δ-Conotoxin SuVIA suggests an evolutionary link between ancestral predator defence and the origin of fish-hunting behaviour in carnivorous cone snails

Abstract

Some venomous cone snails feed on small fishes using an immobilizing combination of synergistic venom peptides that target K v and Na v channels. As part of this envenomation strategy, d-conotoxins are potent ichtyotoxins that enhance Na v channel function. d-Conotoxins belong to an ancient and widely distributed gene superfamily, but any evolutionary link from ancestral worm-eating cone snails to modern piscivorous species has not been elucidated. Here, we report the discovery of SuVIA, a potent vertebrate-active d-conotoxin characterized from a vermivorous cone snail (Conus suturatus). SuVIA is equipotent at hNa V 1.3, hNa V 1.4 and hNa V 1.6 with EC 50 s in the low nanomolar range. SuVIA also increased peak hNa V 1.7 current by approximately 75% and shifted the voltage-dependence of activation to more hyperpolarized potentials from -15 mV to -25 mV, with little effect on the voltage-dependence of inactivation. Interestingly, the proximal venom gland expression and pain-inducing effect of SuVIA in mammals suggest that d-conotoxins in vermivorous cone snails play a defensive role against higher order vertebrates. We propose that d-conotoxins originally evolved in ancestral vermivorous cones to defend against larger predators including fishes have been repurposed to facilitate a shift to piscivorous behaviour, suggesting an unexpected underlying mechanism for this remarkable evolutionary transition.

The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus)

“…Another species of arboreal elapid snake, the Stephens’ banded snake ( Hoplocephalus stephensi ), uses natriuretic peptide toxins to cause a precipitous drop in the blood pressure of prey animals [121]. In the case of cone snails, the venom was first evolved for worm-hunting, with the subsequent evolution of fish-specific venom for defence against predators, which was then co-opted on at least two occasions for fish-specialist prey preference [122,123,124]. Piscivorus cone snails also risk being unable to recover their prey if the fish are able to escape after envenomation—even if the fish only swims a small distance before dying, the slow-moving snail faces a high risk of losing its meal to an opportune scavenger.…”

The role of defensive ecological interactions in the evolution of conotoxins

“…However, the localization of peptide expression within the venom gland has become an accepted proxy to confirm their functional role (Jin et al . ; Safavi‐Hemami et al . ).…”

“…; Jin et al . ). At the molecular level, a parallel diversification of conotoxins is facilitated by rapidly evolving conotoxin genes, underpinned by processes such as gene recombination, gene duplication (Espiritu et al .…”

A blood bond: evolutionary, pathophysiological and biodiscovery implications of coagulotoxic snake venoms

“…Thus, there may be a stronger selection pressure operating upon T. mossambicanus for a venom which rapidly immobilises prey. This is consistent with what has been observed in other lineages of venomous animals in which prey escape potential is a significant shaping factor and thus the venom is under extreme selection pressure for rapid immobilising action (Aman et al, 2015;Dutertre et al, 2014;Eng et al, 2015;Fry et al, 2015a;Fry et al, 2015c;Harvey and Anderson, 1985;Harvey and Karlsson, 1980;Herrera et al, 2012;Jackson et al, 2013;Jin et al, 2015;Karlsson et al, 1983;Osman et al, 1973;Utkin et al, 2015;Yang et al, 2016).…”