Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 110, Issue 51, Pages 20651-20656Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1314702110
Keywords
genomics; phylogenetics; serpentes
Categories
Funding
- Naturalis Biodiversity Center
- Netherlands Organization for Scientific Research
- United Kingdom Natural Environment Research Council
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- United Kingdom Biotechnology and Biological Sciences Research Council
- Dutch Government
- Natural Environment Research Council [NE/J018678/1] Funding Source: researchfish
- NERC [NE/J018678/1] Funding Source: UKRI
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Snakes are limbless predators, and many species use venom to help overpower relatively large, agile prey. Snake venoms are complex protein mixtures encoded by several multilocus gene families that function synergistically to cause incapacitation. To examine venom evolution, we sequenced and interrogated the genome of a venomous snake, the king cobra (Ophiophagus hannah), and compared it, together with our unique transcriptome, microRNA, and proteome datasets from this species, with data from other vertebrates. In contrast to the platypus, the only other venomous vertebrate with a sequenced genome, we find that snake toxin genes evolve through several distinct co-option mechanisms and exhibit surprisingly variable levels of gene duplication and directional selection that correlate with their functional importance in prey capture. The enigmatic accessory venom gland shows a very different pattern of toxin gene expression from the main venom gland and seems to have recruited toxin-like lectin genes repeatedly for new nontoxic functions. In addition, tissue-specific microRNA analyses suggested the co-option of core genetic regulatory components of the venom secretory system from a pancreatic origin. Although the king cobra is limbless, we recovered coding sequences for all Hox genes involved in amniote limb development, with the exception of Hoxd12. Our results provide a unique view of the origin and evolution of snake venom and reveal multiple genome-level adaptive responses to natural selection in this complex biological weapon system. More generally, they provide insight into mechanisms of protein evolution under strong selection.
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