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Molecular Phylogeny and Evolution of the Proteins Encoded by Coleoid (Cuttlefish, Octopus, and Squid) Posterior Venom Glands

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Abstract

In this study, we report for the first time a detailed evaluation of the phylogenetic history and molecular evolution of the major coleoid toxins: CAP, carboxypeptidase, chitinase, metalloprotease GON-domain, hyaluronidase, pacifastin, PLA2, SE-cephalotoxin and serine proteases, with the carboxypeptidase and GON-domain documented for the first time in the coleoid venom arsenal. We show that although a majority of sites in these coleoid venom-encoding genes have evolved under the regime of negative selection, a very small proportion of sites are influenced by the transient selection pressures. Moreover, nearly 70 % of these episodically adapted sites are confined to the molecular surface, highlighting the importance of variation of the toxin surface chemistry. Coleoid venoms were revealed to be as complex as other venoms that have traditionally been the recipient of the bulk of research efforts. The presence of multiple peptide/protein types in coleoids similar to those present in other animal venoms identifies a convergent strategy, revealing new information as to what characteristics make a peptide/protein type amenable for recruitment into chemical arsenals. Coleoid venoms have significant potential not only for understanding fundamental aspects of venom evolution but also as an untapped source of novel toxins for use in drug design and discovery.

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Acknowledgments

BGF was funded by the Australian Research Council, University of Queenland, Herman Slade Foundation and a Universitas 21 Edward Clarence Dyason Fellowship. BGF would also like to thank the University of Hong Kong’s Swire Institute of Marine Science for hosting him during Hong Kong fieldwork. SAA was the recipient of postdoctoral fellowship (PDRF Phase II Batch-V) from Higher Education Commission (HEC Islamabad) Pakistan. KS was funded by the PhD grant (SFRH/BD/61959/2009) from Fundação para a Ciência e a Tecnologia (FCT). AA was funded by the project PTDC/AACAMB/, 121301/2010 (FCOMP-01-0124-FEDER-019490) from FCT. EABU acknowledges funding from the University of Queensland (International Postgraduate Research Scholarship, UQ Centennial Scholarship, and UQ Advantage Top-Up Scholarship) and the Norwegian State Education Loans Fund.

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Correspondence to Bryan G. Fry.

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Tim Ruder, Kartik Sunagar, Eivind A. B. Undheim, Syed A. Ali are joint first authors.

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Ruder, T., Sunagar, K., Undheim, E.A.B. et al. Molecular Phylogeny and Evolution of the Proteins Encoded by Coleoid (Cuttlefish, Octopus, and Squid) Posterior Venom Glands. J Mol Evol 76, 192–204 (2013). https://doi.org/10.1007/s00239-013-9552-5

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