Abstract
BackgroundPredatory marine gastropods of the genus Conus exhibit substantial variation in venom composition both within and among species. Apart from mechanisms associated with extensive turnover of gene families and rapid evolution of genes that encode venom components (‘conotoxins’), the evolution of distinct conotoxin expression patterns is an additional source of variation that may drive interspecific differences in the utilization of species’ ‘venom gene space’. To determine the evolution of expression patterns of venom genes of Conus species, we evaluated the expression of A-superfamily conotoxin genes of a set of closely related Conus species by comparing recovered transcripts of A-superfamily genes that were previously identified from the genomes of these species. We modified community phylogenetics approaches to incorporate phylogenetic history and disparity of genes and their expression profiles to determine patterns of venom gene space utilization.ResultsLess than half of the A-superfamily gene repertoire of these species is expressed, and only a few orthologous genes are coexpressed among species. Species exhibit substantially distinct expression strategies, with some expressing sets of closely related loci (‘under-dispersed’ expression of available genes) while others express sets of more disparate genes (‘over-dispersed’ expression). In addition, expressed genes show higher dN/dS values than either unexpressed or ancestral genes; this implies that expression exposes genes to selection and facilitates rapid evolution of these genes. Few recent lineage-specific gene duplicates are expressed simultaneously, suggesting that expression divergence among redundant gene copies may be established shortly after gene duplication.ConclusionsOur study demonstrates that venom gene space is explored differentially by Conus species, a process that effectively permits the independent and rapid evolution of venoms in these species.
Highlights
Predatory marine gastropods of the genus Conus exhibit substantial variation in venom composition both within and among species
Percentages of A-superfamily genes expressed in each species We sequenced 487, 167, 135 and 112 colonies from two individuals each of C. lividus, C. diadema, C. quercinus and one individual of C. sanguinolentus (Table 1)
Based on comparison of these alleles with A-superfamily genes identified from genomic DNA of these species [19], the alleles represent 13 loci in C. lividus, three in C. diadema, three in C. quercinus and five in C. sanguinolentus (Table 1)
Summary
Predatory marine gastropods of the genus Conus exhibit substantial variation in venom composition both within and among species. Apart from mechanisms associated with extensive turnover of gene families and rapid evolution of genes that encode venom components (‘conotoxins’), the evolution of distinct conotoxin expression patterns is an additional source of variation that may drive interspecific differences in the utilization of species’ ‘venom gene space’. Some species may fully explore this space (e.g., express a disparate set of available loci), while others may focus within a specific region of the space. This hypothesis stems from observations that numbers and combinations of expressed venom genes differ among species of predatory marine gastropods (Conus species) and that genes expressed in certain species do not appear to be random subsets of available genes [13]
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