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Hidden morphological diversity among early tetrapods | Nature
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Hidden morphological diversity among early tetrapods

Nature volume 546, pages 642–645 (2017)Cite this article

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Abstract

Phylogenetic analysis of early tetrapod evolution has resulted in a consensus across diverse data sets1,2,3 in which the tetrapod stem group is a relatively homogenous collection of medium- to large-sized animals showing a progressive loss of ‘fish’ characters as they become increasingly terrestrial4,5, whereas the crown group demonstrates marked morphological diversity and disparity6. The oldest fossil attributed to the tetrapod crown group is the highly specialized aïstopod Lethiscus stocki7,8, which shows a small size, extreme axial elongation, loss of limbs, spool-shaped vertebral centra, and a skull with reduced centres of ossification, in common with an otherwise disparate group of small animals known as lepospondyls. Here we use micro-computed tomography of the only known specimen of Lethiscus to provide new information that strongly challenges this consensus. Digital dissection reveals extremely primitive cranial morphology, including a spiracular notch, a large remnant of the notochord within the braincase, an open ventral cranial fissure, an anteriorly restricted parasphenoid element, and Meckelian ossifications. The braincase is elongate and lies atop a dorsally projecting septum of the parasphenoid bone, similar to stem tetrapods such as embolomeres. This morphology is consistent in a second aïstopod, Coloraderpeton, although the details differ. Phylogenetic analysis, including critical new braincase data, places aïstopods deep on the tetrapod stem, whereas another major lepospondyl lineage is displaced into the amniotes. These results show that stem group tetrapods were much more diverse in their body plans than previously thought. Our study requires a change in commonly used calibration dates for molecular analyses, and emphasizes the importance of character sampling for early tetrapod evolutionary relationships.

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Figure 1: Skull and lower jaw of L. stocki, MCZ 2185.
Figure 2: Braincase and endocast of L. stocki, MCZ 2185.
Figure 3: Time-calibrated phylogeny (majority-rule consensus tree) of major Palaeozoic tetrapod lineages illustrating the relationships of aïstopods and trends in early tetrapod body plan evolution.

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  • 14 August 2017

    The Reviewer Information section was corrected.

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Acknowledgements

We thank S. Pierce, J. Cundiff, the late F. A. Jenkins, C. Schaff, the late W. Amaral, D. Berman, A. Henrici, P. Holroyd, A. C. Milner, J. A. Clack, J. Bolt and W. Simpson for access to specimens, and J. Bolt, R. Carroll, J. A. Clack, M. Coates, N. Fröbisch, D. Germain, A. Huttenlocker, M. Laurin, H. Maddin, D. Marjanović, J. Olori, R. R. Reisz, and R. Schoch for discussions. We particularly thank D. Germain for first suggesting reanalysis of the Lethiscus data set with current computational tools. This research was supported in part by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to J.S.A.

Author information

Authors and Affiliations

  1. Department of Comparative Biology and Experimental Medicine, University of Calgary, 3330 Hospital Drive, Calgary, T2N 4N1, Alberta, Canada

    Jason D. Pardo & Jason S. Anderson

  2. Department of Biological Sciences, University of Calgary, 2500 University Drive, Calgary, T2N 1N4, Alberta, Canada

    Matt Szostakiwskyj

  3. Department of Organismal Biology, Uppsala University, Norbyvägen, Uppsala, Sweden

    Per E. Ahlberg

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  3. Per E. Ahlberg
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Contributions

Project instigated by J.S.A. and J.D.P. Micro-CT volumetric data compiled by J.D.P., M.S., P.E.A. and J.S.A. Phylogenetic analysis by J.D.P., M.S., P.E.A. and J.S.A. Paper written by J.S.A., J.D.P., M.S. and P.E.A.

Corresponding author

Correspondence to Jason S. Anderson.

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The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks D. Marjanović and S. Sumida for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 Skull and lower jaw of L. stocki, MCZ 2185, and lower jaw of C. brilli, CM 47687.

a–j, Skull shown in dorsal (a, b), right lateral (c, d), ventral (e, f), anterior (g, i), and occipital (h, j) views. k–n, Lower jaws shown in medial (k, l) and lateral (m, n) views. All are to scale. inf, internarial fontanelle; mllc, mandibular lateral line canal; pp, postparietal; qrpt, quadrate ramus of pterygoid.

Extended Data Figure 2 Skull of L. stocki, MCZ 2185, main block.

a–d, Specimen figured in dorsal (a), right lateral (b), ventral (c), and left lateral (d) views. All are to scale.

Extended Data Figure 3 Skull of L. stocki, MCZ 2185.

a, Skull roof. b, c, Snout. All are to scale.

Extended Data Figure 4 Skull of C. brilli, CM 47687.

a–c, Specimen figured in dorsal (a), lateral (b), and ventral (c) views. All are to scale. pof, postfrontal; prat, proatlas; ?preop, possible preopercular.

Extended Data Figure 5 Braincase of C. brilli, CM 47687.

a–d, Specimens figured in left lateral (a), dorsal (b), ventral (c), and right lateral (d) views. All are to scale. fme, foramen metoticum; fv, fenestra vestibularis; pit, foramen serving pituitary artery; sphen, sphenethmoid.

Extended Data Figure 6 Lower jaws of L. stocki, MCZ 2185 and C. brilli, CM 47687.

CT volumes on left, line drawings on right. a–h, Left lower jaw of Lethiscus shown in dorsal (a, b), medial (c, d), lateral (e, f), and ventral (g, h) views. i–p, Left lower jaw of C. brilli shown in dorsal (i, j), medial (k, l), lateral (m, n), and ventral (o, p) views. Not to scale. c, coronoid; c1, first coronoid; cf, coronoid foramen; mf, Meckelian foramen.

Extended Data Figure 7 Phylogenetic analysis showing relationships of the aïstopods L. stocki and C. brilli, and selected lepospondyls.

Consensus (a) and bootstrap (b) trees, showing relationships of 58 tetrapod and tetrapodomorph taxa. a, Consensus tree represents majority rule consensus of 36 most parsimonious trees (1,684 steps). Node values indicate per cent frequency for this topology appearing among the most parsimonious trees. b, Bootstrap tree shows majority rule consensus of trees produced via 1,000 bootstrap replicates resampled with replacement. Node values indicate bootstrap support.

Supplementary information

Supplementary Information

This file contains Supplementary details regarding the matrix construction and coding changes, the phylogenetic character list, nexus scripts and Supplementary References. (PDF 1331 kb)

Video 1: 3D yaw of main skull block of Lethiscus stocki (MCZ 2185)

3D yaw of main skull block of Lethiscus stocki (MCZ 2185). Scale is in millimeters. (MP4 6561 kb)

Video 2: 3D pitch of main skull block of Lethiscus stocki (MCZ 2185)

3D pitch of main skull block of Lethiscus stocki (MCZ 2185). Scale is in millimeters. (MP4 9449 kb)

Video 3: 3D yaw of braincase of Lethiscus stocki (MCZ 2185)

3D yaw of braincase of Lethiscus stocki (MCZ 2185). Scale is in millimeters. (MP4 2592 kb)

Video 4: 3D yaw of cranial endocast of Lethiscus stocki (MCZ 2185)

3D yaw of cranial endocast of Lethiscus stocki (MCZ 2185). Scale is in millimeters. (MP4 1736 kb)

Video 5: 3D yaw of skull of Coloraderpeton brilli (CM 47687)

3D yaw of skull of Coloraderpeton brilli (CM 47687). Scale is in microns. (MP4 4718 kb)

Video 6: 3D roll of braincase of Coloraderpeton brilli (CM 47687)

3D roll of braincase of Coloraderpeton brilli (CM 47687). Scale is in microns. (MP4 10881 kb)

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Pardo, J., Szostakiwskyj, M., Ahlberg, P. et al. Hidden morphological diversity among early tetrapods. Nature 546, 642–645 (2017). https://doi.org/10.1038/nature22966

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