A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l
The brown dog tick, Rhipicephalus sanguineus sensu lato (s.l.), is an important vector for Rickettsia rickettsii, causative agent of Rocky Mountain spotted fever. Current public health prevention and control efforts to protect people involve preventing tick infestations on domestic animals and in an...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-07-01
|
| Series: | Ticks and Tick-Borne Diseases |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1877959X24000372 |
| _version_ | 1797198773727789056 |
|---|---|
| author | Nathan E. Stone Rebecca Ballard Reanna M. Bourgeois Grant L. Pemberton Ryelan F. McDonough Megan C. Ruby Laura H. Backus Andrés M. López-Pérez Darrin Lemmer Zane Koch Maureen Brophy Christopher D. Paddock Gilbert J. Kersh William L. Nicholson Jason W. Sahl Joseph D. Busch Johanna S. Salzer Janet E. Foley David M. Wagner |
| author_facet | Nathan E. Stone Rebecca Ballard Reanna M. Bourgeois Grant L. Pemberton Ryelan F. McDonough Megan C. Ruby Laura H. Backus Andrés M. López-Pérez Darrin Lemmer Zane Koch Maureen Brophy Christopher D. Paddock Gilbert J. Kersh William L. Nicholson Jason W. Sahl Joseph D. Busch Johanna S. Salzer Janet E. Foley David M. Wagner |
| author_sort | Nathan E. Stone |
| collection | DOAJ |
| description | The brown dog tick, Rhipicephalus sanguineus sensu lato (s.l.), is an important vector for Rickettsia rickettsii, causative agent of Rocky Mountain spotted fever. Current public health prevention and control efforts to protect people involve preventing tick infestations on domestic animals and in and around houses. Primary prevention tools rely on acaricides, often synthetic pyrethroids (SPs); resistance to this chemical class is widespread in ticks and other arthropods. Rhipicephalus sanguineus s.l. is a complex that likely contains multiple unique species and although the distribution of this complex is global, there are differences in morphology, ecology, and perhaps vector competence among these major lineages. Two major lineages within Rh. sanguineus s.l., commonly referred to as temperate and tropical, have been documented from multiple locations in North America, but are thought to occupy different ecological niches. To evaluate potential acaricide resistance and better define the distributions of the tropical and temperate lineages throughout the US and in northern Mexico, we employed a highly multiplexed amplicon sequencing approach to characterize sequence diversity at: 1) three loci within the voltage-gated sodium channel (VGSC) gene, which contains numerous genetic mutations associated with resistance to SPs; 2) a region of the gamma-aminobutyric acid-gated chloride channel gene (GABA-Cl) containing several mutations associated with dieldrin/fipronil resistance in other species; and 3) three mitochondrial genes (COI, 12S, and 16S). We utilized a geographically diverse set of Rh sanguineus s.l. collected from domestic pets in the US in 2013 and a smaller set of ticks collected from canines in Baja California, Mexico in 2021. We determined that a single nucleotide polymorphism (T2134C) in domain III segment 6 of the VGSC, which has previously been associated with SP resistance in Rh. sanguineus s.l., was widespread and abundant in tropical lineage ticks (>50 %) but absent from the temperate lineage, suggesting that resistance to SPs may be common in the tropical lineage. We found evidence of multiple copies of GABA-Cl in ticks from both lineages, with some copies containing mutations associated with fipronil resistance in other species, but the effects of these patterns on fipronil resistance in Rh. sanguineus s.l. are currently unknown. The tropical lineage was abundant and geographically widespread, accounting for 79 % of analyzed ticks and present at 13/14 collection sites. The temperate and tropical lineages co-occurred in four US states, and as far north as New York. None of the ticks we examined were positive for Rickettsia rickettsii or Rickettsia massiliae. |
| first_indexed | 2024-04-24T07:05:11Z |
| format | Article |
| id | doaj.art-34de3f60796342df95fcd42d5ad0c5e7 |
| institution | Directory Open Access Journal |
| issn | 1877-9603 |
| language | English |
| last_indexed | 2024-04-24T07:05:11Z |
| publishDate | 2024-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ticks and Tick-Borne Diseases |
| spelling | doaj.art-34de3f60796342df95fcd42d5ad0c5e72024-04-22T04:11:33ZengElsevierTicks and Tick-Borne Diseases1877-96032024-07-01154102344A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.lNathan E. Stone0Rebecca Ballard1Reanna M. Bourgeois2Grant L. Pemberton3Ryelan F. McDonough4Megan C. Ruby5Laura H. Backus6Andrés M. López-Pérez7Darrin Lemmer8Zane Koch9Maureen Brophy10Christopher D. Paddock11Gilbert J. Kersh12William L. Nicholson13Jason W. Sahl14Joseph D. Busch15Johanna S. Salzer16Janet E. Foley17David M. Wagner18Pathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesDepartment of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, United StatesDepartment of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, United States; Red de Biología y Conservación de Vertebrados, Instituto de Ecología, A.C., Xalapa 91073, MexicoTranslational Genomics Research Institute (TGen North), 3051 West Shamrell Boulevard, Suite 106, Flagstaff, AZ 86005, United StatesTranslational Genomics Research Institute (TGen North), 3051 West Shamrell Boulevard, Suite 106, Flagstaff, AZ 86005, United StatesRickettsial Zoonoses Branch, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, United StatesRickettsial Zoonoses Branch, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, United StatesRickettsial Zoonoses Branch, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, United StatesRickettsial Zoonoses Branch, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United StatesRickettsial Zoonoses Branch, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30329, United StatesDepartment of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, United StatesPathogen and Microbiome Institute, Northern Arizona University, PO Box 4073, Flagstaff, AZ 86011, United States; Corresponding author.The brown dog tick, Rhipicephalus sanguineus sensu lato (s.l.), is an important vector for Rickettsia rickettsii, causative agent of Rocky Mountain spotted fever. Current public health prevention and control efforts to protect people involve preventing tick infestations on domestic animals and in and around houses. Primary prevention tools rely on acaricides, often synthetic pyrethroids (SPs); resistance to this chemical class is widespread in ticks and other arthropods. Rhipicephalus sanguineus s.l. is a complex that likely contains multiple unique species and although the distribution of this complex is global, there are differences in morphology, ecology, and perhaps vector competence among these major lineages. Two major lineages within Rh. sanguineus s.l., commonly referred to as temperate and tropical, have been documented from multiple locations in North America, but are thought to occupy different ecological niches. To evaluate potential acaricide resistance and better define the distributions of the tropical and temperate lineages throughout the US and in northern Mexico, we employed a highly multiplexed amplicon sequencing approach to characterize sequence diversity at: 1) three loci within the voltage-gated sodium channel (VGSC) gene, which contains numerous genetic mutations associated with resistance to SPs; 2) a region of the gamma-aminobutyric acid-gated chloride channel gene (GABA-Cl) containing several mutations associated with dieldrin/fipronil resistance in other species; and 3) three mitochondrial genes (COI, 12S, and 16S). We utilized a geographically diverse set of Rh sanguineus s.l. collected from domestic pets in the US in 2013 and a smaller set of ticks collected from canines in Baja California, Mexico in 2021. We determined that a single nucleotide polymorphism (T2134C) in domain III segment 6 of the VGSC, which has previously been associated with SP resistance in Rh. sanguineus s.l., was widespread and abundant in tropical lineage ticks (>50 %) but absent from the temperate lineage, suggesting that resistance to SPs may be common in the tropical lineage. We found evidence of multiple copies of GABA-Cl in ticks from both lineages, with some copies containing mutations associated with fipronil resistance in other species, but the effects of these patterns on fipronil resistance in Rh. sanguineus s.l. are currently unknown. The tropical lineage was abundant and geographically widespread, accounting for 79 % of analyzed ticks and present at 13/14 collection sites. The temperate and tropical lineages co-occurred in four US states, and as far north as New York. None of the ticks we examined were positive for Rickettsia rickettsii or Rickettsia massiliae.http://www.sciencedirect.com/science/article/pii/S1877959X24000372TicksRhipicephalus sanguineusAcaricide resistanceSpotted fever group rickettsia spp.Rocky Mountain spotted fever |
| spellingShingle | Nathan E. Stone Rebecca Ballard Reanna M. Bourgeois Grant L. Pemberton Ryelan F. McDonough Megan C. Ruby Laura H. Backus Andrés M. López-Pérez Darrin Lemmer Zane Koch Maureen Brophy Christopher D. Paddock Gilbert J. Kersh William L. Nicholson Jason W. Sahl Joseph D. Busch Johanna S. Salzer Janet E. Foley David M. Wagner A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l Ticks and Tick-Borne Diseases Ticks Rhipicephalus sanguineus Acaricide resistance Spotted fever group rickettsia spp. Rocky Mountain spotted fever |
| title | A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l |
| title_full | A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l |
| title_fullStr | A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l |
| title_full_unstemmed | A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l |
| title_short | A mutation associated with resistance to synthetic pyrethroids is widespread in US populations of the tropical lineage of Rhipicephalus sanguineus s.l |
| title_sort | mutation associated with resistance to synthetic pyrethroids is widespread in us populations of the tropical lineage of rhipicephalus sanguineus s l |
| topic | Ticks Rhipicephalus sanguineus Acaricide resistance Spotted fever group rickettsia spp. Rocky Mountain spotted fever |
| url | http://www.sciencedirect.com/science/article/pii/S1877959X24000372 |
| work_keys_str_mv | AT nathanestone amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT rebeccaballard amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT reannambourgeois amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT grantlpemberton amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT ryelanfmcdonough amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT megancruby amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT laurahbackus amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT andresmlopezperez amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT darrinlemmer amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT zanekoch amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT maureenbrophy amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT christopherdpaddock amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT gilbertjkersh amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT williamlnicholson amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT jasonwsahl amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT josephdbusch amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT johannassalzer amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT janetefoley amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT davidmwagner amutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT nathanestone mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT rebeccaballard mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT reannambourgeois mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT grantlpemberton mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT ryelanfmcdonough mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT megancruby mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT laurahbackus mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT andresmlopezperez mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT darrinlemmer mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT zanekoch mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT maureenbrophy mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT christopherdpaddock mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT gilbertjkersh mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT williamlnicholson mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT jasonwsahl mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT josephdbusch mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT johannassalzer mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT janetefoley mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl AT davidmwagner mutationassociatedwithresistancetosyntheticpyrethroidsiswidespreadinuspopulationsofthetropicallineageofrhipicephalussanguineussl |