1932

Abstract

The voltage-sensitive sodium channel (VSSC) is a critical component of the insect nervous system. Pyrethroids and DDT are insecticides that have been widely used, and they kill insects by perturbations of the VSSC. Decades of insecticide use selected for mutations in that give rise to resistance in almost all pest insects. However, the mutations responsible for the resistance are not always the same, and some unusual patterns have emerged. This review focuses on what pyrethroid/DDT selection has done, in terms of changes that have occurred, using four well-studied species as examples of the differences that have evolved. Information is provided about the mutations that occur, potential pathways by which alleles with multiple mutations arose, the relative fitness of the alleles, the levels of resistance conferred, and the geographic distribution of the mutations. The lessons learned and exciting new areas of research are discussed.

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2019-01-07
2024-06-18
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Literature Cited

  1. 1.  Alvarez-Gonzalez LC, Briceño A, Ponce-Garcia G, Villanueva-Segura OK, Davila-Barboza JA et al. 2017. Assessing the effect of selection with deltamethrin on biological parameters and detoxifying enzymes in Aedes aegypti (L.). Pest Manag. Sci. 73:2287–93
    [Google Scholar]
  2. 2.  Anstead JA, Williamson MS, Denholm I 2005. Evidence for multiple origins of identical insecticide resistance mutations in the aphid Myzus persicae. Insect Biochem. Mol. Biol 35:249–56
    [Google Scholar]
  3. 3.  Argentine JA, Clark JM, Ferro DN 1989. Genetics and synergism of resistance to azinphosmethyl and permethrin in the Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 82:698–705
    [Google Scholar]
  4. 4.  Argentine JA, Lee SH, Sos MA, Barry SR, Clark JM 1995. Permethrin resistance in a near isogenic strain of Colorado potato beetle. Pestic. Biochem. Physiol. 53:97–115
    [Google Scholar]
  5. 5.  Bourguet D, Guillemaud T, Chevillon C, Raymond M 2004. Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution 58:128–35
    [Google Scholar]
  6. 6.  Brito L, Linss J, Lima-Camara T, Belinato T, Peixoto A et al. 2013. Assessing the effects of Aedes aegypti kdr mutations on pyrethroid resistance and its fitness cost. PLOS ONE 8:e60878
    [Google Scholar]
  7. 7.  Brown AWA 1958. The spread of insecticide resistance in pest species. In Advances in Pest Control Research 2 RL Metcalf 351–414 London: Intersci. Publ.
    [Google Scholar]
  8. 8.  Brown AWA, Pal R 1971. Insecticide Resistance in Arthropods Geneva, Switz: World Health Org.
    [Google Scholar]
  9. 9.  Burton MJ, Mellor IR, Duce IR, Davies TGE, Field LM, Williamson MS 2011. Differential resistance of insect sodium channels with kdr mutations to deltamethrin, permethrin and DDT. Insect Biochem. Mol. Biol. 41:723–32
    [Google Scholar]
  10. 10.  Busvine JR 1951. Mechanism of resistance to insecticide in houseflies. Nature 168:193–95
    [Google Scholar]
  11. 11.  Cao XM, Song FL, Zhao TY, Dong YD, Sun CX, Lu BL 2006. Survey of deltamethrin resistance in house flies (Musca domestica) from urban garbage dumps in northern China. Environ. Entomol. 35:1–9
    [Google Scholar]
  12. 12.  Dennehy TJ, Granett J, Leigh TF 1983. Relevance of slide-dip and residual bioassay comparisons to detection of resistance in spider mites. J. Econ. Entomol. 76:1225–30
    [Google Scholar]
  13. 13.  Dong K 2007. Insect sodium channels and insecticide resistance. Invertebr. Neurosci. 7:17–30
    [Google Scholar]
  14. 14.  Dong K, Du Y, Rinkevich F, Nomura Y, Xu P et al. 2014. Molecular biology of insect sodium channels and pyrethroid resistance. Insect Biochem. Mol. Biol. 50:1–17
    [Google Scholar]
  15. 15.  Douris V, Papapostolou K-M, Ilias A, Roditakis E, Kounadi S et al. 2017. Investigation of the contribution of RyR target-site mutations in diamide resistance by CRISPR/Cas9 genome modification in Drosophila. Insect Biochem. Mol. Biol 87:127–35
    [Google Scholar]
  16. 16.  Du Y, Nomura Y, Satar G, Hu Z, Nauen R et al. 2013. Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel. PNAS 110:11785–90
    [Google Scholar]
  17. 17.  Du Y, Nomura Y, Zhorov B, Dong K 2016. Sodium channel mutations and pyrethroid resistance in Aedes aegypti. Insects 7:60
    [Google Scholar]
  18. 18.  Deleted in proof
  19. 19.  Duneau D, Sun H, Revah J, San Miguel K, Kunerth HD et al. 2018. Signatures of insecticide selection in the genome of Drosophila melanogaster. G3 In press. https://doi.org/10.1534/g3.118.200537
    [Crossref] [Google Scholar]
  20. 20.  Farnham AW 1973. Genetics of resistance of pyrethroid-selected houseflies, Musca domestica L. Pestic. Sci. 4:513–20
    [Google Scholar]
  21. 21.  Farnham AW 1977. Genetics of resistance of houseflies (Musca domestica L.) to pyrethroids. Pestic. Sci. 8:631–36
    [Google Scholar]
  22. 22.  ffrench-Constant RH, Roush RT, Mortlock D, Dively GP 1990. Isolation of dieldrin resistance from field populations of Drosophila melanogaster (Diptera: Drosophilidae). J. Econ. Entomol. 83:1733–37
    [Google Scholar]
  23. 23.  Georghiou GP 1972. The evolution of resistance to pesticides. Annu. Rev. Ecol. System. 3:133–68
    [Google Scholar]
  24. 24.  Grenier JK, Arguello JR, Moreira MC, Gottipati S, Mohammed J et al. 2015. Global Diversity Lines—a five-continent reference panel of sequenced Drosophila melanogaster strains. G3 5:593–603
    [Google Scholar]
  25. 25.  Haddi K, Tomé HVV, Du Y, Valbon WR, Nomura Y et al. 2017. Detection of a new pyrethroid resistance mutation (V410L) in the sodium channel of Aedes aegypti: a potential challenge for mosquito control. Sci. Rep. 7:46549
    [Google Scholar]
  26. 25a.  Hanai D, Yoshimizu MH, Scott JG 2018. The insecticide resistance allele kdr-his has a fitness cost in the absence of insecticide exposure. J. Econ. Entomol. In press. https://doi.org/10.1093/jee/toy300
    [Crossref] [Google Scholar]
  27. 26.  Hardstone MC, Lazzaro BP, Scott JG 2009. The effect of three environmental conditions on the fitness of cytochrome P450 monooxygenase-mediated permethrin resistance in Culex pipiens quinquefasciatus. BMC Evol. Biol 9:42
    [Google Scholar]
  28. 27.  Harris AF, Rajatileka S, Ranson H 2010. Pyrethroid resistance in Aedes aegypti from Grand Cayman. Am. J. Trop. Med. Hyg. 83:277–84
    [Google Scholar]
  29. 28.  Hawthorne DJ 2001. AFLP-based genetic linkage map of the Colorado potato beetle Leptinotarsa decemlineata: sex chromosomes and a pyrethroid-resistance candidate gene. Genetics 158:695–700
    [Google Scholar]
  30. 29.  Heim DC, Kennedy GG, Gould FL, Van Duyn JW 1992. Inheritance of fenvalerate and carbofuran resistance in Colorado beetles—Leptinotarsa decemlineata (Say)—from North Carolina. Pestic. Sci. 34:303–11
    [Google Scholar]
  31. 30.  Hirata K, Komagata O, Itokawa K, Yamamoto A, Tomita T, Kasai S 2014. A single crossing-over event in voltage-sensitive Na+ channel genes may cause critical failure of dengue mosquito control by insecticides. PLOS Negl. Trop. Dis. 8:e3085
    [Google Scholar]
  32. 31.  Hsiao TH, Hsiao C 1983. Chromosomal analysis of Leptinotarsa and Labidomera species (Coleoptera: Chrysomelidae). Genetica 60:139–50
    [Google Scholar]
  33. 32.  Huang J, Kristensen M, Qiao C, Jespersen JB 2004. Frequency of kdr gene in house fly field populations: correlation of pyrethroid resistance and kdr frequency. J. Econ. Entomol. 97:1036–41
    [Google Scholar]
  34. 33.  Jaramillo-O. N, Fonseca-González I, Chaverra-Rodrıguez D 2014. Geometric morphometrics of nine field isolates of Aedes aegypti with different resistance levels to lambda-cyhalothrin and relative fitness of one artificially selected for resistance. PLOS ONE 9:e96379
    [Google Scholar]
  35. 34.  Kasai S, Sun H, Scott JG 2017. Diversity of knockdown resistance alleles in a single house fly population facilitates adaptation to pyrethroid insecticides. Insect Mol. Biol. 26:13–24
    [Google Scholar]
  36. 35.  Kawada H, Higa Y, Futami K, Muranami Y, Kawashima E et al. 2016. Discovery of point mutations in the voltage-gated sodium channel from African Aedes aegypti populations: potential phylogenetic reasons for gene introgression. PLOS Negl. Trop. Dis. 10:e0004780
    [Google Scholar]
  37. 36.  Kim HJ, Hawthorne DJ, Peters T, Dively GP, Clark JM 2005. Application of DNA-based genotyping techniques for the detection of kdr-like pyrethroid resistance in field populations of Colorado potato beetle. Pestic. Biochem. Physiol. 81:85–96
    [Google Scholar]
  38. 37.  Knipple DC, Doyle KE, Marsella-Herrick PA, Soderlund DM 1994. Tight genetic linkage between the kdr insecticide resistance trait and a voltage-sensitive sodium channel gene in the house fly. PNAS 91:2483–87
    [Google Scholar]
  39. 38.  Kumar S, Thomas A, Samuel T, Sahgal A, Verma A, Pillai M 2009. Diminished reproductive fitness associated with the deltamethrin resistance in an Indian strain of dengue vector mosquito, Aedes aegypti L. Trop. Biomed. 26:155–64
    [Google Scholar]
  40. 39.  Lee SH, Dunn JB, Clark JM, Soderlund DM 1999. Molecular analysis of kdr-like resistance in a permethrin-resistant strain of Colorado potato beetle. Pestic. Biochem. Physiol. 63:63–75
    [Google Scholar]
  41. 40.  Lee SH, Smith TJ, Knipple DC, Soderlund DM 1999. Mutations in the house fly Vssc1 sodium channel gene associated with super-kdr resistance abolish the pyrethroid sensitivity of Vssc1/tipE sodium channels expressed in Xenopus oocytes. Insect Biochem. Mol. Biol. 29:185–94
    [Google Scholar]
  42. 41.  Lee SH, Yoon K-S, Williamson MS, Goodson SJ, Takano-Lee M et al. 2000. Molecular analysis of kdr-like resistance in permethrin-resistant strains of head lice. Pediculus capitis. Pestic. Biochem. Physiol. 66:130–43
    [Google Scholar]
  43. 42.  Lin W-H, Gunay C, Marley R, Prinz AA, Baines RA 2012. Activity-dependent alternative splicing increases persistent sodium current and promotes seizure. J. Neurosci. 32:7267–77
    [Google Scholar]
  44. 43.  Lin W-H, Wright DE, Muraro NI, Baines RA 2009. Alternative splicing in the voltage-gated sodium channel DmNav regulates activation, inactivation, and persistent current. J. Neurophys. 102:1994–2006
    [Google Scholar]
  45. 44.  Liu N, Pridgeon JW 2002. Metabolic detoxication and the kdr mutation in pyrethroid resistant house flies, Musca domestica (L.). Pestic. Biochem. Physiol. 73:157–63
    [Google Scholar]
  46. 45.  Liu N, Yue X 2000. Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J. Econ. Entomol. 93:1269–75
    [Google Scholar]
  47. 46.  Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482:173–78
    [Google Scholar]
  48. 47.  Martinez-Torres D, Foster SP, Field LM, Devonshire AL, Williamson MS 1999. A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Insect Mol. Biol. 8:339–46
    [Google Scholar]
  49. 48.  Mazzoni E, Chiesa O, Puggioni V, Pannini M, Manicardi GC, Bizzaro D 2015. Presence of kdr and s-kdr resistance in Musca domestica populations collected in Piacenza province (Northern Italy). Bull. Insectol. 68:65–72
    [Google Scholar]
  50. 49.  Milani R 1954. Comportamento mendeliano della resistenza alia azione abbattente del DDT e correlazione tra abbattimento e mortalita in Musca domestica L. Riv. Parasitol. 15:513–42
    [Google Scholar]
  51. 50.  Milani R, Travaglino A 1957. Ricerche genetiche sulla resistenza al DDT in Musca domestica concatenazione del gene kdr (knockdown-resistance) con due mutanti morfologigi. Riv. Parasitol. 18:199–202
    [Google Scholar]
  52. 51.  Miyazaki M, Ohyama K, Dunlap D, Matsumura F 1996. Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica). Mol. Gen. Genet. 252:61–68
    [Google Scholar]
  53. 52.  Olson RO, Liu Z, Nomura Y, Song W, Dong K 2008. Molecular and functional characterization of voltage-gated sodium channel variants from Drosophila melanogaster. Insect Biochem. Mol. Biol 38:604–10
    [Google Scholar]
  54. 53.  O'Reilly AO, Khambay BPS, Williamson MS, Field LA, Wallace BA, Davies TGE 2006. Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochem. J. 396:255–63
    [Google Scholar]
  55. 54.  O'Reilly AO, Williamson MS, Gonzalez-Cabrera J, Turberg A, Field LM et al. 2014. Predictive 3D modelling of the interactions of pyrethroids with the voltage-gated sodium channels of ticks and mites. Pest Manag. Sci. 70:369–77
    [Google Scholar]
  56. 55.  Pittendrigh B, Reenan R, ffrench-Constant RH, Ganetzky B 1997. Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides. Mol. Gen. Genet. 256:602–10
    [Google Scholar]
  57. 56.  Plernsub S, Stenhouse SA, Tippawangkosol P, Lumjuan N, Yanola J et al. 2013. Relative developmental and reproductive fitness associated with F1534C homozygous knockdown resistant gene in Aedes aegypti from Thailand. Trop. Biomed. 30:621–30
    [Google Scholar]
  58. 57.  Qiu X, Li M, Luo H, Fu T 2007. Molecular analysis of resistance in a deltamethrin-resistant strain of Musca domestica from China. Pestic. Biochem. Physiol. 89:146–50
    [Google Scholar]
  59. 58.  Rinkevich FD, Du Y, Tolinski J, Ueda A, Wu C-F et al. 2015. Distinct roles of the DmNav and DSC1 channels in the action of DDT and pyrethroids. Neurotox 47:99–106
    [Google Scholar]
  60. 59.  Rinkevich FD, Hamm RL, Geden CJ, Scott JG 2007. Dynamics of insecticide resistance alleles in two different climates over an entire field season. Insect Biochem. Mol. Biol. 37:550–58
    [Google Scholar]
  61. 60.  Rinkevich FD, Hedtke SM, Leichter CA, Harris SA, Su C et al. 2012. Multiple origins of kdr-type resistance in the house fly. Musca domestica. PLOS ONE 7:e52761
    [Google Scholar]
  62. 61.  Rinkevich FD, Leichter CA, Lazo TA, Hardstone MC, Scott JG 2013. Variable fitness costs for pyrethroid resistance alleles in the house fly, Musca domestica, in the absence of insecticide pressure. Pestic. Biochem. Physiol. 105:161–68
    [Google Scholar]
  63. 62.  Rinkevich FD, Su C, Lazo TA, Hawthorne DJ, Tingey WM et al. 2012. Multiple evolutionary origins of knockdown resistance (kdr) in pyrethroid-resistant Colorado potato beetle. Leptinotarsa decemlineata. Pestic. Biochem. Physiol. 104:192–200
    [Google Scholar]
  64. 63.  Rinkevich FD, Zhang L, Hamm RL, Brady SG, Lazzaro BP, Scott JG 2006. Frequencies of the pyrethroid resistance alleles of Vssc1 and CYP6D1 in house flies from the eastern United States. Insect Mol. Biol. 15:157–67
    [Google Scholar]
  65. 64.  Saavedra-Rodriguez K, Maloof CL, Campbell J, Garcia-Rejon A, Lenhart P et al. 2018. Parallel evolution of vgsc mutations at domains IS6, IIS6 and IIIS6 in pyrethroid resistant Aedes aegypti from Mexico. Sci. Rep. 8:6747
    [Google Scholar]
  66. 65.  Saavedra-Rodriguez K, Strode C, Suarez A, Salas I, Ranson H et al. 2008. Quantitative trait loci mapping of genome regions controlling permethrin resistance in the mosquito Aedes aegypti. Genetics 180:1137–52
    [Google Scholar]
  67. 66.  Sawicki RM 1978. Unusual response of DDT-resistant houseflies to carbinol analogues of DDT. Nature 275:443–44
    [Google Scholar]
  68. 67.  Schmidt JM, Battlay P, Gledhill-Smith RS, Good RT, Lumb C et al. 2017. Insights into DDT resistance from the Drosophila melanogaster genetic reference panel. Genetics 207:1181–93
    [Google Scholar]
  69. 68.  Scott JG, Dong K 1994. kdr-Type resistance in insects with special reference to the German cockroach, Blattella germanica. Comp. Biochem. Physiol. B 109:191–98
    [Google Scholar]
  70. 69.  Scott JG, Leichter CA, Rinkevich FD, Harris SA, Su C et al. 2013. Insecticide resistance in house flies from the United States: resistance levels and frequency of pyrethroid resistance alleles. Pestic. Biochem. Physiol. 107:377–84
    [Google Scholar]
  71. 70.  Scott JG, Ramaswamy SB, Matsumura F, Tanaka K 1986. Effect of method of application on resistance to pyrethroid insecticides in Blattella germanica (Orthoptera: Blattellidae). J. Econ. Entomol. 79:571–75
    [Google Scholar]
  72. 71.  Shono T, Kasai S, Kamiya E, Kono Y, Scott JG 2002. Genetics and mechanisms of permethrin resistance in the YPER strain of house fly. Pestic. Biochem. Physiol. 73:27–36
    [Google Scholar]
  73. 72.  Shono T, Zhang L, Scott JG 2004. Indoxacarb resistance in the house fly. Musca domestica. Pestic. Biochem. Physiol. 80:106–12
    [Google Scholar]
  74. 73.  Sidorenko AP, Berezovska OP 2002. Genetic structure of populations of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Russ. J. Genet. 38:1256–61
    [Google Scholar]
  75. 74.  Smith LB, Kasai S, Scott JG 2016. Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pestic. Biochem. Physiol. 133:1–12
    [Google Scholar]
  76. 75.  Smith LB, Kasai S, Scott JG 2018. Voltage-sensitive sodium channel mutations S989P + V1016G in Aedes aegypti confer variable resistance to pyrethroids, DDT and oxadiazines. Pest Manag. Sci. 74:737–45
    [Google Scholar]
  77. 76.  Soderlund D 2012. Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances. Arch. Toxicol. 86:165–81
    [Google Scholar]
  78. 77.  Sun H, Kasai S, Scott JG 2017. Two novel house fly Vssc mutations, D600N and T929I, give rise to new insecticide resistance alleles. Pestic. Biochem. Physiol. 143:116–21
    [Google Scholar]
  79. 78.  Sun H, Tong KP, Kasai S, Scott JG 2016. Overcoming super-kdr mediated resistance: Multi-halogenated benzyl pyrethroids are more toxic to super-kdr than kdr house flies. Insect Mol. Biol. 25:126–37
    [Google Scholar]
  80. 79.  Tan J, Liu Z, Tsai T-D, Valles SM, Goldin AL, Dong K 2002. Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin. Insect Biochem. Mol. Biol. 32:445–54
    [Google Scholar]
  81. 80.  Taskin V, Baskurt S, Dogac E, Taskin BG 2011. Frequencies of pyrethroid resistance-associated mutations of Vssc1 and CYP6D1 in field populations of Musca domestica L. in Turkey. J. Vector Ecol. 36:239–47
    [Google Scholar]
  82. 81.  Usherwood PNR, Vais H, Khambay BPS, Davies TGE, Williamson MS 2005. Sensitivity of the Drosophila para sodium channel to DDT is not lowered by the super-kdr mutation M918T on the IIS4–S5 linker that profoundly reduces sensitivity to permethrin and deltamethrin. FEBS Lett 579:6317–25
    [Google Scholar]
  83. 82.  Vais H, Atkinson S, Pluteanu F, Goodson SJ, Devonshire AL et al. 2003. Mutations of the para sodium channel of Drosophila melanogaster identify putative binding sites for pyrethroids. Mol. Pharmacol. 64:914–22
    [Google Scholar]
  84. 83.  Vais H, Williamson MS, Goodson SJ, Devonshire AL, Warmke JW et al. 2000. Activation of Drosophila sodium channels promotes modification by deltamethrin: reductions in affinity caused by knock-down resistance mutations. J. Gen. Physiol. 115:305–18
    [Google Scholar]
  85. 84.  Vera-Maloof FZ, Saavedra-Rodriguez K, Elizondo-Quiroga AE, Lozano-Fuentes S, Black WCI 2016. Coevolution of the Ile1,016 and Cys1,534 mutations in the voltage gated sodium channel gene of Aedes aegypti in Mexico. PLOS Negl. Trop. Dis. 9:e0004263
    [Google Scholar]
  86. 85.  von Stein R, Silver K, Soderlund D 2013. Indoxacarb, metaflumizone, and other sodium channel inhibitor insecticides: mechanism and site of action on mammalian voltage-gated sodium channels. Pestic. Biochem. Physiol. 106:101–12
    [Google Scholar]
  87. 86.  Wang Q, Li M, Pan J, Di M, Liu Q et al. 2012. Diversity and frequencies of genetic mutations involved in insecticide resistance in field populations of the house fly (Musca domestica L.) from China. Pestic. Biochem. Physiol. 102:153–59
    [Google Scholar]
  88. 87.  Williamson MS, Denholm I, Bell CA, Devonshire AL 1993. Knockdown resistance (kdr) to DDT and pyrethroid insecticides maps to a sodium channel gene locus in the housefly (Musca domestica). Mol. Gen. Genet. 240:17–22
    [Google Scholar]
  89. 88.  Williamson M, Martinez-Torres D, Hick C, Devonshire A 1996. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol. Gen. Genet. 252:51–60
    [Google Scholar]
  90. 89.  Wu S, Nomura Y, Du Y, Zhorov BS, Dong K 2017. Molecular basis of selective resistance of the bumblebee BiNav1 sodium channel to tau-fluvalinate. PNAS 114:12922–27
    [Google Scholar]
  91. 90.  Zichová T, Kocourek F, Salava J, Nad'ová K, Stará J 2010. Detection of organophosphate and pyrethroid resistance alleles in Czech Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) populations by molecular methods. Pest Man. Sci. 66:853–60
    [Google Scholar]
  92. 91.  Zuo Y, Wang H, Xu Y, Huang J, Wu S et al. 2017. CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides. Insect Biochem. Mol. Biol. 89:79–85
    [Google Scholar]
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