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Evolutionary history of a complex adaptation: tetrodotoxin resistance in salamanders.

ABSTRACT: Understanding the processes that generate novel adaptive phenotypes is central to evolutionary biology. We used comparative analyses to reveal the history of tetrodotoxin (TTX) resistance in TTX-bearing salamanders. Resistance to TTX is a critical component of the ability to use TTX defensively but the origin of the TTX-bearing phenotype is unclear. Skeletal muscle of TTX-bearing salamanders (modern newts, family: Salamandridae) is unaffected by TTX at doses far in excess of those that block action potentials in muscle and nerve of other vertebrates. Skeletal muscle of non-TTX-bearing salamandrids is also resistant to TTX but at lower levels. Skeletal muscle TTX resistance in the Salamandridae results from the expression of TTX-resistant variants of the voltage-gated sodium channel NaV 1.4 (SCN4a). We identified four substitutions in the coding region of salSCN4a that are likely responsible for the TTX resistance measured in TTX-bearing salamanders and variation at one of these sites likely explains variation in TTX resistance among other lineages. Our results suggest that exaptation has played a role in the evolution of the TTX-bearing phenotype and provide empirical evidence that complex physiological adaptations can arise through the accumulation of beneficial mutations in the coding region of conserved proteins.

SUBMITTER: Hanifin CT

PROVIDER: S-EPMC5333673 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Evolutionary history of a complex adaptation: tetrodotoxin resistance in salamanders.

Hanifin Charles T CT Gilly William F WF

Evolution; international journal of organic evolution 20141216 1

Understanding the processes that generate novel adaptive phenotypes is central to evolutionary biology. We used comparative analyses to reveal the history of tetrodotoxin (TTX) resistance in TTX-bearing salamanders. Resistance to TTX is a critical component of the ability to use TTX defensively but the origin of the TTX-bearing phenotype is unclear. Skeletal muscle of TTX-bearing salamanders (modern newts, family: Salamandridae) is unaffected by TTX at doses far in excess of those that block act ...[more]

PMID: 25346116

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Project description:BackgroundIsland populations are excellent model systems for studies of phenotypic, ecological and molecular evolution. In this study, molecular markers of mitochondrial and nuclear derivation were used to investigate the evolution, structure and origin of populations of the California slender salamander (Batrachoseps attenuatus) inhabiting the six major islands of San Francisco Bay, formed following the rising of sea level around 9,000 years ago.ResultsThere was a high degree of congruence in the results of analyses of nucleotide and allozyme data, both of which strongly support the hypothesis that, for the majority of the islands, salamanders are descended from hilltop populations that became isolated with the formation of the Bay ca. 9,000 years ago. There are two exceptions (Alcatraz and Yerba Buena) where the evidence suggests that salamander populations are wholly or in part, the result of anthropogenic introductions.Comparison of the molecular data and the interpretations drawn therefrom with an earlier morphological study of many of the same salamander populations show some of the same evolutionary trends.ConclusionIn spite of marked differences between the evolutionary rates of the two kinds of molecular markers, both indicate distinctive and similar patterns of population structure for B. attenuatus in the San Francisco Bay Area and its islands. With the two noted exceptions, it is clear that most island populations were established prior to the 9,000 years since the formation of the Bay. Results of coalescence-based analyses suggest that for most island populations the mtDNA lineages from which they were derived date from the Pleistocene.It can be said that, based on observed values of genetic diversity, the last 9,000 years of evolution on these islands have been characterized by relative stability, with the occasional extinction of some haplotypes or alleles that were formerly shared between island and mainland populations but overall maintaining high levels of variation (with the exception of Alcatraz). In contrast, there is some evidence for rapid morphological changes between populations in some islands and their closest mainland counterparts. This pattern of rapid morphological divergence (e. g., resulting from founder effects) is similar to that observed in other studies about recent colonization of island habitats.

Dataset Information

Evolutionary history of a complex adaptation: tetrodotoxin resistance in salamanders.

Publications

Evolutionary history of a complex adaptation: tetrodotoxin resistance in salamanders.

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