The geographic mosaic in parallel: Matching patterns of newt tetrodotoxin levels and snake resistance in multiple predator–prey pairs

Reimche, Jessica S.; Brodie, Edmund D.; Stokes, Amber N.; Ely, Erica J.; Moniz, Haley A.; Thill, Vicki L.; Hallas, Joshua M.; Pfrender, Michael E.; Feldman, Chris R.

doi:10.1111/1365-2656.13212

Cited by 29 publications

(51 citation statements)

References 66 publications

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“…Local venom adaptation helps explain why, in all populations investigated to date, small mammals resistant to rattlesnake venom are still the primary prey of local snakes. This scenario is similar to the pattern documented in the newt‐garter snake system, wherein there are populations of garter snakes that are resistant enough to prey toxins to consume any sympatric newt (Hanifin et al., 2008; Reimche et al., 2020). This outcome is due in part to the molecular mechanism of resistance in snakes, where a few simple genetic changes to molecular targets of newt toxins can lead to dramatic increases in toxin resistance (Feldman et al., 2009, 2010; Geffeney et al., 2005).…”

Section: Discussionsupporting

confidence: 69%

“…The extensive geographic variation we found in venom chemistry and SVMP inhibition is a common pattern in co‐evolved systems, as expected from the Geographic Mosaic processes of trait remixing creating coevolutionary ‘hotspots’ and ‘coldspots’ (Benkman et al., 2001; Brodie & Brodie, 1990; Hanifin et al., 2008; Reimche et al., 2020; Thompson, 1999, 2005). Although multiple predators can lead to specialist strategies that diverge or alternate between populations in space or time (Edeline et al., 2008; Nuismer & Thompson, 2006; Soler, 2014), species subject to asymmetrical selection pressures are generally expected to evolve specialized defences against their primary threat (Benkman et al., 2001; Toor & Best, 2016).…”

Section: Discussionsupporting

confidence: 66%

“…Mussels differentially alter the ability of both crabs and sea stars to consume them (Freeman, 2007), and bacterial communities consumed by a number of protists evolve different defences depending on predator community composition (Friman et al., 2016). Even putatively dyadic systems with well‐characterized mechanisms of adaptation can be altered in the presence of third parties: the expression of tetrodotoxin in newts is well known to be under selection by garter snakes (Brodie et al., 2002; Reimche et al., 2020), but caddisfly predation on newt eggs may also present a selective pressure (Gall et al., 2012; Hague et al., 2016).…”

Section: Introductionmentioning

confidence: 99%

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Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey

Robinson

Holding

Whitford

et al. 2021

J of Evolutionary Biology

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Predator–prey interactions often lead to the coevolution of adaptations associated with avoiding predation and, for predators, overcoming those defences. Antagonistic coevolutionary relationships are often not simple interactions between a single predator and prey but rather a complex web of interactions between multiple coexisting species. Coevolution between venomous rattlesnakes and small mammals has led to physiological venom resistance in several mammalian taxa. In general, viperid venoms contain large quantities of snake venom metalloproteinase toxins (SVMPs), which are inactivated by SVMP inhibitors expressed in resistant mammals. We explored variation in venom chemistry, SVMP expression, and SVMP resistance across four co‐distributed species (California Ground Squirrels, Bryant's Woodrats, Southern Pacific Rattlesnakes, and Red Diamond Rattlesnakes) collected from four different populations in Southern California. Our aim was to understand phenotypic and functional variation in venom and venom resistance in order to compare coevolutionary dynamics of a system involving two sympatric predator–prey pairs to past studies that have focused on single pairs. Proteomic analysis of venoms indicated that these rattlesnakes express different phenotypes when in sympatry, with Red Diamonds expressing more typical viperid venom (with a diversity of SVMPs) and Southern Pacifics expressing a more atypical venom with a broader range of non‐enzymatic toxins. We also found that although blood sera from both mammals were generally able to inhibit SVMPs from both rattlesnake species, inhibition depended strongly on the snake population, with snakes from one geographic site expressing SVMPs to which few mammals were resistant. Additionally, we found that Red Diamond venom, rather than woodrat resistance, was locally adapted. Our findings highlight the complexity of coevolutionary relationships between multiple predators and prey that exhibit similar offensive and defensive strategies in sympatry.

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Section: Discussionsupporting

confidence: 69%

Section: Discussionsupporting

confidence: 66%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey

Robinson

Holding

Whitford

et al. 2021

J of Evolutionary Biology

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“…Taricha newts (Taricha torosa, T. granulosa, T. sierrae, and T. rivularis, herein collectively referred to as Taricha) have TTX present on their skin (Brodie et al, 1974;Reimche et al, 2020) that likely functions as an anti-predator defense (Brodie et al 2002). Taricha (and other salamandrids) possess amino acid changes in Nav1.4 that help them resist their own TTX defenses (Hanifin and Gilly, 2015;Gendreau et al, 2021).…”

Section: Ko Montana Et Almentioning

confidence: 99%

Are Pacific Chorus Frogs (Pseudacris regilla) Resistant to Tetrodotoxin (TTX)? Characterizing Potential TTX Exposure and Resistance in an Ecological Associate of Pacific Newts (Taricha)

Montana

Ramírez‐Castañeda

Tarvin

2022

Preprint

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Animals that frequently encounter toxins often evolve mechanisms of toxin resistance. Both predators that consume toxic prey and organisms in physical contact with a toxin or pollutant in their environment may experience natural selection for resistance. Based on observations that Pacific Chorus Frogs (Pseudacris regilla) sometimes eat and mistakenly amplect tetrodotoxin (TTX)-defended Taricha newts, we hypothesized that P. regilla may possess resistance to TTX. We tested this prediction by comparing the amino acid sequences of the domain IV pore loop of the muscle voltage-gated sodium channel gene SCN4A (Nav1.4 protein) in populations of P. regilla that are sympatric and allopatric with Taricha. We identified a single substitution in the domain IV pore loop of Nav1.4 in P. regilla that has been hypothesized to provide TTX resistance based on computational modeling, though its role in resistance has been challenged. Nonetheless, both allopatric and sympatric P. regilla had this substitution, suggesting that it may be unrelated to TTX exposure from Taricha. Thus, there is no conclusive evidence that P. regilla has evolved TTX resistance encoded by amino acid substitutions in this domain. In addition, California occurrence data from the last 50 years indicate that Taricha activity peaks in January while the activity of P. regilla peaks in April. These relatively distinct activity patterns suggest that P. regilla may not be exposed to levels of TTX from Taricha that are high enough to require mutations in SCN4A. Nevertheless, other unidentified mechanisms of TTX resistance could be present in P. regilla and other species that are sympatric with toxic newts.

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“…Coevolution What does reciprocal selection mean, and how might this play out between toxic newts and predatory snakes (Hague et al, 2020;Reimche et al, 2020)?…”

Section: Phenotypic Matching Between Garter Snakes and Toxic Newtsmentioning

confidence: 99%

Of Newts and Neurotoxins

Fisher¹

2022

The American Biology Teacher

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Storytelling can stimulate learning by delivering scientific content within a narrative that increases comprehension and engagement. In this article I describe the coevolutionary arms race between toxic newts and predatory garter snakes. This engaging story centers on the use of a deadly neurotoxin called tetrodotoxin (TTX) as an antipredator defense. Some species of newts contain TTX in their tissues, but resistance to TTX has developed through convergent evolution in garter snakes and other species. TTX resistance results from mutated voltage-gated sodium channels. These channels, whether TTX resistant or not, are found in all animals and are vital to the function of nervous and muscle tissues. Through reciprocal selection, coevolution has created phenotypic matching between toxic newts and TTX-resistant garter snakes across their range in the western United States. In other words, as newts became more poisonous, garter snakes became more resistant. These results and the scientific process behind them are discussed in detail. This story can be used by educators to provide a unifying and engaging backdrop as students learn multiple aspects of biology, such as protein structure, genetics, phylogenetics, electrical signaling, evolution, and the process of science.

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The geographic mosaic in parallel: Matching patterns of newt tetrodotoxin levels and snake resistance in multiple predator–prey pairs

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 29 publications

References 66 publications

Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey

Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey

Are Pacific Chorus Frogs (Pseudacris regilla) Resistant to Tetrodotoxin (TTX)? Characterizing Potential TTX Exposure and Resistance in an Ecological Associate of Pacific Newts (Taricha)

Of Newts and Neurotoxins

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