Dietary breadth is positively correlated with venom complexity in cone snails

Abstract

Background: Although 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.

Results: We 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.

Conclusions: The 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.

Keywords: Comparative biology; Phylogenetics; Venom duct transcriptome.

Fig. 1

Conotoxin expression in a phylogenetic context. Time-calibrated maximum likelihood phylogeny of Conidae species sequenced in this study generated from 821 loci. Values at nodes represent bootstrap support and • indicates bootstrap support = 100. Tree is rooted with Californiconus californicus. Taxa are colored by diet (green = generalist, black = vermivore, orange = molluscivore). Heat map shows relative contribution (measured as percentage of total conotoxin TPM per species) of gene superfamilies that contributed to at least 10 % of overall conotoxin expression in at least one species

Fig. 2

Conotoxin composition overlap and dietary preference. Boxplots showing the distribution of conotoxin overlap values (D) categorized by whether the species comparison occurred between a generalist and a vermivore, a molluscivore and a vermivore, or two vermivores. Values were calculated by the percentage of mature toxins belonging to each gene superfamily (D_mature) and the percent expression of gene superfamilies (D_expression)

Fig. 3

Dietary breadth and conotoxin complexity. Correlations between dietary breadth (Averaged H’) and measures of conotoxin complexity: number of mature toxins, number of gene superfamilies, and number of cysteine frameworks. Graphs are labelled with correlation coefficients. *denotes significant correlation from a PGLS analysis