Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico

Nathan E. Stone, Pia U. Olafson, Ronald B. Davey, Greta Buckmeier, Deanna Bodine, Lindsay C. Sidak-Loftis, John R. Giles, Roberta Duhaime, Robert J. Miller, Juan Mosqueda, Glen A. Scoles, David M Wagner, Joseph D. Busch

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Abstract

BACKGROUND: Acaricide resistant Rhipicephalus microplus populations have become a major problem for many cattle producing areas of the world. Pyrethroid resistance in arthropods is typically associated with mutations in domains I, II, III, and IV of voltage-gated sodium channel genes. In R. microplus, known resistance mutations include a domain II change (C190A) in populations from Australia, Africa, and South America and a domain III mutation (T2134A) that only occurs in Mexico and the U.S.

METHODS: We investigated pyrethroid resistance in cattle fever ticks from Texas and Mexico by estimating resistance levels in field-collected ticks using larval packet discriminating dose (DD) assays and identifying single nucleotide polymorphisms (SNPs) in the para-sodium channel gene that associated with resistance. We then developed qPCR assays for three SNPs and screened a larger set of 1,488 R. microplus ticks, representing 77 field collections and four laboratory strains, for SNP frequency.

RESULTS: We detected resistance SNPs in 21 of 68 U.S. field collections and six of nine Mexico field collections. We expected to identify the domain III SNP (T2134A) at a high frequency; however, we only found it in three U.S. collections. A much more common SNP in the U.S. (detected in 19 of 21 field collections) was the C190A domain II mutation, which has never before been reported from North America. We also discovered a novel domain II SNP (T170C) in ten U.S. and two Mexico field collections. The T170C transition mutation has previously been associated with extreme levels of resistance (super-knockdown resistance) in insects. We found a significant correlation (r = 0.81) between the proportion of individuals in field collections that carried any two resistance SNPs and the percent survivorship of F1 larvae from these collections in DD assays. This relationship is accurately predicted by a simple linear regression model (R2 = 0.6635).

CONCLUSIONS: These findings demonstrate that multiple mutations in the para-sodium channel gene independently associate with pyrethroid resistance in R. microplus ticks, which is likely a consequence of human-induced selection.

Original languageEnglish (US)
Pages (from-to)456
Number of pages1
JournalParasites and Vectors
Volume7
DOIs
StatePublished - 2014

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Rhipicephalus
Pyrethrins
Sodium Channels
Mexico
Single Nucleotide Polymorphism
Mutation
Ticks
Genes
Linear Models
Acaricides
Voltage-Gated Sodium Channels
Arthropods
South America
North America
Population
Larva
Insects
Fever

ASJC Scopus subject areas

  • Medicine(all)

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Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico. / Stone, Nathan E.; Olafson, Pia U.; Davey, Ronald B.; Buckmeier, Greta; Bodine, Deanna; Sidak-Loftis, Lindsay C.; Giles, John R.; Duhaime, Roberta; Miller, Robert J.; Mosqueda, Juan; Scoles, Glen A.; Wagner, David M; Busch, Joseph D.

In: Parasites and Vectors, Vol. 7, 2014, p. 456.

Research output: Contribution to journalArticle

Stone, NE, Olafson, PU, Davey, RB, Buckmeier, G, Bodine, D, Sidak-Loftis, LC, Giles, JR, Duhaime, R, Miller, RJ, Mosqueda, J, Scoles, GA, Wagner, DM & Busch, JD 2014, 'Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico', Parasites and Vectors, vol. 7, pp. 456. https://doi.org/10.1186/s13071-014-0456-z
Stone, Nathan E. ; Olafson, Pia U. ; Davey, Ronald B. ; Buckmeier, Greta ; Bodine, Deanna ; Sidak-Loftis, Lindsay C. ; Giles, John R. ; Duhaime, Roberta ; Miller, Robert J. ; Mosqueda, Juan ; Scoles, Glen A. ; Wagner, David M ; Busch, Joseph D. / Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico. In: Parasites and Vectors. 2014 ; Vol. 7. pp. 456.
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abstract = "BACKGROUND: Acaricide resistant Rhipicephalus microplus populations have become a major problem for many cattle producing areas of the world. Pyrethroid resistance in arthropods is typically associated with mutations in domains I, II, III, and IV of voltage-gated sodium channel genes. In R. microplus, known resistance mutations include a domain II change (C190A) in populations from Australia, Africa, and South America and a domain III mutation (T2134A) that only occurs in Mexico and the U.S.METHODS: We investigated pyrethroid resistance in cattle fever ticks from Texas and Mexico by estimating resistance levels in field-collected ticks using larval packet discriminating dose (DD) assays and identifying single nucleotide polymorphisms (SNPs) in the para-sodium channel gene that associated with resistance. We then developed qPCR assays for three SNPs and screened a larger set of 1,488 R. microplus ticks, representing 77 field collections and four laboratory strains, for SNP frequency.RESULTS: We detected resistance SNPs in 21 of 68 U.S. field collections and six of nine Mexico field collections. We expected to identify the domain III SNP (T2134A) at a high frequency; however, we only found it in three U.S. collections. A much more common SNP in the U.S. (detected in 19 of 21 field collections) was the C190A domain II mutation, which has never before been reported from North America. We also discovered a novel domain II SNP (T170C) in ten U.S. and two Mexico field collections. The T170C transition mutation has previously been associated with extreme levels of resistance (super-knockdown resistance) in insects. We found a significant correlation (r = 0.81) between the proportion of individuals in field collections that carried any two resistance SNPs and the percent survivorship of F1 larvae from these collections in DD assays. This relationship is accurately predicted by a simple linear regression model (R2 = 0.6635).CONCLUSIONS: These findings demonstrate that multiple mutations in the para-sodium channel gene independently associate with pyrethroid resistance in R. microplus ticks, which is likely a consequence of human-induced selection.",
author = "Stone, {Nathan E.} and Olafson, {Pia U.} and Davey, {Ronald B.} and Greta Buckmeier and Deanna Bodine and Sidak-Loftis, {Lindsay C.} and Giles, {John R.} and Roberta Duhaime and Miller, {Robert J.} and Juan Mosqueda and Scoles, {Glen A.} and Wagner, {David M} and Busch, {Joseph D.}",
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T1 - Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico

AU - Stone, Nathan E.

AU - Olafson, Pia U.

AU - Davey, Ronald B.

AU - Buckmeier, Greta

AU - Bodine, Deanna

AU - Sidak-Loftis, Lindsay C.

AU - Giles, John R.

AU - Duhaime, Roberta

AU - Miller, Robert J.

AU - Mosqueda, Juan

AU - Scoles, Glen A.

AU - Wagner, David M

AU - Busch, Joseph D.

PY - 2014

Y1 - 2014

N2 - BACKGROUND: Acaricide resistant Rhipicephalus microplus populations have become a major problem for many cattle producing areas of the world. Pyrethroid resistance in arthropods is typically associated with mutations in domains I, II, III, and IV of voltage-gated sodium channel genes. In R. microplus, known resistance mutations include a domain II change (C190A) in populations from Australia, Africa, and South America and a domain III mutation (T2134A) that only occurs in Mexico and the U.S.METHODS: We investigated pyrethroid resistance in cattle fever ticks from Texas and Mexico by estimating resistance levels in field-collected ticks using larval packet discriminating dose (DD) assays and identifying single nucleotide polymorphisms (SNPs) in the para-sodium channel gene that associated with resistance. We then developed qPCR assays for three SNPs and screened a larger set of 1,488 R. microplus ticks, representing 77 field collections and four laboratory strains, for SNP frequency.RESULTS: We detected resistance SNPs in 21 of 68 U.S. field collections and six of nine Mexico field collections. We expected to identify the domain III SNP (T2134A) at a high frequency; however, we only found it in three U.S. collections. A much more common SNP in the U.S. (detected in 19 of 21 field collections) was the C190A domain II mutation, which has never before been reported from North America. We also discovered a novel domain II SNP (T170C) in ten U.S. and two Mexico field collections. The T170C transition mutation has previously been associated with extreme levels of resistance (super-knockdown resistance) in insects. We found a significant correlation (r = 0.81) between the proportion of individuals in field collections that carried any two resistance SNPs and the percent survivorship of F1 larvae from these collections in DD assays. This relationship is accurately predicted by a simple linear regression model (R2 = 0.6635).CONCLUSIONS: These findings demonstrate that multiple mutations in the para-sodium channel gene independently associate with pyrethroid resistance in R. microplus ticks, which is likely a consequence of human-induced selection.

AB - BACKGROUND: Acaricide resistant Rhipicephalus microplus populations have become a major problem for many cattle producing areas of the world. Pyrethroid resistance in arthropods is typically associated with mutations in domains I, II, III, and IV of voltage-gated sodium channel genes. In R. microplus, known resistance mutations include a domain II change (C190A) in populations from Australia, Africa, and South America and a domain III mutation (T2134A) that only occurs in Mexico and the U.S.METHODS: We investigated pyrethroid resistance in cattle fever ticks from Texas and Mexico by estimating resistance levels in field-collected ticks using larval packet discriminating dose (DD) assays and identifying single nucleotide polymorphisms (SNPs) in the para-sodium channel gene that associated with resistance. We then developed qPCR assays for three SNPs and screened a larger set of 1,488 R. microplus ticks, representing 77 field collections and four laboratory strains, for SNP frequency.RESULTS: We detected resistance SNPs in 21 of 68 U.S. field collections and six of nine Mexico field collections. We expected to identify the domain III SNP (T2134A) at a high frequency; however, we only found it in three U.S. collections. A much more common SNP in the U.S. (detected in 19 of 21 field collections) was the C190A domain II mutation, which has never before been reported from North America. We also discovered a novel domain II SNP (T170C) in ten U.S. and two Mexico field collections. The T170C transition mutation has previously been associated with extreme levels of resistance (super-knockdown resistance) in insects. We found a significant correlation (r = 0.81) between the proportion of individuals in field collections that carried any two resistance SNPs and the percent survivorship of F1 larvae from these collections in DD assays. This relationship is accurately predicted by a simple linear regression model (R2 = 0.6635).CONCLUSIONS: These findings demonstrate that multiple mutations in the para-sodium channel gene independently associate with pyrethroid resistance in R. microplus ticks, which is likely a consequence of human-induced selection.

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