Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction.
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.
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ABSTRACT: Members of a gene family expressed in a single species often experience common selection pressures. Consequently, the molecular basis of complex adaptations may be expected to involve parallel evolutionary changes in multiple paralogs. Here, we use BAC library scans to investigate the evolution of the voltage-gated sodium channel (Nav) family in the garter snake Thamnophis sirtalis, a predator of highly toxic Taricha newts. Newts possess tetrodotoxin (TTX), which blocks voltage-gated sodium channels, arresting action potentials in nerves and muscle. Some Thamnophis populations have evolved resistance to extremely high levels of TTX. Previous work has identified amino acid sites in the skeletal muscle sodium channel Nav1.4 that confer resistance to TTX and vary across populations. We identify parallel evolution of TTX resistance in two additional Nav paralogs, Nav1.6 and 1.7, which are known to be expressed in the peripheral nervous system and should thus be exposed to ingested TTX. Each paralog contains at least one TTX-resistant substitution identical to a substitution previously identified in Nav1.4. These sites are fixed across populations, suggesting that the resistant peripheral nerves antedate resistant muscle. In contrast, three sodium channels expressed solely in the central nervous system (Nav1.1-1.3) showed no evidence of TTX resistance, consistent with protection from toxins by the blood-brain barrier. We also report the exon-intron structure of six Nav paralogs, the first such analysis for snake genes. Our results demonstrate that the molecular basis of adaptation may be both repeatable across members of a gene family and predictable based on functional considerations.Molecular Biology and Evolution 08/2014; 31(11). DOI:10.1093/molbev/msu237 · 14.31 Impact Factor
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ABSTRACT: Consumption of nassariid gastropods often leads to poisoning incidents in some coastal provinces in China. To elucidate the pattern of toxicity dynamics and origin of toxins, samples of gastropod Nassarius spp. were collected from late May to early August 2007 from Lianyungang, Jiangsu province, where the poisoning incidents have been frequently reported. Toxicity was first screened with the mouse bioassay method, and tetrodotoxin and its analogues (TTXs) were analysed with high-performance liquid chromatography coupled with an ion-trap mass spectrometer (HPLC-MS(n)). The toxicity of nassariid N. semiplicatus showed an 'M'-shaped pattern of fluctuation during the sampling season. Two peaks of toxicity appeared in late May and late July. The maximum toxicity was recorded on 24 May, with the value of 846 mouse unit (MU) g(-1) of tissue (wet weight). TTX and its analogues trideoxyTTX, 4-epiTTX, anhydroTTX and oxoTTX were detected in the nassariid samples. TrideoxyTTX but not TTX was the major toxin in all the samples. No paralytic shellfish poison (PSP) was detected in the sample with the maximum toxicity by HPLC-FLD analysis. Variation of TTX content in the tissue of nassariid gastropods correlates well with the dynamics of toxicity. It is suggested that TTXs are the major toxins corresponding to the toxicity of the nassariids, and May and July are the high-risk seasons for consumption of nassariids, which is critical for the management of poisoning incidents.Food Additives and Contaminants - Part A Chemistry, Analysis, Control, Exposure and Risk Assessment 01/2012; 29(1):117-27. DOI:10.1080/19440049.2011.615069 · 2.34 Impact Factor
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ABSTRACT: Lethal chemical defenses in prey species can have profound effects on interactions with predators. The presence of lethal defenses in prey can correct the selective imbalance suggested by the life-dinner principle in which the fitness consequences of an encounter between predator and prey should be much greater for the prey species than the predator. Despite the apparent adaptive advantages of lethality the evolution of deadly prey presents a fundamental dilemma. How might lethal defenses confer an individual fitness advantage if both predators and prey die during interactions? We examined the interaction between the rough-skinned newt (Taricha granulosa), which contains a powerful neurotoxin called tetrodotoxin (TTX), and the common garter snake (Thamnophis sirtalis). In some sympatric populations, Th. sirtalis have evolved physiological resistance to TTX. Whether the newts’ toxin confers protection from snake predators or has been disarmed by the snakes’ physiological resistance has not yet been directly tested. In predator–prey trials, newts that were rejected by snakes had greater concentrations of TTX in their skin (4.52±3.49mgTTX/g skin) than those that were eaten (1.72±1.53mgTTX/g skin). Despite the plethora of taxa that appear to use TTX defensively, this is the first direct and quantitative demonstration of the antipredator efficacy of TTX. Because the survival probability of a newt (and thus fitness) is affected by individual TTX concentration, selection can drive the escalation of toxin levels in newts. The variable fitness consequences associated with both TTX levels of newts and resistance to TTX in snakes that may promote a strong and symmetrical coevolutionary relationship have now been demonstrated. Keywords Thamnophis sirtalis - Taricha granulosa -Coevolution-Predator–prey-Tetrodotoxin-Antipredator-DefenseChemoecology 12/2010; 20(4):285-290. DOI:10.1007/s00049-010-0057-z · 1.96 Impact Factor