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.
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References
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 38:940–949
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 505:409–422
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 260:165–175
Apperson C, Georghiou GP (1975) Mechanisms of resistance to organophosphorous insecticides in Culex tarsalis. J Econ Entomol 68:153–157
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 11:57
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 5:14529
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:e2000618
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 109:1591–1598
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 113:9268–9273
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 112:51–55
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:e1692
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 12:51
Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Physiol 121:78–87
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:e1000802
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 189:675–679
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 60:1051–1055
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 25:5692–5704
Bloomquist JR, Soderlund DM (1985) Neurotoxic insecticides inhibit GABA-dependent chloride uptake by mouse brain vesicles. Biochem Biophys Res Commun 133:37–43
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 34:351–362
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 16:218–222
Butenandt A, Beckmann R, Stamm D, Hecker E (1959) Über den sexual-lockstoff des seidensspinners Bombyx mori. Reindarstellung Konstitution Z Naturforsch 14b:283–284
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 35:17–40
Casida JE, Quistad GB (1998) Golden age of insecticide research: past, present, or future? Annu Rev Entomol 43:1–16
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 13:2491–2504
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:e0144879
Chen M, Han Z, Qiao X, Qu M (2007) Resistance mechanisms and associated mutations in acetylcholinesterase genes in Sitobion (Fabricius). Pestic Biochem Physiol 87:189–195
Chopra AK, Sharma MK, Chamoli S (2011) Bioaccumulation of organochlorine pesticides in aquatic system – an overview. Environ Monit Assess 173:905–916
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 53:4643–4653
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 29:675–686
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 297:2253–2256
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 109:1028–1033
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 102:4080–4084
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 368:20120429
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 64:1126–1130
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 48:242–250
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:89–110
Devonshire AL, Sawicki RM (1979) Insecticide-resistant Myzus persicae as an example of evolution by gene duplication. Nature 280:140–141
Devonshire AL, Field LM (1991) Gene amplification and insecticide resistance. Annu Rev Entomol 36:1–23
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 387:879–888
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 7:409
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:e2172
Djogbenou L, Labbe P, Chandre F, Pasteur N, Weill M (2009) Ace-1 duplication in Anopheles gambiae: a challenge for malaria control. Malar J 8:70
Dlugosz A, Janecka A (2016) ABC transporters in the development of multidrug resistance in cancer therapy. Curr Pharm Des 22:4705–4716
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 27:93–100
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 14:179–183
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 53:231–234
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 7:349
Fairbrother A, Purdy J, Anderson T, Fell R (2014) Risks of neonicotinoid insecticides to honeybees. Environ Toxicol Chem 33:719–731
Feyereisen R, Dermauw W, Van Leeuwen T (2015) Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pestic Biochem Physiol 121:61–77
Ffrench-Constant RH, Roush RT (1991) Gene mapping and cross-resistance in cyclodiene insecticide-resistant Drosophila melanogaster (Mg.). Genet Res 57:17–21
Ffrench-Constant RH, Rocheleau TA, Steichen JC, Chalmers AE (1993) A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363:449–451
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 251:309–312
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):569–574
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):543–547
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):737–742
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 22:648–658
Fine BC, Goodin PJ, Thain EM (1963) Penetration of pyrethrin I labelled with carbon-14 into susceptible and pyrethroids resistant houseflies. Nature 199:927
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:e61408
Fournier D, Bride JM, Hoffmann F, Karch F (1992) Acetylcholinesterase. Two types of modifications confer resistance to insecticide. J Biol Chem 267:14270–14274
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 59:1338–1349
Fukuto TR (1990) Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245–254
Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45
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:e1001248
Galm U, Sparks TC (2016) Natural product derived insecticides: discovery and development of spinetoram. J Ind Microbiol Biotechnol 43:185–193
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 142:1–8
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: 107–115
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 73:301–305
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 22:103–118
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 231:119–162
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 37:355–358
Grutter T, Changeux JP (2001) Nicotinic receptors in wonderland. Trends Biochem Sci 26:459–463
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:e1005124
Hall LM, Spierer P (1986) The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an unusual 5′ leader. EMBO J 5:2949–2954
Hayatsu M, Hirano M, Tokuda S (2000) Involvement of two plasmids in fenitrothion degradation by Burkholderia sp. strain NF100. Appl Environ Microbiol 66:1737–1740
Hemingway J, Karunaratne SH (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med Vet Entomol 12:1–12
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 78:993–1007
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 478–490
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 42:806–815
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 273:2595–2604
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 66:1106–1115
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:e45995
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 64:65–73
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 109:15206–15211
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:e112194
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):575–579
Kaviraj A, Gupta A (2014) Biomarkers of type II synthetic pyrethroid pesticides in freshwater fish. Biomed Res Int 2014:928063
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 71:4035–4043
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 73:4308–4316
Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460
Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622
Kim YH, Lee SH (2013) Which acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta? Insect Biochem Mol Biol 43:47–53
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 64:789–792
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 55:91–97
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 31:991–997
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 112:13–18
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 24:1056–1067
Lawrence LJ, Casida JE (1983) Stereospecific action of pyrethroid insecticides on the gamma-aminobutyric acid receptor-ionophore complex. Science 221:1399–1401
Le Goff G, Hilliou F (2017) Resistance evolution in Drosophila: the case of CYP6G1. Pest Manag Sci 73:493–499
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 92:1295–1305
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 481–486
Lee KS, Walker CH, McCaffery AR, Ahmad M, Little E (1989) Metabolism of trans-cypermethrin by Helicoverpa armigera and H. virescens. Pestic Biochem Physiol 34:49–57
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 533:180–187
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 109:964–966
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 102:8420–8425
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 459:44–53
Loughney K, Kreber R, Ganetzky B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143–1154
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 35:861–871
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 41:203–209
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 30:1051–1059
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 7:179–184
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 8:339–346
Melander AL (1914) Can insects become resistant to sprays? J Econ Entomol 7:167–173
Melo AL, Soccol VT, Soccol CR (2016) Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Crit Rev Biotechnol 36:317–326
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 4:4
Misra JR, Horner MA, Lam G, Thummel CS (2011) Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes Dev 25:1796–1806
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:e92662
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 252:61–68
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 233:778–780
Mutero A, Pralavorio M, Bride JM, Fournier D (1994) Resistance-associated point mutations in insecticide-insensitive acetylcholinesterase. Proc Natl Acad Sci U S A 91:5922–5926
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 313:794–801
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 97:262–266
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 104:646–652
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 16:985
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 94:7464–7468
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 62:172–178
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 59:1023–1030
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 13:28
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 100:1803–1807
Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994
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 95:1–5
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 373:957–963
Palma L, Munoz D, Berry C, Murillo J, Caballero P (2014) Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins (Basel) 6:3296–3325
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 93:105–111
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 37:184–188
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 256:602–610
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:e1000999
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 124:590–601
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 109:14858–14863
Ratcliffe DA (1967) Decrease in eggshell weight in certain birds of prey. Nature 215:208–210
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 110:14705–14710
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 39:913–919
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 10:25–33
Rinkevich FD, Du Y, Dong K (2013) Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 106:93–100
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:R27
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):555–561
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 79:84–93
Salgado VL, Saar R (2004) Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J Insect Physiol 50:867–879
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 27:366–376
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 59:409
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:e1000998
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 219:136–142
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 29:526–533
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 70:1255–1263
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 131:1–8
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 68:634–638
Soderlund DM, Bloomquist JR (1989) Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34:77–96
Sparks TC (2013) Insecticide discovery: an evaluation and analysis. Pestic Biochem Physiol 107:8–17
Stone BF, Brown AW (1969) Mechanisms of resistance to fenthion in Culex pipiens fatigans Wied. Bull World Health Organ 40:401–408
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 96:423–431
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 107:207–217
Tago K, Yonezawa S, Ohkouchi T, Hashimoto M, Hayatsu M (2006) Purification and characterization of fenitrothion hydrolase from Burkholderia sp. NF100. J Biosci Bioeng 101:80–82
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 67:513–522
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 280:1782–1794
Then C (2010) Risk assessment of toxins derived from Bacillus thuringiensis-synergism, efficacy, and selectivity. Environ Sci Pollut Res Int 17:791–797
Thompson M, Steichen JC, ffrench-Constant RH (1993) Conservation of cyclodiene insecticide resistance-associated mutations in insects. Insect Mol Biol 2:149–154
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 16:146
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 51:57–62
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 34:537–544
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 42:127–138
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 64:914–922
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 362:329–337
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 359:175–181
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:419–423
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 122:81–85
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 63:6126–6132
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 408:2966–2984
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 269:2007–2016
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 423:136–137
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 13:1–7
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 121:572–585
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 252:51–60
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 3:67
Wright RH (1964) After pesticides – what? Nature 204:121–125
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 5:15322
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):65–75
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 55:100–108
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 73:62–69
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Le Goff, G., Giraudo, M. (2019). Effects of Pesticides on the Environment and Insecticide Resistance. In: Picimbon, JF. (eds) Olfactory Concepts of Insect Control - Alternative to insecticides. Springer, Cham. https://doi.org/10.1007/978-3-030-05060-3_3
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