Abstract
Snakes are renowned for their ability to engulf extremely large prey, and their highly flexible skulls and extremely wide gape are among the most striking adaptations found in vertebrates1,2,3,4,5. However, the evolutionary transition from the relatively inflexible lizard skull to the highly mobile snake skull remains poorly understood, as they appear to be fundamentally different and no obvious intermediate stages have been identified4,5. Here we present evidence that mosasaurs — large, extinct marine lizards related to snakes — represent a crucial intermediate stage. Mosasaurs, uniquely among lizards, possessed long, snake-like palatal teeth for holding prey. Also, although they retained the rigid upper jaws typical of lizards, they possessed highly flexible lower jaws that were not only morphologically similar to those of snakes, but also functionally similar. The highly flexible lower jaw is thus inferred to have evolved before the highly flexible upper jaw — in the macrophagous common ancestor of mosasaurs and snakes — for accommodating large prey. The mobile upper jaw evolved later — in snakes — for dragging prey into the oesophagus. Snakes also have more rigid braincases than lizards, and the partially fused meso- and metakinetic joints of mosasaurs are transitional between the loose joints of lizards and the rigid joints of snakes. Thus, intermediate morphologies in snake skull evolution should perhaps be sought not in small burrowing lizards, as commonly assumed, but in large marine forms.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Gans, C. The feeding mechanism of snakes and its possible evolution. Am. Zool. 1, 207–227 (1961).
Greene, H. W. Dietary correlates of the origin and radiation of snakes. Am. Zool. 23, 431–441 (1983).
Cundall, D. in Snakes: Ecology and Evolutionary Biology (eds Seigel, R. A., Collins, J. T. & Novak, S. S.) 106–140 (Macmillan, New York, 1987).
Rieppel, O. Areview of the origin of snakes. Evol. Biol. 22, 37–130 (1988).
Kardong, K. V., Kiene, T. L. & Bels, V. Evolution of trophic systems in squamates. Neth. J. Zool. 47, 411–427 (1997).
Lee, M. S. Y. Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate phylogeny. Biol. J. Linn. Soc. 65, 369–453 (1998).
Caldwell, M. W. Squamate phylogeny and the relationships of snakes and mosasauroids. Zool. J. Linn. Soc. 125, 115–147 (1999).
Russell, D. A. Systematics and morphology of American mosasaurs. Bull. Peabody Mus. Nat. Hist. 23, 1–237 (1967).
Bell, G. L. J in Ancient Marine Reptiles (eds Nicholls, E. L. & Callaway, J.) 293–332 (Academic, New York, 1997).
DeBraga, M. & Carroll, R. L. The origin of mosasaurs as a model of macroevolutionary patterns and processes. Evol. Biol. 27, 245–322 (1993).
Lee, M. S. Y. & Caldwell, M. W. Anatomy and relationships of Pachyrhachis problematicus, a primitive snake with hindlimbs. Phil. Trans. R. Soc. Lond. B 353, 1521–1552 (1998).
Estes, R., Frazzetta, T. H. & Williams, E. E. Studies on the fossil snake Dinilysia patagonica Woodward: Pt 1. Cranial morphology. Bull. Mus. Comp. Zool. Harv. 140, 25–74 (1970).
Underwood, G. Acontribution to the classification of snakes. Br. Mus. (Nat. Hist.) Publs 653, 1–179 (1967).
Cundall, D., Wallach, V. & Rossman, D. A. The systematic relationships of the snake genus Anomochilus. Zool. J. Linn. Soc. 109, 275–299 (1993).
Greer, A. The Biology and Evolution of Australian Snakes (Surrey Beatty, Sydney, 1997).
Frazetta, T. H. The origin of amphikinesis in lizards: a problem in functional morphology and the evolution of adaptive systems. Evol. Biol. 20, 419–461 (1986).
Arnold, E. N. Cranial kinesis in lizards: variations, uses, and origins. Evol. Biol. 30, 323–357 (1998).
Callison, G. Intracranial mobility in Kansas mosasaurs. Paleontol. Contr. Univ. Kansas 26, 1–15 (1967).
Lingham-Soliar, T. Anatomy and functional morphology of the largest marine reptile known, Mosasaurus hoffmani (Mosasauridae, Reptilia) from the Upper Cretaceous, Upper Maastrichtian of The Netherlands. Phil. Trans. R. Soc. Lond. B 347, 155–180 (1995).
Pregill, G. K., Gauthier, J. A. & Greene, H. W. The evolution of helodermatid squamates, with description of a new taxon and an overview of Varanoidea. Trans. San Diego Nat. Hist. Soc. 21, 167–202 (1986).
Frazzetta, TH. Studies on the fossil snake Dinilysia patagonica Woodward. II. Jaw machinery in the earliest snakes. Forma Functio 3, 205–221 (1970).
Cundall, D. Feeding behaviour in Cylindrophis and its bearing on the evolution of alethinophidian snakes. J. Zool. 237, 353–376 (1995).
Boltt, R. E. & Ewer, R. F. The functional anatomy of the head of the puff adder, Bitis arietans (Merr.). J. Morphol. 114, 83–106 (1964).
Kardong, K. V. Kinematics of swallowing in the yellow rat snake, Elaphe obsoleta quadrivittata : a reappraisal. Jap. J. Herpetol. 11, 96–109 (1986).
Young, B. A. The comparative morphology of the intermandibular connective tissue in snakes (Reptillia: Squamata). Zool. Anz. 237, 59–84 (1998).
Iordansky, N. N. Jaw apparatus and feeding mechanics of Typhlops (Ophidia: Typhlopidae): a reconsideration. Russ. J. Herpetol. 4, 120–127 (1997).
Kauffman, E. G. & Kesling, R. V. An upper Cretaceous ammonite bitten by a mosasaur. Contr. Mus. Paleont. Univ. Michigan 15, 193–248 (1960).
Russell, D. A. Intracranial mobility in mosasaurs. Postilla 86, 1–19 (1964).
Gregory, J. T. Convergent evolution: the jaws of Hesperornis and the mosasaurs. Evolution 5, 345–354 (1951).
Massare, J. A. Tooth morphology and prey preference of Mesozoic marine reptiles. J. Vert. Paleontol. 7, 121–137 (1987).
Acknowledgements
We thank V. Wallach, G. Underwood, K. Karding, N. Kley, J. Scanlon and A. Greer for discussion and comments on the manuscript; J. Rosado and J. Cadle (Museum of Comparative Zoology, Harvard University), O. Rieppel and A. Resatar (Field Museum of Natural History), C. Holton, T.Trombone and L. Ford (American Museum of Natural History), S. Chapman and C. McCarthy (British Museum of Natural History) and B.Purdy and K. de Queiroz (National Museum of Natural History, Smithsonian Institution) for access to materials under their care; and the Australian Research Council, Fulbright Foundation and NERC (Canada) for funding.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lee, M., Bell, G. & Caldwell, M. The origin of snake feeding. Nature 400, 655–659 (1999). https://doi.org/10.1038/23236
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/23236
This article is cited by
-
Molecular and cellular mechanisms underlying the evolution of form and function in the amniote jaw
EvoDevo (2019)
-
The ecological origins of snakes as revealed by skull evolution
Nature Communications (2018)
-
A transitional snake from the Late Cretaceous period of North America
Nature (2012)
-
‘Total evidence’ in phylogenetic systematics
Biology & Philosophy (2009)
-
A Cretaceous terrestrial snake with robust hindlimbs and a sacrum
Nature (2006)
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.