Abstract
Inducible phenotypic responses to environmental variation are ubiquitous across the tree of life, but it remains an open question whether amphibian chemical defense phenotypes are inducible. Tetrodotoxin (TTX) is a key chemical defense trait in North American and Eurasian newts (Salamandridae). We tested if TTX can be induced by exposing populations of adult and larval California newts (Taricha torosa) to sustained stressful conditions while longitudinally quantifying TTX concentrations. Adult newts rapidly increased chemical defenses in response to simulated predator attacks and consistently maintained elevated TTX concentrations relative to wild, non-captive individuals. We also found that laboratory-reared larvae maintained chemical defenses nearly three-fold greater than those of siblings reared in streams. Collectively, our results indicate that amphibian chemical defenses are not fixed. Instead, toxins are maintained at a baseline concentration that can quickly be increased in response to perceived risk with substantial increases to toxicity. Therefore, it is crucial that inducible variation be accounted for when considering ecological dynamics of chemically defended animals and coevolutionary predator-prey and mimic-model relationships.
Highlights
Phenotypic variation, or plasticity, is a ubiquitous strategy taxa use to cope with variable environmental conditions and ecological challenges[1,2,3,4] with demonstrated adaptive significance[5,6,7]
We found that the central California population rapidly increased and maintained elevated TTX concentrations in response to simulated predator attacks (Fig. 1d, black squares), indicating that chemical defenses can be modulated over a relatively short temporal scale
When we evaluated whether chemical defenses of initially sampled (Bi) and repeatedly sampled (Br) males in the stratified sampling treatment (Fig. 1d; compare hollow and dotted diamonds) differed, we found that TTX concentrations temporally varied among repeatedly-sampled males (Br: β = 0.014, SE = 0.006, P = 0.025), but not initially-sampled males (Bi β = −0.023, SE = 0.013, P = 0.103)
Summary
Phenotypic variation, or plasticity, is a ubiquitous strategy taxa use to cope with variable environmental conditions and ecological challenges[1,2,3,4] with demonstrated adaptive significance[5,6,7]. The mechanisms underlying this variation remain unknown, including the fundamental question of whether newts produce TTX via microbial symbionts or if the genus is uniquely capable among metazoans of de novo synthesis. Such ambiguities present a challenge to understanding both the ecological and evolutionary dynamics of amphibian chemical defenses. Current theories maintain that amphibian chemical defenses are a fixed evolutionary response to local predation pressure, incapable of short-term environmental responses, and stable within wild individuals and populations over ecological time scales[15, 17, 18]. Models explaining the evolution and ecology of amphibian chemical defenses, coevolutionary relationships, and mimic-model systems that assume chemical defenses cannot be induced, must account for this previously unrecognized source of variation
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