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Venom Insulins of Cone Snails Diversify Rapidly and Track Prey Taxa.

ABSTRACT: A specialized insulin was recently found in the venom of a fish-hunting cone snail, Conus geographus Here we show that many worm-hunting and snail-hunting cones also express venom insulins, and that this novel gene family has diversified explosively. Cone snails express a highly conserved insulin in their nerve ring; presumably this conventional signaling insulin is finely tuned to the Conus insulin receptor, which also evolves very slowly. By contrast, the venom insulins diverge rapidly, apparently in response to biotic interactions with prey and also possibly the cones' own predators and competitors. Thus, the inwardly directed signaling insulins appear to experience predominantly purifying sele\ction to target an internal receptor that seldom changes, while the outwardly directed venom insulins frequently experience directional selection to target heterospecific insulin receptors in a changing mix of prey, predators and competitors. Prey insulin receptors may often be constrained in ways that prevent their evolutionary escape from targeted venom insulins, if amino-acid substitutions that result in escape also degrade the receptor's signaling functions.

SUBMITTER: Safavi-Hemami H

PROVIDER: S-EPMC5062327 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Venom Insulins of Cone Snails Diversify Rapidly and Track Prey Taxa.

Safavi-Hemami Helena H Lu Aiping A Li Qing Q Fedosov Alexander E AE Biggs Jason J Showers Corneli Patrice P Seger Jon J Yandell Mark M Olivera Baldomero M BM

Molecular biology and evolution 20160814 11

A specialized insulin was recently found in the venom of a fish-hunting cone snail, Conus geographus Here we show that many worm-hunting and snail-hunting cones also express venom insulins, and that this novel gene family has diversified explosively. Cone snails express a highly conserved insulin in their nerve ring; presumably this conventional signaling insulin is finely tuned to the Conus insulin receptor, which also evolves very slowly. By contrast, the venom insulins diverge rapidly, appare ...[more]

PMID: 27524826

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Project description:BackgroundAlthough diet is believed to be a major factor underlying the evolution of venom, few comparative studies examine both venom composition and diet across a radiation of venomous species. Cone snails within the family, Conidae, comprise more than 700 species of carnivorous marine snails that capture their prey by using a cocktail of venomous neurotoxins (conotoxins or conopeptides). Venom composition across species has been previously hypothesized to be shaped by (a) prey taxonomic class (i.e., worms, molluscs, or fish) and (b) dietary breadth. We tested these hypotheses under a comparative phylogenetic framework using ecological data from past studies in conjunction with venom duct transcriptomes sequenced from 12 phylogenetically disparate cone snail species, including 10 vermivores (worm-eating), one molluscivore, and one generalist.ResultsWe discovered 2223 unique conotoxin precursor peptides that encoded 1864 unique mature toxins across all species, >90 % of which are new to this study. In addition, we identified two novel gene superfamilies and 16 novel cysteine frameworks. Each species exhibited unique venom profiles, with venom composition and expression patterns among species dominated by a restricted set of gene superfamilies and mature toxins. In contrast with the dominant paradigm for interpreting Conidae venom evolution, prey taxonomic class did not predict venom composition patterns among species. We also found a significant positive relationship between dietary breadth and measures of conotoxin complexity.ConclusionsThe poor performance of prey taxonomic class in predicting venom components suggests that cone snails have either evolved species-specific expression patterns likely as a consequence of the rapid evolution of conotoxin genes, or that traditional means of categorizing prey type (i.e., worms, mollusc, or fish) and conotoxins (i.e., by gene superfamily) do not accurately encapsulate evolutionary dynamics between diet and venom composition. We also show that species with more generalized diets tend to have more complex venoms and utilize a greater number of venom genes for prey capture. Whether this increased gene diversity confers an increased capacity for evolutionary change remains to be tested. Overall, our results corroborate the key role of diet in influencing patterns of venom evolution in cone snails and other venomous radiations.

Dataset Information

Venom Insulins of Cone Snails Diversify Rapidly and Track Prey Taxa.

Publications

Venom Insulins of Cone Snails Diversify Rapidly and Track Prey Taxa.

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