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.

  • Article
  • Published:

Snake-like limb loss in a Carboniferous amniote

Nature Ecology & Evolution volume 6, pages 614–621 (2022)Cite this article

Subjects

Abstract

Among living tetrapods, many lineages have converged on a snake-like body plan, where extreme axial elongation is accompanied by reduction or loss of paired limbs. However, when and how this adaptive body plan first evolved in amniotes remains poorly understood. Here, we provide insights into this question by reporting on a new taxon of molgophid recumbirostran, Nagini mazonense gen. et sp. nov., from the Francis Creek Shale (309–307 million years ago) of Illinois, United States, that exhibits extreme axial elongation and corresponding limb reduction. The molgophid lacks entirely the forelimb and pectoral girdle, thus representing the earliest occurrence of complete loss of a limb in a taxon recovered phylogenetically within amniotes. This forelimb-first limb reduction is consistent with the pattern of limb reduction that is seen in modern snakes and contrasts with the hindlimb-first reduction process found in many other tetrapod groups. Our findings suggest that a snake-like limb-reduction mechanism may be operating more broadly across the amniote tree.

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

Fig. 1: Photographs of N. mazonense gen. et sp. nov.
Fig. 2: Interpretive illustrations of N. mazonense gen. et sp. nov.
Fig. 3: Interpretive illustrations of N. mazonense gen. et sp. nov.
Fig. 4: Cranial reconstructions of known molgophids.
Fig. 5: Evolution of body elongation and limb reduction in Recumbirostra.

Similar content being viewed by others

Data availability

All fossils contained in this manuscript, including MPM VP359229.2 and FMNH PR 1031, have been properly accessioned into a public repository in this case the Milwaukee Public Museum and Field Museum of Natural History, respectively. The data matrix used in the phylogenetic parsimony analysis is available in Supplementary Information 3. This published work and the nomenclatural acts it contains have been registered in ZooBank, the proposed online registration system for the International Code of Zoological Nomenclature (ICZN). The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix http://zoobank.org/. The LSIDs for this publication are: urn:lsid:zoobank.org:pub:FFCEB3D4-E869-464F-AE2E-E8926C7DD5DE (article); urn:lsid:zoobank.org:act:8B4D6648-FACE-458E-97BB-4BCACB34AD8B (genus); and urn:lsid:zoobank.org:act:84DDBF1C-7AF5-4700-AAEF-8BBB70CCBD8C (species).

References

  1. Caldwell, M. W. “Without a leg to stand on”: on the evolution and development of axial elongation and limblessness in tetrapods. Can. J. Earth Sci. 40, 573–588 (2003).

    Article  Google Scholar 

  2. Bejder, L. & Hall, B. K. Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss. Evol. Dev. 4, 445–458 (2002).

    Article  PubMed  Google Scholar 

  3. Gans, C. Locomotion and burrowing in limbless vertebrates. Nature 242, 414–415 (1973).

    Article  Google Scholar 

  4. Gans, C. Tetrapod limblessness: evolution and functional corollaries. Am. Zool. 15, 455–467 (1975).

    Article  Google Scholar 

  5. Camaiti, M., Evans, A. R., Hipsley, C. A. & Chapple, D. G. A farewell to arms and legs: a review of limb reduction in squamates. Biol. Rev. 96, 1035–1050 (2021).

    Article  PubMed  Google Scholar 

  6. Brandley, M. C., Huelsenbeck, J. P. & Wiens, J. J. Rates and patterns in the evolution of snake‐like body form in squamate reptiles: evidence for repeated re‐evolution of lost digits and long‐term persistence of intermediate body forms. Evol. Int. J. Org. Evol. 62, 2042–2064 (2008).

    Article  Google Scholar 

  7. Skinner, A., Lee, M. S. & Hutchinson, M. N. Rapid and repeated limb loss in a clade of scincid lizards. BMC Evol. Biol. 8, 310 (2008).

  8. Marjanović, D. & Laurin, M. Phylogeny of Paleozoic limbed vertebrates reassessed through revision and expansion of the largest published relevant data matrix. PeerJ 6, e5565 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Woltering, J. M. et al. Axial patterning in snakes and caecilians: evidence for an alternative interpretation of the Hox code. Dev. Biol. 332, 82–89 (2009).

    Article  CAS  PubMed  Google Scholar 

  10. Cohn, M. J. & Tickle, C. Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474–479 (1999).

    Article  CAS  PubMed  Google Scholar 

  11. Jaekel, O. Über die klassen der tetrapoden [About the classes of the tetrapods]. Zool. Anz. 34, 193–212 (1909).

    Google Scholar 

  12. Anderson J. S. in Major Transitions in Vertebrate Evolution (eds Anderson, J. S. & Sues, H.-D.) 182–227 (Indiana Univ. Press, 2007).

  13. Cope, E. D. Synopsis of the extinct Batrachia from the Coal Measures. Ohio Geol. Surv. 2, 349–411 (1875).

    Google Scholar 

  14. Farrell, Ú. Pyritization of soft tissues in the fossil record: an overview. Paleontol. Soc. Pap. 20, 35–58 (2014).

    Article  Google Scholar 

  15. Mann, A. Cranial ornamentation of a large Brachydectes newberryi (Recumbirostra: Lysorophia) from Linton, Ohio. Vertebr. Anat. Morphol. Palaeontol. 6, 91–96 (2018).

    Article  Google Scholar 

  16. Mann, A., Pardo, J. D. & Maddin, H. C. Infernovenator steenae, a new serpentine recumbirostran from the ‘Mazon Creek’ Lagerstätte further clarifies lysorophian origins. Zool. J. Linn. Soc. 187, 506–517 (2019).

    Article  Google Scholar 

  17. Maisano, J. A. A survey of state of ossification in neonatal squamates. Herpetol. Monogr. 15, 135–157 (2001).

  18. Maisano, J. A. Terminal fusions of skeletal elements as indicators of maturity in squamates. J. Vertebr. Paleontol. 22, 268–275 (2002).

    Article  Google Scholar 

  19. Maisano, J. A. Terminal fusions of skeletal elements as indicators of maturity in squamates. J. Vertebr. Paleontol. 22, 268–275 (2002).

    Article  Google Scholar 

  20. 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  PubMed  PubMed Central  Google Scholar 

  21. Milner, A. R. Small temnospondyl amphibians from the Middle Pennsylvanian of Illinois. Paleontology 25, 635–664 (1982).

    Google Scholar 

  22. Godfrey, S. A diminutive temnospondyl amphibian from the Pennsylvanian of Illinois. Can. J. Earth Sci. 40, 507–514 (2003).

    Article  Google Scholar 

  23. Mann, A. & Maddin, H. C. Diabloroter bolti, a short-bodied recumbirostran ‘microsaur’ from the Francis Creek Shale, Mazon Creek, Illinois. Zool. J. Linn. Soc. 187, 494–505 (2019).

    Article  Google Scholar 

  24. Mann, A., McDaniel, E. J., McColville, E. R. & Maddin, H. C. Carbonodraco lundi gen et sp. nov., the oldest parareptile, from Linton, Ohio, and new insights into the early radiation of reptiles. R. Soc. Open Sci. 6, 191191 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mann, A. & Gee, B. M. Lissamphibian-like toepads in an exceptionally preserved amphibamiform from Mazon Creek. J. Vertebr. Paleontol. 39, e1727490 (2020).

    Article  Google Scholar 

  26. Wellstead, C. F. Taxonomic revision of the Lysorophia, Permo-Carboniferous lepospondyl amphibians. Bull. Am. Mus. Nat. Hist. 209, 1–90 (1991).

    Google Scholar 

  27. Sallan, L. C. & Coates, M. I. The long-rostrumed elasmobranch Bandringa Zangerl, 1969, and taphonomy within a Carboniferous shark nursery. J. Vertebr. Paleontol. 34, 22–33 (2014).

    Article  Google Scholar 

  28. Allison, P. A. & Briggs, D. E. Exceptional fossil record: distribution of soft-tissue preservation through the Phanerozoic. Geology 21, 527–530 (1993).

    Article  Google Scholar 

  29. Briggs, D. E. The role of decay and mineralization in the preservation of soft-bodied fossils. Annu. Rev. Earth Planet. Sci. 31, 275–301 (2003).

    Article  CAS  Google Scholar 

  30. Rieppel, O. Studies on skeleton formation in reptiles. V. Patterns of ossification in the skeleton of Alligator mississippiensis Daudin (Reptilia, Crocodylia). Zool. J. Linn. Soc. 109, 301–325 (1993).

    Article  Google Scholar 

  31. Sheil, C. A. Skeletal development of Macrochelys temminckii (Reptilia: Testudines: Chelydridae). J. Morphol. 263, 71–106 (2005).

    Article  PubMed  Google Scholar 

  32. Roscito, J. G. & Rodrigues, M. T. Skeletal development in the fossorial gymnophthalmids Calyptommatus sinebrachiatus and Nothobachia ablephara. Zoology 115, 289–301 (2012).

    Article  PubMed  Google Scholar 

  33. Boisvert, C. A. Vertebral development of modern salamanders provides insights into a unique event of their evolutionary history. J. Exp. Zool. B 312, 1–29 (2009).

    Article  Google Scholar 

  34. Klembara, J. & Janiga, M. Variation in Discosauriscus austriacus (Makowsky, 1876) from the Lower Permian of the Boskovice Furrow (Czech Republic). Zool. J. Linn. Soc. 108, 247–270 (1993).

    Article  Google Scholar 

  35. Pardo, J. D., Szostakiwskyj, M., Ahlberg, P. E. & Anderson, J. S. Hidden morphological diversity among early tetrapods. Nature 546, 642–645 (2017).

    Article  CAS  PubMed  Google Scholar 

  36. Mann, A., Calthorpe, A. S. & Maddin, H. C. Joermungandr bolti, an exceptionally preserved ‘microsaur’ from the Mazon Creek Lagerstätte reveals patterns of integumentary evolution in Recumbirostra. R. Soc. Open Sci. 8, 210319 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Swofford, D. Phylogenetic analysis using parsimony (PAUP) v.4.0b10 (Sinauer Associates, 2002).

  38. Cohn, M. J. & Bright, P. E. Molecular control of vertebrate limb development, evolution and congenital malformations. Cell Tissue Res. 296, 3–17 (1999).

    Article  CAS  PubMed  Google Scholar 

  39. Mizuhashi, K. et al. Resting zone of the growth plate houses a unique class of skeletal stem cells. Nature 563, 254–258 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Marchini, M. & Rolian, C. Artificial selection sheds light on developmental mechanisms of limb elongation. Evolution 72, 825–837 (2018).

    Article  PubMed  Google Scholar 

  41. Rolian, C. Endochondral ossification and the evolution of limb proportions. WIREs Dev. Biol. 9, e373 (2020).

  42. Weir, E. C. et al. Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc. Natl Acad. Sci. USA 93, 10240–10245 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Terpstra, L. et al. Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrin-linked kinase in chondrocytes. J. Cell Biol. 162, 139–148 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Marchini, M., Hernandez, E. S. & Rolian, C. Morphology and development of a novel murine skeletal dysplasia. PeerJ 7, e7180 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Shapiro, M. D., Hanken, J. & Rosenthal, N. Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis. J. Exp. Zool. B 297, 48–56 (2003).

    Article  Google Scholar 

  46. Leal, F. & Cohn, M. J. Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and HOXD enhancers. Curr. Biol. 26, 2966–2973 (2016).

    Article  CAS  PubMed  Google Scholar 

  47. Leal, F. & Cohn, M. J. Developmental, genetic, and genomic insights into the evolutionary loss of limbs in snakes. Genesis 56, e23077 (2018).

  48. Lande, R. Evolutionary mechanisms of limb loss in tetrapods. Evolution 32, 73–92 (1978).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  50. Anderson, J. S. A new aïstopod (Tetrapoda: Lepospondyli) from Mazon Creek, Illinois. J. Vertebr. Paleontol. 23, 79–88 (2003).

    Article  Google Scholar 

  51. Shapiro, M. D. Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): chondrogenesis, osteogenesis, and heterochrony. J. Morphol. 254, 211–231 (2002).

    Article  PubMed  Google Scholar 

  52. Herbst, E. C. & Hutchinson, J. R. New insights into the morphology of the Carboniferous tetrapod Crassigyrinus scoticus from computed tomography. Earth Environ. Sci. Trans. R. Soc. Edinb. 109, 157–175 (2019).

    CAS  Google Scholar 

  53. Carroll, R. L. & Gaskill, P. The order Microsauria. Mem. Am. Philos. Soc. 126, 1–211 (1978).

    Google Scholar 

  54. Tchernov, E., Rieppel, O., Zaher, H., Polcyn, M. J. & Jacobs, L. L. A fossil snake with limbs. Science 287, 2010–2012 (2000).

    Article  CAS  PubMed  Google Scholar 

  55. Zaher, H., Apesteguia, S. & Scanferla, C. A. The anatomy of the Upper Cretaceous snake Najash rionegrina Apesteguía & Zaher, 2006, and the evolution of limblessness in snakes. Zool. J. Linn. Soc. 156, 801–826 (2009).

    Article  Google Scholar 

  56. Jenkins, F. A., Walsh, D. M. & Carroll, R. L. Anatomy of Eocaecilia micropodia, a limbed caecilian of the Early Jurassic. Bull. Mus. Comp. Zool. 158, 285–365 (2007).

    Article  Google Scholar 

  57. Camp, C. L. Classification of the lizards. Bull. Am. Mus. Nat. Hist. 48, 289–480 (1923).

    Google Scholar 

  58. Essex, R. Studies in reptilian degeneration. Proc. Zool. Soc. Lond. 97, 879–945 (1927).

    Article  Google Scholar 

  59. Sewertzoff, A. N. Studien über die reduktion der organe der wirbeltiere. Zool. Jahrb. Abt. Anat. Ontog. Tiere 53, 611–699 (1931).

    Google Scholar 

Download references

Acknowledgements

We would like to thank P. Coorough Burke, D. Scott, R. R. Reisz, D. S. Berman, A. C. Henrici and R. W. Hook for access to comparative material and specimens. We further thank R. W. Hook, B. M. Gee and A. S. Calthorpe for stimulating discussions. Finally, we thank A. S. Calthorpe for her tireless assistance with assembling figures. A. Prieditis is thanked for his aid in taking photographs of the counterparts of MPM VP359229.2. Funding was in part provided by an Ontario Graduate Scholarship awarded to A.M.

Author information

Authors and Affiliations

  1. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington DC, USA

    Arjan Mann

  2. Department of Comparative Biology and Experimental Medicine, University of Calgary, Calgary, Alberta, Canada

    Jason D. Pardo

  3. McCaig Institute for Bone and Joint Health, University of Calgary, Calgary, Alberta, Canada

    Jason D. Pardo

  4. Department of Earth Sciences, Carleton University, Ottawa, Ontario, Canada

    Hillary C. Maddin

Authors
  1. Arjan Mann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jason D. Pardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hillary C. Maddin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.M. analysed the fossil data, performed phylogenetic analyses, constructed the figures and wrote the paper. J.D.P. analysed the fossil data, aided in figure edits and wrote the paper. H.C.M. provided edits to both the manuscript and final figures.

Corresponding author

Correspondence to Arjan Mann.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks David Ford, Marco Camaiti, Hussam Zaher and Timothy Smithson for their contribution to the peer review of this work.

Additional information

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

Extended data

Extended Data Fig. 1 Scanning Electron Micrographs (SEMs) of FMNH PR 1031.

A–D, showing incomplete ossification of the cranium. A–D, respectively show progressively smaller images including close up images of framboidal pyrite D, which likely is replacing cartilage and other soft tissues.

Extended Data Fig. 2 Images of FMNH PR 1031.

Photographs of the part A, and counterpart B, of the referred specimen (FMNH PR 1031) of Nagini mazonense.

Extended Data Fig. 3 Anatomy of the hindlimb and pelvic region of Nagini mazonense.

Close up Images of the well-developed pelvic girdle and hindlimb preserved on FMNH PR 1031. Anatomical Abbreviations: as=astragalus; dt=distal tarsal; ca=calcaneum; fe=femur; fib=fibula; il=Ilium; ph=phalanx; tib=tibia.

Extended Data Fig. 4 Results of the Phylogenetic analysis.

Strict consensus results of the phylogenetic parsimony analysis showing the position of Nagini mazonense as a molgophid in a polytomy with the taxa to Infernovenator and Brachydectes. Bootstrap values are located on top of nodes (only those over 50 reported).

Supplementary information

Supplementary Information

Supplementary Sections 1–3, Fig. 1 and references.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mann, A., Pardo, J.D. & Maddin, H.C. Snake-like limb loss in a Carboniferous amniote. Nat Ecol Evol 6, 614–621 (2022). https://doi.org/10.1038/s41559-022-01698-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-022-01698-y

This article is cited by

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