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MBE Advance Access originally published online on October 6, 2008
Molecular Biology and Evolution 2009 26(1):15-25; doi:10.1093/molbev/msn211
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© 2008 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Articles

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

Mandë Holford*,{dagger}, Nicolas Puillandre{ddagger}, Yves Terryn§, Corinne Cruaud||, Baldomero Olivera* and Philippe Bouchet{ddagger}

* Biology Department, University of Utah
{dagger} Chemistry Department, The City University of New York-York College
{ddagger} Muséum National d'Histoire Naturelle (MNHN), Departement Systematique et Evolution, Unité Mixte de Recherche 7138 Systématique, Adaptation, Evolution, 55 rue Buffon, 75231 Paris Cedex 05, France
§ NaturalArt, Gent, Belgium
|| GENOSCOPE, Centre National de Séquençage, Evry, France

E-mail: mholford{at}york.cuny.edu.

Accepted for publication September 10, 2008.

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.

Key Words: Toxoglossa evolution • Terebridae phylogeny • venomous marine snails • peptide toxins • venom apparatus

Douglas Crawford, Associate Editor


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