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Edmund D. Brodie - One of the best experts on this subject based on the ideXlab platform.
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convergent adaptation to dangerous prey proceeds through the same first step mutation in the Garter Snake thamnophis sirtalis
Evolution, 2017Co-Authors: Michael T. J. Hague, Chris R. Feldman, Edmund D. BrodieAbstract:Convergent phenotypes often result from similar underlying genetics, but recent work suggests convergence may also occur in the historical order of substitutions en route to an adaptive outcome. We characterized convergence in the mutational steps to two independent outcomes of tetrodotoxin (TTX) resistance in separate geographic lineages of the common Garter Snake (Thamnophis sirtalis) that coevolved with toxic newts. Resistance is largely conferred by amino acid changes in the skeletal muscle sodium channel (NaV1.4) that interfere with TTX-binding. We sampled variation in NaV1.4 throughout western North America and found clear evidence that TTX-resistant changes in both lineages began with the same isoleucine-valine mutation (I1561V) within the outer pore of NaV1.4. Other point mutations in the pore, shown to confer much greater resistance, accumulate later in the evolutionary progression and always occur together with the initial I1561V change. A gene tree of NaV1.4 suggests the I1561V mutations in each lineage are not identical-by-decent, but rather they arose independently. Convergence in the evolution of channel resistance is likely the result of shared biases in the two lineages of Th. sirtalis – only a few mutational routes can confer TTX resistance while maintaining the conserved function of voltage-gated sodium channels. This article is protected by copyright. All rights reserved
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Convergent adaptation to dangerous prey proceeds through the same first‐step mutation in the Garter Snake Thamnophis sirtalis
Evolution; international journal of organic evolution, 2017Co-Authors: Michael T. J. Hague, Chris R. Feldman, Edmund D. BrodieAbstract:Convergent phenotypes often result from similar underlying genetics, but recent work suggests convergence may also occur in the historical order of substitutions en route to an adaptive outcome. We characterized convergence in the mutational steps to two independent outcomes of tetrodotoxin (TTX) resistance in separate geographic lineages of the common Garter Snake (Thamnophis sirtalis) that coevolved with toxic newts. Resistance is largely conferred by amino acid changes in the skeletal muscle sodium channel (NaV1.4) that interfere with TTX-binding. We sampled variation in NaV1.4 throughout western North America and found clear evidence that TTX-resistant changes in both lineages began with the same isoleucine-valine mutation (I1561V) within the outer pore of NaV1.4. Other point mutations in the pore, shown to confer much greater resistance, accumulate later in the evolutionary progression and always occur together with the initial I1561V change. A gene tree of NaV1.4 suggests the I1561V mutations in each lineage are not identical-by-decent, but rather they arose independently. Convergence in the evolution of channel resistance is likely the result of shared biases in the two lineages of Th. sirtalis – only a few mutational routes can confer TTX resistance while maintaining the conserved function of voltage-gated sodium channels. This article is protected by copyright. All rights reserved
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A rticle Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake
2016Co-Authors: Thamnophis Sirtalis, Edmund D. Brodie, Scott V. Edwards, Michael E. Pfrender, Joel W. Mcglothlin, Chris R. Feldman, John P. Chuckalovcak, Daniel E. JanesAbstract: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 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 substi-tution 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 th
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A proposal to sequence the genome of a Garter Snake (Thamnophis sirtalis)
Standards in genomic sciences, 2011Co-Authors: Todd A. Castoe, Anne M. Bronikowski, Edmund D. Brodie, Scott V. Edwards, Michael E. Pfrender, Michael D. Shapiro, David D. Pollock, Wesley C. WarrenAbstract:Here we develop an argument in support of sequencing a Garter Snake (Thamnophis sirtalis) genome, and outline a plan to accomplish this. This Snake is a common, widespread, nonvenomous North American species that has served as a model for diverse studies in evolutionary biology, physiology, genomics, behavior and coevolution. The anole lizard is currently the only genome sequence available for a non-avian reptile. Thus, the Garter Snake at this time would be the first available Snake genome sequence and as such would provide much needed comparative representation of non-avian reptilian genomes, and would also allow critical new insights for vertebrate comparative genomic studies. We outline the major areas of discovery that the availability of the Garter Snake genome would enable, and describe a plan for whole-genome sequencing.
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Genetic architecture of a feeding adaptation: Garter Snake (Thamnophis) resistance to tetrodotoxin bearing prey
Proceedings. Biological sciences, 2010Co-Authors: Chris R. Feldman, Edmund D. Brodie, Michael E. PfrenderAbstract:Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in Garter Snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Nav1.4) in three Garter Snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Nav1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Nav1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Nav1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Nav1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Nav1.4 is a major effect locus. The simple genetic architecture of TTX resistance in Garter Snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some Garter Snake populations may have led to the evolution of extreme phenotypes and an ‘escape’ from the arms race with newts.
Anne M. Bronikowski - One of the best experts on this subject based on the ideXlab platform.
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Merging the "Morphology-Performance-Fitness" Paradigm and Life-History Theory in the Eagle Lake Garter Snake Research Project.
Integrative and Comparative Biology, 2017Co-Authors: Elizabeth A. Addis, Eric J Gangloff, Maria G Palacios, Katherine E. Carr, Anne M. BronikowskiAbstract:The morphology-performance-fitness paradigm for testing selection on morphological traits has seen decades of successful application. At the same time, life-history approaches using matrix methods and perturbation studies have also allowed the direct estimate of selection acting on vital rates and the traits that comprise them. Both methodologies have been successfully applied to the Garter Snakes of the long-term Eagle Lake research project to reveal selection on morphology, such as color pattern, number of vertebrae, and gape size; and life-history traits such as birth size, growth rates, and juvenile survival. Here we conduct a reciprocal transplant study in a common laboratory environment to study selection on morphology and life-history. To place our results in the ecomorphology paradigm, we measure performance outcomes (feeding rates, growth, insulin-like growth factor 1 titers) of morphological variation (body size, condition) and their fitness consequences for juvenile survival-a trait that has large fitness sensitivities in these Garter Snake populations, and therefore is thought to be subject to strong selection. To better merge these two complementary theories, we end by discussing our findings in a nexus of morphology-performance-fitness-life history to highlight what these approaches, when combined, can reveal about selection in the wild.
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vertical transmission of hepatozoon in the Garter Snake thamnophis elegans
Journal of Wildlife Diseases, 2017Co-Authors: Kiera L Kauffman, Anne M. Bronikowski, Amanda M Sparkman, Maria G PalaciosAbstract:Abstract Vertical transmission of blood parasites has been demonstrated in humans and some domestic species, but it has not been well documented in wild populations. We assessed whether Hepatozoon blood parasites are vertically transmitted in naturally infected individuals of the viviparous western terrestrial Garter Snake (Thamnophis elegans). Blood smears were taken from nine wild-caught gravid female Snakes at capture, preparturition, and postparturition, and then from their laboratory-born offspring at age 2 mo and 1 yr. All infected offspring were born to four infected females, although not all offspring in a given litter were necessarily infected. Parasites were not detected in offspring born to the five uninfected mothers. The highest parasite loads were found in neonates at 2 mo of age. Parasite prevalence did not vary between sexes in offspring, but females showed higher loads than did males when 2 mo old. This study supports vertical transmission of Hepatozoon in naturally infected viviparous sn...
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hormonal and metabolic responses to upper temperature extremes in divergent life history ecotypes of a Garter Snake
The Journal of Experimental Biology, 2016Co-Authors: Eric J Gangloff, Kaitlyn G Holden, Rory S Telemeco, L H Baumgard, Anne M. BronikowskiAbstract:Extreme temperatures constrain organismal physiology and impose both acute and chronic effects. Additionally, temperature-induced hormone-mediated stress response pathways and energetic trade-offs are important drivers of life-history variation. This study employs an integrative approach to quantify acute physiological responses to high temperatures in divergent life-history ecotypes of the western terrestrial Garter Snake ( Thamnophis elegans ). Using wild-caught animals, we measured oxygen consumption rate and physiological markers of hormonal stress response, energy availability, and anaerobic respiration in blood plasma across five ecologically relevant temperatures (24, 28, 32, 35, and 38° C; 3-hour exposure). Corticosterone, insulin, and glucose concentrations all increased with temperature, but with different thermal response curves, suggesting that high temperatures differently affect energy-regulation pathways. Additionally, oxygen consumption rate increased without plateau and lactate concentration did not increase with temperature, challenging the recent hypothesis that oxygen limitation sets upper thermal tolerance limits. Finally, animals had similar physiological thermal responses to high-temperature exposure regardless of genetic background, suggesting that local adaptation has not resulted in fixed differences between ecotypes. Together, these results identify some of the mechanisms by which higher temperatures alter hormonal-mediated energy balance in reptiles and potential limits to the flexibility of this response.
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Appendix C. Annual estimates of vital rates for each population of Garter Snake.
2016Co-Authors: David A. Miller, Stevan J. Arnold, William R. Clark, Anne M. BronikowskiAbstract:Annual estimates of vital rates for each population of Garter Snake
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gene expression of components of the insulin insulin like signaling pathway in response to heat stress in the Garter Snake thamnophis elegans
The Journal of the Iowa Academy of Science: JIAS, 2014Co-Authors: Tonia S Schwartz, Anne M. BronikowskiAbstract:The insulin/insulin-like signaling (IIS) pathway is an evolutionary conserved molecular signaling pathway that regulates growth, reproduction, stress resistance, and longevity in response to nutrition and external stress. While the constituents of this pathway and their functions are relatively well understood in laboratory model animals, they have not been explored in many other organisms, with notable exceptions in the fisheries literature. We tested for the gene expression of four key components of this pathway in the Garter Snake (Thamnophis elegans) liver, and determine how the transcription of these components responds to heat stress. We found that the two insulin-like growth factor ligands (IGF-1 and IGF-2) and the receptors (IGF-1 Receptor and M6P/IGF-2 Receptor, or IGF-1R and IGF-2R) are expressed in Garter Snake liver tissue. Under normal laboratory conditions, IGF-2 and IGF-2R are expressed at a higher level than IGF-1 and IGF-1R. In response to heat stress, IGF-1 expression remained the same, ...
Stevan J. Arnold - One of the best experts on this subject based on the ideXlab platform.
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Appendix C. Annual estimates of vital rates for each population of Garter Snake.
2016Co-Authors: David A. Miller, Stevan J. Arnold, William R. Clark, Anne M. BronikowskiAbstract:Annual estimates of vital rates for each population of Garter Snake
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avian predation and the evolution of life histories in the Garter Snake thamnophis elegans
American Midland Naturalist, 2013Co-Authors: Amanda M Sparkman, A M Bronikowski, J G Billings, D Von Borstel, Stevan J. ArnoldAbstract:Predation pressure has often been postulated as a major selective force for the evolution of life histories, with high predation (particularly on small sizes) resulting in a fast- living strategy characterized by fast growth, early maturation, and short lifespan. However, due to the difficulty of assessing actual predation pressure in the wild, evidence for a role of predation in life-history evolution is rare. We examined the relationship between avian predation and life-history strategy in replicate populations of fast and slow-living Garter Snake ecotypes. To assess avian predation, we first compiled a list of known and suspected predators based on direct observations of predation events recorded in our long term detailed field notes from 1978 - present. Furthermore, we added to this list with published records of Snake predation involving avian species known to occur in our study site, and a novel method of inferring predator identity via analysis of bill marks on live Snakes. Using this list of candidate predators, we conducted surveys quantifying predator incidence in replicate habitats of both ecotypes. We found that known and suspected predators are more abundant in habitats of the fast-living ecotype than in those of the slow-living ecotype. We also show a higher incidence of bill marks on slow-living Snakes, which may indicate an increased effectiveness at escaping predation attempts. In general, we provide evidence to suggest that predation pressure may indeed have been an important selective force in the evolution of fast growth and early maturation in the fast-living ecotype and may continue to constitute an important source of extrinsic mortality leading to differences in lifespan between the two ecotypes.
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adaptive divergence within and between ecotypes of the terrestrial Garter Snake thamnophis elegans assessed with fst qst comparisons
Journal of Evolutionary Biology, 2007Co-Authors: Mollie K Manier, C M Seyler, Stevan J. ArnoldAbstract:Populations of the terrestrial Garter Snake (Thamnophis elegans) around Eagle Lake in California exhibit dramatic ecotypic differentiation in life history, colouration and morphology across distances as small as a few kilometres. We assayed the role of selection in ecotypic differentiation in T. elegans using FSTQST analysis and identified selective agents using direct and indirect observations. We extended the conventional implementation of the FST-QST approach by using three-level analyses of genetic and phenotypic variance to assess the role of selection in differentiating populations both within and between ecotypes. These results suggest that selection has driven differentiation between as well as within ecotypes, and in the presence of moderate to high gene flow. Our findings are discussed in the context of previous correlational selection analyses which revealed stabilizing and correlational selection for some of the traits examined.
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an empirical test of evolutionary theories for reproductive senescence and reproductive effort in the Garter Snake thamnophis elegans
Proceedings of The Royal Society B: Biological Sciences, 2007Co-Authors: Amanda M Sparkman, Stevan J. Arnold, Anne M. BronikowskiAbstract:Evolutionary theory predicts that differential reproductive effort and rate of reproductive senescence will evolve under different rates of external mortality. We examine the evolutionary divergence of age-specific reproduction in two life-history ecotypes of the western terrestrial Garter Snake, Thamnophis elegans. We test for the signature of reproductive senescence (decreasing fecundity with age) and increasing reproductive effort with age (increasing reproductive productivity per gram female) in replicate populations of two life-history ecotypes: Snakes that grow fast, mature young and have shorter lifespans, and Snakes that grow slow, mature late and have long lives. The difference between life-history ecotypes is due to genetic divergence in growth rate. We find (i) reproductive success (live litter mass) increases with age in both ecotypes, but does so more rapidly in the fast-growth ecotype, (ii) reproductive failure increases with age in both ecotypes, but the proportion of reproductive failure to total reproductive output remains invariant, and (iii) reproductive effort remains constant in fast-growth individuals with age, but declines in slow-growth individuals. This illustration of increasing fecundity with age, even at the latest ages, deviates from standard expectations for reproductive senescence, as does the lack of increases in reproductive effort. We discuss our findings in light of recent theories regarding the phenomenon of increased reproduction throughout life in organisms with indeterminate growth and its potential to offset theoretical expectations for the ubiquity of senescence.
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population genetic analysis identifies source sink dynamics for two sympatric Garter Snake species thamnophis elegans and thamnophis sirtalis
Molecular Ecology, 2005Co-Authors: Mollie K Manier, Stevan J. ArnoldAbstract:Population genetic structure can be shaped by multiple ecological and evolutionary factors, but the genetic consequences of these factors for multiple species inhabiting the same environment remain unexplored. We used microsatellite markers to examine the population structures of two coexisting species of Garter Snake, Thamnophis elegans and Thamnophis sirtalis , to determine if shared landscape and biology imposed similar population genetic structures. These Snakes inhabit a series of ponds, lakes and flooded meadows in northern California and tend to converge on prey type wherever they coexist. Both Garter Snakes had comparable effective population sizes and bidirectional migration rates (estimated using a maximum-likelihood method based on the coalescent) with low but significant levels of genetic differentiation ( F ST = 0.024 for T . elegans and 0.035 for T . sirtalis ). Asymmetrical gene flow revealed large source populations for both species as well as potential sinks, suggesting frequent extinction–recolonization and metapopulation dynamics. In addition, we found a significant correlation between their genetic structures based on both pairwise F ST s for shared populations ( P = 0.009) and for bidirectional migration rates ( P = 0.024). Possible ecological and evolutionary factors influencing similarities and differences in genetic structure for the two species are discussed. Genetic measures of effective population size and migration rates obtained in this study are also compared with estimates obtained from mark–recapture data.
Robert T. Mason - One of the best experts on this subject based on the ideXlab platform.
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Seasonal anorexia in the male red-sided Garter Snake, Thamnophis sirtalis parietalis
Behavioral Ecology and Sociobiology, 2004Co-Authors: Ryan P. O’donnell, Richard Shine, Robert T. MasonAbstract:Many animals show seasonal shifts in behaviors that coincide with breeding, migration, or hibernation. These behavioral shifts provide ideal opportunities to study the regulation of behavior. The red-sided Garter Snake ( Thamnophis sirtalis parietalis ) spends 8 months of the year inactive in underground hibernacula, 1 month breeding, and 3 months feeding to build up enough energy stores to survive the following winter. Although they emerge from 8 months of hibernation with severely depleted energy reserves, they do not feed until weeks later, after the breeding season. We tested the hypothesis that this lack of feeding during the breeding season is due to a shift in behavior rather than the distribution of food and potential mates. Male Garter Snakes were given a series of choices between pursuing a breeding or feeding opportunity. The proportion of tests in which males selected feeding over breeding gradually increased throughout the study period, reaching almost 100% in the final tests. Males also were given opportunities to feed and court at the beginning and end of the study. Males initially refused food and courted females, but when retested at the end of the study they fed and did not court females. Thus aphagia during the breeding season is due at least in part to an endogenous shift in behavior.
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the influence of sex steroids on the sexual size dimorphism in the red spotted Garter Snake thamnophis sirtalis concinnus
General and Comparative Endocrinology, 2001Co-Authors: Darren T Lerner, Robert T. MasonAbstract:Abstract The red-spotted Garter Snake exhibits adult size dimorphism in which females are the larger sex. To understand which hormones may influence differential growth in this species, growth curves and hormone profiles of estradiol-17β (E 2 ) and testosterone (T) were constructed in male and female neonates. Growth was manipulated via implantation of exogenous hormones and hormone antagonists. Female neonates are heavier or longer beginning at either 20 or 24 weeks of age, respectively. Although low circulating levels of E 2 and T were present in males and females from birth through 15 weeks of age, these levels were not significantly different between the sexes. Differences in the growth curves of the treated and untreated Snakes were significant after 24 weeks of age. Antiestrogen produced male-like growth in females but had no effect on males. Antiandrogen had no effect on either males or females. Exogenous T reduced female growth to that observed in males, and E 2 reduced male growth. These results suggest that a basal level of either E 2 or T is sufficient in males to retain typical male growth patterns. Similar endogenous levels of E 2 appear to have growth-promoting effects in females. Endogenous T does not appear to play a role in female growth.
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behavioral and hormonal responses to corticosterone in the male red sided Garter Snake thamnophis sirtalis parietalis
Physiology & Behavior, 2001Co-Authors: Ignacio T Moore, Robert T. MasonAbstract:Stress and glucocorticoids are generally thought to suppress reproductive function at multiple levels. We tested the hypotheses that exogenous corticosterone would suppress sexual behavior in a dose-dependent manner, as well as drive a decrease in plasma testosterone levels in the male red-sided Garter Snake, Thamnophis sirtalis parietalis. We examined this by challenging individual males with intraperitoneal injections of exogenous corticosterone, and subsequently exposing them to sexually attractive females or taking a blood sample. Previous work has demonstrated a hormonal but no behavioral response to stress in this species. In this study, increasing concentrations of exogenous corticosterone rapidly suppressed mating behavior in a threshold manner. However, exogenous corticosterone had no effect on plasma levels of testosterone. Thus, these data suggest that the mechanism is in place for corticosterone to suppress mating behavior in this species and that these effects do not occur because of an indirect effect on plasma levels of testosterone but rather are the direct effect of the hormone itself. In addition, the negative relationship observed previously between plasma levels of corticosterone and testosterone in this species was probably not the direct result of corticosterone acting on the hypothalamic-pituitary-gonadal (HPG) axis. Rather, our results seem to indicate that the negative associations between the hypothalamic-pituitary-adrenal axis (HPA) and the HPG axis occur at other levels of these neuroendocrine pathways.
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environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two populations of the male Garter Snake thamnophis sirtalis
Journal of Experimental Zoology, 2001Co-Authors: Michael J Greene, Ignacio T Moore, Robert T. MasonAbstract:Stress and reproduction are generally thought to work in opposition to one another. This is often manifested as reciprocal relationships between glucocorticoid stress hormones and sex steroid hormones. However, seasonal differences in how animals respond to stressors have been described in extreme environments. We tested the hypothesis that Garter Snakes, Thamnophis sirtalis, with limited reproductive opportunities will suppress their hormonal stress response during the breeding season relative to conspecifics with an extended breeding season. The red-sided Garter Snake, T.s. parietalis, of Manitoba, Canada, has a brief breeding season during which males displayed no change in either plasma levels of testosterone or corticosterone, which were both elevated above basal levels, in response to capture stress. During the summer, capture stress resulted in increased plasma corticosterone and decreased testosterone. During the fall, when mating can also occur, males exhibited a significant decrease in testosterone but no increase in corticosterone in response to capture stress. The red-spotted Garter Snake, T.s. concinnus, of western Oregon, has an extended breeding season during which males displayed a stress response of increased plasma corticosterone and decreased testosterone levels. The corticosterone response to capture stress was similar during the spring, summer, and fall. In contrast, the testosterone response was suppressed during the summer and fall when gametogenesis was occurring. These data suggest that male Garter Snakes, in both populations, seasonally adapt their stress response but for different reasons and by potentially different mechanisms. J. Exp. Zool. 289:99-108, 2001.
Chris R. Feldman - One of the best experts on this subject based on the ideXlab platform.
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convergent adaptation to dangerous prey proceeds through the same first step mutation in the Garter Snake thamnophis sirtalis
Evolution, 2017Co-Authors: Michael T. J. Hague, Chris R. Feldman, Edmund D. BrodieAbstract:Convergent phenotypes often result from similar underlying genetics, but recent work suggests convergence may also occur in the historical order of substitutions en route to an adaptive outcome. We characterized convergence in the mutational steps to two independent outcomes of tetrodotoxin (TTX) resistance in separate geographic lineages of the common Garter Snake (Thamnophis sirtalis) that coevolved with toxic newts. Resistance is largely conferred by amino acid changes in the skeletal muscle sodium channel (NaV1.4) that interfere with TTX-binding. We sampled variation in NaV1.4 throughout western North America and found clear evidence that TTX-resistant changes in both lineages began with the same isoleucine-valine mutation (I1561V) within the outer pore of NaV1.4. Other point mutations in the pore, shown to confer much greater resistance, accumulate later in the evolutionary progression and always occur together with the initial I1561V change. A gene tree of NaV1.4 suggests the I1561V mutations in each lineage are not identical-by-decent, but rather they arose independently. Convergence in the evolution of channel resistance is likely the result of shared biases in the two lineages of Th. sirtalis – only a few mutational routes can confer TTX resistance while maintaining the conserved function of voltage-gated sodium channels. This article is protected by copyright. All rights reserved
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Convergent adaptation to dangerous prey proceeds through the same first‐step mutation in the Garter Snake Thamnophis sirtalis
Evolution; international journal of organic evolution, 2017Co-Authors: Michael T. J. Hague, Chris R. Feldman, Edmund D. BrodieAbstract:Convergent phenotypes often result from similar underlying genetics, but recent work suggests convergence may also occur in the historical order of substitutions en route to an adaptive outcome. We characterized convergence in the mutational steps to two independent outcomes of tetrodotoxin (TTX) resistance in separate geographic lineages of the common Garter Snake (Thamnophis sirtalis) that coevolved with toxic newts. Resistance is largely conferred by amino acid changes in the skeletal muscle sodium channel (NaV1.4) that interfere with TTX-binding. We sampled variation in NaV1.4 throughout western North America and found clear evidence that TTX-resistant changes in both lineages began with the same isoleucine-valine mutation (I1561V) within the outer pore of NaV1.4. Other point mutations in the pore, shown to confer much greater resistance, accumulate later in the evolutionary progression and always occur together with the initial I1561V change. A gene tree of NaV1.4 suggests the I1561V mutations in each lineage are not identical-by-decent, but rather they arose independently. Convergence in the evolution of channel resistance is likely the result of shared biases in the two lineages of Th. sirtalis – only a few mutational routes can confer TTX resistance while maintaining the conserved function of voltage-gated sodium channels. This article is protected by copyright. All rights reserved
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A rticle Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake
2016Co-Authors: Thamnophis Sirtalis, Edmund D. Brodie, Scott V. Edwards, Michael E. Pfrender, Joel W. Mcglothlin, Chris R. Feldman, John P. Chuckalovcak, Daniel E. JanesAbstract: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 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 substi-tution 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 th
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Genetic architecture of a feeding adaptation: Garter Snake (Thamnophis) resistance to tetrodotoxin bearing prey
Proceedings. Biological sciences, 2010Co-Authors: Chris R. Feldman, Edmund D. Brodie, Michael E. PfrenderAbstract:Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in Garter Snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Nav1.4) in three Garter Snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Nav1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Nav1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Nav1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Nav1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Nav1.4 is a major effect locus. The simple genetic architecture of TTX resistance in Garter Snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some Garter Snake populations may have led to the evolution of extreme phenotypes and an ‘escape’ from the arms race with newts.
