Comparison of the Venom Peptides and Their Expression in Closely Related Conus Species: Insights into Adaptive Post-speciation Evolution of Conus Exogenomes

Genes that encode products with exogenous targets, which comprise an organism's “exogenome,” typically exhibit high rates of evolution. The genes encoding the venom peptides (conotoxins or conopeptides) in Conus sensu lato exemplify this class of genes. Their rapid diversification has been established and is believed to be linked to the high speciation rate in this genus. However, the molecular mechanisms that underlie venom peptide diversification and ultimately emergence of new species remain poorly understood. In this study, the sequences and expression levels of conotoxins from several specimens of two closely related worm-hunting species, Conus tribblei and Conus lenavati, were compared through transcriptome analysis. Majority of the identified putative conopeptides were novel, and their diversity, even in each specimen, was remarkably high suggesting a wide range of prey targets for these species. Comparison of the interspecific expression patterns of conopeptides at the superfamily level resulted in the discovery of both conserved as well as species-specific expression patterns, indicating divergence in the regulatory network affecting conotoxin gene expression. Comparison of the transcriptomes of the individual snails revealed that each specimen produces a distinct set of highly expressed conopeptides, reflecting the capability of individual snails to fine-tune the composition of their venoms. These observations reflect the role of sequence divergence and divergence in the control of expression for specific conopeptides in the evolution of the exogenome and hence venom composition in Conus.