Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts

Williams, Becky L.; Hanifin, Charles T.; Brodie, Edmund D.

doi:10.1007/s00049-011-0093-3

Cited by 17 publications

(9 citation statements)

References 53 publications

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“…That these additional replacements do not occur in P. aurotaenia is not surprising because P. terribilis is known to be much more toxic, and resistance tends to increase with toxicity (Feldman et al 2009;Petschenka, Fandrich, et al 2013). Such stepwise increases in resistance and toxicity have also been observed in newts and their garter-snake predators (Geffeney et al 2005;Williams et al 2012;Hanifin and Gilly 2015) and across many insect herbivores and their hosts (Despr es et al 2007;Aardema et al 2012). A more complete sampling of species in the Phyllobates clade may reveal genotypes with intermediate resistance.…”

Section: Species-level Aa Replacement Patterns and Their Relationshipmentioning

confidence: 99%

Convergent Substitutions in a Sodium Channel Suggest Multiple Origins of Toxin Resistance in Poison Frogs

Tarvin

Santos

O’Connell

et al. 2016

Molecular Biology and Evolution

108

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Complex phenotypes typically have a correspondingly multifaceted genetic component. However, the genotype-phenotype association between chemical defense and resistance is often simple: genetic changes in the binding site of a toxin alter how it affects its target. Some toxic organisms, such as poison frogs (Anura: Dendrobatidae), have defensive alkaloids that disrupt the function of ion channels, proteins that are crucial for nerve and muscle activity. Using protein-docking models, we predict that three major classes of poison frog alkaloids (histrionicotoxins, pumiliotoxins, and batrachotoxins) bind to similar sites in the highly conserved inner pore of the muscle voltage-gated sodium channel, Nav1.4. We predict that poison frogs are somewhat resistant to these compounds because they have six types of amino acid replacements in the Nav1.4 inner pore that are absent in all other frogs except for a distantly related alkaloid-defended frog from Madagascar, Mantella aurantiaca. Protein-docking models and comparative phylogenetics support the role of these replacements in alkaloid resistance. Taking into account the four independent origins of chemical defense in Dendrobatidae, phylogenetic patterns of the amino acid replacements suggest that 1) alkaloid resistance in Nav1.4 evolved independently at least seven times in these frogs, 2) variation in resistance-conferring replacements is likely a result of differences in alkaloid exposure across species, and 3) functional constraint shapes the evolution of the Nav1.4 inner pore. Our study is the first to demonstrate the genetic basis of autoresistance in frogs with alkaloid defenses.

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Section: Species-level Aa Replacement Patterns and Their Relationshipmentioning

confidence: 99%

Convergent Substitutions in a Sodium Channel Suggest Multiple Origins of Toxin Resistance in Poison Frogs

Tarvin

Santos

O’Connell

et al. 2016

Molecular Biology and Evolution

108

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“…First, the molecular structure of INDOX is very different from TTX (McCann et al, 2001;Narahashi, 2001) and thus the snake's body likely processes the toxin in a different manner. Unfortunately, there is limited reptilian toxicokinetic data for TTX (Williams et al, 2012) and none for INDOX to either substantiate or refute this possibility. Second, the evolutionary history that snakes share with TTX exposure (through eating T. granulosa) may reduce responses to TTX exposure.…”

Section: Discussionmentioning

confidence: 99%

Comparing the Natural and Anthropogenic Sodium Channel Blockers Tetrodotoxin and Indoxacarb in Garter Snakes

et al. 2016

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Synthetic chemicals, such as pesticides, are used in a variety of ways in the agricultural industry. Anthropogenic chemicals pose a unique challenge to organisms because of the lack of evolutionary history between the chemical and the organism. However, research has shown that some organisms have a resistance to these synthetic chemicals due to their evolved resistance to a natural compound with a similar structure or mode of action. Indoxacarb (INDOX) is a relatively new pesticide with a similar mode of action to that of tetrodotoxin (TTX). Tetrodotoxin is a naturally occurring toxin that is used as an antipredator defense in the rough-skinned newt (Taricha granulosa). Some populations of the common garter snake (Thamnophis sirtalis) have developed a resistance to tetrodotoxin. Here, we investigated the correlation between TTX and INDOX resistance in snakes. We hypothesized that INDOX would induce a much higher stress response than the naturally occurring TTX. We injected each snake with tetrodotoxin (1 mass-adjusted mouse unit). We did the same with mass-adjusted units of INDOX. We measured corticosterone, testosterone, and bactericidal ability. Our results show an acute stress response to INDOX, but not TTX through an elevate corticosterone and innate immune response, although there was no difference in testosterone concentration. These results suggest that, although INDOX may have a similar mechanism of action, garter snakes do not react in a similar manner as to TTX. This research gives a physiological perspective on the differences between naturally occurring compounds and synthetic compounds.

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“…Thamnophis garter snakes, in contrast, have evolved a resistance to TTX, which allows them to consume newts (Feldman et al 2012) and accumulate the poison in their own tissues as a prédation defense (Williams et al 2012). Thus, trophic transmission of TTX either by newts or resistant snakes can result in top-predator mortality with cascading effects throughout terrestrial and freshwater food webs (Borer et al 2006).…”

Section: The Broken Arrows Indicate Deterrent or Inhibitory Effects Omentioning

confidence: 99%

Molecules of Keystone Significance

Ferrer

Zimmer

2013

BioScience

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The keystone species concept provides a valuable framework for integrating findings across traditional disciplines that scale from the cellular level (chemical defense and chemosensory reception) and the organismal level (behavioral traits) to the community level (species interactions). Select bioactive compounds cause disproportionately large effects by connecting such seemingly disparate processes as microbial loop dynamics and apex prédation. Outstanding examples of these "molecules of keystone significance" draw on four distinct compounds: dimethylsulfoniopropionate, saxitoxin, tetrodotoxin, and pyrrolizidine alkaloids. Through convergent evolution, they inform phylogenetically diverse species; initiate major trophic cascades; and structure respective communities within terrestrial, freshwater, coastal-ocean, and open-ocean environments. Their relevance to conservation biology involves the protection of threatened species or habitats in the face of natural-and human-induced disturbances.

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Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts

Cited by 17 publications

References 53 publications

Convergent Substitutions in a Sodium Channel Suggest Multiple Origins of Toxin Resistance in Poison Frogs

Convergent Substitutions in a Sodium Channel Suggest Multiple Origins of Toxin Resistance in Poison Frogs

Comparing the Natural and Anthropogenic Sodium Channel Blockers Tetrodotoxin and Indoxacarb in Garter Snakes

Molecules of Keystone Significance

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