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


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.


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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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).


PA Jenkins, DM Walsh, An early Jurassic caecilian with limbs. Nature 365, 246–250 (1993).
FA Jenkins, DM Walsh, RL Carroll, Anatomy of Eocaecilia micropodia, a limbed caecilian of the Early Jurassic. Bull Mus Comp Zool 158, 285–365 (2007).
SE Evans, D Sigogneau‐Russell, A stem‐group caecilian (Lissamphibia: Gymnophiona) from the Lower Cretaceous of North Africa. Palaeontol 44, 259–273 (2001).
HC Maddin, Jr FA Jenkins, JS Anderson, The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of Caecilians. PLoS One 7, e50743 (2012).
HC Maddin, JS Anderson, Evolution of the amphibian ear with implications for lissamphibian phylogeny: Insight gained from the caecilian inner ear. Fieldiana Life Earth Sci 5, 59–76 (2012).
JS Anderson, RR Reisz, D Scott, NB Fröbisch, SS Sumida, A stem batrachian from the Early Permian of Texas and the origin of frogs and salamanders. Nature 453, 515–518 (2008).
RL Carroll, The Palaeozoic ancestry of salamanders, frogs, and caecilians. Zool J Linn Soc 150, 1–140 (2007).
K Roelants, et al., Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci USA 104, 887–892 (2007).
P Zhang, DB Wake, Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. Mol Phylogenet Evol 53, 492–508 (2009).
D San Mauro, A multilocus timescale for the origin of extant amphibians. Mol Phylogenet Evol 56, 554–561 (2010).
RA Pyron, Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Sys Biol 60, 466–481 (2011).
RA Pyron, JJ Wiens, A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61, 543–583 (2011).
BJ Small, JW Martz, A new aetosaur from the Upper Triassic Chinle Formation of the Eagle Basin, Colorado USA. Geol Soc Lond Spec Publ 379, 393–412 (2013).
RR Schoch, AR Milner, Temnospondyli II: Stereospondyli. Handbuch der Paläoherpetologie, ed P Wellnhofer (Verlag, Munich), pp. 1–203 (2000).
JR Bolt, S Chatterjee, A new temnospondyl amphibian from the Late Triassic of Texas. J Paleontol 74, 670–683 (2000).
AM Yates, AA Warren, The phylogeny of the ‘higher’ temnospondyls (Vertebrata: Choanata) and its implications for the monophyly and origins of the Stereospondyli. Zool J Linn Soc 128, 77–121 (2000).
EM Stephenson, The anatomy of the head of the New Zealand frog. Leiopelma Trans Zool Soc Lond 27, 255–305 (1951).
KQ Gao, NH Shubin, Late Jurassic salamanders from northern China. Nature 410, 574–577 (2001).
M Vater, Is the prefrontal bone in Alpine newt (Triturus alpestris Laurenti, 1768) of dual origin? J Anat 211, 290–295 (2007).
MH Wake, J Hanken, Development of the Skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J Morphol 173, 203–223 (1982).
H Müller, OV Oommen, P Bartsch, Skeletal development of the direct-developing caecilian Gegenophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae). Zoomorphology 124, 171–188 (2005).
H Müller, Ontogeny of the skull, lower jaw, and hyobranchial skeleton of Hypogeophis rostratus (Amphibia: Gymnophiona: Caeciliidae) revisited. J Morphol 267, 968–986 (2006).
RR Schoch, The evolution of major temnospondyl clades: An inclusive phylogenetic analysis. J Syst Palaeontology 11, 673–705 (2013).
RA Pyron, A likelihood method for assessing molecular divergence time estimates and the placement of fossil calibrations. Syst Biol 59, 185–194 (2010).
Y Okajima, Y Kumazawa, Mitogenomic perspectives into iguanid phylogeny and biogeography: Gondwanan vicariance for the origin of Madagascan oplurines. Gene 441, 28–35 (2009).
AF Hugall, R Foster, MS Lee, Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Syst Biol 56, 543–563 (2007).
ME Alfaro, et al., Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Natl Acad Sci USA 106, 13410–13414 (2009).
XX Shen, D Liang, JZ Wen, P Zhang, Multiple genome alignments facilitate development of NPCL markers: A case study of tetrapod phylogeny focusing on the position of turtles. Mol Biol Evol 28, 3237–3252 (2011).
Y Kumazawa, Mitochondrial genomes from major lizard families suggest their phylogenetic relationships and ancient radiations. Gene 388, 19–26 (2007).
XX Shen, D Liang, P Zhang, The development of three long universal nuclear protein-coding locus markers and their application to osteichthyan phylogenetics with nested PCR. PLoS One 7, e39256 (2012).
P Zhang, MH Wake, A mitogenomic perspective on the phylogeny and biogeography of living caecilians (Amphibia: Gymnophiona). Mol Phylogenet Evol 53, 479–491 (2009).
SB Hedges, S Kumar The Timetree of Life (Oxford Univ Press, Oxford, 2009).
D Marjanović, M Laurin, Fossils, molecules, divergence times, and the origin of lissamphibians. Syst Biol 56, 369–388 (2007).
T Sigurdsen, JR Bolt, The Lower Permian amphibamid Doleserpeton (Temnospondyli: Dissorophoidea), the interrelationships of amphibamids, and the origin of modern amphibians. J Vert Paleont 30, 1360–1377 (2010).
AM Jeannot, R Damiani, BS Rubidge, Cranial anatomy of the Early Triassic stereospondyl Lydekkerina huxleyi (Tetrapoda: Temnospondyli) and the taxonomy of South African lydekkerinids. J Vert Paleont 26, 822–838 (2006).
HC Maddin, JC Olori, JS Anderson, A redescription of Carrolla craddocki (Lepospondyli: Brachystelechidae) based on high-resolution CT, and the impacts of miniaturization and fossoriality on morphology. J Morphol 272, 722–743 (2011).
M Szostakiwskyj, JD Pardo, JS Anderson, Micro-CT study of Rhynchonkos stovalli (Lepospondyli, Recumbirostra), with description of two new genera. PLoS One 10, e0127307 (2015).
JD Pardo, M Szostakiwskyj, JS Anderson, Cranial morphology of the brachystelechid ‘microsaur’ Quasicaecilia texana Carroll provides new insights into the diversity and evolution of braincase morphology in recumbirostran ‘microsaurs’. PLoS One 10, e0130359 (2015).
JS Anderson, Incorporating ontogeny into the matrix: A phylogenetic evaluation of developmental evidence for the origin of modern amphibians. Major Transitions in Vertebrate Evolution, eds JS Anderson, H-D Sues (Indiana Univ Press, Bloomington), pp. 182–227 (2007).
RA Nussbaum, The evolution of a unique dual jaw‐closing mechanism in caecilians:(Amphibia: Gymnophiona) and its bearing on caecilian ancestry. J Zool 199, 545–554 (1983).
G Vallin, M Laurin, Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians. J Vert Paleont 24, 56–72 (2004).
JD Pardo, M Szostakiwskyj, PE Ahlberg, JS Anderson, Hidden morphological diversity among early tetrapods. Nature, in press.
F Witzmann, I Werneburg, The palatal interpterygoid vacuities of temnospondyls and the implications for the associated eye and jaw musculature. Anat Rec (Hoboken), 2017).
V Fernandez, et al., Synchrotron reveals Early Triassic odd couple: Injured amphibian and aestivating therapsid share burrow. PLoS One 8, e64978 (2013).
TE Hetherington, MH Wake, The lateral line system in larval Ichthyophis (Amphibia: Gymnophiona). Zoomorphology 93, 209–225 (1979).
JA Clack, AR Milner, Morphology and systematics of the Pennsylvanian amphibian Platyrhinops lyelli (Amphibia: Temnospondyli). Earth Environ Sc Trans Roy Soc Edinburgh 100, 275–295 (2009).
RR Schoch, AR Milner, Temnospondyli. Handbuch der Paläoherpetologie, ed Wellnhofer IP (Verlag, Munich), pp. 1–150 (2014).
JC Rage, Z Roček, Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the early Triassic. Palaeontogr Abt A 206, 1–16 (1989).
SE Evans, M Borsuk-Bialynicka, A stem-group frog from the Early Triassic of Poland. Acta Palaeontol Pol 43, 573–580 (1998).
F Ronquist, P van der Mark, JP Huelsenbeck, Bayesian phylogenetic analysis using MrBayes. The Phylogenetic Handbook, eds AM Vandamme, M Salemi, P Lemey (Cambridge Univ Press, 2nd Ed, Cambridge, UK), pp. 210–266 (2009).
D Swofford PAUP* Phylogenetic Analysis Using Parsimony v. 4.0a151 (Sinauer Associates, Sunderland, MA, 1999).
PO Lewis, A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50, 913–925 (2001).

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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


Submission history

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


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


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.


This article is a PNAS Direct Submission.



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


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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