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Molecular & Cellular Proteomics 7:215-246, 2008.
© 2008 by The American Society for Biochemistry and Molecular Biology, Inc.

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Research

Evolution of an Arsenal

Structural and Functional Diversification of the Venom System in the Advanced Snakes (Caenophidia)^*

Bryan G. Fry^,, Holger Scheib^¶,||, Louise van der Weerd^**, Bruce Young, Judith McNaughtan, S. F. Ryan Ramjan, Nicolas Vidal^¶¶, Robert E. Poelmann^** and Janette A. Norman^,||||

From the Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute and Department of Oral Medicine and Surgery, School of Dental Science, University of Melbourne, Parkville, Victoria 3010, Australia, ^¶ SBC Lab AG, Seebüelstrasse 26, 8185 Winkel, Switzerland, ^** Molecular Imaging Laboratories Leiden, MRI Facility, Departments of Anatomy and Radiology, 2300 RC, Leiden, The Netherlands, Department of Biology, Washburn University, Topeka, Kansas 66621, ^¶¶ UMR 7138, Département Systématique et Evolution, Muséum National d’Histoire Naturelle, CP 26, 57 rue Cuvier, 75005 Paris, France, and ^|||| Molecular Biology, Museum Victoria, G. P. O. Box 666, Melbourne, Victoria 3001, Australia

Venom is a key innovation underlying the evolution of advanced snakes (Caenophidia). Despite this, very little is known about venom system structural diversification, toxin recruitment event timings, or toxin molecular evolution. A multidisciplinary approach was used to examine the diversification of the venom system and associated toxins across the full range of the 100 million-year-old advanced snake clade with a particular emphasis upon families that have not secondarily evolved a front-fanged venom system (80% of the 2500 species). Analysis of cDNA libraries revealed complex venom transcriptomes containing multiple toxin types including three finger toxins, cobra venom factor, cysteine-rich secretory protein, hyaluronidase, kallikrein, kunitz, lectin, matrix metalloprotease, phospholipase A₂, snake venom metalloprotease/a disintegrin and metalloprotease, and waprin. High levels of sequence diversity were observed, including mutations in structural and functional residues, changes in cysteine spacing, and major deletions/truncations. Morphological analysis comprising gross dissection, histology, and magnetic resonance imaging also demonstrated extensive modification of the venom system architecture in non-front-fanged snakes in contrast to the conserved structure of the venom system within the independently evolved front-fanged elapid or viperid snakes. Further, a reduction in the size and complexity of the venom system was observed in species in which constriction has been secondarily evolved as the preferred method of prey capture or dietary preference has switched from live prey to eggs or to slugs/snails. Investigation of the timing of toxin recruitment events across the entire advanced snake radiation indicates that the evolution of advanced venom systems in three front-fanged lineages is associated with recruitment of new toxin types or explosive diversification of existing toxin types. These results support the role of venom as a key evolutionary innovation in the diversification of advanced snakes and identify a potential role for non-front-fanged venom toxins as a rich source for lead compounds for drug design and development.

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