Evolution of the Toxoglossa Venom Apparatus as Inferred by Molecular Phylogeny of the Terebridae

Type Article
Date 2009-01
Language English
Author(s) Holford Mande1, 2, Puillandre Nicolas3, Terryn Yves4, Cruaud Corinne5, Olivera Baldomero1, Bouchet Philippe3
Affiliation(s) 1 : Univ Utah, Dept Biol, Salt Lake City, UT 84112 USA.
2 : City Univ New York York Coll, Dept Chem, New York, NY USA.
3 : Museum Natl Hist Nat, Dept Systemat & Evolut, Unite Mixte Tech Systemat Adaptat 7138, F-75231 Paris 05, France.
4 : NaturalArt, Ghent, Belgium.
5 : GENOSCOPE, Ctr Natl Sequencage, Evry, France.
Source Molecular Biology And Evolution (0737-4038) (Oxford Univ Press), 2009-01 , Vol. 26 , N. 1 , P. 15-25
DOI 10.1093/molbev/msn211
WOS© Times Cited 31
Keyword(s) life history similarities, similar proboscis type, morphology, biology, peptides, radula
Abstract Toxoglossate marine gastropods, traditionally assigned to the families Conidae, Terebridae, and Turridae, are one of the most populous animal groups that use venom to capture their prey. These marine animals are generally characterized by a venom apparatus that consists of a muscular venom bulb and a tubular venom gland. The toxoglossan radula, often compared with a hypodermic needle for its use as a conduit to inject toxins into prey, is considered a major anatomical breakthrough that assisted in the successful initial radiation of these animals in the Cretaceous and early Tertiary. The pharmacological success of toxins from cone snails has made this group a star among biochemists and neuroscientists, but very little is known about toxins from the other Toxoglossa, and the phylogeny of these families is largely in doubt. Here we report the first molecular phylogeny for the Terebridae and use the results to infer the evolution of the venom apparatus for this group. Our findings indicate that most of the genera of terebrids are polyphyletic, and one species ("Terebra" (s.l.) jungi) is the sister group to all other terebrids. Molecular analyses combined with mapping of venom apparatus morphology indicate that the Terebridae have lost the venom apparatus at least twice during their evolution. Species in the genera Terebra and Hastula have the typical venom apparatus found in most toxoglossate gastropods, but all other terebrid species do not. For venomous organisms, the dual analysis of molecular phylogeny and toxin function is an instructive combination for unraveling the larger questions of phylogeny and speciation. The results presented here suggest a paradigm shift in the current understanding of terebrid evolution, while presenting a road map for discovering novel terebrid toxins, a largely unexplored resource for biomedical research and potential therapeutic drug development.
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Holford Mande, Puillandre Nicolas, Terryn Yves, Cruaud Corinne, Olivera Baldomero, Bouchet Philippe (2009). Evolution of the Toxoglossa Venom Apparatus as Inferred by Molecular Phylogeny of the Terebridae. Molecular Biology And Evolution, 26(1), 15-25. Publisher's official version : https://doi.org/10.1093/molbev/msn211 , Open Access version : https://archimer.ifremer.fr/doc/00207/31788/