A transitional snake from the Late Cretaceous period of North America

Journal name:
Nature
Volume:
488,
Pages:
205–208
Date published:
DOI:
doi:10.1038/nature11227
Received
Accepted
Published online

Snakes are the most diverse group of lizards1, but their origins and early evolution remain poorly understood owing to a lack of transitional forms. Several major issues remain outstanding, such as whether snakes originated in a marine2, 3, 4 or terrestrial5, 6 environment and how their unique feeding mechanism evolved1, 7, 8. The Cretaceous Coniophis precedens was among the first Mesozoic snakes discovered9, but until now only an isolated vertebra has been described9, 10 and it has therefore been overlooked in discussions of snake evolution. Here we report on previously undescribed material11 from this ancient snake, including the maxilla, dentary and additional vertebrae. Coniophis is not an anilioid as previously thought11; a revised phylogenetic analysis of Ophidia shows that it instead represents the most primitive known snake. Accordingly, its morphology and ecology are critical to understanding snake evolution. Coniophis occurs in a continental floodplain environment, consistent with a terrestrial rather than a marine origin; furthermore, its small size and reduced neural spines indicate fossorial habits, suggesting that snakes evolved from burrowing lizards. The skull is intermediate between that of lizards and snakes. Hooked teeth and an intramandibular joint indicate that Coniophis fed on relatively large, soft-bodied prey. However, the maxilla is firmly united with the skull, indicating an akinetic rostrum. Coniophis therefore represents a transitional snake, combining a snake-like body and a lizard-like head. Subsequent to the evolution of a serpentine body and carnivory, snakes evolved a highly specialized, kinetic skull, which was followed by a major adaptive radiation in the Early Cretaceous period. This pattern suggests that the kinetic skull was a key innovation that permitted the diversification of snakes.

At a glance

Figures

  1. Dentary of Coniophis precedens.
    Figure 1: Dentary of Coniophis precedens.

    UCMP (University of California Museum of Paleontology) 50000 in lateral (a), medial (b), ventral (c) and dorsal (d) view. mec, Meckelian canal; mf, mental foramen; sp, splenial facet; sr, subdental ridge; sur, surangular notch; th, thecae.

  2. Maxilla of Coniophis precedens.
    Figure 2: Maxilla of Coniophis precedens.

    ae, UCMP 53935, anterior part of maxilla in medial (a), lateral (b), ventral (c), dorsal (d) and anterior (e) view. fi, UCMP 49999, posterior maxilla in medial (f), lateral (g), ventral (h) and dorsal (i) view. j, k, AMNH (American Museum of Natural History) 22413, posterior maxilla in lateral (j) and medial (k) view. fos, fossa for nasal capsule; fp, facial process; idr, interdental ridge; ju, jugal articulation; lf, labial foramina; nar, narial margin; nas, nasal contact; pp, palatine process; pmp, premaxillary process; prf, prefrontal facet; saf, superior alveolar foramen; ss, supradental shelf; vom, vomerine process.

  3. Vertebrae of Coniophis precedens.
    Figure 3: Vertebrae of Coniophis precedens.

    a, AMNH 26999,vertebra from cervical region. b USNM (United States National Museum) 2143, holotype anterior trunk vertebra. c, AMNH 26833, middle trunk vertebra, d, YPM-PU (Yale Peabody Museum, Princeton collection) 16845, posterior trunk vertebra. Shown (from top to bottom) in anterior, posterior, dorsal, ventral and lateral views.

  4. Skull in lizards, Coniophis and modern snakes.
    Figure 4: Skull in lizards, Coniophis and modern snakes.

    a, Heloderma (Varanoidea). b, Reconstruction of Coniophis, with missing elements after Anguidae and basal snakes Najash and Dinilysia. c, Epicrates (Macrostomata).

  5. Phylogeny of Ophidia, showing relationships of Coniophis and evolution of cranial kinesis.
    Figure 5: Phylogeny of Ophidia, showing relationships of Coniophis and evolution of cranial kinesis.

    Adaptations permitting cranial kinesis (shown at left in the boa Epicrates) cluster near the base of the snake tree, but following the divergence of Coniophis. Coniophis exhibits an intramandibular joint (1). Serpentes exhibits a maxilla–premaxilla joint (2), loss of maxilla–vomer contact (3), a nasofrontal joint (4), a maxilla–prefrontal joint (5), a mobile dentary symphysis (6) and an articular saddle joint (7). Alethinophidia is characterized by a reduced postorbital bar (8) and a palatine–pterygoid hinge (9). Macrostomata is characterized by a hinged supratemporal (10). Characters 4* and 7* are unknown for either Coniophis or Najash. Stratigraphic data from ref. 18.

References

  1. Greene, H. W. Snakes: the Evolution of Mystery in Nature (Univ. California Press, 1997)
  2. Caldwell, M. W. & Lee, M. S. Y. A snake with legs from the marine Cretaceous of the Middle East. Nature 386, 705709 (1997)
  3. Cope, E. D. On the reptilian orders Pythonomorpha and Streptosauria. Proc. Bost. Soc. Nat. Hist. 12, 250267 (1869)
  4. Lee, M. S. Y. Molecular evidence and marine snake origins. Biol. Lett. 1, 227230 (2005)
  5. Apesteguía, S. & Zaher, H. A Cretaceous terrestrial snake with robust hindlimbs and a sacrum. Nature 440, 10371040 (2006)
  6. Vidal, N. & Hedges, S. B. Molecular evidence for a terrestrial origin of snakes. Proc. R. Soc. Lond. B 271, S226S229 (2004)
  7. Lee, M. S. Y., Bell, G. L. & Caldwell, M. W. The origin of snake feeding. Nature 400, 655659 (1999)
  8. Cundall, D. & Greene, H. W. in Feeding: Form, Function, and Evolution in Terrestrial Vertebrates (ed. Schwenk, K.) 293333 (Academic, 2000)
  9. Marsh, O. C. Notice of new reptiles from the Laramie Formation. Am. J. Sci. 43, 449453 (1892)
  10. Gilmore, C. W. Fossil snakes of North America. Geol. Soc. Am. Bull. 9, 196 (1938)
  11. Estes, R. Fossil Vertebrates from the Late Cretaceous Lance Formation, Eastern Wyoming. Univ. Calif. Publ. Geol. Sci. 49, 140141 (1964)
  12. Zaher, H., Apesteguía, 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, 801826 (2009)
  13. Cundall, D. & Irish, F. in Biology of the Reptilia Vol. 20 (eds Gans, C., Gaunt, A. S. & Adler, K.) 349692 (Society for the Study of Amphibians and Reptiles, 2008)
  14. Hoffstetter, R. in Traité de Paléontologie (ed. Piveteau, J.) 606662 (Maison et Cie, 1955)
  15. Rage, J.-C. & Augé, M. Squamate reptiles from the middle Eocene of Lissieu (France). Geobios 43, 253268 (2010)
  16. Scanlon, J. D. & Lee, M. S. Y. Varanoid-like dentition in primitive snakes (Madtsoiidae). J. Herpetol. 36, 100106 (2002)
  17. Cundall, D. Feeding behavior in Cylindrophis and its bearing on the evolution of alethinophidian snakes. J. Zool. 237, 353376 (1995)
  18. Wilson, J. A., Mohabey, D. M., Peters, S. E. & Head, J. J. Predation upon hatchling dinosaurs by a new snake from the Late Cretaceous of India. PLoS Biol. 8, e1000322 (2010)
  19. Zaher, H. & Scanferla, C. A. The skull of the Upper Cretaceous snake Dinilysia patagonica Smith-Woodward 1901, and its phylogenetic position revisited. Zool. J. Linn. Soc. 164, 194238 (2012)
  20. Scanlon, J. D. & Lee, M. S. Y. The Pleistocene serpent Wonambi and the early evolution of snakes. Nature 403, 416420 (2000)
  21. Scanlon, J. D. Skull of the large non-macrostomatan snake Yurlunggur from the Australian Oligocene. Nature 439, 839842 (2006)
  22. Rage, J.-C. & Albino, A. M. Dinilysia patagonica (Reptilia, Serpentes): matériel vertébral additionel du Crétacé supérieur d’Argentine. Étude complémentaire des vertèbres, variations intraspécifiques etintracolumnaires. Neues Jahrb. Geol. Paläontol. Monatsh. 1989, 433447 (1989)
  23. Hoffstetter, R. & Gasc, J.-P. Vertebrae and ribs of modern reptiles.. in Biology of the Reptilia Vol. 1 (ed. Gans, C.) 201310 (Academic, 1969).
  24. Prasad, G. V. R. Rage, J.-C. Amphibians and squamates from the Maastrichtian of Naskal, India. Cretac. Res. 16, 95107 (1995)
  25. Caldwell, M. W. & Albino, A. M. Palaeoenvironment and palaeoecology of three Cretaceous snakes: Pachyophis, Pachyrhachis, and Dinilysia. Acta Palaeontol. Pol. 46, 203218 (2001)
  26. Kearney, M. Systematics of the Amphisbaenia (Lepidosauria: Squamata) based on morphological evidence from recent and fossil forms. Herpetological Monogr. 17, 174 (2003)
  27. Rage, J.-C. & Escuil, F. The Cenomanian: stage of hindlimbed snakes. Carnets Géol. 2003, 2003/01. (2003)
  28. Rage, J.-C. & Werner, C. Mid-Cretaceous (Cenomanian) snakes from Wadi Abu Hashim, Sudan: the earliest snake assemblage. Palaeontol. Afr. 35, 85110 (1999)
  29. Gardner, J. D. & Cifelli, R. L. A primitive snake from the Cretaceous of Utah. Spec. Pap. Palaeontol. 60, 87100 (1999)

Download references

Author information

Affiliations

  1. Department of Geology and Geophysics, Yale University, PO Box 208109, New Haven, Connecticut 06520-8109, USA

    • Nicholas R. Longrich &
    • Jacques A. Gauthier
  2. Department of Organismic and Evolutionary Biology, Biological Laboratories, 16 Divinity Avenue, Harvard University, Cambridge, Massachusetts 02138 USA

    • Bhart-Anjan S. Bhullar

Contributions

N.R.L. designed the research, identified specimens, collected data, performed the phylogenetic analysis and wrote the paper. B.-A.S.B. designed the research, collected data and wrote the paper. J.A.G. collected data, contributed data and wrote the paper.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information 1 (554K)

    This file contains Supplementary Text and Data 1-2, Supplementary Figures 1-2 and additional references.

  2. Supplementary Information 2 (1.1M)

    This file contains Supplementary Text and Data, Supplementary Materials, Supplementary Results, a Supplementary Discussion and additional references.

  3. Supplementary Information 3 (3M)

    This file contains the Supplementary Character illustrations 155-228.

Text files

  1. Supplementary Information 4 (8.5K)

    This file contains the Supplementary Character-taxon matrix.

Additional data