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Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey.

ABSTRACT: Adaptive evolution in response to one selective challenge may disrupt other important aspects of performance. Such evolutionary trade-offs are predicted to arise in the process of local adaptation, but it is unclear if these phenotypic compromises result from the antagonistic effects of simple amino acid substitutions. We tested for trade-offs associated with beneficial mutations that confer tetrodotoxin (TTX) resistance in the voltage-gated sodium channel (NaV1.4) in skeletal muscle of the common garter snake (Thamnophis sirtalis). Separate lineages in California and the Pacific Northwest independently evolved TTX-resistant changes to the pore of NaV1.4 as a result of arms race coevolution with toxic prey, newts of the genus Taricha. Snakes from the California lineage that were homozygous for an allele known to confer large increases in toxin resistance (NaV1.4LVNV) had significantly reduced crawl speed compared to individuals with the ancestral TTX-sensitive channel. Heterologous expression of native snake NaV1.4 proteins demonstrated that the same NaV1.4LVNV allele confers a dramatic increase in TTX resistance and a correlated decrease in overall channel excitability. Our results suggest the same mutations that accumulate during arms race coevolution and beneficially interfere with toxin-binding also cause changes in electrophysiological function of the channel that may affect organismal performance. This trade-off was only evident in the predator lineage where coevolution has led to the most extreme resistance phenotype, determined by four critical amino acid substitutions. If these biophysical changes also translate to a fitness cost-for example, through the inability of T. sirtalis to quickly escape predators-then pleiotropy at this single locus could contribute to observed variation in levels of TTX resistance across the mosaic landscape of coevolution.

SUBMITTER: Hague MTJ

PROVIDER: S-EPMC6121790 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey.

Hague Michael T J MTJ Toledo Gabriela G Geffeney Shana L SL Hanifin Charles T CT Brodie Edmund D ED Brodie Edmund D ED

Evolution letters 20180731 4

Adaptive evolution in response to one selective challenge may disrupt other important aspects of performance. Such evolutionary trade-offs are predicted to arise in the process of local adaptation, but it is unclear if these phenotypic compromises result from the antagonistic effects of simple amino acid substitutions. We tested for trade-offs associated with beneficial mutations that confer tetrodotoxin (TTX) resistance in the voltage-gated sodium channel (Na<sub>V</sub>1.4) in skeletal muscle ...[more]

PMID: 30283691

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Project description:Seemingly unrelated traits often share the same underlying molecular mechanisms, potentially generating a pleiotropic relationship whereby selection shaping one trait can simultaneously compromise another. While such functional trade-offs are expected to influence evolutionary outcomes, their actual relevance in nature is masked by obscure links between genotype, phenotype, and fitness. Here, we describe functional trade-offs that likely govern a key adaptation and coevolutionary dynamics in a predator-prey system. Several garter snake (Thamnophis spp.) populations have evolved resistance to tetrodotoxin (TTX), a potent chemical defense in their prey, toxic newts (Taricha spp.). Snakes achieve TTX resistance through mutations occurring at toxin-binding sites in the pore of snake skeletal muscle voltage-gated sodium channels (NaV1.4). We hypothesized that these mutations impair basic NaV functions, producing molecular trade-offs that should ultimately scale up to compromised organismal performance. We investigate biophysical costs in two snake species with unique and independently evolved mutations that confer TTX resistance. We show electrophysiological evidence that skeletal muscle sodium channels encoded by toxin-resistant alleles are functionally compromised. Furthermore, skeletal muscles from snakes with resistance genotypes exhibit reduced mechanical performance. Lastly, modeling the molecular stability of these sodium channel variants partially explains the electrophysiological and muscle impairments. Ultimately, adaptive genetic changes favoring toxin resistance appear to negatively impact sodium channel function, skeletal muscle strength, and organismal performance. These functional trade-offs at the cellular and organ levels appear to underpin locomotor deficits observed in resistant snakes and may explain variation in the population-level success of toxin-resistant alleles across the landscape, ultimately shaping the trajectory of snake-newt coevolution.

Dataset Information

Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey.

Publications

Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey.

Similar Datasets

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