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Evolution of Conus Peptide Genes: Duplication and Positive Selection in the A-Superfamily

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Abstract

A remarkable diversity of venom peptides is expressed in the genus Conus (known as “conotoxins” or “conopeptides”). Between 50 and 200 different venom peptides can be found in a single Conus species, each having its own complement of peptides. Conopeptides are encoded by a few gene superfamilies; here we analyze the evolution of the A-superfamily in a fish-hunting species clade, Pionoconus. More than 90 conopeptide sequences from 11 different Conus species were used to build a phylogenetic tree. Comparison with a species tree based on standard genes reveals multiple gene duplication events, some of which took place before the Pionoconus radiation. By analysing several A-conopeptides from other Conus species recorded in GenBank, we date the major duplication events after the divergence between fish-hunting and non-fish-hunting species. Furthermore, likelihood approaches revealed strong positive selection; the magnitude depends on which A-conopeptide lineage and amino-acid locus is analyzed. The four major A-conopeptide clades defined are consistent with the current division of the superfamily into families and subfamilies based on the Cys pattern. The function of three of these clades (the κA-family, the α4/7-subfamily, and α3/5-subfamily) has previously been characterized. The function of the remaining clade, corresponding to the α4/4-subfamily, has not been elucidated. This subfamily is also found in several other fish-hunting species clades within Conus. The analysis revealed a surprisingly diverse origin of α4/4 conopeptides from a single species, Conus bullatus. This phylogenetic approach that defines different genetic lineages of Conus venom peptides provides a guidepost for identifying conopeptides with potentially novel functions.

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Acknowledgments

This work was supported by NIH Program Project grant GM48677 (to BMO). We are pleased to thank Jon Seger, Nicole Kraus, Naoko Takezaki, and two anonymous reviewers for constructive comments on a previous version of the manuscript.

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Authors and Affiliations

  1. Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, UT, 84112, USA

    Nicolas Puillandre, Maren Watkins & Baldomero M. Olivera

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  1. Nicolas Puillandre
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  2. Maren Watkins
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  3. Baldomero M. Olivera
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Correspondence to Nicolas Puillandre.

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Puillandre, N., Watkins, M. & Olivera, B.M. Evolution of Conus Peptide Genes: Duplication and Positive Selection in the A-Superfamily. J Mol Evol 70, 190–202 (2010). https://doi.org/10.1007/s00239-010-9321-7

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  • DOI: https://doi.org/10.1007/s00239-010-9321-7

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