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Genome Biol Evol. 2014 Aug;6(8):2088-95. doi: 10.1093/gbe/evu166.

Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins.

Author information

1
School of Biological Sciences, Bangor University, United Kingdom.
2
Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, United Kingdom.
3
Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
4
School of Biological Sciences, Bangor University, United Kingdom j.mulley@bangor.ac.uk.

Abstract

Snake venom has been hypothesized to have originated and diversified through a process that involves duplication of genes encoding body proteins with subsequent recruitment of the copy to the venom gland, where natural selection acts to develop or increase toxicity. However, gene duplication is known to be a rare event in vertebrate genomes, and the recruitment of duplicated genes to a novel expression domain (neofunctionalization) is an even rarer process that requires the evolution of novel combinations of transcription factor binding sites in upstream regulatory regions. Therefore, although this hypothesis concerning the evolution of snake venom is very unlikely and should be regarded with caution, it is nonetheless often assumed to be established fact, hindering research into the true origins of snake venom toxins. To critically evaluate this hypothesis, we have generated transcriptomic data for body tissues and salivary and venom glands from five species of venomous and nonvenomous reptiles. Our comparative transcriptomic analysis of these data reveals that snake venom does not evolve through the hypothesized process of duplication and recruitment of genes encoding body proteins. Indeed, our results show that many proposed venom toxins are in fact expressed in a wide variety of body tissues, including the salivary gland of nonvenomous reptiles and that these genes have therefore been restricted to the venom gland following duplication, not recruited. Thus, snake venom evolves through the duplication and subfunctionalization of genes encoding existing salivary proteins. These results highlight the danger of the elegant and intuitive "just-so story" in evolutionary biology.

KEYWORDS:

evolution; gene duplication; neofunctionalization; snake venom; subfunctionalization

PMID:
25079342
PMCID:
PMC4231632
DOI:
10.1093/gbe/evu166
[Indexed for MEDLINE]
Free PMC Article

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