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Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus
Nathan E Stone, Pia U Olafson, Ronald B Davey
1Center for Microbial Genetics and Genomics, Northern Arizona University, 1298 S Knoles Drive, Flagstaff 86011-4073, AZ, USA. Joseph.Busch@nau.edu.
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.
Insights
Pyrethroid resistance in cattle ticks is driven by multiple gene mutations, not just one. New mutations in the para-sodium channel gene are emerging in Rhipicephalus microplus populations, indicating ongoing adaptation to acaricides.
Area of Science:
- Veterinary Entomology
- Molecular Genetics
- Pest Management
Background:
- Acaricide resistance in Rhipicephalus microplus poses a significant threat to global cattle production.
- Pyrethroid resistance in arthropods is often linked to mutations in voltage-gated sodium channel genes.
Purpose of the Study:
- To investigate pyrethroid resistance mechanisms in cattle fever ticks from Texas and Mexico.
- To identify single nucleotide polymorphisms (SNPs) in the para-sodium channel gene associated with resistance.
Main Methods:
- Larval packet discriminating dose (DD) assays were used to estimate resistance levels.
- Quantitative PCR (qPCR) assays were developed to screen 1,488 Rhipicephalus microplus ticks for three specific SNPs.
- Field-collected ticks from Texas and Mexico were analyzed for SNP frequency.
Main Results:
- Resistance SNPs were detected in numerous U.S. and Mexican field collections.
- The C190A domain II mutation, previously unreported in North America, was common in U.S. ticks.
- A novel domain II SNP (T170C), associated with extreme resistance, was discovered in both U.S. and Mexican collections.
- A strong correlation was found between the presence of multiple resistance SNPs and larval survivorship in DD assays.
Conclusions:
- Multiple para-sodium channel gene mutations independently contribute to pyrethroid resistance in Rhipicephalus microplus.
- These findings suggest human-induced selection is driving the evolution of acaricide resistance in these ticks.
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