Evolutionary origin and development of snake fangs

Abstract

Many advanced snakes use fangs-specialized teeth associated with a venom gland-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 jaw. A fundamental controversy in snake evolution is whether or not front and rear fangs share the same evolutionary and developmental origin. 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 marker, 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 today.

Dynamic evolution of venom proteins in squamate reptiles

“…However, our results also revealed that only two of the nine toxin families (crotamine and veficolin) contained a strongly supported monophyletic clade of snake toxins (Table 1), although the monophyly of snake toxins was also not rejected in the cystatin and hyaluronidase gene trees ( Table 2). As the single origin of venom in advanced snakes is strongly supported by multiple independent sources of evidence 2,4,5 , this suggests that the non-monophyly of their toxins may instead be due to multiple, independent recruitment events or as the result of reverse recruitment. Logically, those same phenomena, rather than multiple independent origins of venom, may also be responsible for the non-monophyly of Toxicoferan toxins.…”

“…The origin of the venom apparatus of squamates has been the subject of considerable recent research interest. The homology of the venom apparatus across the advanced snakes (Caenophidia) is robustly supported by anatomical evidence [1][2][3][4] , as well as comparative embryology and developmental genetics 5 . A recent addition to the body of evidence supporting the single early evolution of venom in snakes has been the use of protein amino acid or DNA gene sequences from toxins, and their homologues among non-venom body proteins 6,7 .…”

Role of the inflammasome in defense against venoms

“…These venoms, which consist of a complex mixture of toxic components, are usually delivered into their victims via bites or stings (2). The targeting of mammalian species by venomous animals has presumably introduced evolutionarily relevant selective pressures to either avoid or minimize the toxic effects of envenomation (3).…”

Caracterização estrutural e funcional de um fator de crescimento endotelial vascular, VEGF, da peçonha da serpente Crotalus durissus collilineatus

“…Possuem um aparelho inoculador solenóglifo (as maxilas possuem apenas um par de dentes funcional agudo e oco) (MELGAREJO et al, 2003). Em associação ao aparato inoculador, estão presentes as glândulas de peçonha na região pós-orbital e, quando comprimidas por músculos acessórios, secretam seu conteúdo (JACKSON, 2007;FRY et al, 2008;VONK et al, 2008). A subfamília Crotalinae, incluída na família Viperidae, apresenta um par de fosseta loreal, um órgão que é termorreceptor e se encontra localizado entre a narina e o olho da serpente.…”