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Effects of Pesticides on the Environment and Insecticide Resistance

  • Gaelle Le GoffEmail author
  • Maeva Giraudo
Chapter

Abstract

The fight against pest insects has become a major challenge nowadays to eliminate disease vectors such as malaria, dengue fever or Zika virus, and to grow healthy crops to be able to feed a constantly increasing world population. Insecticides represent one of the main solutions to this challenge but with the introduction of every new insecticide comes inevitably the apparition of resistance a few years later. This chapter provides an overview of the evolution of the different insecticide families over time and their effects on the environment. Resistance mechanisms involving target modification and increased metabolism are detailed for each chemical family. The recent emergence of other resistance mechanisms such as the modification of insect cuticle permeability, the role of ABC transporters in xenobiotic excretion, and the involvement of symbionts are also discussed.

References

  1. Alon M, Alon F, Nauen R, Morin S (2008) Organophosphates’ resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase. Insect Biochem Mol Biol 38:940–949CrossRefPubMedGoogle Scholar
  2. Anderson JC, Dubetz C, Palace VP (2015) Neonicotinoids in the Canadian aquatic environment: a literature review on current use products with a focus on fate, exposure, and biological effects. Sci Total Environ 505:409–422CrossRefPubMedGoogle Scholar
  3. Anthony N, Unruh T, Ganser D, ffrench-Constant R (1998) Duplication of the Rdl GABA receptor subunit gene in an insecticide-resistant aphid, Myzus persicae. Mol Gen Genet 260:165–175CrossRefPubMedGoogle Scholar
  4. Apperson C, Georghiou GP (1975) Mechanisms of resistance to organophosphorous insecticides in Culex tarsalis. J Econ Entomol 68:153–157CrossRefPubMedGoogle Scholar
  5. Asih PB, Syahrani L, Rozi IE, Pratama NR, Marantina SS, Arsyad DS, Mangunwardoyo W, Hawley W, Laihad F, Shinta, Sukowati S, Lobo NF, Syafruddin D (2012) Existence of the rdl mutant alleles among the anopheles malaria vector in Indonesia. Malar J 11:57CrossRefPubMedPubMedCentralGoogle Scholar
  6. Assogba BS, Djogbenou LS, Milesi P, Berthomieu A, Perez J, Ayala D, Chandre F, Makoutode M, Labbe P, Weill M (2015) An ace-1 gene duplication resorbs the fitness cost associated with resistance in Anopheles gambiae, the main malaria mosquito. Sci Rep 5:14529CrossRefPubMedPubMedCentralGoogle Scholar
  7. Assogba BS, Milesi P, Djogbenou LS, Berthomieu A, Makoundou P, Baba-Moussa LS, Fiston-Lavier AS, Belkhir K, Labbe P, Weill M (2016) The ace-1 locus is amplified in all resistant Anopheles gambiae mosquitoes: fitness consequences of homogeneous and heterogeneous duplications. PLoS Biol 14:e2000618CrossRefPubMedPubMedCentralGoogle Scholar
  8. Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S, Sezutsu H, Kobayashi I, Uchino K, Tamura T, Mita K, Kadono-Okuda K, Wada S, Kanda K, Goldsmith MR, Noda H (2012) Single amino acid mutation in an ATP-binding cassette transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc Natl Acad Sci U S A 109:1591–1598CrossRefGoogle Scholar
  9. Balabanidou V, Kampouraki A, MacLean M, Blomquist GJ, Tittiger C, Juarez MP, Mijailovsky SJ, Chalepakis G, Anthousi A, Lynd A, Antoine S, Hemingway J, Ranson H, Lycett GJ, Vontas J (2016) Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae. Proc Natl Acad Sci U S A 113:9268–9273CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bao WX, Narai Y, Nakano A, Kaneda T, Murai T, Sonoda S (2014) Spinosad resistance of melon thrips, Thrips palmi, is conferred by G275E mutation in alpha6 subunit of nicotinic acetylcholine receptor and cytochrome P450 detoxification. Pestic Biochem Physiol 112:51–55CrossRefPubMedGoogle Scholar
  11. Bariami V, Jones CM, Poupardin R, Vontas J, Ranson H (2012) Gene amplification, ABC transporters and cytochrome P450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, Aedes aegypti. PLoS Negl Trop Dis 6:e1692CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bass C, Puinean AM, Andrews M, Cutler P, Daniels M, Elias J, Paul VL, Crossthwaite AJ, Denholm I, Field LM, Foster SP, Lind R, Williamson MS, Slater R (2011) Mutation of a nicotinic acetylcholine receptor beta subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neurosci 12:51CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Physiol 121:78–87CrossRefPubMedGoogle Scholar
  14. Baxter SW, Chen M, Dawson A, Zhao JZ, Vogel H, Shelton AM, Heckel DG, Jiggins CD (2010) Mis-spliced transcripts of nicotinic acetylcholine receptor alpha6 are associated with field evolved spinosad resistance in Plutella xylostella (L.). PLoS Genet 6:e1000802CrossRefPubMedPubMedCentralGoogle Scholar
  15. Baxter SW, Badenes-Perez FR, Morrison A, Vogel H, Crickmore N, Kain W, Wang P, Heckel DG, Jiggins CD (2011) Parallel evolution of Bacillus thuringiensis toxin resistance in lepidoptera. Genetics 189:675–679CrossRefPubMedPubMedCentralGoogle Scholar
  16. Benting J, Nauen R (2004) Biochemical evidence that an S431F mutation in acetylcholinesterase-1 of Aphis gossypii mediates resistance to pirimicarb and omethoate. Pest Manag Sci 60:1051–1055CrossRefPubMedGoogle Scholar
  17. Berger M, Puinean AM, Randall E, Zimmer CT, Silva WM, Bielza P, Field LM, Hughes D, Mellor I, Hassani-Pak K, Siqueira HA, Williamson MS, Bass C (2016) Insecticide resistance mediated by an exon skipping event. Mol Ecol 25:5692–5704CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bloomquist JR, Soderlund DM (1985) Neurotoxic insecticides inhibit GABA-dependent chloride uptake by mouse brain vesicles. Biochem Biophys Res Commun 133:37–43CrossRefPubMedGoogle Scholar
  19. Bourguet D, Raymond M, Bisset J, Pasteur N, Arpagaus M (1996) Duplication of the Ace.1 locus in Culex pipiens mosquitoes from the Caribbean. Biochem Genet 34:351–362CrossRefPubMedGoogle Scholar
  20. Buss DS, McCaffery AR, Callaghan A (2002) Evidence for p-glycoprotein modification of insecticide toxicity in mosquitoes of the Culex pipiens complex. Med Vet Entomol 16:218–222CrossRefPubMedGoogle Scholar
  21. Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den sexual-lockstoff des seidensspinners Bombyx mori. Reindarstellung Konstitution Z Naturforsch 14b:283–284Google Scholar
  22. Campbell PM, Trott JF, Claudianos C, Smyth KA, Russell RJ, Oakeshott JG (1997) Biochemistry of esterases associated with organophosphate resistance in Lucilia cuprina with comparisons to putative orthologues in other Diptera. Biochem Genet 35:17–40CrossRefPubMedGoogle Scholar
  23. Casida JE, Quistad GB (1998) Golden age of insecticide research: past, present, or future? Annu Rev Entomol 43:1–16CrossRefPubMedGoogle Scholar
  24. Catania F, Kauer MO, Daborn PJ, Yen JL, Ffrench-Constant RH, Schlotterer C (2004) World-wide survey of an Accord insertion and its association with DDT resistance in Drosophila melanogaster. Mol Ecol 13:2491–2504CrossRefPubMedGoogle Scholar
  25. Charreton M, Decourtye A, Henry M, Rodet G, Sandoz JC, Charnet P, Collet C (2015) A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honeybee Apis mellifera. PLoS One 10:e0144879CrossRefPubMedPubMedCentralGoogle Scholar
  26. Chen M, Han Z, Qiao X, Qu M (2007) Resistance mechanisms and associated mutations in acetylcholinesterase genes in Sitobion (Fabricius). Pestic Biochem Physiol 87:189–195CrossRefGoogle Scholar
  27. Chopra AK, Sharma MK, Chamoli S (2011) Bioaccumulation of organochlorine pesticides in aquatic system – an overview. Environ Monit Assess 173:905–916CrossRefPubMedGoogle Scholar
  28. Clark BW, Phillips TA, Coats JR (2005) Environmental fate and effects of Bacillus thuringiensis (Bt) proteins from transgenic crops: a review. J Agric Food Chem 53:4643–4653CrossRefPubMedGoogle Scholar
  29. Claudianos C, Russell RJ, Oakeshott JG (1999) The same amino acid substitution in orthologous esterases confers organophosphate resistance on the house fly and a blowfly. Insect Biochem Mol Biol 29:675–686CrossRefPubMedGoogle Scholar
  30. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG, ffrench-Constant RH (2002) A single p450 allele associated with insecticide resistance in Drosophila. Science 297:2253–2256CrossRefPubMedGoogle Scholar
  31. Dai PL, Jia HR, Geng LL, Diao QY (2016) Bt toxin Cry1Ie causes no negative effects on survival, pollen consumption, or olfactory learning in worker honey bees (Hymenoptera: Apidae). J Econ Entomol 109:1028–1033CrossRefGoogle Scholar
  32. David JP, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli PM, Louis C, Hemingway J, Ranson H (2005) The Anopheles gambiae detoxification chip: a highly specific microarray to study metabolic-based insecticide resistance in malaria vectors. Proc Natl Acad Sci U S A 102:4080–4084CrossRefPubMedPubMedCentralGoogle Scholar
  33. David JP, Ismail HM, Chandor-Proust A, Paine MJ (2013) Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos Trans R Soc Lond Ser B Biol Sci 368:20120429CrossRefGoogle Scholar
  34. Davies TE, O’Reilly AO, Field LM, Wallace B, Williamson MS (2008) Knockdown resistance to DDT and pyrethroids: from target-site mutations to molecular modelling. Pest Manag Sci 64:1126–1130CrossRefPubMedGoogle Scholar
  35. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, Pham-Delegue MH (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48:242–250CrossRefPubMedGoogle Scholar
  36. Dermauw W, Van Leeuwen T (2014) The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol 45C:89–110CrossRefGoogle Scholar
  37. Devonshire AL, Sawicki RM (1979) Insecticide-resistant Myzus persicae as an example of evolution by gene duplication. Nature 280:140–141CrossRefGoogle Scholar
  38. Devonshire AL, Field LM (1991) Gene amplification and insecticide resistance. Annu Rev Entomol 36:1–23CrossRefPubMedGoogle Scholar
  39. Ding Y, Hawkes N, Meredith J, Eggleston P, Hemingway J, Ranson H (2005) Characterization of the promoters of Epsilon glutathione transferases in the mosquito Anopheles gambiae and their response to oxidative stress. Biochem J 387:879–888CrossRefPubMedPubMedCentralGoogle Scholar
  40. Djegbe I, Agossa FR, Jones CM, Poupardin R, Cornelie S, Akogbeto M, Ranson H, Corbel V (2014) Molecular characterization of DDT resistance in Anopheles gambiae from Benin. Parasit Vectors 7:409CrossRefPubMedPubMedCentralGoogle Scholar
  41. Djogbenou L, Chandre F, Berthomieu A, Dabire R, Koffi A, Alout H, Weill M (2008) Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s. s. PLoS One 3:e2172CrossRefPubMedPubMedCentralGoogle Scholar
  42. Djogbenou L, Labbe P, Chandre F, Pasteur N, Weill M (2009) Ace-1 duplication in Anopheles gambiae: a challenge for malaria control. Malar J 8:70CrossRefPubMedPubMedCentralGoogle Scholar
  43. Dlugosz A, Janecka A (2016) ABC transporters in the development of multidrug resistance in cancer therapy. Curr Pharm Des 22:4705–4716CrossRefPubMedGoogle Scholar
  44. Dong K (1997) A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroach. Insect Biochem Mol Biol 27:93–100CrossRefPubMedGoogle Scholar
  45. Du W, Awolola TS, Howell P, Koekemoer LL, Brooke BD, Benedict MQ, Coetzee M, Zheng L (2005) Independent mutations in the Rdl locus confer dieldrin resistance to Anopheles gambiae and An. arabiensis. Insect Mol Biol 14:179–183CrossRefPubMedGoogle Scholar
  46. Eldefrawi ME, Miskus R, Sutcher V (1960) Methylenedioxyphenyl derivatives as synergists for carbamate insecticides on susceptible, DDT and parathion resistant house flies. J Econ Entomol 53:231–234CrossRefGoogle Scholar
  47. Epis S, Porretta D, Mastrantonio V, Comandatore F, Sassera D, Rossi P, Cafarchia C, Otranto D, Favia G, Genchi C, Bandi C, Urbanelli S (2014) ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi. Parasit Vectors 7:349CrossRefPubMedPubMedCentralGoogle Scholar
  48. Fairbrother A, Purdy J, Anderson T, Fell R (2014) Risks of neonicotinoid insecticides to honeybees. Environ Toxicol Chem 33:719–731CrossRefPubMedPubMedCentralGoogle Scholar
  49. Feyereisen R, Dermauw W, Van Leeuwen T (2015) Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pestic Biochem Physiol 121:61–77CrossRefPubMedGoogle Scholar
  50. Ffrench-Constant RH, Roush RT (1991) Gene mapping and cross-resistance in cyclodiene insecticide-resistant Drosophila melanogaster (Mg.). Genet Res 57:17–21CrossRefPubMedGoogle Scholar
  51. Ffrench-Constant RH, Rocheleau TA, Steichen JC, Chalmers AE (1993) A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363:449–451CrossRefPubMedGoogle Scholar
  52. Field LM, Devonshire AL, Forde BG (1988) Molecular evidence that insecticide resistance in peach-potato aphids (Myzus persicae Sulz.) results from amplification of an esterase gene. Biochem J 251:309–312CrossRefPubMedPubMedCentralGoogle Scholar
  53. Field LM, Williamson MS, Moores GD, Devonshire AL (1993) Cloning and analysis of the esterase genes conferring insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). Biochem J 294(Part 2):569–574CrossRefPubMedPubMedCentralGoogle Scholar
  54. Field LM, Devonshire AL, Tyler-Smith C (1996) Analysis of amplicons containing the esterase genes responsible for insecticide resistance in the peach-potato aphid Myzus persicae (Sulzer). Biochem J 313(Part 2):543–547CrossRefPubMedPubMedCentralGoogle Scholar
  55. Field LM, Blackman RL, Tyler-Smith C, Devonshire AL (1999) Relationship between amount of esterase and gene copy number in insecticide-resistant Myzus persicae (Sulzer). Biochem J 339(Part 3):737–742CrossRefPubMedPubMedCentralGoogle Scholar
  56. Figueira-Mansur J, Ferreira-Pereira A, Mansur JF, Franco TA, Alvarenga ES, Sorgine MH, Neves BC, Melo AC, Leal WS, Masuda H, Moreira MF (2013) Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Mol Biol 22:648–658CrossRefPubMedGoogle Scholar
  57. Fine BC, Goodin PJ, Thain EM (1963) Penetration of pyrethrin I labelled with carbon-14 into susceptible and pyrethroids resistant houseflies. Nature 199:927CrossRefGoogle Scholar
  58. Fossog Tene B, Poupardin R, Costantini C, Awono-Ambene P, Wondji CS, Ranson H, Antonio-Nkondjio C (2013) Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaounde Cameroon. PLoS One 8:e61408CrossRefPubMedPubMedCentralGoogle Scholar
  59. Fournier D, Bride JM, Hoffmann F, Karch F (1992) Acetylcholinesterase. Two types of modifications confer resistance to insecticide. J Biol Chem 267:14270–14274PubMedGoogle Scholar
  60. Fukami J, Shishido T (1966) Nature of a soluble, glutathione-dependent enzyme system active in cleavage of methyl parathion to desmethyl parathion. J Econ Entomol 59:1338–1349CrossRefPubMedGoogle Scholar
  61. Fukuto TR (1990) Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245–254CrossRefPubMedPubMedCentralGoogle Scholar
  62. Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45CrossRefPubMedGoogle Scholar
  63. Gahan LJ, Pauchet Y, Vogel H, Heckel DG (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet 6:e1001248CrossRefPubMedPubMedCentralGoogle Scholar
  64. Galm U, Sparks TC (2016) Natural product derived insecticides: discovery and development of spinetoram. J Ind Microbiol Biotechnol 43:185–193CrossRefPubMedGoogle Scholar
  65. Garrood WT, Zimmer CT, Gutbrod O, Luke B, Williamson MS, Bass C, Nauen R, Emyr Davies TG (2017) Influence of the RDL A301S mutation in the brown planthopper Nilaparvata lugens on the activity of phenylpyrazole insecticides. Pestic Biochem Physiol 142:1–8CrossRefPubMedPubMedCentralGoogle Scholar
  66. Gellatly KJ, Yoon KS, Doherty JJ, Sun W, Pittendrigh BR, Clark JM (2015) RNAi validation of resistance genes and their interactions in the highly DDT-resistant 91-R strain of Drosophila melanogaster. Pestic Biochem Physiol 121: 107–115Google Scholar
  67. Georghiou GP, Pasteur N, Hawley MN (1980) Linkage relathionships between organophosphate resistance and a highly active esterase-B in Culex quinquefasciatus from California. J Econ Entomol 73:301–305CrossRefPubMedGoogle Scholar
  68. Gibbons D, Morrissey C, Mineau P (2015) A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res Int 22:103–118CrossRefPubMedGoogle Scholar
  69. Giddings JM, Williams WM, Solomon KR, Giesy JP (2014) Risks to aquatic organisms from use of chlorpyrifos in the United States. Rev Environ Contam Toxicol 231:119–162PubMedGoogle Scholar
  70. Goldberg LJ, Margalit J (1977) A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegypti, and Culex pipiens. Mosq News 37:355–358Google Scholar
  71. Grutter T, Changeux JP (2001) Nicotinic receptors in wonderland. Trends Biochem Sci 26:459–463CrossRefPubMedGoogle Scholar
  72. Guo Z, Kang S, Chen D, Wu Q, Wang S, Xie W, Zhu X, Baxter SW, Zhou X, Jurat-Fuentes JL, Zhang Y (2015) MAPK signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in diamondback moth. PLoS Genet 11:e1005124CrossRefPubMedPubMedCentralGoogle Scholar
  73. Hall LM, Spierer P (1986) The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an unusual 5′ leader. EMBO J 5:2949–2954CrossRefPubMedPubMedCentralGoogle Scholar
  74. Hayatsu M, Hirano M, Tokuda S (2000) Involvement of two plasmids in fenitrothion degradation by Burkholderia sp. strain NF100. Appl Environ Microbiol 66:1737–1740CrossRefPubMedPubMedCentralGoogle Scholar
  75. Hemingway J, Karunaratne SH (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med Vet Entomol 12:1–12CrossRefPubMedGoogle Scholar
  76. Holderbaum DF, Cuhra M, Wickson F, Orth AI, Nodari RO, Bohn T (2015) Chronic responses of Daphnia magna under dietary exposure to leaves of a transgenic (Event MON810) Bt-maize hybrid and its conventional near-isoline. J Toxicol Environ Health A 78:993–1007CrossRefPubMedGoogle Scholar
  77. Hsu AT (1991) 1,2-diacyl-1-1-alkylhydrazine: anovel class of insect growth regulators. In: Baker DR, Fenyes JG, Moberg WK (eds) Synthesis and chemistry of agrochemicals II. Am Chem Soc, Washington, DC, pp 478–490CrossRefGoogle Scholar
  78. Hsu JC, Feng HT, Wu WJ, Geib SM, Mao CH, Vontas J (2012) Truncated transcripts of nicotinic acetylcholine subunit gene Bdalpha6 are associated with spinosad resistance in Bactrocera dorsalis. Insect Biochem Mol Biol 42:806–815CrossRefPubMedGoogle Scholar
  79. Huchard E, Martinez M, Alout H, Douzery EJ, Lutfalla G, Berthomieu A, Berticat C, Raymond M, Weill M (2006) Acetylcholinesterase genes within the Diptera: takeover and loss in true flies. Proc Biol Sci 273:2595–2604CrossRefPubMedPubMedCentralGoogle Scholar
  80. Jones RT, Bakker SE, Stone D, Shuttleworth SN, Boundy S, McCart C, Daborn PJ, Ffrench-Constant RH, van den Elsen JM (2010) Homology modelling of Drosophila cytochrome P450 enzymes associated with insecticide resistance. Pest Manag Sci 66:1106–1115CrossRefPubMedGoogle Scholar
  81. Jones CM, Toe HK, Sanou A, Namountougou M, Hughes A, Diabaté A, Dabire R, Simard F, Ranson H (2012) Additional selection for insecticide resistance in urban malaria vectors: DDT resistance in Anopheles arabiensis from Bobo-Dioulasso, Burkina Faso. PLoS ONE 7:e45995CrossRefPubMedPubMedCentralGoogle Scholar
  82. Joussen N, Heckel DG, Haas M, Schuphan I, Schmidt B (2008) Metabolism of imidacloprid and DDT by P450 CYP6G1 expressed in cell cultures of Nicotiana tabacum suggests detoxification of these insecticides in Cyp6g1-overexpressing strains of Drosophila melanogaster, leading to resistance. Pest Manag Sci 64:65–73CrossRefPubMedGoogle Scholar
  83. Joussen N, Agnolet S, Lorenz S, Schone SE, Ellinger R, Schneider B, Heckel DG (2012) Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. Proc Natl Acad Sci U S A 109:15206–15211CrossRefPubMedPubMedCentralGoogle Scholar
  84. Kadala A, Charreton M, Jakob I, Cens T, Rousset M, Chahine M, Le Conte Y, Charnet P, Collet C (2014) Pyrethroids differentially alter voltage-gated sodium channels from the honeybee central olfactory neurons. PLoS One 9:e112194CrossRefPubMedPubMedCentralGoogle Scholar
  85. Karunaratne SH, Jayawardena KG, Hemingway J, Ketterman AJ (1993) Characterization of a B-type esterase involved in insecticide resistance from the mosquito Culex quinquefasciatus. Biochem J 294(Part 2):575–579CrossRefPubMedPubMedCentralGoogle Scholar
  86. Kaviraj A, Gupta A (2014) Biomarkers of type II synthetic pyrethroid pesticides in freshwater fish. Biomed Res Int 2014:928063PubMedPubMedCentralGoogle Scholar
  87. Kikuchi Y, Meng XY, Fukatsu T (2005) Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl Environ Microbiol 71:4035–4043CrossRefPubMedPubMedCentralGoogle Scholar
  88. Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73:4308–4316CrossRefPubMedPubMedCentralGoogle Scholar
  89. Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460CrossRefPubMedGoogle Scholar
  90. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622CrossRefPubMedPubMedCentralGoogle Scholar
  91. Kim YH, Lee SH (2013) Which acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta? Insect Biochem Mol Biol 43:47–53CrossRefPubMedGoogle Scholar
  92. Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M (2008) The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag Sci 64:789–792CrossRefPubMedGoogle Scholar
  93. Koo HN, An JJ, Park SE, Kim JI, Kim GH (2014) Regional susceptibilities to 12 insecticides of melon and cotton aphid, Aphis gossypii (Hemiptera: Aphilididae) and a point mutation associated with imidacloprid resistance. Crop Prot 55:91–97CrossRefGoogle Scholar
  94. Kozaki T, Shono T, Tomita T, Kono Y (2001) Fenitroxon insensitive acetylcholinesterases of the housefly, Musca domestica associated with point mutations. Insect Biochem Mol Biol 31:991–997CrossRefPubMedGoogle Scholar
  95. Kwon DH, Kim JH, Kim YH, Yoon KS, Clark JM, Lee SH (2014) Identification and characterization of an esterase involved in malathion resistance in the head louse Pediculus humanus capitis. Pestic Biochem Physiol 112:13–18CrossRefPubMedGoogle Scholar
  96. Labbé P, Berthomieu A, Berticat C, Alout H, Raymond M, Lenormand T, Weill M (2007) Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Mol Biol Evol 24:1056–1067CrossRefPubMedGoogle Scholar
  97. Lawrence LJ, Casida JE (1983) Stereospecific action of pyrethroid insecticides on the gamma-aminobutyric acid receptor-ionophore complex. Science 221:1399–1401CrossRefPubMedGoogle Scholar
  98. Le Goff G, Hilliou F (2017) Resistance evolution in Drosophila: the case of CYP6G1. Pest Manag Sci 73:493–499CrossRefPubMedGoogle Scholar
  99. Le Goff G, 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 92:1295–1305CrossRefPubMedGoogle Scholar
  100. Le DP, Thirugnanam M, Lidert Z, Carlson GR, Ryan JB (1996) RH-2485: a new selective insecticide for caterpillar control. In: Council BCP (ed) Brighton crop protection conference. British Crop Protection Enterprises, Brighton, pp 481–486Google Scholar
  101. Lee KS, Walker CH, McCaffery AR, Ahmad M, Little E (1989) Metabolism of trans-cypermethrin by Helicoverpa armigera and H. virescens. Pestic Biochem Physiol 34:49–57CrossRefGoogle Scholar
  102. Lei Y, Zhu X, Xie W, Wu Q, Wang S, Guo Z, Xu B, Li X, Zhou X, Zhang Y (2014) Midgut transcriptome response to a Cry toxin in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Gene 533:180–187CrossRefPubMedGoogle Scholar
  103. Lima EP, Goulart MO, Rolim Neto ML (2014) Evaluation of the role of ATP-binding cassette transporters as a defence mechanism against temephos in populations of Aedes aegypti. Mem Inst Oswaldo Cruz 109:964–966CrossRefPubMedGoogle Scholar
  104. Liu Z, Williamson MS, Lansdell SJ, Denholm I, Han Z, Millar NS (2005) A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc Natl Acad Sci U S A 102:8420–8425CrossRefPubMedPubMedCentralGoogle Scholar
  105. Lombet A, Mourre C, Lazdunski M (1988) Interaction of insecticides of the pyrethroid family with specific binding sites on the voltage-dependent sodium channel from mammalian brain. Brain Res 459:44–53CrossRefPubMedGoogle Scholar
  106. Loughney K, Kreber R, Ganetzky B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143–1154CrossRefPubMedGoogle Scholar
  107. Lumjuan N, McCarroll L, Prapanthadara LA, Hemingway J, Ranson H (2005) Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect Biochem Mol Biol 35:861–871CrossRefPubMedGoogle Scholar
  108. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara LA, Somboon P, Lycett G, Ranson H (2011) The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochem Mol Biol 41:203–209CrossRefPubMedGoogle Scholar
  109. Martin RL, Pittendrigh B, Liu J, Reenan R, Ffrench-Constant R, Hanck DA (2000) Point mutations in domain III of a Drosophila neuronal Na channel confer resistance to allethrin. Insect Biochem Mol Biol 30:1051–1059CrossRefPubMedGoogle Scholar
  110. Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, Guillet P, Pasteur N, Pauron D (1998) Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s. s. Insect Mol Biol 7:179–184CrossRefPubMedGoogle Scholar
  111. 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 8:339–346CrossRefPubMedGoogle Scholar
  112. Melander AL (1914) Can insects become resistant to sprays? J Econ Entomol 7:167–173CrossRefGoogle Scholar
  113. Melo AL, Soccol VT, Soccol CR (2016) Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Crit Rev Biotechnol 36:317–326CrossRefPubMedGoogle Scholar
  114. Menozzi P, Shi MA, Lougarre A, Tang ZH, Fournier D (2004) Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evol Biol 4:4CrossRefPubMedPubMedCentralGoogle Scholar
  115. Misra JR, Horner MA, Lam G, Thummel CS (2011) Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev 25:1796–1806CrossRefPubMedPubMedCentralGoogle Scholar
  116. Mitchell SN, Rigden DJ, Dowd AJ, Lu F, Wilding CS, Weetman D, Dadzie S, Jenkins AM, Regna K, Boko P, Djogbenou L, Muskavitch MA, Ranson H, Paine MJ, Mayans O, Donnelly MJ (2014) Metabolic and target-site mechanisms combine to confer strong DDT resistance in Anopheles gambiae. PLoS One 9:e92662CrossRefPubMedPubMedCentralGoogle Scholar
  117. Miyazaki M, Ohyama K, Dunlap DY, 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 252:61–68PubMedGoogle Scholar
  118. Mouches C, Pasteur N, Berge JB, Hyrien O, Raymond M, de Saint Vincent BR, de Silvestri M, Georghiou GP (1986) Amplification of an esterase gene is responsible for insecticide resistance in a California Culex mosquito. Science 233:778–780CrossRefPubMedGoogle Scholar
  119. Mutero A, Pralavorio M, Bride JM, Fournier D (1994) Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc Natl Acad Sci U S A 91:5922–5926CrossRefPubMedPubMedCentralGoogle Scholar
  120. Nabeshima T, Mori A, Kozaki T, Iwata Y, Hidoh O, Harada S, Kasai S, Severson DW, Kono Y, Tomita T (2004) An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochem Biophys Res Commun 313:794–801CrossRefPubMedGoogle Scholar
  121. Nakao T, Naoi A, Kawahara N, Hirase K (2010) Mutation of the GABA receptor associated with fipronil resistance inthe whitebacked planthopper, Sogatella furcifera. Pestic Biochem Physiol 97:262–266CrossRefGoogle Scholar
  122. Nakao T, Kawase A, Kinoshita A, Abe R, Hama M, Kawahara N, Hirase K (2011) The A2′N mutation of the RDL gamma-aminobutyric acid receptor conferring fipronil resistance in Laodelphax striatellus (Hemiptera: Delphacidae). J Econ Entomol 104:646–652CrossRefPubMedGoogle Scholar
  123. Nascimento AR, Fresia P, Consoli FL, Omoto C (2015) Comparative transcriptome analysis of lufenuron-resistant and susceptible strains of Spodoptera frugiperda (Lepidoptera: Noctuidae). BMC Genomics 16:985CrossRefPubMedPubMedCentralGoogle Scholar
  124. Newcomb RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, Oakeshott JG (1997) A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc Natl Acad Sci U S A 94:7464–7468CrossRefPubMedPubMedCentralGoogle Scholar
  125. Nishimura K, Tanaka M, Iwaya K, Kagabu S (1998) Relationship between insecticidal and nerve-excitatory activities of imidacloprid and its alkylated congeners at the imidazolidine NH site. Pestic Biochem Physiol 62:172–178CrossRefGoogle Scholar
  126. Nishiwaki H, Nakagawa Y, Kuwamura M, Sato K, Akamatsu M, Matsuda K, Komai K, Miyagawa H (2003) Correlations of the electrophysiological activity of neonicotinoids with their binding and insecticidal activities. Pest Manag Sci 59:1023–1030CrossRefPubMedGoogle Scholar
  127. Nkya TE, Akhouayri I, Poupardin R, Batengana B, Mosha F, Magesa S, Kisinza W, David JP (2014) Insecticide resistance mechanisms associated with different environments in the malaria vector Anopheles gambiae: a case study in Tanzania. Malar J 13:28CrossRefPubMedPubMedCentralGoogle Scholar
  128. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807CrossRefPubMedPubMedCentralGoogle Scholar
  129. Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994CrossRefPubMedPubMedCentralGoogle Scholar
  130. Orr N, Shaffner AJ, Richey K, Crouse GD (2009) Novel mode of action of spinosad: receptor binding studies demonstrating lack of interaction with known insecticidal target sites. Pestic Biochem Physiol 95:1–5CrossRefGoogle Scholar
  131. Ortelli F, Rossiter LC, Vontas J, Ranson H, Hemingway J (2003) Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochem J 373:957–963CrossRefPubMedPubMedCentralGoogle Scholar
  132. Palma L, Munoz D, Berry C, Murillo J, Caballero P (2014) Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins (Basel) 6:3296–3325CrossRefGoogle Scholar
  133. Pan C, Zhou Y, Mo J (2009) The clone of laccase gene and its potential function in cuticular penetration resistance of Culex pipiens pallens to fenvalerate. Pestic Biochem Physiol 93:105–111CrossRefGoogle Scholar
  134. Perry T, McKenzie JA, Batterham P (2007) A Dalpha6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem Mol Biol 37:184–188CrossRefPubMedGoogle Scholar
  135. 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 256:602–610CrossRefPubMedGoogle Scholar
  136. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, Williamson MS, Bass C (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 6:e1000999CrossRefPubMedPubMedCentralGoogle Scholar
  137. Puinean AM, Lansdell SJ, Collins T, Bielza P, Millar NS (2013) A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis. J Neurochem 124:590–601CrossRefPubMedPubMedCentralGoogle Scholar
  138. Qiu Y, Tittiger C, Wicker-Thomas C, Le Goff G, Young S, Wajnberg E, Fricaux T, Taquet N, Blomquist GJ, Feyereisen R (2012) An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci U S A 109:14858–14863CrossRefPubMedPubMedCentralGoogle Scholar
  139. Ratcliffe DA (1967) Decrease in eggshell weight in certain birds of prey. Nature 215:208–210CrossRefPubMedGoogle Scholar
  140. Remnant EJ, Good RT, Schmidt JM, Lumb C, Robin C, Daborn PJ, Batterham P (2013) Gene duplication in the major insecticide target site, Rdl, in Drosophila melanogaster. Proc Natl Acad Sci U S A 110:14705–14710CrossRefPubMedPubMedCentralGoogle Scholar
  141. Revuelta L, Piulachs MD, Belles X, Castanera P, Ortego F, Diaz-Ruiz JR, Hernandez-Crespo P, Tenllado F (2009) RNAi of ace1 and ace2 in Blattella germanica reveals their differential contribution to acetylcholinesterase activity and sensitivity to insecticides. Insect Biochem Mol Biol 39:913–919CrossRefPubMedGoogle Scholar
  142. Rinkevich FD, Chen M, Shelton AM, Scott JG (2010) Transcripts of the nicotinic acetylcholine receptor subunit gene Pxylalpha6 with premature stop codons are associated with spinosad resistance in diamondback moth, Plutella xylostella. Invertebr Neurosci 10:25–33CrossRefGoogle Scholar
  143. Rinkevich FD, Du Y, Dong K (2013) Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 106:93–100CrossRefPubMedPubMedCentralGoogle Scholar
  144. Riveron JM, Yunta C, Ibrahim SS, Djouaka R, Irving H, Menze BD, Ismail HM, Hemingway J, Ranson H, Albert A, Wondji CS (2014) A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector. Genome Biol 15:R27CrossRefPubMedPubMedCentralGoogle Scholar
  145. Rooker S, Guillemaud T, Berge J, Pasteur N, Raymond M (1996) Coamplification of esterase A and B genes as a single unit in Culex pipiens mosquitoes. Heredity (Edinb) 77(Part 5):555–561Google Scholar
  146. Russell RJ, Claudianos C, Campbell PM, Horne I, Sutherland TD, Oakeshott JG (2004) Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides. Pestic Biochem Physiol 79:84–93CrossRefGoogle Scholar
  147. Salgado VL, Saar R (2004) Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J Insect Physiol 50:867–879CrossRefPubMedGoogle Scholar
  148. Sattelle DB, Jones AK, Sattelle BM, Matsuda K, Reenan R, Biggin PC (2005) Edit, cut and paste in the nicotinic acetylcholine receptor gene family of Drosophila melanogaster. BioEssays 27:366–376CrossRefPubMedGoogle Scholar
  149. Sawicki RM, Farnham AW (1968) Examination of the isolated autosomes of the SKA strain of houseflies for resistance to several insecticides with and without pretreatment with sesamex and TBTP. Bull Entomol Res 59:409CrossRefGoogle Scholar
  150. Schmidt JM, Good RT, Appleton B, Sherrard J, Raymant GC, Bogwitz MR, Martin J, Daborn PJ, Goddard ME, Batterham P, Robin C (2010) Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet 6:e1000998CrossRefPubMedPubMedCentralGoogle Scholar
  151. Senthilkumaran B (2015) Pesticide- and sex steroid analogue-induced endocrine disruption differentially targets hypothalamo-hypophyseal-gonadal system during gametogenesis in teleosts – a review. Gen Comp Endocrinol 219:136–142CrossRefPubMedGoogle Scholar
  152. Shang Q, Pan Y, Fang K, Xi J, Wong A, Brennan JA, Cao C (2014) Extensive Ace2 duplication and multiple mutations on Ace1 and Ace2 are related with high level of organophosphates resistance in Aphis gossypii. Environ Toxicol 29:526–533CrossRefPubMedGoogle Scholar
  153. Shimomura M, Yokota M, Ihara M, Akamatsu M, Sattelle DB, Matsuda K (2006) Role in the selectivity of neonicotinoids of insect-specific basic residues in loop D of the nicotinic acetylcholine receptor agonist binding site. Mol Pharmacol 70:1255–1263CrossRefPubMedGoogle Scholar
  154. Silva WM, Berger M, Bass C, Williamson M, Moura DM, Ribeiro LM, Siqueira HA (2016) Mutation (G275E) of the nicotinic acetylcholine receptor alpha6 subunit is associated with high levels of resistance to spinosyns in Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Pestic Biochem Physiol 131:1–8CrossRefPubMedGoogle Scholar
  155. Slater R, Paul VL, Andrews M, Garbay M, Camblin P (2011) Identifying the presence of neonicotinoidresistant peach-potato aphid (Myzus persicae) in the peach-growing regions of southern France and northern Spain. Pest Manag Sci 68:634–638CrossRefPubMedGoogle Scholar
  156. Soderlund DM, Bloomquist JR (1989) Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34:77–96CrossRefPubMedGoogle Scholar
  157. Sparks TC (2013) Insecticide discovery: an evaluation and analysis. Pestic Biochem Physiol 107:8–17CrossRefPubMedGoogle Scholar
  158. Stone BF, Brown AW (1969) Mechanisms of resistance to fenthion in Culex pipiens fatigans Wied. Bull World Health Organ 40:401–408PubMedPubMedCentralGoogle Scholar
  159. Struger J, Grabuski J, Cagampan S, Sverko E, Marvin C (2016) Occurrence and distribution of carbamate pesticides and metalaxyl in Southern Ontario surface waters 2007–2010. Bull Environ Contam Toxicol 96:423–431CrossRefPubMedPubMedCentralGoogle Scholar
  160. Strycharz J, Lao A, Li H, Qiu X, Lee SH, Sun W, Yoon KS, Doherty JJ, Pittendrigh B, Clark JM (2013) Resistance in the highly DDT-resistant 91-R strain of Drosophila melanogaster involves decreased penetration, increased metabolism, and direct excretion. Pestic Biochem Physiol 107:207–217CrossRefGoogle Scholar
  161. Tago K, Yonezawa S, Ohkouchi T, Hashimoto M, Hayatsu M (2006) Purification and characterization of fenitrothion hydrolase from Burkholderia sp. NF100. J Biosci Bioeng 101:80–82CrossRefPubMedGoogle Scholar
  162. Tan J, Liu Z, Wang R, Huang ZY, Chen AC, Gurevitz M, Dong K (2005) Identification of amino acid residues in the insect sodium channel critical for pyrethroid binding. Mol Pharmacol 67:513–522CrossRefPubMedGoogle Scholar
  163. Tanaka S, Miyamoto K, Noda H, Jurat-Fuentes JL, Yoshizawa Y, Endo H, Sato R (2013) The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. FEBS J 280:1782–1794CrossRefPubMedGoogle Scholar
  164. Then C (2010) Risk assessment of toxins derived from Bacillus thuringiensis-synergism, efficacy, and selectivity. Environ Sci Pollut Res Int 17:791–797CrossRefPubMedGoogle Scholar
  165. Thompson M, Steichen JC, ffrench-Constant RH (1993) Conservation of cyclodiene insecticide resistance-associated mutations in insects. Insect Mol Biol 2:149–154CrossRefPubMedGoogle Scholar
  166. Toe KH, N’Fale S, Dabire RK, Ranson H, Jones CM (2015) The recent escalation in strength of pyrethroid resistance in Anopheles coluzzi in West Africa is linked to increased expression of multiple gene families. BMC Genomics 16:146CrossRefPubMedPubMedCentralGoogle Scholar
  167. Toumi H, Burga-Perez KF, Férard JF (2016) Acute and chronic ecotoxicity of carbaryl with a battery of aquatic bioassays. J Environ Sci Health B 51:57–62CrossRefPubMedGoogle Scholar
  168. Toyota K, Kato Y, Miyakawa H, Yatsu R, Mizutani T, Ogino Y, Miyagawa S, Watanabe H, Nishide H, Uchiyama I, Tatarazako N, Iguchi T (2014) Molecular impact of juvenile hormone agonists on neonatal Daphnia magna. J Appl Toxicol 34:537–544CrossRefPubMedGoogle Scholar
  169. Urlacher E, Monchanin C, Rivière C, Richard FJ, Lombardi C, Michelsen-Heath S, Hageman KJ, Mercer AR (2016) Measurements of chlorpyrifos levels in forager bees and comparison with levels that disrupt honey bee odor-mediated learning under laboratory conditions. J Chem Ecol 42:127–138CrossRefPubMedGoogle Scholar
  170. Vais H, Atkinson S, Pluteanu F, Goodson SJ, Devonshire AL, Williamson MS, Usherwood PN (2003) Mutations of the para sodium channel of Drosophila melanogaster identify putative binding sites for pyrethroids. Mol Pharmacol 64:914–922CrossRefPubMedGoogle Scholar
  171. Vontas JG, Small GJ, Nikou DC, Ranson H, Hemingway J (2002) Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper, Nilaparvata lugens. Biochem J 362:329–337CrossRefPubMedPubMedCentralGoogle Scholar
  172. Walsh SB, Dolden TA, Moores GD, Kristensen M, Lewis T, Devonshire AL, Williamson MS (2001) Identification and characterization of mutations in housefly (Musca domestica) acetylcholinesterase involved in insecticide resistance. Biochem J 359:175–181CrossRefPubMedPubMedCentralGoogle Scholar
  173. Walter CM, Price NR (1989) The uptake and penetration of pirimiphos-methyl into susceptible and resistant strains of the red flour beetle Tribolium castaneum. Comp Biochem Physiol 94C:419–423Google Scholar
  174. Wang Y, Chen C, Zhao X, Wang Q, Qian Y (2015a) Assessing joint toxicity of four organophosphate and carbamate insecticides in common carp (Cyprinus carpio) using acetylcholinesterase activity as an endpoint. Pestic Biochem Physiol 122:81–85CrossRefPubMedGoogle Scholar
  175. Wang YY, Li YH, Huang ZY, Chen XP, Romeis J, Dai PL, Peng YF (2015b) Toxicological, biochemical, and histopathological analyses demonstrating that Cry1C and Cry2A are not toxic to larvae of the honeybee, Apis mellifera. J Agric Food Chem 63:6126–6132CrossRefPubMedGoogle Scholar
  176. Weber J, Halsall CJ, Muir D, Teixeira C, Small J, Solomon K, Hermanson M, Hung H, Bidleman T (2010) Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic. Sci Total Environ 408:2966–2984CrossRefPubMedGoogle Scholar
  177. Weill M, Fort P, Berthomieu A, Dubois MP, Pasteur N, Raymond M (2002) A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila. Proc Biol Sci 269:2007–2016CrossRefPubMedPubMedCentralGoogle Scholar
  178. Weill M, Lutfalla G, Mogensen K, Chandre F, Berthomieu A, Berticat C, Pasteur N, Philips A, Fort P, Raymond M (2003) Comparative genomics: insecticide resistance in mosquito vectors. Nature 423:136–137CrossRefPubMedGoogle Scholar
  179. Weill M, Malcolm C, Chandre F, Mogensen K, Berthomieu A, Marquine M, Raymond M (2004) The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol 13:1–7CrossRefPubMedGoogle Scholar
  180. Williams CM (1967) The juvenile hormone II. Its role in the endocrine control of molting, pupation, and adult development in the cecropia silkworm. Biol Bull Woods Hole 121:572–585CrossRefGoogle Scholar
  181. Williamson MS, Martinez-Torres D, Hick CA, Devonshire AL (1996) Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol Gen Genet 252:51–60CrossRefPubMedGoogle Scholar
  182. Wood O, Hanrahan S, Coetzee M, Koekemoer L, Brooke B (2010) Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus. Parasit Vectors 3:67CrossRefPubMedPubMedCentralGoogle Scholar
  183. Wright RH (1964) After pesticides – what? Nature 204:121–125CrossRefPubMedGoogle Scholar
  184. Wright GA, Softley S, Earnshaw H (2015) Low doses of neonicotinoid pesticides in food rewards impair short-term olfactory memory in foraging-age honeybees. Sci Rep 5:15322CrossRefPubMedPubMedCentralGoogle Scholar
  185. Zhang HG, ffrench-Constant RH, Jackson MB (1994) A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J Physiol 479(Part 1):65–75CrossRefPubMedPubMedCentralGoogle Scholar
  186. Zhu KY, Lee SH, Clark JM (1996) A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pestic Biochem Physiol 55:100–108CrossRefPubMedGoogle Scholar
  187. Zimmer CT, Garrood WT, Puinean AM, Eckel-Zimmer M, Williamson MS, Davies TG, Bass C (2016) A CRISPR/Cas9 mediated point mutation in the alpha 6 subunit of the nicotinic acetylcholine receptor confers resistance to spinosad in Drosophila melanogaster. Insect Biochem Mol Biol 73:62–69CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Université Côte d’AzurINRA, CNRS, ISASophia AntipolisFrance
  2. 2.Environment and Climate Change CanadaMontrealCanada

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