Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Hidden morphological diversity among early tetrapods

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

Subjects

This article has been updated

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

Change history

  • 14 August 2017

    The Reviewer Information section was corrected.

References

  1. Anderson, J. S., Reisz, R. R., Scott, D., Fröbisch, N. B. & Sumida, S. S. A stem batrachian from the Early Permian of Texas and the origin of frogs and salamanders. Nature 453, 515–518 (2008)

    Article  CAS  ADS  Google Scholar 

  2. Vallin, G. & Laurin, M. Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians. J. Vertebr. Paleontol. 24, 56–72 (2004)

    Article  Google Scholar 

  3. Ruta, M. & Coates, M. I. Dates, nodes, and character conflict: addressing the lissamphibian origin problem. J. Syst. Palaeontol. 5, 69–122 (2007)

    Article  Google Scholar 

  4. Coates, M. I. The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod relationships and patterns of skeletal evolution. Trans. R. Soc. Edinb. Earth Sci. 87, 363–421 (1996)

    Article  Google Scholar 

  5. Clack, J. A. An early tetrapod from ‘Romer’s Gap’. Nature 418, 72–76 (2002)

    Article  CAS  ADS  Google Scholar 

  6. Anderson, P. S. L., Friedman, M. & Ruta, M. Late to the table: diversification of tetrapod mandibular biomechanics lagged behind the evolution of terrestriality. Integr. Comp. Biol. 53, 197–208 (2013)

    Article  Google Scholar 

  7. Wellstead, C. F. A Lower Carboniferous aïstopod amphibian from Scotland. Palaeontology 25, 193–208 (1982)

    Google Scholar 

  8. Anderson, J. S., Carroll, R. L. & Rowe, T. B. New information on Lethiscus stocki (Tetrapoda: Lepospondyli: Aistopoda) from high-resolution computed tomography and a phylogenetic analysis of Aistopoda. Can. J. Earth Sci. 40, 1071–1083 (2003)

    Article  ADS  Google Scholar 

  9. Anderson, J. S. Revision of the aïstopod genus Phlegethontia (Tetrapoda, Lepospondyli). J. Paleontol. 76, 1029–1046 (2002)

    Article  Google Scholar 

  10. Carroll, R. L. Cranial anatomy of ophiderpetontid aïstopods: Palaeozoic limbless amphibians. Zool. J. Linn. Soc. 122, 143–166 (1998)

    Article  Google Scholar 

  11. Anderson, J. S. Cranial anatomy of Coloraderpeton brilli, postcranial anatomy of Oestocephalus amphiuminus, and a reconsideration of Ophiderpetontidae (Tetrapoda: Lepospondyli: Aistopoda). J. Vertebr. Paleontol. 23, 532–543 (2003)

    Article  Google Scholar 

  12. Smithson, T. R. The morphology and relationships of the Carboniferous amphibian Eoherpeton watsoni Panchen. Zool. J. Linn. Soc. 85, 317–410 (1985)

    Article  Google Scholar 

  13. Holmes, R. The Carboniferous amphibian Proterogyrinus scheelei Romer, and the early evolution of tetrapods. Phil. Trans. R. Soc. Lond. B 306, 431–524 (1984)

    Article  ADS  Google Scholar 

  14. Porro, L. B., Rayfield, E. J. & Clack, J. A. Descriptive anatomy and three-dimensional reconstruction of the skull of the early tetrapod Acanthostega gunnari Jarvik, 1952. PLoS One 10, e0118882 (2015)

    Article  Google Scholar 

  15. Clack, J. A. et al. A uniquely specialized ear in a very early tetrapod. Nature 425, 65–69 (2003)

    Article  CAS  ADS  Google Scholar 

  16. Ahlberg, P. E. & Clack, J. A. Lower jaws, lower tetrapods – a review based on the Devonian genus Acanthostega. Trans. R. Soc. Edinb. Earth Sci. 89, 11–46 (1998)

    Article  Google Scholar 

  17. Dawson, J. W. Air-Breathers of the Coal Period: a Descriptive Account on the remains of Land Animals found in the Coal Formation of Nova Scotia, with Remarks on their Bearing on Theories of the Formation of Coal and of the Origin of Species (Dawson Brothers, 1863)

  18. Vaughn, P. P. The Paleozoic microsaurs as close relatives of reptiles, again. Am. Midl. Nat. 67, 79–84 (1962)

    Article  Google Scholar 

  19. Carroll, R. L. & Baird, D. The Carboniferous amphibian Tuditanus (Eosauravus) and the distinction between microsaurs and reptiles Am. Mus. Novit. 2337, 1–50 (1968)

    Google Scholar 

  20. Panchen, A. L. On the amphibian Crassigyrinus scoticus Watson from the Carboniferous of Scotland. Phil. Trans. R. Soc. Lond. B 309, 505–568 (1985)

    Article  ADS  Google Scholar 

  21. Beaumont, E. H. & Smithson, T. R. The cranial morphology and relationships of the aberrant Carboniferous amphibian Spathicephalus mirus Watson. Zool. J. Linn. Soc. 122, 187–209 (1998)

    Article  Google Scholar 

  22. Pardo, J. D. & Anderson, J. S. Cranial morphology of the Carboniferous-Permian tetrapod Brachydectes newberryi (Lepospondyli, Lysorophia): new data from μCT. PLoS One 11, e0161823 (2016)

    Article  Google Scholar 

  23. Maddin, H. C., Olori, J. C. & Anderson, J. S. 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)

    Article  Google Scholar 

  24. Reisz, R. R. A diapsid reptile from the Pennsylvanian of Kansas. Univ. Kansas Museum of Natural History Special Publications 7, 1–74 (1981)

    ADS  Google Scholar 

  25. Milner, A. R. & Sequeira, S. E. K. The temnospondyl amphibians from the Viséan of East Kirkton, West Lothian, Scotland. Trans. R. Soc. Edinb. Earth Sci. 84, 331–361 (1994)

    Google Scholar 

  26. Smithson, T. R., Carroll, R. L., Panchen, A. L. & Andrews, S. M. Westlothiana lizziae from the Viséan of East Kirkton, West Lothian, Scotland, and the amniote stem. Trans. R. Soc. Edinb. Earth Sci. 84, 383–412 (1994)

    Google Scholar 

  27. Benton, M. J., Donoghue, P. C. J., Asher, R. J., Friedman, M., Near, T. J. & Vinter, J. Constraints on the timescale of animal evolutionary history. Palaeontol. Electron. 18.1.1FC (2015)

  28. Huttenlocker, A. K., Pardo, J. D., Small, B. J. & Anderson, J. S. Cranial morphology of recumbirostrans (Lepospondyli) from the Permian of Kansas and Nebraska, and early morphological evolution inferred by micro-computed tomography. J. Vertebr. Paleontol. 33, 540–552 (2013)

    Article  Google Scholar 

  29. Maddin, H. C. & Anderson, J. S. 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)

    Article  Google Scholar 

  30. Clack, J. A., Ahlberg, P. E., Blom, H. & Finney, S. M. A new genus of Devonian tetrapod from North-East Greenland, with new information on the lower jaw of Ichthyostega. Palaeontology 55, 73–86 (2012)

    Article  Google Scholar 

Download references

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

Authors
  1. Jason D. Pardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matt Szostakiwskyj
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Per E. Ahlberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jason S. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

Competing interests

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.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature22966

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing