrecognized stepwise acquisition of typical caecilian cranial apomorphies during the Triassic. A major implication is that many Paleozoic total group lissamphibians (i.e., higher temnospondyls, including the stereospondyl subclade) fall within crown Lissamphibia, which must have originated before 315 million years ago.

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Acknowledgments

The authors thank Robert Douglass, Heather Finlayson, Jacqueline Lungmus, and Tyler Schlotterbeck for assistance in the field; Harley Armstrong and Vanessa Caranese, Colorado Bureau of Land Management; and Jason Anderson and Hillary Maddin for helpful discussion. HRXCT was performed at the University of Utah HSC Cores Research Facility. The specimens are reposited at the Denver Museum of Nature & Science.

Supporting Information

Supporting Information (PDF)
Appendix (PDF)
Movie S1.
1type_yaw.MPG—3D yaw of holotypic skull (DMNH 56658).
Movie S2.
2type_roll.MPG—3D roll of holotypic skull (DMNH 56658).
Movie S3.
3type_otic.MPG—3D yaw of otic notch and acoustic canal in holotype (DMNH 56658), showing supraoccipital (green), tabular (magenta), squamosal (red), and pterygoid (orange) bones in articulation.
Movie S4.
4type_jaw.MPG—3D roll of mandible in holotype (DMNH 56658).
Movie S5.
5paratype_yaw.MPG—3D yaw of referred (burrow) specimen (DMNH 39033).
Movie S6.
6paratype_roll.MPG—3D roll of referred (burrow) specimen (DMNH 39033).
Movie S7.
7paratype_jaw_roll.MPG—3D roll of referred mandible (DMNH 39033).

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 27
July 3, 2017
PubMed: 28630337

Classifications

Submission history

Published online: June 19, 2017
Published in issue: July 3, 2017

Keywords

  1. burrow
  2. Gymnophiona
  3. temnospondyl
  4. tetrapod
  5. Triassic

Acknowledgments

The authors thank Robert Douglass, Heather Finlayson, Jacqueline Lungmus, and Tyler Schlotterbeck for assistance in the field; Harley Armstrong and Vanessa Caranese, Colorado Bureau of Land Management; and Jason Anderson and Hillary Maddin for helpful discussion. HRXCT was performed at the University of Utah HSC Cores Research Facility. The specimens are reposited at the Denver Museum of Nature & Science.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Jason D. Pardo
Department of Comparative Biology and Experimental Medicine, University of Calgary, Calgary, Alberta, Canada T2N 4N1;
Bryan J. Small
Museum of Texas Tech University, Lubbock, TX 79415;
Adam K. Huttenlocker1 [email protected]
Department of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA 90089

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: J.D.P., B.J.S., and A.K.H. designed research, performed research, contributed new reagents/analytic tools, analyzed data, and wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Stem caecilian from the Triassic of Colorado sheds light on the origins of Lissamphibia
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 27
    • pp. 6873-E5485

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