The roles of balancing selection and recombination in the evolution of rattlesnake venom

Schield, Drew R.; Perry, Blair W.; Adams, Richard H.; Holding, Matthew L.; Nikolakis, Zachary L.; Gopalan, Siddharth S; Smith, Cara F.; Parker, Joshua; Meik, Jesse M.; DeGiorgio, Michael; Mackessy, Stephen P.; Castoe, Todd A.

doi:10.1038/s41559-022-01829-5

Cited by 19 publications

(11 citation statements)

References 108 publications

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“…Further investigation of fauna that interact with αNTX producing snakes is needed to determine whether αNTX resistance translates to whole venom resistance, and whether these substitutions are the result of present or past ecological interactions with venomous species. Our analyses, along with other recent work, suggest that snake and other animal venoms are a source of strong selection pressure likely facilitated via complex coevolutionary interactions that may be the rule rather than the exception, particularly for animals which share habitat with many venomous snakes [5,19,47].…”

Section: Discussionsupporting

confidence: 58%

Widespread convergent evolution of alpha-neurotoxin resistance in African mammals

Drabeck

Holt

McGaugh

2022

Preprint

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Convergent evolution is central to the study of adaptation and has been used to understand both the limits of evolution and the diverse patterns and processes which result in adaptive change. Resistance to snake venom α-neurotoxins (αNTXs) is a case of widespread convergence having evolved several times in snakes, lizards, and mammals. Despite extreme toxicity of αNTXs, substitutions in its target, the nicotinic acetylcholine receptor (nAChR), prevent αNTX binding and render species resistant. Recently, the published meerkat (Herpestidae) genome revealed that meerkats have the same substitutions in nAChR as the venom resistant Egyptian mongoose (Herpestidae), suggesting that venom-resistant nAChRs may be ancestral to Herpestids. Like the mongoose, many other species of feliform carnivores prey on venomous snakes, though their venom resistance has never been explored. To evaluate the prevalence and ancestry of αNTX resistance in mammals, we generate a dataset of mammalian nAChR utilizing museum specimens and public datasets. We find five instances of convergent evolution within feliform carnivores, and an additional eight instances across all mammals sampled. Tests of selection show that these substitutions are evolving under positive selection. Repeated convergence suggests that this adaptation played an important role in the evolution of mammalian physiology and potentially venom evolution.

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Section: Discussionsupporting

confidence: 58%

Widespread convergent evolution of alpha-neurotoxin resistance in African mammals

Drabeck

Holt

McGaugh

2022

Preprint

View full text Add to dashboard Cite

show abstract

Section: (D) Conclusionsupporting

confidence: 56%

Widespread convergent evolution of alpha-neurotoxin resistance in African mammals

2022

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Convergent evolution is central to the study of adaptation and has been used to understand both the limits of evolution and the diverse patterns and processes which result in adaptive change. Resistance to snake venom alpha-neurotoxins ( α NTXs) is a case of widespread convergence having evolved several times in snakes, lizards and mammals. Despite extreme toxicity of α NTXs, substitutions in its target, the nicotinic acetylcholine receptor (nAChR), prevent α NTX binding and render species resistant. Recently, the published meerkat (Herpestidae) genome revealed that meerkats have the same substitutions in nAChR as the venom-resistant Egyptian mongoose (Herpestidae), suggesting that venom-resistant nAChRs may be ancestral to Herpestids. Like the mongoose, many other species of feliform carnivores prey on venomous snakes, though their venom resistance has never been explored. To evaluate the prevalence and ancestry of α NTX resistance in mammals, we generate a dataset of mammalian nAChR using museum specimens and public datasets. We find five instances of convergent evolution within feliform carnivores, and an additional eight instances across all mammals sampled. Tests of selection show that these substitutions are evolving under positive selection. Repeated convergence suggests that this adaptation played an important role in the evolution of mammalian physiology and potentially venom evolution.

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“…For example, in FL, some individuals have lost Nv1 completely, whereas others maintain two diploid copies. The role of balancing selection in venom evolution has been proposed in recent studies focusing on snakes, in which the maintenance of genetic diversity better explains the evolution of multiple venom gene families than directional positive selection ( 35 , 36 ). We hypothesize that balancing selection may indeed be the major force driving the observed variation in Nv1 copy number.…”

Section: Discussionmentioning

confidence: 99%

Venom trade-off shapes interspecific interactions, physiology, and reproduction

Surm,

Birch,

Macrander

et al. 2024

Sci. Adv.

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The ability of an animal to effectively capture prey and defend against predators is pivotal for survival. Venom is often a mixture of many components including toxin proteins that shape predator-prey interactions. Here, we used the sea anemone Nematostella vectensis to test the impact of toxin genotypes on predator-prey interactions. We developed a genetic manipulation technique to demonstrate that both transgenically deficient and a native Nematostella strain lacking a major neurotoxin (Nv1) have a reduced ability to defend themselves against grass shrimp, a native predator. In addition, secreted Nv1 can act indirectly in defense by attracting mummichog fish, which prey on grass shrimp. Here, we provide evidence at the molecular level of an animal-specific tritrophic interaction between a prey, its antagonist, and a predator. Last, this study reveals an evolutionary trade-off, as the reduction of Nv1 levels allows for faster growth and increased reproductive rates.

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The roles of balancing selection and recombination in the evolution of rattlesnake venom

Cited by 19 publications

References 108 publications

Widespread convergent evolution of alpha-neurotoxin resistance in African mammals

Widespread convergent evolution of alpha-neurotoxin resistance in African mammals

Widespread convergent evolution of alpha-neurotoxin resistance in African mammals

Venom trade-off shapes interspecific interactions, physiology, and reproduction

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