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Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus

  1. Baldomero M. Oliveraa,1
  1. aDepartment of Biology, University of Utah, Salt Lake City, UT 84112;
  2. bNew York University Langone Medical Center, New York, NY 10016;
  3. cInstituto de Neurobiología, Universidad Nacional Autónoma de México, Campus Juriquilla, Querétaro 76230, Mexico;
  4. dMarine Science Institute, University of the Philippines–Diliman, Quezon City 1101, Philippines; and
  5. eMarine Laboratory, University of Guam, Mangilao 96923, Guam

  1. Contributed by Baldomero M. Olivera, January 8, 2015 (sent for review February 11, 2014)

Significance

Only rarely is it possible to reconstruct molecular events that trigger the radiation of new lineages. Here we report key evidence that allows reconstruction of the transition from worm hunting to fish hunting among the species-rich family (Conidae) of marine cone snails (>700 species), which resulted in the emergence of multiple biodiverse piscivorous clades. A priori, the evolution of fish-hunting specialists would seem extremely improbable in a lineage of slowly moving snails that cannot swim, unlike their fish prey. The combination of results from molecular neuroscience, phylogenetic analysis, and chemical biology demonstrates that an ancestral cone snail venom peptide similar to δ-conotoxin TsVIA, a defensive venom component, preadapted a worm-hunting cone snail lineage, enabling the shift to a piscivorous lifestyle.

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.

Footnotes

  • ↵1To whom correspondence may be addressed. Email: russ.teichert{at}utah.edu or olivera{at}biology.utah.edu.

  • Author contributions: J.S.I., B.U., M.-M.Z., M.A., M.W., D.Y., P.S.-C., H.S.-H., J.B., R.W.T., and B.M.O. designed research; J.W.A., J.S.I., B.U., M.-M.Z., M.A., D.T., M.W., P.S.-C., H.S.-H., and J.B. performed research; J.W.A., J.S.I., B.U., M.-M.Z., M.A., M.W., D.Y., P.S.-C., H.S.-H., R.W.T., and B.M.O. analyzed data; and J.W.A., J.S.I., B.U., M.W., D.Y., P.S.-C., H.S.-H., R.W.T., and B.M.O. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database. For a list of accession numbers, see Table S1.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1424435112/-/DCSupplemental.

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