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Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalis

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dc.contributorVirginia Tech. Department of Biological Sciencesen
dc.contributorUniversity of Virginia. Department of Biologyen
dc.contributorBio-Rad Laboratoriesen
dc.contributorHarvard University. Department of Organismic and Evolutionary Biologyen
dc.contributorNational Institutes of Health. Division of Genetics and Developmental Biologyen
dc.contributorUniversity of Nevada, Reno. Department of Biologyen
dc.contributorUtah State University. Department of Biologyen
dc.contributorUniversity of Notre Dame. Department of Biological Sciences and Environmental Change Initiativeen
dc.contributorUniversity of Virginia. Mountain Lake Biological Stationen
dc.contributor.authorMcGlothlin, Joel W.en
dc.contributor.authorChuckalovcak, John P.en
dc.contributor.authorJanes, Daniel E.en
dc.contributor.authorEdwards, Scott V.en
dc.contributor.authorFeldman, Chris R.en
dc.contributor.authorBrodie, Edmund D.en
dc.contributor.authorPfrender, Michael E.en
dc.contributor.authorBrodie, Edmund D.en
dc.contributor.departmentBiological Sciencesen
dc.contributor.editorIrwin, Daviden
dc.date.accessed2016-02-12en
dc.date.accessioned2016-02-16T08:03:28Zen
dc.date.available2016-02-16T08:03:28Zen
dc.date.issued2014-08-18en
dc.description.abstractMembers 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 bacterial artificial chromosome 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 Nav’s, 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.en
dc.description.sponsorshipNational Science Foundationen
dc.description.sponsorshipDEB 0922216en
dc.description.sponsorshipDEB 1034686en
dc.description.sponsorshipVirginia Tech. Open Access Subvention Funden
dc.format.extent11 p.en
dc.format.mimetypeapplication/pdfen
dc.identifier.citationMcGlothlin, J. W., Chuckalovcak, J. P., Janes, D. E., Edwards, S. V., Feldman, C. R., Brodie, E. D., . . . Brodie, E. D. (2014). Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalis. Molecular Biology and Evolution, 31(11), 2836-2846. doi:10.1093/molbev/msu237en
dc.identifier.doihttps://doi.org/10.1093/molbev/msu237en
dc.identifier.issn0737-4038en
dc.identifier.issue11en
dc.identifier.urihttp://hdl.handle.net/10919/64818en
dc.identifier.urlhttp://mbe.oxfordjournals.org/content/31/11/2836.abstracten
dc.identifier.volume31en
dc.language.isoen_USen
dc.publisherOxford University Pressen
dc.rightsCreative Commons Attribution-NonCommercial 4.0 Internationalen
dc.rights.holderMcGlothlin, Joel W.en
dc.rights.holderChuckalovcak, John P.en
dc.rights.holderJanes, Daniel E.en
dc.rights.holderEdwards, Scott V.en
dc.rights.holderFeldman, Chris R.en
dc.rights.holderBrodie, Edmund D., Jr.en
dc.rights.holderPfrender, Michael E.en
dc.rights.holderBrodie, Edmund D., IIIen
dc.rights.urihttp://creativecommons.org/licenses/by-nc/4.0/en
dc.subjectAdaptationen
dc.subjectCoevolutionen
dc.subjectGene familiesen
dc.subjectMolecular evolutionen
dc.subjectPredator–prey interactionsen
dc.subjectToxinsen
dc.titleParallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalisen
dc.title.serialMolecular Biology and Evolutionen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten

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