title: Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus.
abstract: Prey shifts in carnivorous predators are events that can initiate the accelerated generation of new biodiversity. However, it is seldom possible to reconstruct how the change in prey preference occurred. Here we describe an evolutionary "smoking gun" that illuminates the transition from worm hunting to fish hunting among marine cone snails, resulting in the adaptive radiation of fish-hunting lineages comprising ∼100 piscivorous Conus species. This smoking gun is δ-conotoxin TsVIA, a peptide from the venom of Conus tessulatus that delays inactivation of vertebrate voltage-gated sodium channels. C. tessulatus is a species in a worm-hunting clade, which is phylogenetically closely related to the fish-hunting cone snail specialists. The discovery of a δ-conotoxin that potently acts on vertebrate sodium channels in the venom of a worm-hunting cone snail suggests that a closely related ancestral toxin enabled the transition from worm hunting to fish hunting, as δ-conotoxins are highly conserved among fish hunters and critical to their mechanism of prey capture; this peptide, δ-conotoxin TsVIA, has striking sequence similarity to these δ-conotoxins from piscivorous cone snail venoms. Calcium-imaging studies on dissociated dorsal root ganglion (DRG) neurons revealed the peptide's putative molecular target (voltage-gated sodium channels) and mechanism of action (inhibition of channel inactivation). The results were confirmed by electrophysiology. This work demonstrates how elucidating the specific interactions between toxins and receptors from phylogenetically well-defined lineages can uncover molecular mechanisms that underlie significant evolutionary transitions.
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Joseph W
authors.initials: JW
authors.lastname: Aman
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Julita S
authors.initials: JS
authors.lastname: Imperial
authors.affiliation: New York University Langone Medical Center, New York, NY 10016;
authors.forename: Beatrix
authors.initials: B
authors.lastname: Ueberheide
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Min-Min
authors.initials: MM
authors.lastname: Zhang
authors.affiliation: Instituto de Neurobiología, Universidad Nacional Autónoma de México, Campus Juriquilla, Querétaro 76230, Mexico;
authors.forename: Manuel
authors.initials: M
authors.lastname: Aguilar
authors.affiliation: Marine Science Institute, University of the Philippines-Diliman, Quezon City 1101, Philippines; and.
authors.forename: Dylan
authors.initials: D
authors.lastname: Taylor
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Maren
authors.initials: M
authors.lastname: Watkins
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Doju
authors.initials: D
authors.lastname: Yoshikami
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Patrice
authors.initials: P
authors.lastname: Showers-Corneli
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112;
authors.forename: Helena
authors.initials: H
authors.lastname: Safavi-Hemami
authors.affiliation: Marine Laboratory, University of Guam, Mangilao 96923, Guam.
authors.forename: Jason
authors.initials: J
authors.lastname: Biggs
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112; russ.teichert@utah.edu olivera@biology.utah.edu.
authors.forename: Russell W
authors.initials: RW
authors.lastname: Teichert
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112; russ.teichert@utah.edu olivera@biology.utah.edu.
authors.forename: Baldomero M
authors.initials: BM
authors.lastname: Olivera
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001681:Biological Assay; D020916:Conotoxins / Q000737:chemistry / Q000633:toxicity; D052078:Conus Snail / Q000033:anatomy & histology / Q000502:physiology*; D005399:Fishes / Q000502:physiology*; D008969:Molecular Sequence Data; D010455:Peptides / Q000378:metabolism; D010802:Phylogeny; D011235:Predatory Behavior / Q000502:physiology*
chemical_list: D020916:Conotoxins; D010455:Peptides
keywords: cone snails; conotoxin; evolution; prey preference
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