Biodiversity of Cone Snails and Other Venomous Marine Gastropods: Evolutionary Success Through Neuropharmacology

Abstract

Venomous marine snails (superfamily Conoidea) are a remarkably biodiverse marine invertebrate lineage (featuring more than 10,000 species). Conoideans use complex venoms (up to 100 different components for each species) to capture prey and for other biotic interactions. Molecular phylogeny and venom peptide characterization provide an unusual multidisciplinary view of conoidean biodiversity at several taxonomic levels. Venom peptides diverge between species at an unprecedented rate through hypermutation within gene families. Clade divergence within a genus occurs without recruiting new gene families when a saltatory event, such as colonization of new prey types (e.g., fish), leads to a new radiation. Divergence between genera in the same family involves substantial divergence in gene families. In the superfamily Conoidea, the family groups recruited distinct sets of different venom gene superfamilies. The associated morphological, behavioral, and prey-preference changes that accompany these molecular changes are unknown for most conoidean lineages, except for one genus, Conus, for which many associated phenotypic changes have been documented.

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

“…In contrast, when all of the relevant fish-hunting lineages are compared, δ-conotoxins are found to be highly conserved; all belong to the O superfamily, and share strong sequence similarity. We demonstrate a striking sequence similarity with δ-conotoxins TsVIA and ErVIA from C. tessulatus and C. eburneus but not with the δ-conotoxins from molluscivorous Conus species (36,40). The sequences of δ-conotoxins from two mollusc-hunting species, six fish-hunting species, and the two species from the Tesseliconus clade, C. eburneus and C. tessulatus (Table 1), demonstrate the remarkable sequence similarity of the δ-conotoxins from worm-hunting and fish-hunting species and the greater sequence divergence of δ-conotoxins from mollusc-hunting species.…”

“…The role of δ-conotoxins in fish hunting is critical in piscivorous cone snail species that belong to the Pionoconus or Chelyconus lineages; δ-conotoxins are a major component of the so-called lightning-strike cabal (8,36). This is a key physiological strategy for the capture of fish by the much slower-moving cone snails that causes an extreme hyperexcitability of the fish nervous system, resulting in an almost instant tetanic paralysis, as though the fish had been hit with a Taser.…”

“…In effect, the nervous system is subjected to an electrical storm that originates from axons near the venominjection site. Thus, the evolution of appropriate δ-conotoxins and κ-conotoxins was postulated to be key to the evolutionary shift from worm hunting to fish hunting in cone snails (9,36).…”

“…We have presented evidence that supports a specific hypothesis for how the transition from worm hunting to fish hunting occurred in cone snails. We previously suggested (36) that as an ancestral lineage of vermivorous cone snails attacked their worm prey, fish would try to steal the prey and that vermivorous Conus may have evolved δ-conotoxins to deter fish competitors. The basis for this hypothesis was that in diverse lineages of fish-hunting cone snails, the same gene superfamily had been recruited for the δ-conotoxins used to capture fish.…”

Molecular interaction of δ-conopeptide EVIA with voltage-gated Na+ channels

“…[1][2][3] Because of their specific target interaction, some conotoxins are of medicinal value; for example, the ω-conotoxin MVIIA from Conus magus (trade name: Prialt ® ), which inhibits voltage-gated N-type Ca 2+ channels in dorsal root ganglia neurons, is used as a potent analgesic. [4][5][6][7] Given that every cone snail species produces several hundreds of conopeptides, a plethora of biologically interesting substances is yet to be discovered.…”