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Experimental and Applied Acarology

, Volume 78, Issue 2, pp 149–172 | Cite as

Molecular markers and their application in the monitoring of acaricide resistance in Rhipicephalus microplus

  • Rinesh KumarEmail author
Review Paper

Abstract

Monitoring acaricide resistance and understanding the underlying mechanisms are critically important in developing strategies for resistance management and tick control. Identification of single nucleotide polymorphisms in the acaricide-resistant associated gene of Rhipicephalus microplus has enabled the development of molecular markers for detection and monitoring of resistance against different types of acaricide. There are many molecular markers developed for resistance monitoring, including mutations on target genes such as sodium channel, acetylcholinesterase, carboxylesterase, β-adrenergic octopamine receptor, octopamine–tyramine etc. Molecular genotyping through molecular markers can detect the presence of resistance-associated genes in a tick population before it reaches high frequency. This review aims to provide an update on the various molecular markers discovered to date from different regions of the world.

Keywords

Molecular diagnosis Molecular markers Rhipicephalus microplus Acaricide resistance 

Notes

Acknowledgements

I would like to thank Nicholas Jonsson, professor of production animal health from the University of Glasgow, UK, for commenting on a draft of the manuscript.

Compliance with ethical standards

Conflict of interest

The author declares that he has no competing interests.

References

  1. Adakal H, Stachurski F, Chevillon C (2013) Tick control practices in Burkina Faso and acaricide resistance survey in Rhipicephalus (Boophilus) geigyi (Acari: Ixodidae). Exp Appl Acarol 59:483–491Google Scholar
  2. Aguilar-Tipacamu G, Rodriguez-Vivas RI (2003) Effect of moxidectinagainst natural infestation of the cattle tick Boophilus microplus (Aca-rina: Ixodidae) in the Mexican tropics. Vet Parasitol 111:211–216Google Scholar
  3. Alonso-Diaz MA, Fernandez-Salas A, Martinez-Ibanez F, Osorio-Miranda J (2013) Amblyomma cajennense (Acari: Ixodidae) tick populations susceptible or resistant to acaricides in the Mexican Tropics. Vet Parasitol 197:326–331Google Scholar
  4. Angus BM (1996) The history of the cattle tick Boophilus microplus in Australia and achievements in its control. Int J Parasitol 26:1341–1355Google Scholar
  5. Baffi MA, Pereira CD, de Souza GRL, Bonetti AM, Ceron CR, Goulart LR (2005) Esterase profile in a pyrethroid resistant Brazilian strain of Boophilus microplus cattle ticks (Acari, Ixodidae). Gen Mol Biol 28:749–753Google Scholar
  6. Baffi MA, de Souza GRL, Vieira CU, de Sousa CS, Goulart LR, Bonetti AM (2007) Identification of point mutation in a putative caboxylesterase and their association with acaricide resistance in Rhipicephalus (Boophilus) microplus (Acri:Ixodidae). Vet Parasitol 148:301–309Google Scholar
  7. Bandara KMUJ, Karunaratne SHPP (2017) Mechanisms of acaricide resistance in the cattle tick Rhipicephalus (Boophilus) microplus in Sri Lanka. Pestic Biochem Physiol 138:68–72Google Scholar
  8. Baron S, van der Merwe NA, Madder M, Maritz-Olivier C (2015) SNP analysis infers that recombination is involved in the evolution of amitraz resistance in Rhipicephalus microplus. PLoS ONE 10(7):e0131341Google Scholar
  9. Baxter GD, Barker SC (1998) Acetylcholinesterase cDNA of the cattle tick, Boophilus microplus: characterization and role in organophosphate resistance. Insect Biochem Mol Biol 28:581–589Google Scholar
  10. Baxter GD, Barker SC (1999) Isolation of a cDNA for an octopamine like, G-protein coupled receptor from the cattle tick, Boophilus microplus. Insect Biochem Mol Biol 29:461–467Google Scholar
  11. Bloomquist JR (2003) Chloride channels as tools for developing selective insecticides. Arch Insect Biochem Physiol 54:145–156Google Scholar
  12. Bloomquist JR, Soderlund DM (1985) Neurotoxic insecticides inhibit GABA-dependent chloride uptake by mouse brain vesicles. Biochem Biophys Res Commun 133:37–43Google Scholar
  13. Bourguinat C, Keller K, Blagburn B, Schenker R, Geary TG, Prichard RK (2011) Correlation between loss of efficacy of macrocyclic lactone heartworm anthelmintics and P-glycoprotein genotype. Vet Parasitol 176:374–381Google Scholar
  14. Castro-Janer E, Rifran L, Piaggio J, Gil A, Miller RJ, Schumaker TTS (2009) In vitro tests to establish LC50 and discriminating concentrations for fipronil against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) and their standardization. Vet Parasitol 162:120–128Google Scholar
  15. Castro-Janer E, Martins J, Mendes M, Namindome A, Klafke G, Schumaker T (2010) Diagnoses of fipronil resistance in Brazilian cattle ticks Rhipicephalus (Boophilus) microplus using in vitro larval bioassays. Vet Parasitol 173:300–306Google Scholar
  16. Chen ZZ, Newcomb R, Forbes E, McKenzie J, Batterham P (2001) The acetylcholinesterase gene and organophosphorus resistance in the Australian sheep blowfly Lucilia cuprina. Insect Biochem Mol Biol 31:805–816Google Scholar
  17. Chen AC, He H, Davey RB (2007) Mutations in a putative octopamine receptor gene in amitraz-resistant cattle ticks. Vet Parasitol 148:379–383Google Scholar
  18. Chen AC, He H, Temeyer KB, Jones S, Green P, Barker SC (2009) A survey of Rhipicephalus microplus populations for mutations associated with pyrethroid resistance. J Econ Entomol 102(1):373–380Google Scholar
  19. Chevillon C, Ducornez S, de Meeûs T, Koffi BB, Gaia H, Delathière J-M, Barré N (2007) Accumulation of acaricide resistance mechanism in Rhipicephalus (Boophilus) microplus (Acri: ixodidae) populations from New Caledonia Island. Vet Parasitol 147:276–288Google Scholar
  20. Clark JM, Yoon KS, Lee SH, Pittendrigh BR (2013) Human lice: past, present and future control. Pestic Biochem Physiol 106:162–171Google Scholar
  21. Cole LM, Nicholson RA, Casida JE (1993) Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Est Biochem Physiol 46:47–54Google Scholar
  22. Coles GC, Watson CL, Anziani OS (2001) Ivermectin-resistant Cooperia in cattle. Vet Rec 148:283–284Google Scholar
  23. Coles GC, Rhodes AC, Wolstenholme AJ (2005) Rapid selection for ivermectin resistance in Haemonchus contortus. Vet Parasitol 129:345–347Google Scholar
  24. Corley SW, Piper EK, Jonsson NN (2012) Generation of full-length cDNAs for eight putative GPCnR from the cattle tick, R. microplus using a targeted degenerate PCR and sequencing strategy. PLoS ONE 7(3):e32480Google Scholar
  25. Corley SW, Jonsson NN, Piper EK, Cutulle C, Stear MJ, Seddon JM (2013) Mutation in the RmβAOR gene is associated with amitraz resistance in the cattle tick Rhipicephalus microplus. Proc Natl Acad Sci USA 110:16772–16777Google Scholar
  26. Cossio-Bauygar R, Miranda-Miranda E, Ortiz-Najera A, Neri-Ornates S (2008) Boophilus microplus pyrethroid resistance associated to increased levels of monooxygenase enzymatic activity in field isolated Mexican ticks. J Biol Sci 8:404–409Google Scholar
  27. Crampton AL, Green P, Baxter GD, Barker SC (1999) Monooxygenase play only a minor role in resistance to synthetic pyrethroids in the cattle tick, Boophilus microplus. Exp Appl Acarol 23:897–905Google Scholar
  28. Cully DF, Vassilatis DK, Liu KK, Paress PS, Van Der Ploeg LHT, Schaeffer JM, Arena JP (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channels from Caenorhabditis elegans. Nature 371:707–711Google Scholar
  29. Cuore U, Trelles A, Sanchís J, Gayo V, Solari MA (2007) Primer diagnostic de resistencia al Fipronil en la garrapata común del Ganado Boophilus microplus. Veterinaria (Montevideo) 42:35–41Google Scholar
  30. Currie BJ, Harumal P, McKinnon M, Walton SF (2004) First documentation of in vivo and in vitro ivermectin resistance in Sarcoptes scabiei. Clin Infect Dis 39:8–12Google Scholar
  31. Curtis RJ (1985) Amitraz in the control of non-ixodidae ectoparasites of livestock. Vet Parasitol 18:251–264Google Scholar
  32. da Silva Vaz I Jr, Torino Lermen TT, Michelon A, Sanchez Ferreira CA, Joaquim de Freitas DR, Termignoni C, Masuda A (2004) Effect of acaricides on the activity of a Boophilus microplus glutathione S-transferase. Vet Parasitol 119:237–245Google Scholar
  33. de la Fuente J, Almazan C, Canales M, Perez de la Lastra JM, Kocan KM, Willadsen P (2007) A ten-year review of commercial vaccine performance for control of tick infestations on cattle. Anim Heal Res Rev 8:23–28Google Scholar
  34. Dent JA, Smith MM, Vassilatis DK, Avery L (2000) The genetics of ivermectin resistance in Caenorhabditis elegans. Proc Natl Acad Sci USA 97:2674–2679Google Scholar
  35. Drummond RO, Ernst SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and Boophilus microplus: laboratory test of insecticides. J Econ Entomol 66:130–133Google Scholar
  36. Ducornez S, Barre N, Miller R, De Garine-Wichatitsky M (2005) Diagnosis of amitraz resistance in Boophilus microplus in New Caledonia with the modified larval packet test. Vet Parasitol 130:285–292Google Scholar
  37. Elfassy OJ, Goodman FW, Levy SA, Carter LL (2001) Efficacy of an amitraz-impregnated collar in preventing transmission of Borrelia burgdorferi by adult Ixodes scapularis to dogs. J Am Vet Med Assoc 219:185–189Google Scholar
  38. Enayati AA, Haghi FM (2007) Biochemistry of pyrethroid resistance in German cockroach (Dictyopters, Blatellidae) from Hospitals of Sari, Iran. Iran Biomed J 11:251–258Google Scholar
  39. Evans PD, Gee JD (1980) Action of formamidine pesticides on octopamine receptors. Nature 287:60–62Google Scholar
  40. Evans PD, Maqueira B (2005) Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invertebr Neurosci 5:111–118Google Scholar
  41. Faza AP, Pinto ISB, Fonseca I, Antunes GR, de Oliveira Monteiro CM, Daemon E, de Souza Muniz M, Martins MF, Furlong J, de Azevedo Prata MC (2013) A new approach to characterization of the resistance of populations of Rhipicephalus microplus (Acari: Ixodidae) to organophosphate and pyrethroid in the state of Minas Gerais, Brazil. Exp Parasitol 134:519–523Google Scholar
  42. Floris I, Satta A, Garau VL, Melis M, Cabras P, Aloul N (2001) Effectiveness, persistence, and residue of amitraz plastic strips in the apiary control of Varroa destructor. Apidologie 32:577–585Google Scholar
  43. Fournier D, Mutero A (1994) Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comp Biochem Physiol 108C:19–31Google Scholar
  44. Fox LM (2006) Ivermectin: uses and impact 20 years on. Curr Opin Infect Dis 19:588–593Google Scholar
  45. Fragoso-Sanchez H, Garcia-Vazquez Z, Tapia-Perez A, Ortiz-Najera A, Rosario-Cruz R, Rodriguez-Vivas I (2011) Response of Mexican Rhipicephalus (Boophilus) microplus ticks to selection by amitraz and genetic analysis of attained resistance. J Entomol 8:218–228Google Scholar
  46. Fukoto TR (1990) Mechanism of action of organophosphorous and carbamate insecticides. Environ Health Perspect 87:245–254Google Scholar
  47. Garris GI, George JE (1985) Field evaluation of amitraz applied to cattle as sprays for control of Boophilus microplus (Acari:Ixodidae) in the eradication program in Puerto Rico. Prev Vet Med 3:363–369Google Scholar
  48. George JE, Pound JM, Davey RB (2004) Chemical control of ticks on cattle and the resistance of these parasites to acaricides. Parasitol 129:S353–S366Google Scholar
  49. Ghosh S, Azhahianambi P, Furente JDL (2006) Control of ticks of ruminants, with special emphasis on livestock farming systems in India: present and future possibilities for integrated control-a review. Exp Appl Acarol 46:49–66Google Scholar
  50. Ghosh S, Azhahianambi P, Yadav MP (2007) Upcoming and future strategies of tick control: a review. J Vector Borne Dis 44:79–89Google Scholar
  51. Ghosh S, Kumar R, Nagar G, Kumar S, Sharma AK, Srivastava A, Kumar S, Ajith Kumar KG, Saravanan BC (2015) Survey of acaricides resistance status of Rhipiciphalus (Boophilus) microplus collected from selected places of Bihar, an eastern state of India. Ticks Tick-Borne Dis 6:668–675Google Scholar
  52. Goff GL, Hamon A, Berge JB, Amichot M (2005) Resistance to fipronil in Drosophila simulans: influence of two point mutations in the RDL GABA receptor subunit. J Neurochem 92:1295–1301Google Scholar
  53. Guerrero FD, Davey RB, Miller RJ (2001) Use of an allele-specific polymerase chain reaction assay to genotype pyrethroid resistant strains of Boophilus microplus (Acari: Ixodidae). J Med Entomol 38:44–50Google Scholar
  54. Guerrero FD, Li AY, Hernandez R (2002) Molecular diagnosis of pyrethroid resistance in Mexican strains of Boophilus microplus (Acari: Ixodidae). J Med Entomol 39:770–776Google Scholar
  55. Guerrero FD, Bendele KG, Chen AC, Li AY, Miller RJ, Pleasance E (2007) Serial analysis of gene expression in the southern cattle tick following acaricide treatment of larvae from organophosphate resistant and susceptible strains. Insect Biochem Mol Bio 16:49–60Google Scholar
  56. Guerrero FD, Lovis L, Martins JR (2012) Acaricide resistance mechanisms in Rhipicephalus (Boophilus) microplus. Rev Bras Parasitol Vet 21:1–6Google Scholar
  57. Guglielmone AA, Volpogni MM, Mangold AJ, Anziani OS, Castelli MC (2000) Evaluacion de una formulacion comercial “pour on” con fipronil al 1% para el control de Haematobia irritans en vaquillonas Holando naturalmente infestadas. Veterinaria (Argentina) 17:108–113Google Scholar
  58. He H, Chen AC, Davey RB, Ivie GW, George JE (1999) Identification of a point mutation in the para-type voltage-gated sodium channel gene from a pyrethroid-resistant cattle tick. Biochem Biophys Res Commun 261:558–561Google Scholar
  59. Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Bio 34:653–665Google Scholar
  60. Hernandez R, He H, Chen AC, Waghela SD, Ivie GH, George JE, Wagner G (1999) Cloning and sequencing of a putative acetylcholinesterase cDNA from Boophilus microplus (Acari: Ixodidae). J Med Entomol 36:764–770Google Scholar
  61. Hernandez R, He H, Chen AC, Waghela SD, Ivie GW, George JE, Wagner GG (2000) Identification of a point mutation in an esterase gene in different populations of the southern cattle tick, Boophilus microplus. Insect Biochem Mol Biol 30:969–977Google Scholar
  62. Hernandez R, Guerrero FD, George JE, Wagner GG (2002) Allele frequency and gene expression of a putative carboxylesterase-encoding gene in a pyrethroid resistant strain of the tick, Boophilus microplus. Insect Biochem Mol Biol 32:1009–1016Google Scholar
  63. Hollingworth RM, Lund AE (1982) Biological and neurotoxic effect of amidine pesticides. In: Coats JR (ed) Insecticide mode of action, 1st edn. Academic, New York, pp 189–227Google Scholar
  64. Hope M, Menzies M, Kemp D (2010) Identification of a dieldrin resistance-associated mutation in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). J Econ Entomol 103:1355–1359Google Scholar
  65. Jamroz RC, Guerrero FD, Pruett JH, Oehler DD, Miller RJ (2000) Molecular and biochemical survey of acaricide resistance mechanisms in larvae from Mexican strains of the southern cattle tick, Boophilus microplus. J Insect Physiol 46:685–695Google Scholar
  66. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitol 129:S1–S12Google Scholar
  67. Jonsson NN, Mayer DG, Green PE (2000) Possible risk factors on Queensland dairy farms for acaricide resistance in cattle tick (Boophilus microplus). Vet Parasitol 88:79–92Google Scholar
  68. Jonsson NN, Cutulle C, Corley SW, Seddon JM (2010) Identification of a mutation in the para-voltage-gated sodium channel gene of the cattle tick Rhipicephalus microplus associated with resistance to flumethrin but not to cypermethrin. Int J Parasitol 40:1659–1664Google Scholar
  69. Jonsson NN, Klafke G, Corley SW, Tidwell J, Berry CM, Koh-Tan HHC (2018) Molecular biology of amitraz resistance in cattle ticks of the genus Rhipicephalus. Front Biosci (Landmark Ed) 23:796–810Google Scholar
  70. Jyoti Singh NK, Singh H, Singh NK, Rath SS (2016) Multiple mutations in the acetylcholinesterase 3 gene associated with organophosphate resistance in Rhipicephalus (Boophilus) microplus ticks from Punjab, India. Vet Parasitol 216:108–117Google Scholar
  71. Kagaruki LK (1996) The efficacy of amitraz against cattle ticks in Tanzania. Onderstepoort J Vet Res 63:91–96Google Scholar
  72. Kane NS, Hirschberg B, Qian S (2000) Drug-resistant Drosophila indicate glutamate-gated chloride channels are target for the antiparasitic nodulospuric acid and ivermectin. Proc Natl Acad Sci USA 97:13949–13954Google Scholar
  73. Kaplan RM (2004) Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20:477–481Google Scholar
  74. Klafke GM, Sabatini GA, de Albuquerque TA, Martins JR, Kemp DH, Miller RJ, Schumaker TT (2006) Larval immersion tests with ivermectin in populations of the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) from State of Sao Paulo, Brazil. Vet Parasitol 142:386–390Google Scholar
  75. Knowles CO, Roulston WJ (1972) Antagonism of chlorphenamidine toxicity to the cattle tick Boophilus microplus by piperonyl butoxide. J Aust Entomol Soc 11:349–350Google Scholar
  76. Kumar S, Jayakumar K, Srinivasan MR, Udupa V, Ramesh N (2001) Biological efficacy of amitraz against the three host tick Rhipicephalus sanguineus. Indian J Anim Sci 71:527–528Google Scholar
  77. Kumar R, Nagar G, Sharma AK, Kumar S, Ray DD, Chaudhuri P, Ghosh S (2013) Survey of pyrethroids resistance in Indian isolates of Rhipicephalus (Boophilus) microplus: identification of C190A mutation in the domain II of the para-voltage-gated sodium channel gene. Acta Trop 125:237–245Google Scholar
  78. Kunz SE, Kemp DH (1994) Insecticides and acaricides resistance and environmental impacts. Rev Sci Tech Off Int Epiz 13:1249–1286Google Scholar
  79. Kwon DH, Yoon KS, Clark JM, Lee SH (2010) A point mutation in a glutamate gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch. Insect Mol Biol 19:583–591Google Scholar
  80. Lara FA, Pohl PC, Gandara AC, Ferreira JDS, Nascimento-Silva MC, Bechara GH, Sorgine MHF, Almeida IC, Vaz ID, Oliveira PL (2015) ATP binding cassette transporter mediates both heme and pesticide detoxification in tick midgut cells. PLoS ONE 10:8Google Scholar
  81. Lawrence LJ, Casida JE (1983) Stereospecific action of pyrethroid insecticides on the γ-aminobutyric acid receptor-ionophore complex. Science 221:1399–1401Google Scholar
  82. Lees K, Bowman AS (2007) Tick neurobiology: recent advances and the post-genomic era. Invertebr Neurosci 7:183–198Google Scholar
  83. Lespine A, Alvinerie M, Vercruysse J, Prichard RK, Geldhof P (2008) ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics. Trends Parasitol 24:293–298Google Scholar
  84. Li AY, Davey RB, Miller RJ, George JE (2003) Resistance to coumaphos and diazinon in Boophilus microplus (Acari: Ixodidae) and evidence for the involvement of an oxidative. J Med Entomol 40:482–490Google Scholar
  85. Li AY, Davey RB, Miller RJ, George JE (2004) Detection and characterization of amitraz resistance in the southern cattle tick, Boophilus microplus (Acari: Ixodidae). J Med Entomol 41:193–200Google Scholar
  86. Li AY, Davey RB, George JE (2005a) Carbaryl resistance in Mexican strains of the southern cattle tick (Acari: Ixodidae). J Econ Entomol 98(2):552–556Google Scholar
  87. Li AY, Davey RB, Miller RJ, George JE (2005b) Mode of inheritance of amitraz resistance in a Brazilian strain of the southern cattle tick, Boophilus microplus (acari: Ixodidae). Exp Appl Acarol 37:183–198Google Scholar
  88. Li AY, Chen AC, Davey RB, Miller RJ, George JE (2007a) Acaricide resistance and synergism between permethrin and amitraz against susceptible and resistant strains of Boophilus microplus (Acari, Ixodidae). Pest Manag Sci 63:882–889Google Scholar
  89. Li X, Huang Q, Yuan J, Tang Z (2007b) Fipronil resistance mechanisms in the rice stem borer, Chilo suppressalis Walker. Pestic Biochem Physiol 89:169–174Google Scholar
  90. Lovis L, Perret JL, Bouvier J, Fellay JM, Kaminsky R, Betschart B, Sager H (2011) A new in vitro test to evaluate the resistance level against acaricides of the cattle tick, Rhipicephalus (Boophilus) microplus. Vet Parasitol 182:269–280Google Scholar
  91. Lovis L, Guerrero FD, Miller RJ, Bodine DM, Betschart B, Sager H (2012) Distribution pattern of three sodium channel mutations associated with pyrethroid resistance in Rhipicephalus (Boophilus) microplus populations from North and South America, South Africa and Australia. Int J Parasitol: Drug Drug Resist 2:216–224Google Scholar
  92. Lynen G, Zeman P, Bakuname C, Di Giulio G, Mtui P, Sanka P, Jongejan F (2007) Cattle ticks of the genera Rhipicephalus and Amblyomma of economic importance in Tanzania: distribution assessed with GIS based on an extensive field survey. Exp Appl Acarol 43:303–319Google Scholar
  93. Madder M, Thys E, Achi L, Toure A, De Deken R (2011) Rhipicephalus (Boophilus) microplus: a most successful invasive tick species in West-Africa. Exp Appl Acarol 53:139–145Google Scholar
  94. Martins JR, Furlong J (2001) Avermectin resistance of the cattle tick Boophilus microplus Brazil. Vet Rec 149:64Google Scholar
  95. McCavera S, Rogers AT, Yates DM, Woods DJ, Wolstenholme AJ (2009) An ivermectin-sensitive glutamate-gated chloride channel from the parasitic nematode Haemonchus contortus. Mol Pharmacol 75:1347–1355Google Scholar
  96. Mendes MC, Lima CK, Nogueira AH, Yoshihara E, Chiebao DP, Gabriel FH, Namindome Ueno TE, Klafke GM (2011) Resistance to cypermethrin, deltamethrin and chlorpyriphos in populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) from small farms of the State of São Paulo, Brazil. Vet Parasitol 178:383–388Google Scholar
  97. Mendes MC, Duarte FC, Martins JR, Klafke GM, Fiorini LC, de Barros ATM (2013) Characterization of the pyrethroid resistance profile of Rhipicephalus (Boophilus) microplus populations from the states of Rio Grande do Sul and Mato Grosso do Sul, Brazil. Rev Bras Parasitol Vet 22:379–384Google Scholar
  98. Miller RJ, Davey RB, George JE (1999) Characterization of pyrethroid resistance and susceptibility to coumaphos in Mexican Boophilus microplus (Acari: Ixodidae). J Med Entomol 36:533–538Google Scholar
  99. Miller RJ, Almazan C, Ortiz-Estrada M, Davey RB, George JE, De Leon AP (2013) First report of fipronil resistance in Rhipicephalus (Boophilus) microplus of Mexico. Vet Parasitol 191:97–101Google Scholar
  100. MingZhang C, JinLiang S, JinZhen Z, Mei L, XiaioYu L, WeiJun Z (2004) Monitoring of insecticide resistance and inheritance analysis of triazophos resistance in the striped stem borer (Lepidoptera:Pyralidae). Chin J Rice Sci 18:73–79Google Scholar
  101. Morgan JAT, Corley SW, Jackson LA, Lew-Tabor AE, Moolhuijzen PM, Jonsson NN (2009) Identification of a mutation in the para-voltage-gated sodium channel gene of the cattle tick Rhipicephalus (Boophilus) microplus associated with resistance to synthetic pyrethroid acaricides. Int J Parasitol 39:775–779Google Scholar
  102. Nagar G, Sharma AK, Chigure G, Manjunathachar HV, Saravanan BC, Rai A, Ghosh S (2016) Identification of mutations in acetylcholinesterase 2 gene of acaricide resistant isolates of Rhipicephalus (Boophilus) microplus. Int J Sci Environ Technol 5:3440–3447Google Scholar
  103. Nakao T, Naoi A, Kawahara N, Hirase K (2010) Mutation of the GABA receptor associated with fipronil resistance in the whitebacked planthopper, Sogatella furcifera. Pestic Biochem Physiol 97:262–266Google Scholar
  104. Nolan J (1987) New approaches in the development and management of drugs used in ectoparasite control. Vet Parasitol 25:135–145Google Scholar
  105. Nolan J, Roulston WJ, Wharton RH (1977) Resistance to synthetic pyrethroids in a DDT resistant strain of Boophilus microplus. Aust Vet J 66:179–182Google Scholar
  106. Nyangiwe N, Harrison A, Horak IG (2013) Displacement of Rhipicephalus decoloratus by Rhipicephalus microplus (Acari: Ixodidae) in the Eastern Cape Province, South Africa. Exp Appl Acarol 61:371–382Google Scholar
  107. Perez-Cogollo LC, Rodriguez-Vivas RI, Ramirez-Cruz GT, Miller RJ (2010) First report of the cattle tick Rhipicephalus microplus resistant to ivermectin in Mexico. Vet Parasitol 168:165–169Google Scholar
  108. Pohl PC, Klafke GM, Júnior JR, Martins JR, da Silva Vaz I Jr, Masuda A (2012) ABC transporters as a multidrug detoxification mechanism in Rhipicephalus (Boophilus) microplus. Parasitol Res 111:2345–2351Google Scholar
  109. Pound JM, Miller JA, George JE (2000) Efficacy of amitraz applied to white-tailed deer by the O4-posterolateral topical treatment device in controlling free-living long star ticks (Acari: Ixodidae). J Med Entomol 37:878–884Google Scholar
  110. Pruett JH, Guerrero FD, Hernandez R (2002) Isolation and identification of an esterase from a Mexican strain of Boophilus microplus (Acari: Ixodidae). J Econ Entomol 95:1001–1007Google Scholar
  111. Robbertse L, Baron S, van der Merwe NA, Madder M, Stoltsz WH, Maritz-Olivier C (2016) Genetic diversity, acaricide resistance status and evolutionary potential of a Rhipicephalus microplus population from a disease-controlled cattle farming area in South Africa. Ticks Tick Borne Dis 7:595–603Google Scholar
  112. Rodriguez-Vivas RI, Alonso-Diaz MA, Rodriguez-Arevalo F, Fragoso-Sanchez H, Santamaria VM, Rosario-Cruz R (2006a) Prevalence and potential risk factors for organophosphate and pyrethroid resistance in Boophilus microplus ticks on cattle ranches from the State of Yucatan, Mexico. Vet Parasitol 136:242–335Google Scholar
  113. Rodriguez-Vivas RI, Rodriguez-Arevalo F, Alonso-Diaz MA, Fragoso-Sanchez H, Santamaria VM, Rosario-Cruz R (2006b) Amitraz resistance in Boophilus microplus ticks in cattle farms from the state of Yucatan, Mexico, prevalence and potential risk factors. Prev Vet Med 75:280–286Google Scholar
  114. Rodriguez-Vivas RI, Trees AJ, Rosado-Aguilar JA, Villegas-Perez SL, Hodgkinson JE (2011) Evolution of acaricide resistance: phenotypic and genotypic changes in field populations of Rhipicephalus (Boophilus) microplus in response to pyrethroid selection pressure. Int J Parasitol 41:895–903Google Scholar
  115. Rodriguez-Vivas RI, Perez-Cogollo LC, Rosado-Aguilar JA, Ojeda-Chi MM, Trinidad-Martinez I, Miller RJ, Li AY, Perez de Leon AA, Guerrero FD, Klafke GM (2014a) Rhipicephalus microplus resistant to acaricides and ivermectin in cattle farms of Mexico. Braz J Vet Parasitol 23:113–122Google Scholar
  116. Rodriguez-Vivas RI, Perez-Cogollo LC, Rosado-Aguilar JA, Ojeda-Chi MM, Trinidad-Martinez I, Miller RJ, Li AY, Perez de Leon AA, Guerrero FD, Klafke GM (2014b) Rhipicephalus microplus resistant to acaricides and ivermectin in cattle farms of Mexico. Braz J Vet Parasitol 23:113–122Google Scholar
  117. Rodriguez-Vivas RI, Jonsson NN, Bhusan C (2018) Strategies for the control of Rhipicephalus microplus ticks in a world of conventional acaricide and macrocyclic lactone resistance. Parasitol Res 117:3–29Google Scholar
  118. Rosario-Cruz R, Guerrero FD, Miller RJ, Rodriguez-Vivas RI, Dominguez-Garcia DI, Cornel AJ, Hernandez-Ortiz R, George JE (2005) Roles played by esterase activity and by a sodium channel mutation involved in pyrethroid resistance in populations of Boophilus microplus (Acari: Ixodidae) collected from Yucatan, Mexico. J Med Entomol 42:1020–1025Google Scholar
  119. Rosario-Cruz R, Guerrero FD, Miller RJ, Rodriguez-Vivas RI, Tijerina M, Dominguez-Garcia DI, Hernandez-Ortiz R, Cornel AJ, McAbee RD, Alonso- Diaz MA (2009) Molecular survey of pyrethroid resistance mechanisms in Mexican field populations of Rhipicephalus (Boophilus) microplus. Parasitol Res 105:1145–1153Google Scholar
  120. Rugg D, Kotze AC, Thompson DR, Rose HA (1998) Susceptibility of laboratory-selected and field strains of the Lucilia cuprina (Diptera: Calliphoridae) to ivermectin. J Econ Entomol 91:601–607Google Scholar
  121. Sabatini GA, Kemp DH, Hughes S, Nari A, Hansen J (2001) Tests to determine LC50 and discriminating doses for macrocyclic lactones against the cattle tick, Boophilus microplus. Vet Parasitol 95:53–62Google Scholar
  122. Saldivar L, Guerrero FD, Miller RJ, Bendele KG, Gondro C, Brayton KA (2008) Microarray analysis of acaricide- inducible gene expression in the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Mol Biol 17:597–606Google Scholar
  123. Schnitzerling HJ, Nolan J, Hughes S (1983) Toxicology and metabolism of some synthetic pyrethroids in larvae of susceptible and resistant strains of the cattle tick Boophilus microplus (Can.). Pestic Sci 14:64–72Google Scholar
  124. Shaw RD (1966) Culture of an organophosphorus-resistant strain of Boophilus microplus (Can.) and an assessment of its resistance spectrum. Bull Ent Res 56:389–405Google Scholar
  125. Soberanes MJ, Santamaria VM, Fragoso SH, Gracia ZV (2002) First case reported of amitraz resistance in the cattle tick Boohilus microplus in Mexico. Tec Pecu Mex 40:81–92Google Scholar
  126. Solorio RJ, Rodriguez VRI, Perez GE, Wagner G (1999) Management factors associated with Babesis bovis seropravelance in cattle from eastern Yucatan. Prev Vet Med 40:261–269Google Scholar
  127. Stone BF, Haydock P (1962) A method for measuring the acaricides susceptibility of the cattle tick Boophilus microplus (Can.). Bull Entomol Res 53:563–578Google Scholar
  128. Stone NE, Olafson PO, 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 paravoltage-gated sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico. Parasit Vectors 7:456Google Scholar
  129. Sungirai M, Baron S, Moyo DZ, Clercqe PD, Maritz-oliver C, Maddar M (2018) Genotyping acaricide resistance profiles of Rhipicephalus microplus tick populations from communal land areas of Zimbabwe. Ticks Tick Borne Dis 9:2–9Google Scholar
  130. Temeyer KB, Davey RB, Chen AC (2004) Identification of a third Boophilus microplus (Acari: Ixodidae) cDNA presumptively encoding an acetylcholinesterase. J Med Entomol 41:259–268Google Scholar
  131. Temeyer KB, Pruett JH, Olafson PU, Chen AC (2007) R86Q, a mutation in BmAChE3 yielding a Rhipicephalus microplus organophosphate insensitive acetylcholinesterase. J Med Entomol 44:1013–1018Google Scholar
  132. Temeyer KB, Olafson PU, Miller RJ (2009) Genotyping mutations in BmAChE3: a survey of organophosphate-resistant and -susceptible strains of Rhipicephalus (Boophilus) microplus. J Med Entomol 46:1355–1360Google Scholar
  133. Temeyer KB, Pruett JH, Olafson PU (2010) Baculovirus expression, biochemical characterization and organophosphate sensitivity of rBmAChE1, rBmAChE2, and rBmAChE3 of Rhipicephalus (Boophilus) microplus. Vet Parasitol 172:114–121Google Scholar
  134. Temeyer KB, Olafson PU, Brake DK, Tuckow AP, Li AY, Perez de Leon AA (2013) Acetylcholinesterase of Rhipicephalus (Boophilus) microplus and Phlebotomus papatasi: gene identification, expression, and biochemical properties of recombinant proteins. Pestic Biochem Physiol 106:118–123Google Scholar
  135. Tonnensen BLP, Bryson NR, Stoltsz WH, Masibigiri TMH (2004) Displacement of Boophilus decoloratus by Boophilus microplus in the Soutpansberg region, Limpopo Province, South Africa. Exp Appl Acarol 32:199–208Google Scholar
  136. Townson S, Tagboto SK, Castro J, Lujan A, Awadzi K, Titanji VP (1994) Comparison of the sensitivity of different geographical races of Onchocerca volvulus microfilariae to ivermectin: studies in vitro. Trans R Soc Trop Med Hyg 88:101–106Google Scholar
  137. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanism in the two spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572Google Scholar
  138. Veiga LP, Souza AP, Bellato V, Sartor AA, Nunes AP, Cardoso HM (2012) Resistance to cypermethrin and amitraz in Rhipicephalus (Boophilus) microplus on the Santa Catarina Plateau, Brazil. Rev Bras Parasitol Vet 21:133–136Google Scholar
  139. Villatte F, Ziliani P, Marcel V, Menozzi P, Fournier D (2000) A high number of mutations in insect acetylcholinesterase may provide insecticide resistance. Pest Biochem Physiol 67:95–102Google Scholar
  140. Vontas JG, Enayati AA, Small GJ, Hemingway J (2000) A simple biochemical assay for glutathione S-transferase activity and its possible field application for screening glutathione S-transferasebased insecticide resistance. Pest Biochem Physiol 68:184–192Google Scholar
  141. White WH, Plummer PR, Kemper CJ, Miller RJ, Davey RB, Kemp DH, Hughes S, Smith CK II, Gutierrez JA (2004) An in vitro larval immersion microassay for identifying and characterizing candidate acaricides. J Med Entomol 41:1034–1042Google Scholar
  142. Wolstenholme AJ, Rogers AT (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131:S85–S95Google Scholar
  143. World Health Organization (WHO) (2012) Global plan for insecticide resistance management in malaria vectors (GPIRM). WHO, GenevaGoogle Scholar
  144. Yessinoua RE, Akpo Y, Sidick A, Adoligbea C, Karima IYA, Akogbetob M, Farougoua S (2018) Evidence of multiple mechanisms of alpha-cypermethrin and deltamethrin resistance in ticks Rhipicephalus microplus in Benin, West Africa. Ticks Ticks Borne Dis 9:665–671Google Scholar
  145. Zhu KY, Lee SH, Clark JM (1996) A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pest Biochem Physiol 55:100–108Google Scholar

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Authors and Affiliations

  1. 1.College of Veterinary Science and Animal HusbandryRewaIndia

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