Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction

ArticleinNature 434(7034):759-63 · May 2005with22 Reads
DOI: 10.1038/nature03444 · Source: PubMed
Abstract
Understanding the molecular genetic basis of adaptations provides incomparable insight into the genetic mechanisms by which evolutionary diversification takes place. Whether the evolution of common traits in different lineages proceeds by similar or unique mutations, and the degree to which phenotypic evolution is controlled by changes in gene regulation as opposed to gene function, are fundamental questions in evolutionary biology that require such an understanding of genetic mechanisms. Here we identify novel changes in the molecular structure of a sodium channel expressed in snake skeletal muscle, tsNa(V)1.4, that are responsible for differences in tetrodotoxin (TTX) resistance among garter snake populations coevolving with toxic newts. By the functional expression of tsNa(V)1.4, we show how differences in the amino-acid sequence of the channel affect TTX binding and impart different levels of resistance in four snake populations. These results indicate that the evolution of a physiological trait has occurred through a series of unique functional changes in a gene that is otherwise highly conserved among vertebrates.
    • "Taricha granulosa and other congeners possess tetrodotoxin (TTX), a lethal neurotoxin that deters most predators. However, multiple species of garter snake, including Th. sirtalis, independently evolved resistance to the toxin (Geffeney et al. 2002Geffeney et al. , 2005 Feldman et al. 2009 ). Geographic patterns of phenotypic exaggeration in newt toxicity and snake TTX resistance are closely correlated across the co-occurring range of the species in western North America, implying the existence of strong reciprocal selection (Hanifin et al. 2008). "
    [Show abstract] [Hide abstract] ABSTRACT: Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from one location to the next. Under this framework, allopatric populations should lack variation in coevolutionary traits due to the absence of reciprocal selection. We examine phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough-Skinned Newt (Taricha granulosa) in regions of allopatry with its TTX-resistant predator, the Common Garter Snake (Thamnophis sirtalis). In sympatry, geographic patterns of phenotypic exaggeration in toxicity and toxin-resistance are closely correlated in prey and predator, implying that reciprocal selection drives phenotypic variation in coevolutionary traits. Therefore, in allopatry with TTX-resistant predators, we expect to find uniformly low levels of newt toxicity. We characterized TTX toxicity in northwestern North America, including the Alaskan panhandle where Ta. granulosa occur in allopatry with Th. sirtalis. First, we used microsatellite markers to estimate population genetic structure and determine if any phenotypic variation in toxicity might be explained by historical divergence. We found northern populations of Ta. granulosa generally lacked population structure in a pattern consistent with northern range expansion after the Pleistocene. Next, we chose a cluster of sites in Alaska, which uniformly lacked genetic divergence, to test for phenotypic divergence in toxicity. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among- and within-population variation in toxicity. Most notably, a small number of individuals contained large doses of TTX that rival means of toxic populations in sympatry with Th. sirtalis. Phenotypic variation in toxicity, despite limited neutral genetic divergence, suggests that factors other than reciprocal selection with Th. sirtalis likely contribute to geographic patterns of toxicity in Ta. granulosa.
    Full-text · Article · Mar 2016
    • "are also venomous (see Weinstein et al., 2011). In addition, some North American garter snakes (Thamnophis spp., Natricidae) found in the Pacific Northwest have evolved a voltage-gated sodium channel with point mutations (Na V 1.4) that confers resistance to the potent sodium channel antagonist, tetrodotoxin (Geffeney et al., 2005). Thus, these could be considered potentially poisonous on ingestion as they might be accumulating toxin in their visceral organs such as occurs in other tetrodotoxin-resistant animals (e.g. "
    [Show abstract] [Hide abstract] ABSTRACT: The ancient perceptions of "venomous" and "poisonous snakes", as well as the Indo-European (IE) etymological origins of the term "venom" specifically associated with snakes are considered. Although several ancient cultures perceived snakes as symbols of fecundity and renewal, concurrent beliefs also associated venomous snakes with undesirable human characteristics or as portending non-propitious events. The respective IE roots of the terms "venom" and "poison", "wen" and "poi" refer to desire or the act of ingesting liquids. The origin of the term, "venom", is associated with polytheistic cults that emphasized attainment of desires sometimes assisted by "love potions", a term later interpolated with the word, "poison". Specific interpretation of the term, venom, has varied since its first probable use in the mid-Thirteenth Century. The definition of snake venom has long been contended, and interpretations have often reflected emphasis on the pharmacological or experimental toxicity of medically relevant snake venoms with less regard for the basic biological bases of these venoms, as well as those from snakes with no known medical significance. Several definitions of "snake venom" and their defining criteria are reviewed, and critical consideration is given to traditional criteria that might facilitate the future establishment of a biologically accurate definition. Copyright © 2015. Published by Elsevier Ltd.
    Full-text · Article · Jul 2015
    • "are also venomous (see Weinstein et al., 2011). In addition, some North American garter snakes (Thamnophis spp., Natricidae) found in the Pacific Northwest have evolved a voltage-gated sodium channel with point mutations (Na V 1.4) that confers resistance to the potent sodium channel antagonist, tetrodotoxin (Geffeney et al., 2005). Thus, these could be considered potentially poisonous on ingestion as they might be accumulating toxin in their visceral organs such as occurs in other tetrodotoxin-resistant animals (e.g. "
    Full-text · Article · Jul 2015 · Toxicon
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