Evolution of the Toxoglossa venom apparatus as inferred by molecular phylogeny of the Terebridae

Toxoglossate marine gastropods, traditionally assigned to thefamilies Conidae, Terebridae, and Turridae, are one of the mostpopulous animal groups that use venom to capture their prey.These marine animals are generally characterized by a venomapparatus that consists of a muscular venom bulb and a tubularvenom gland. The toxoglossan radula, often compared with a hypodermicneedle for its use as a conduit to inject toxins into prey,is considered a major anatomical breakthrough that assistedin the successful initial radiation of these animals in theCretaceous and early Tertiary. The pharmacological success oftoxins from cone snails has made this group a star among biochemistsand neuroscientists, but very little is known about toxins fromthe other Toxoglossa, and the phylogeny of these families islargely in doubt. Here we report the first molecular phylogenyfor the Terebridae and use the results to infer the evolutionof the venom apparatus for this group. Our findings indicatethat most of the genera of terebrids are polyphyletic, and onespecies ("Terebra" (s.l.) jungi) is the sister group to allother terebrids. Molecular analyses combined with mapping ofvenom apparatus morphology indicate that the Terebridae havelost the venom apparatus at least twice during their evolution.Species in the genera Terebra and Hastula have the typical venomapparatus found in most toxoglossate gastropods, but all otherterebrid species do not. For venomous organisms, the dual analysisof molecular phylogeny and toxin function is an instructivecombination for unraveling the larger questions of phylogenyand speciation. The results presented here suggest a paradigmshift in the current understanding of terebrid evolution, whilepresenting a road map for discovering novel terebrid toxins,a largely unexplored resource for biomedical research and potentialtherapeutic drug development.