Natural selection is generally expected to favor one form of a given trait within a population. The presence of multiple functional variants of traits involved in activities such as feeding, reproduction, or the defense against predators is relatively uncommon within animal species. The genetic architecture and evolutionary mechanisms underlying the origin and maintenance of such polymorphisms are of special interest. Among rattlesnakes, several instances of the production of biochemically distinct neurotoxic or hemorrhagic venom types within the same species are known. Here, we investigated the genetic basis of this phenomenon in three species and found that neurotoxic and hemorrhagic individuals of the same species possess markedly different haplotypes at two toxin gene complexes. For example, neurotoxic and hemorrhagic Crotalus scutulatus individuals differ by 5 genes at the phospholipase A2 (PLA2) toxin gene complex and by 11 genes at the metalloproteinase (MP) gene complex. A similar set of extremely divergent haplotypes also underlies alternate venom types within C. helleri and C. horridus. We further show that the MP and PLA2 haplotypes of neurotoxic C. helleri appear to have been acquired through hybridization with C. scutulatus-a rare example of the horizontal transfer of a potentially highly adaptive suite of genes. These large structural variants appear analogous to immunity gene complexes in host-pathogen arms races and may reflect the impact of balancing selection at the PLA2 and MP complexes for predation on different prey.
Keywords: gene complexes; gene loss; intraspecific variation; metalloproteinases; neurotoxin; phospholipase A2; polymorphism; venom.
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