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Evolutionary origin and development of snake fangs

Nature volume 454, pages 630–633 (2008)Cite this article

Abstract

Many advanced snakes use fangs—specialized teeth associated with a venom gland1,2—to introduce venom into prey or attacker. Various front- and rear-fanged groups are recognized, according to whether their fangs are positioned anterior (for example cobras and vipers) or posterior (for example grass snakes) in the upper jaw3,4,5. A fundamental controversy in snake evolution is whether or not front and rear fangs share the same evolutionary and developmental origin3,4,5,6,7,8,9. Resolving this controversy could identify a major evolutionary transition underlying the massive radiation of advanced snakes, and the associated developmental events. Here we examine this issue by visualizing the tooth-forming epithelium in the upper jaw of 96 snake embryos, covering eight species. We use the sonic hedgehog gene as a marker10,11,12,13, and three-dimensionally reconstruct the development in 41 of the embryos. We show that front fangs develop from the posterior end of the upper jaw, and are strikingly similar in morphogenesis to rear fangs. This is consistent with their being homologous. In front-fanged snakes, the anterior part of the upper jaw lacks sonic hedgehog expression, and ontogenetic allometry displaces the fang from its posterior developmental origin to its adult front position—consistent with an ancestral posterior position of the front fang. In rear-fanged snakes, the fangs develop from an independent posterior dental lamina and retain their posterior position. In light of our findings, we put forward a new model for the evolution of snake fangs: a posterior subregion of the tooth-forming epithelium became developmentally uncoupled from the remaining dentition, which allowed the posterior teeth to evolve independently and in close association with the venom gland, becoming highly modified in different lineages. This developmental event could have facilitated the massive radiation of advanced snakes in the Cenozoic era, resulting in the spectacular diversity of snakes seen today6,14,15.

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Figure 1: Adult maxillary dentition mapped onto a molecular snake phylogeny to show relative positions of the various fang types.
Figure 2: Shh expression in the embryonic snake palate, showing the posterior developmental origins of front fangs.
Figure 3: Sections of the shh in situ hybridizations of the embryonic upper jaw in five snake species, showing the posterior and anterior dental laminae.
Figure 4: Schematic three-dimensional reconstructions showing the similarity in morphogenesis between the rear and front fangs.

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Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Sonic hedgehog complementary DNA clone sequence for the rhombic night adder, Causus rhombeatus, has been deposited in the Genbank database under accession number EU236145.

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Acknowledgements

We thank the following persons and institutions who helped us or contributed material used in this study: J. W. Arntzen, M. Brittijn, M. de Boer, R. van Deutekom, N. Dunstan, K. Van Egmond, P. L. Y. Fung, I. Gavrilov, W. Getreuer, J. Hanken, E. Heida, I. Ineich, T. de Jong, K. V. Kardong, M. Lautenbach, J. Losos, D. Millar, C. Pepermans, J. M. Richman, J. Rosado, R. de Ruiter, P. Schilperoord, M. M. Smith, S. Soubzmaigne, N. Vidal, E. M. Wielhouwer, J. Woltering, National Museum of Natural History Naturalis Leiden, Reptilezoo Serpo, Muséum National d'Histoire Naturelle Paris, AQIS, DEH, APCG and DWLBC (Australia). This work received funding from the following sources: a Toptalent grant from the Netherlands Organization for Scientific Research (NWO; F.J.V.), a Smart Mix grant from the Dutch government (M.K.R.), a Valorisation grant from the Dutch Technology Foundation (STW; M.K.R., F.J.V., B.G.F.), the Curatoren fund (F.J.V.), the LUSTRA fund (F.J.V.), the Australian Research Council and the Australian Academy of Science (B.G.F.), DEST-ISL (B.G.F.), Whitman College (K.J.), a NWO visitors grant (M.K.R., B.G.F.) and the Leiden University Fund (F.J.V.).

Author Contributions F.J.V.: study concept and design; embryo and skull collection, acquisition and processing; probe synthesis; in situ hybridizations; histology; figures; paper. J.F.A.: three-dimensional reconstructions, figures. K.J.: scanning electron microscopy. R.R.: study concept, ablation experiment, histology. E.K.: study concept, embryological data. K.V., I.v.d.B., M.v.A.: in situ hybridizations, histology. M.A.G.d.B.: probe design, in situ hybridizations. A.B.: Naja embryo collection. P.J.M.: supply of Naja material. B.G.F.: study concept, supply of Causus material. A.W.: provision of laboratory space. E.B., F.W.: morphometric analyses. M.K.R. (project leader): study concept and design, provision of funding and laboratory space.

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Authors and Affiliations

  1. Institute of Biology, Leiden University, Kaiserstraat 63, PO Box 9516, 2300 RA, Leiden, The Netherlands ,

    Freek J. Vonk, Jeroen F. Admiraal, Merijn A. G. de Bakker, Kim Vanderschoot, Iris van den Berge, Marit van Atten, Erik Burgerhout, Frans Witte & Michael K. Richardson

  2. Department of Biology, Whitman College, Walla Walla, Washington 99362, USA,

    Kate Jackson

  3. Faculty of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel

    Ram Reshef

  4. Sansom Institute, School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia 5000, Australia ,

    Andrew Beck, Peter J. Mirtschin & Anthony E. Woods

  5. Venom Supplies Pty Ltd, Tanunda, South Australia 5352, Australia ,

    Peter J. Mirtschin

  6. Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel

    Elazar Kochva

  7. Department of Biochemistry & Molecular Biology, Bio21 Institute, University of Melbourne, Parkville, Victoria 3010, Australia,

    Bryan G. Fry

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Correspondence to Michael K. Richardson.

Supplementary information

Supplementary information

The file contains Supplementary Figures 1-7 and Supplementary Tables 1-6. Figure 1 shows a summary of our results. The other figures include additional shh expression data, additional histology data (including our ablation experiment), the results of our scanning electronic microscopy, and the linear regression analyses of the ontogenetic allometric measurements of the developing front fangs. The 6 tables display all material used in this study, and the results of our statistical analyses of the ontogenetic allometry. (PDF 4872 kb)

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Vonk, F., Admiraal, J., Jackson, K. et al. Evolutionary origin and development of snake fangs. Nature 454, 630–633 (2008). https://doi.org/10.1038/nature07178

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