Letter

Nature 454, 630-633 (31 July 2008) | doi:10.1038/nature07178; Received 2 November 2007; Accepted 19 June 2008

Evolutionary origin and development of snake fangs

Freek J. Vonk1, Jeroen F. Admiraal1, Kate Jackson2, Ram Reshef3, Merijn A. G. de Bakker1, Kim Vanderschoot1, Iris van den Berge1, Marit van Atten1, Erik Burgerhout1, Andrew Beck4, Peter J. Mirtschin4,5, Elazar Kochva6, Frans Witte1, Bryan G. Fry7, Anthony E. Woods4 & Michael K. Richardson1

  1. Institute of Biology, Leiden University, Kaiserstraat 63, PO Box 9516, 2300 RA, Leiden, The Netherlands
  2. Department of Biology, Whitman College, Walla Walla, Washington 99362, USA
  3. Faculty of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel
  4. Sansom Institute, School of Pharmacy and Medical Sciences, University of South Australia, Adelaide, South Australia 5000, Australia
  5. Venom Supplies Pty Ltd, Tanunda, South Australia 5352, Australia
  6. Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel
  7. Department of Biochemistry & Molecular Biology, Bio21 Institute, University of Melbourne, Parkville, Victoria 3010, Australia

Correspondence to: Michael K. Richardson1 Correspondence and requests for materials should be addressed to M.K.R. (Email: m.k.richardson@biology.leidenuniv.nl).

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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