TY - JOUR
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.
N1 - Funding Information:
We thank USDA-APHIS mounted patrol inspectors for collecting field samples used in this study. We are grateful to Mr. Ed Bowers, Director of Field Operations (CFTEP), for providing field records of infested properties and valuable insight into the eradication program. We thank Michael G. Moses for cycling and maintaining tick strains and Laurence D. Krska for conducting the larval packet DD assays used in this study. This work was supported by USDA-NIFA award 2010-65104-20386. Use of trade, product, or firm names does not imply endorsement by the U.S. Government. The USDA is an equal opportunity provider and employer.
Publisher Copyright:
© 2014 Stone et al.; licensee BioMed Central Ltd.
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.
KW - Bovine babesiosis
KW - Para-sodium channel gene
KW - Pyrethroid resistance
KW - Rhipicephalus annulatus
KW - Rhipicephalus microplus
KW - Super-kdr
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UR - http://www.scopus.com/inward/citedby.url?scp=84965191395&partnerID=8YFLogxK
U2 - 10.1186/s13071-014-0456-z
DO - 10.1186/s13071-014-0456-z
M3 - Article
C2 - 25266983
AN - SCOPUS:84965191395
SN - 1756-3305
VL - 7
JO - Parasites and Vectors
JF - Parasites and Vectors
IS - 1
M1 - 456
ER -