Parasitology Research

, Volume 115, Issue 4, pp 1363–1373 | Cite as

Insecticide resistance and its molecular basis in urban insect pests

  • Muhammad Nadir Naqqash
  • Ayhan Gökçe
  • Allah Bakhsh
  • Muhammad Salim
Review

Abstract

Insecticide resistance is one of the most important evolutionary phenomena for researchers. Overuse of chemicals has induced resistance in insect pests that ultimately has led to the collapse of disease control programs in many countries. The erroneous and inappropriate management of insect vectors has resulted in dissemination of many vector-borne diseases like dengue, malaria, diarrhea, leishmaniasis, and many others. In most cases, the emergence of new diseases and the revival of old ones can be related with ecological changes that have favored rapid growth of vector densities. Understanding molecular mechanisms in resistant strains can assist in the development of management programs to control the development and spread of resistant insect populations. The dominant, recessive, and co-dominant forms of genes encoding resistance can be investigated, and furthermore, resistance development can be addressed either by the release of susceptible strains or timely insecticide rotation. The present review discusses the resistance level in all important insect vectors of human diseases; the molecular basis of evolvement of resistance has also been discussed.

Keywords

Chemical control Vector-borne diseases Genetics Mutation 

References

  1. Acevedo GR, Zapater M, Toloza AC (2009) Insecticide resistance of house fly, Musca domestica (L.) from Argentina. Parasitol Res 105:489–493CrossRefPubMedGoogle Scholar
  2. Adler PH, McCreadie JW (1997) Insect life: the hidden ecology of black flies: sibling species and ecological scale. Am Entomol 43:153–162CrossRefGoogle Scholar
  3. Adler PH, Cheke RA, Post RJ (2010) Evolution, epidemiology, and population genetics of black flies (Diptera: Simuliidae). Infect Genet Evol 10:846–865CrossRefPubMedGoogle Scholar
  4. Akiner MM, Caglar SS (2006) The status and seasonal changes of organophosphate and pyrethroid resistance in Turkish populations of the house fly, Musca domestica L. (Diptera: Muscidae). J Vector Ecol 31:58–64CrossRefPubMedGoogle Scholar
  5. Amalraj DD, Sivagnaname N, Srinivasan R (1999) Susceptibility of Phlebotomus argentipes and P. papatasi (Diptera: Psychodidae) to insecticides. J Commun Dis 31:177–180PubMedGoogle Scholar
  6. Arnold JTA, Whitten MJ (1976) The genetic basis for organophosphorus resistance in the Australian sheep blowfly, Lucilia cuprina (Wiedemann) (Diptera, Calliphoridae). Bull Entomol Res 66:561–568CrossRefGoogle Scholar
  7. Benelli G (2015) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805CrossRefPubMedGoogle Scholar
  8. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL et al (2013) The global distribution and burden of dengue. Nature 496:504–07CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D (2010) Fleas and flea-borne diseases. Int J Infect Dis 14:667–676CrossRefGoogle Scholar
  10. Bossard RL (1997) Evaluation and use of bioassays for surveying insecticide susceptibility of cat fleas, Ctenocephalides fells felis (Bouch6). In: relation to resistance, Ph.D. dissertation. Kansas State University, ManhattanGoogle Scholar
  11. Brengues C, Hawkes NJ, Chandre F, McCarroll L, Duchon S, Guillet P et al (2003) Pyrethroid and DDT cross‐resistance in Aedes aegypti is correlated with novel mutations in the voltage‐gated sodium channel gene. Med Vet Entomol 17:87–94CrossRefPubMedGoogle Scholar
  12. Brown AWA (1986) Insecticide resistance in mosquitoes: a pragmatic review. J Am Mosq Control Assoc 2:123–40PubMedGoogle Scholar
  13. Chadwick PR, Invest JF, Bowron MJ (1977) An example of cross-resistance to pyrethroids in DDT resistant Aedes aegypti. Pestic Sci 8:618–624CrossRefGoogle Scholar
  14. Chai RY, Lee CY (2010) Insecticide resistance profiles and synergism in field populations of the German cockroach (Dictyoptera: Blattellidae) from Singapore. J Econ Entomol 103:460–471CrossRefPubMedGoogle Scholar
  15. Chen Z, Newcomb R, Forbes E, McKenzie J, Batterham P (2001) The acetylcholinesterase gene and organophosphorus resistance in the Australian sheep blowfly, Lucilia cuprina. Insect Biochem Mol Biol 31:805–816CrossRefPubMedGoogle Scholar
  16. Chen L, Zhong D, Zhang D, Shi L, Zhou G, Gong M et al (2010) Molecular ecology of pyrethroid knockdown resistance in Culex pipiens pallens mosquitoes. PLoS One 5(7):e11681CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chevillon C, Raymond M, Guillemaud T, Lenormand T, Pasteur N (1999) Population genetics of insecticide resistance in the mosquito Culex pipiens. Biol J Linnean Soc 68:147–157CrossRefGoogle Scholar
  18. Chiu TL, Wen Z, Rupasinghe SG, Schuler M (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proc Natl Acad Sci 105:8855–8860CrossRefPubMedPubMedCentralGoogle Scholar
  19. Clark AG, Shamaan NA (1984) Evidence that DDT-dehydrochlorinase from the house fly is a glutathione S-transferase. Pest Biochem Physiol 22:249–261CrossRefGoogle Scholar
  20. 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
  21. Cui F, Raymond M, Qiao C-L (2006) Insecticide resistance in vector mosquitoes in China. Pest Manag Sci 62:1013–1022CrossRefPubMedGoogle Scholar
  22. Depaquit J, Grandadam M, Fouque F, Andry PE, Peyrefitte C (2010) Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: a review. Euro Surveill 15:19507PubMedGoogle Scholar
  23. Desjeux P (1996) Leishmaniasis: public health aspects and control. Clin Derm 14:417–423CrossRefGoogle Scholar
  24. Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27:305–318CrossRefPubMedGoogle Scholar
  25. Diabate A, Baldet T, Chandre F, Akoobeto M, Guiguemde TR, Darriet F et al (2002) The role of agricultural use of insecticides in resistance to pyrethroids in Anopheles gambiae sl in Burkina Faso. Am J Trop Med Hyg 67:617–622PubMedGoogle Scholar
  26. Djogbénou L, Weill M, Hougard JM, Raymond M, Akogbeto M, Chandre F (2007) Characterization of insensitive acetylcholinesterase (ace-1R) in Anopheles gambiae (Diptera: Culicidae): resistance levels and dominance. J Med Entomol 44:805–810PubMedGoogle Scholar
  27. El-Gazzar LM, Milio J, Koehler PG, Patterson RS (1986) Insecticide resistance in the cat flea (Siphonaptera: Pulicidae). J Econ Entomol 79:132–134CrossRefPubMedGoogle Scholar
  28. Enayati AA, Vatandoost H, Ladonni H, Townson H, Hemingway J (2003) Molecular evidence for a kdr‐like pyrethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi. Med Vet Entomol 17:138–144CrossRefPubMedGoogle Scholar
  29. Erzinclioglu YZ (1987) The larvae of some blowflies of medical and veterinary importance. Med Vet Entomol 1:121–125CrossRefPubMedGoogle Scholar
  30. Etang J, Fondjo E, Chandre F, Morlais I, Brengues C, Nwane P et al (2006) First report of knockdown mutations in the malaria vector Anopheles gambiae from Cameroon. Am J Trop Med Hyg 74:795–797PubMedGoogle Scholar
  31. Farnham AW, Sawicki RM (1976) Development of resistance to pyrethroids in insects resistant to other insecticides. Pestic Sci 7:278–282CrossRefGoogle Scholar
  32. Gao J-R, Yoon KS, Lee SH, Takano-Lee M, Edman JD, Meinking TL et al (2003) Increased frequency of the T929I and L932F mutations associated with knockdown resistance in permethrin-resistant populations of the human head louse, Pediculus capitis, from California, Florida, and Texas. Pestic Biochem Physiol 77:115–124CrossRefGoogle Scholar
  33. Gao J-R, Yoon KS, Frisbie RK, Coles GC, Clark JM (2006) Esterase-mediated malathion resistance in the human head louse, Pediculus capitis (Anoplura: Pediculidae). Pestic Biochem Physiol 85:28–37CrossRefGoogle Scholar
  34. Gao JR, Kozaki T, Leichter CA, Rinkevich FD, Shono T, Scott JG (2007) The A302S mutation in Rdl that confers resistance to cyclodienes and limited cross-resistance to fipronil is undetectable in field populations of house flies from the USA. Pest Biochem Physiol 88(1):66–70CrossRefGoogle Scholar
  35. Georghiou GP (1972) The evolution of resistance to pesticides. Annu Rev Ecol Syst 133–168Google Scholar
  36. Gondhalekar AD, Scharf ME (2012) Mechanisms underlying fipronil resistance in a multiresistant field strain of the German cockroach (Blattodea: Blattellidae). J Med Entomol 49:122–131CrossRefPubMedGoogle Scholar
  37. Gong M-Q, Gu Y, Hu X-B, Sun Y, Ma L, Li X-L et al (2005) Cloning and overexpression of CYP6F1, a cytochrome P450 gene, from deltamethrin-resistant Culex pipiens pallens. Acta Bioch Bioph Sin 37:317–326CrossRefGoogle Scholar
  38. Hassan MM, Widaa SO, Osman OM, Numiary MSM, Ibrahim MA, Abushama HM (2012) Insecticide resistance in the sand fly, Phlebotomus papatasi from Khartoum State, Sudan. Parasit Vectors 5:46CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391CrossRefPubMedGoogle Scholar
  40. Hemingway J, Callaghan A, Kurtak DC (1991) Biochemical characterization of chlorphoxim resistance in adults and larvae of the Simulium damnosum complex (Diptera: Simulidae). Bull Entomol Res 81:401–6CrossRefGoogle Scholar
  41. Hemingway J, Small GJ, Monro AG (1993) Possible mechanisms of organophosphorus and carbamate insecticide resistance in German cockroaches (Dictyoptera: Blattelidae) from different geographical areas. J Econ Entomol 86:1623–1630CrossRefPubMedGoogle Scholar
  42. Kaku K, Matsumura F (1994) Identification of the site of mutation within the M2 region of the GABA receptor of the cyclodiene-resistant German cockroach. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 108:367–376CrossRefPubMedGoogle Scholar
  43. Kasai S, Scott J (2000) Overexpression of cytochrome P450 CYP6D1 is associated with monooxygenase-mediated pyrethroid resistance in house flies from Georgia. Pest Biochem Physiol 68:34–41CrossRefGoogle Scholar
  44. Khan HAA, Shad SA, Akram W (2012) Effect of livestock manures on the fitness of house fly, Musca domestica L. (Diptera: Muscidae). Parasitol Res 111:1165–1171CrossRefPubMedGoogle Scholar
  45. Kim NJ, Chang KS, Lee WJ, Ahn YJ (2007) Monitoring of insecticide resistance in field-collected populations of Culex pipiens pallens (Diptera: Culicidae). J Asia Pac Entomol 10:257–261CrossRefGoogle Scholar
  46. Ko CJ, Elston DM (2004) Pediculosis. J Am Acad Dermatol 50:1–12CrossRefPubMedGoogle Scholar
  47. Kobayashi M, Sasaki T, Saito N, Tamura K, Suzuki H, Watanabe H, Agui N (1999) Houseflies are not simple mechanical vectors of enterohemorragic Escherichia coli O157:H7. Am J Trop Med Hyg 61:625–629PubMedGoogle Scholar
  48. Krafsur ES (2009) Tsetse flies: genetics, evolution, and role as vectors. Infect Genet Evol 9:124–141CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kristensen M, Jespersen JB (2003) Larvicide resistance in Musca domestica (Diptera: Muscidae) populations in Denmark and establishment of resistant laboratory strains. J Econ Entomol 96:1300–1306CrossRefPubMedGoogle Scholar
  50. Kristensen M, Jespersen JB, Knorr M (2004) Cross‐resistance potential of fipronil in Musca domestica. Pest Manag Sci 60:894–900CrossRefPubMedGoogle Scholar
  51. Lee SW, Kasai S, Komagata O, Kobayashi M, Agui N, Kono Y et al (2007) Molecular characterization of two acetylcholinesterase cDNAs in Pediculus human lice. J Med Entomol 44:72–79CrossRefPubMedGoogle Scholar
  52. Lemke LA, Koehler PG, Patterson RS (1989) Susceptibility of the cat flea (Siphonaptera: Pulicidae) to pyrethroids. J Econ Entomol 82:839–841CrossRefPubMedGoogle Scholar
  53. Liu W-D (1990) The evolution of insecticides resistance of mosquitoes in China (in Chinese). Chin J Vec Biol Contr 1:41–44Google Scholar
  54. Liu N, Scott JG (1998) Increased transcription of CYP6D1 causes cytochrome P450-mediated insecticide resistance in house fly. Insect Biochem Mol Biol 28:531–535CrossRefPubMedGoogle Scholar
  55. Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J Econ Entomol 93:1269–1275CrossRefPubMedGoogle Scholar
  56. Liu Z, Valles SM, Dong K (2000) Novel point mutations in the German cockroach para sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid insecticides. Insect Biochem Mol Biol 30:991–997CrossRefPubMedPubMedCentralGoogle Scholar
  57. Macnair MR (1991) Genetica 84:213–219CrossRefGoogle Scholar
  58. Macoris MDLG, Andrighetti MTM, Takaku L, Glasser CM, Garbeloto VC, Bracco JE (2003) Resistance of Aedes aegypti from the state of São Paulo, Brazil, to organophosphates insecticides. Mem I Oswaldo Cruz 98:703–708CrossRefGoogle Scholar
  59. Malik A, Singh N, Satya S (2007) House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health Part B 42:453–469CrossRefGoogle Scholar
  60. Mazzarri MB, Georghiou GP (1995) Characterization of resistance to organophosphate, carbamate, and pyrethroid insecticides in field populations of Aedes aegypti from Venezuela. J Am Mosq Control Assoc 11:315–322PubMedGoogle Scholar
  61. McKenzie JA (1985) In Resistance in nematodes to anthelmintic drugs (Anderson, N. and Wailer, P.J.. eds). CSIRO. Australian Wool Corporation, pp. 89–95.Google Scholar
  62. McKenzie JA, O’farrell K (1993) Modification of developmental instability and fitness: malathion-resistance in the Australian sheep blowfly, Lucilia cuprina. Genetica 89:67–76CrossRefGoogle Scholar
  63. Metcalf RL (1989) Insect resistance to insecticides. Pestic Sci 26:333–358CrossRefGoogle Scholar
  64. Montagna CM, Anguiano OL, Gauna LE, Pechen de D’Angelo AM (1999) Resistance to pyrethroids and DDT in a field-mixed population of Argentinean black flies (Diptera: Simuliidae). J Econ Entomol 92:1243–1245CrossRefGoogle Scholar
  65. Montagna CM, Anguiano OL, Gauna LE, Pechen DD, Angelo AM (2003) Mechanisms of resistance to DDT and pyrethroids in Patagonian populations of Simulium blackflies. Med Vet Entomol 17:95–101CrossRefPubMedGoogle Scholar
  66. Montagna CM, Gauna LE, D’Angelo APD, Anguiano OL (2012) Evolution of insecticide resistance in non-target black flies (Diptera: Simuliidae) from Argentina. Mem Inst Oswaldo Cruz 107:458–465CrossRefPubMedGoogle Scholar
  67. Moyses EW (1995) Measurement of insecticide resistance in the adult cat flea. In: Meola RW (ed) Proceedings of the Third International Symposium on Ectoparasites of Pets, 2-4 April, College Station. Texas A&M University, College Station TX, TX, pp 21–34Google Scholar
  68. Murugan K, Vadivalagan C, Karthika P, Panneerselvam C, Paulpandi M, Subramaniam J et al (2015) DNA barcoding and molecular evolution of mosquito vectors of medical and veterinary importance. Parasitol Res 11:1–15Google Scholar
  69. Naeem A, Jaleel W, Saeed Q, Zaka SM, Saeed S, Naqqash MN et al. (2014) Life style of people and surveillance of management related to cockroaches in Southern Punjab, Pakistan. Turk J Agri Nat Sci 1:227–233Google Scholar
  70. Naqqash MN, Saeed Q, Saeed S, Jaleel W, Zaka SM, Faheem M et al (2014) A cross sectional survey of community awareness about typhoid and its major vector cockroach in southern Punjab, Pakistan. Middle-East J Sci Res 21:602–608Google Scholar
  71. 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 94:7464–7468CrossRefPubMedPubMedCentralGoogle Scholar
  72. Parker AG, Russell RJ, Delves AC, Oakeshott JG (1991) Biochemistry and physiology of esterases in organophosphate-susceptible and-resistant strains of the Australian sheep blowfly, Lucilia cuprina. Pestic Biochem Physiol 41:305–318CrossRefGoogle Scholar
  73. Paul A, Harrington LC, Scott JG (2006) Evaluation of novel insecticides for control of dengue vector Aedes aegypti (Diptera: Culicidae). J Med Entomol 43:55–60CrossRefPubMedGoogle Scholar
  74. Peiris HTR, Hemingway J (1993) Characterisation and inheritance of elevated esterases in organophosphorus and carbamate insecticide resistant Culex quinquefasciatus (Diptera: Culicidae) from Sri Lanka. Bull Entomol Res 83:127–132CrossRefGoogle Scholar
  75. Pethuan S, Jirakanjanakit N, Saengtharatip S, Chareonviriyaphap T, Kaewpa D, Rongnoparut P (2007) Biochemical studies of insecticide resistance in Aedes aegypti (Stegomyia) and Aedes albopictus (Stegomyia) (Diptera: Culicidae) in Thailand. Trop Biomed 24:7–15PubMedGoogle Scholar
  76. Pimprikar GD, Georghiou GP (1979) Mechanisms of resistance to diflubenzuron in the house fly, Musca domestica (L.). Pest Biochem Physiol 12:10–22CrossRefGoogle Scholar
  77. Porretta D, Gargani M, Bellini R, Medici A, Punelli F, Urbanelli S (2008) Defence mechanisms against insecticides temephos and diflubenzuron in the mosquito Aedes caspius: the P‐glycoprotein efflux pumps. Med Vet Entomol 22:48–54CrossRefPubMedGoogle Scholar
  78. Pridgeon JW, Zhang L, Liu N (2003) Overexpression of CYP4G19 associated with a pyrethroid-resistant strain of the German cockroach, Blattella germanica (L.). Gene 314:157–163CrossRefPubMedGoogle Scholar
  79. Qiao CL, Sun ZQ, Liu JE (1999) New esterase enzymes involved in organophosphate resistance in Culex pipiens (Diptera: Culicidae) from Guang Zhou, China. J Med Entomol 36:666–670CrossRefPubMedGoogle Scholar
  80. Ranson H, Jensen B, Wang X, Prapanthadara L, Hemingway J, Collins FH (2000) Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Mol Biol 9:499–507CrossRefPubMedGoogle Scholar
  81. Ranson H, Paton MG, Jensen B, McCarroll L, Vaughan A, Hogan JR et al (2004) Genetic mapping of genes conferring permethrin resistance in the malaria vector, Anopheles gambiae. Insect Mol Biol 13:379–386CrossRefPubMedGoogle Scholar
  82. Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbé C, Yangalbé-Kalnoné E et al (2009) Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J 8:299CrossRefPubMedPubMedCentralGoogle Scholar
  83. Riordan EK (1987) Insecticide tolerance of pregnant females of Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae). Bull Entomol Res 77:213–226CrossRefGoogle Scholar
  84. Rodríguez MM, Bisset J, Ruiz M, Soca A (2002) Cross-resistance to pyrethroid and organophosphorus insecticides induced by selection with temephos in Aedes aegypti (Diptera: Culicidae) from Cuba. J Med Entomol 39:882–888CrossRefPubMedGoogle Scholar
  85. Roush RT, McKenzie JA (1987) Annu Rev Entomol 32:361–380CrossRefPubMedGoogle Scholar
  86. Scott JG (1999) Cytochromes P450 and insecticide resistance. Insect Biochem Mol Biol 29:757–777CrossRefPubMedGoogle Scholar
  87. Scott JG, Alefantis TG, Kaufman PE, Rutz DA (2000) Insecticide resistance in house flies from caged-layer poultry facilities. Pest Manag Sci 147–153Google Scholar
  88. Service MW (1993) Mosquitoes (Culicidae). In: Lane RP, Crosskey RW (eds) Medical insects and arachnids. Chapman & Hall, London, pp 120–240CrossRefGoogle Scholar
  89. Shi J, Lan Z, Zhang XG (2011) Characterisation of spinosad 1 resistance in the housefly Musca domestica (Diptera: Muscidae). Pest Manag Sci 67:335–340CrossRefPubMedGoogle Scholar
  90. 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 73:27–36CrossRefGoogle Scholar
  91. Valles SM, Koehler PG, Brenner RJ (1997) Antagonism of fipronil toxicity by piperonyl butoxide and S, S, S-tributyl phosphorotrithioate in the German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 90:1254–1258CrossRefGoogle Scholar
  92. Vatandoost H, McCaffery HR, Townson H (1998) An electrophysiological investigation of target site insensitivity in permethrin-resistant and susceptible strain of Anopheles stephensi. Iran J Publ Health 27:29–38Google Scholar
  93. Walsh S, Dolden T, Moores G, Kristensen M, Lewis T, Devonshire AL, Williamson M (2001) Identification and characterization of mutations in housefly (Musca domestica) acetylcholinesterase involved in insecticide resistance. Biochem J 359:175–181CrossRefPubMedPubMedCentralGoogle Scholar
  94. Wei SH, Clark AG, Syvanen M (2001) Identification and cloning of a key insecticide-metabolizing glutathione S-transferase (MdGST-6A) from a hyper insecticide-resistant strain of the housefly Musca domestica. Insect Biochem mol Biol 31:1145–1153CrossRefPubMedGoogle Scholar
  95. WHO (2011) World Malaria Report 2011. World Health Organization, GenevaGoogle Scholar
  96. WHO-World Health Organization 2003. Dengue (online, access in 03/06/2003). Available at http://www.who.int/inf-fs/en/fact117.html
  97. WHO-World Health Organization, Expert Committee on Vector Biology and Control (1992). Vector resistance to pesticides, 818 report, unpublished document, WHO technical report series, pp. 63Google Scholar
  98. 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 MGG 240:17–22CrossRefPubMedGoogle Scholar
  99. Yoon KS, Gao J-R, Lee SH, Coles GC, Meinking TL, Taplin D et al (2004) Resistance and cross-resistance to insecticides in human head lice from Florida and California. Pestic Biochem Physiol 80:192–201CrossRefGoogle Scholar
  100. Zhang L, Harada K, Shono T (1997) Genetic analysis of pyriproxyfen resistance in the housefly, Musca domestica L. Appl Entomol Zool 32:217–226Google Scholar
  101. Zhang L, Gao X, Liang P (2007) Beta-cypermethrin resistance associated with high carboxylesterase activities in a strain of house fly, Musca domestica (Diptera: Muscidae). Pest Biochem Physiol 89:65–72CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Muhammad Nadir Naqqash
    • 1
  • Ayhan Gökçe
    • 1
  • Allah Bakhsh
    • 2
  • Muhammad Salim
    • 1
  1. 1.Department of Plant Production & Technologies, Ayhan Şahenk Faculty of Agricultural Sciences and TechnologiesNiğde UniversityNiğdeTurkey
  2. 2.Department of Agricultural Genetic Engineering, Ayhan Şahenk Faculty of Agricultural Sciences and TechnologiesNiğde UniversityNiğdeTurkey

Personalised recommendations