Sex linkage of the skeletal muscle sodium channel gene (SCN4A) explains apparent deviations from Hardy-Weinberg equilibrium of tetrodotoxin-resistance alleles in garter snakes (Thamnophis sirtalis)

The arms race between tetrodotoxin-bearing Pacific newts (Taricha) and their garter snake predators (Thamnophis) in western North America has become a classic example of coevolution, shedding light on predator-prey dynamics, the molecular basis of adaptation, and patterns of convergent evolution. Ne...

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Veröffentlicht in:Heredity 2020-05, Vol.124 (5), p.647-657
Hauptverfasser: Gendreau, Kerry L, Hague, Michael T J, Feldman, Chris R, Brodie, Jr, Edmund D, Brodie, 3rd, Edmund D, McGlothlin, Joel W
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container_start_page 647
container_title Heredity
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creator Gendreau, Kerry L
Hague, Michael T J
Feldman, Chris R
Brodie, Jr, Edmund D
Brodie, 3rd, Edmund D
McGlothlin, Joel W
description The arms race between tetrodotoxin-bearing Pacific newts (Taricha) and their garter snake predators (Thamnophis) in western North America has become a classic example of coevolution, shedding light on predator-prey dynamics, the molecular basis of adaptation, and patterns of convergent evolution. Newts are defended by tetrodotoxin (TTX), a neurotoxin that binds to voltage-gated sodium channels (Na proteins), arresting electrical activity in nerves and muscles and paralyzing would-be predators. However, populations of the common garter snake (T. sirtalis) have overcome this defense, largely through polymorphism at the locus SCN4A, which renders the encoded protein (Na 1.4) less vulnerable to TTX. Previous work suggests that SCN4A commonly shows extreme deviations from Hardy-Weinberg equilibrium (HWE) in these populations, which has been interpreted as the result of intense selection imposed by newts. Here we show that much of this apparent deviation can be attributed to sex linkage of SCN4A. Using genomic data and quantitative PCR, we show that SCN4A is on the Z chromosome in Thamnophis and other advanced snakes. Taking Z-linkage into account, we find that most apparent deviations from HWE can be explained by female hemizygosity rather than low heterozygosity. Sex linkage can affect mutation rates, selection, and drift, and our results suggest that Z-linkage of SCN4A may make significant contributions to the overall dynamics of the coevolutionary arms race between newts and snakes.
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subjects Chromosomes
Coevolution
Gene polymorphism
Hemizygosity
Heterozygosity
Muscles
Mutation
Mutation rates
Nerves
Neurotoxins
Polymorphism
Populations
Predator-prey interactions
Predators
Prey
Proteins
Sex
Sex linkage
Skeletal muscle
Snakes
Sodium
Sodium channels
Sodium channels (voltage-gated)
Tetrodotoxin
Thamnophis
Thamnophis sirtalis
Toxins
Z chromosomes
title Sex linkage of the skeletal muscle sodium channel gene (SCN4A) explains apparent deviations from Hardy-Weinberg equilibrium of tetrodotoxin-resistance alleles in garter snakes (Thamnophis sirtalis)
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