Comparative transcriptomics of the venoms of continental and insular radiations of West African cones

Abstract

The transcriptomes of the venom glands of 13 closely related species of vermivorous cones endemic to West Africa from genera Africonus and Varioconus were sequenced and venom repertoires compared within a phylogenetic framework using one Kalloconus species as outgroup. The total number of conotoxin precursors per species varied between 108 and 221. Individuals of the same species shared about one-fourth of the total conotoxin precursors. The number of common sequences was drastically reduced in the pairwise comparisons between closely related species, and the phylogenetical signal was totally eroded at the inter-generic level (no sequence was identified as shared derived), due to the intrinsic high variability of these secreted peptides. A common set of four conotoxin precursor superfamilies (T, O1, O2 and M) was expanded in all studied cone species, and thus, they are considered the basic venom toolkit for hunting and defense in the West African vermivorous cone snails. Maximum-likelihood ancestral character reconstructions inferred shared conotoxin precursors preferentially at internal nodes close to the tips of the phylogeny (between individuals and between closely related species) as well as in the common ancestor of Varioconus. Besides the common toolkit, the two genera showed significantly distinct catalogues of conotoxin precursors in terms of type of superfamilies present and the abundance of members per superfamily, but had similar relative expression levels indicating functional convergence. Differential expression comparisons between vermivorous and piscivorous cones highlighted the importance of the A and S superfamilies for fish hunting and defense.

Keywords: Africonus; Varioconus; conotoxin precursors; transcriptomes; vermivorous cones.

Figure 1.

Venom compositions of the 16 studied specimens. The bars represent the total number of conotoxin precursors. The proportion of superfamilies with five or more members is shown in colours. The dotted line represents the number of different superfamilies identified in the venom. The species codes in green, blue and black belong to Africonus, Varioconus and Kalloconus, respectively.

Figure 2.

Maximum-likelihood ancestral reconstruction of conotoxin precursors along the phylogeny of cones from West Africa (see electronic supplementary material, figure S1). Statistical supports for inferred shared-derived conotoxin precursor are provided in electronic supplementary material, table S3. The table on the right shows the conotoxin precursors that are shared derived at a particular node (see electronic supplementary material, table S4). The red numbers are common conotoxin precursors found in distantly related nodes, which could represent potential instances of convergence. (Online version in colour.)

Figure 3.

MCA and PCA comparing venom compositions of genera Africonus and Varioconus. The two-dimensional scatter plots are shown. The venom composition was defined as presence/absence of conotoxin precursor superfamilies (a); superfamily conotoxin precursor abundance expressed as percentage over total number of members (b) and relative expression (TPM) levels (c). The percentages of the eigenvalue (MCA) or variance (PCA) for each of the axis are indicated on the corresponding labels. Extremes and outliers are labelled. (Online version in colour.)

Figure 4.

Differences in venom compositions of vermivorous and piscivorous cones. (a) Average expression (measured in TPMs) of conotoxin precursor superfamilies per genus. Vermivorous genera (Africonus and Varioconus) were compared to piscivorous genera (Chelyconus and Pionoconus). The bar plot depicts those superfamilies differentially expressed between diets. (b) PCA comparing conotoxin precursor abundance per superfamily between vermivorous and piscivorous species. The percentages of variance for each of the axis are indicated on the corresponding labels. In both panels, the genera Africonus, Varioconus, Chelyconus and Pionoconus are depicted in green, blue, yellow and red, respectively.