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Cross-resistance, genetics, and realized heritability of resistance to fipronil in the house fly, Musca domestica (Diptera: Muscidae): a potential vector for disease transmission

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Abstract

Houseflies, Musca domestica (L.), are ubiquitous pests that have the potential to spread a variety of pathogens to humans, poultries, and dairies. Pesticides are commonly used for the management of this pest. Fipronil is a GABA-gated chloride channel-inhibiting insecticide that has been commonly used for the management of different pests including M. domestica throughout the world. Many pests have developed resistance to this insecticide. A field-collected strain of M. domestica was selected with fipronil for continuous 11 generations to assess the cross-resistance, genetics, and realized heritability for designing a resistance management strategy. Laboratory bioassays were performed using the feeding method of mixing insecticide concentrations with 20 % sugar solutions and cotton soaks dipped in insecticide solutions were provided to tested adult flies. Bioassay results at G12 showed that the fipronil-selected strain developed a resistance ratio of 140-fold compared to the susceptible strain. Synergism bioassay with piperonyl butoxide (PBO) and S,S,S,-tributyl phosphorotrithioate (DEF) indicated that fipronil resistance was associated with microsomal oxidase and also esterase. Reciprocal crosses between resistant and susceptible strains showed an autosomal and incompletely dominant resistance to fipronil. The LC50 values of F1 and F′1 strains were not significantly different and dominance values were 0.74 and 0.64, respectively. The resistance to fipronil was completely recessive (D ML  = 0.00) at the highest dose and incompletely dominant at the lowest dose (D ML  = 0.87). The monogenic resistance based on chi-square goodness of fit test and calculation of the minimum number of segregating genes showed that resistance to fipronil is controlled by multiple genes. The fipronil resistance strain confirmed very low cross-resistance to emamectin benzoate and spinosad while no cross-resistance to chlorpyrifos and acetamiprid when compared to that of the field population. The heritability values were 0.112, 0.075, 0.084, 0.008, and 0.052 for fipronil, emamectin benzoate, spinosad, acetamiprid, and chlorpyrifos, respectively. It was concluded that fipronil resistance in M. domestica was autosomally inherited, incompletely dominant, and polygenic. These findings would be helpful for the better and successful management of M. domestica.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Google Scholar 

  • Acevedo GR, Zapater M, Toloza AC (2009) Insecticide resistance of house fly, Musca domestica (L.) from Argentina. Parasitol Res 105:489–493

    Article  PubMed  Google Scholar 

  • Ahmad M, Sayyed AH, Crickmore N, Saleem MA (2007) Genetics and mechanism of resistance to deltamethrin in a field population of Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci 63:1002–1010

    Article  CAS  PubMed  Google Scholar 

  • Ahmad M, Sayyed AH, Saleem MA, Ahmad M (2008) Evidence for field evolved resistance to newer insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. Crop Prot 27:1367–1372

    Article  CAS  Google Scholar 

  • Ali A, Nayar JK, Gu WD (1998) Toxicity of a phenyl pyrazole insecticide, fipronil, to mosquito and chironomid midge larvae in the laboratory. J Am Mosq Control Assoc 14:216–218

    CAS  PubMed  Google Scholar 

  • Barin A, Arabkhazaeli F, Rahbari S, Madani S (2010) The house fly, Musca domestica, as a possible mechanical vector of Newcastle disease virus in the laboratory and field. Med Vet Entomol 24:88–90

    Article  CAS  PubMed  Google Scholar 

  • Barnes EH, Dobson RJ, Barger IA (1995) Worm control and anthelmintic resistance: adventures with a model. Parasitol Today 11:56–63

    Article  CAS  PubMed  Google Scholar 

  • Bell HA, Robinson KA, Weaver RJ (2010) First report of cyromazine resistance in a population of UK housefly (Musca domestica) associated with intensive livestock production. Pest Manag Sci 66:693–695

    Article  CAS  PubMed  Google Scholar 

  • Bourguet D, Genissel A, Raymond M (2000) Insecticide resistance and dominance levels. J Econ Entomol 93:1588–1595

    Article  CAS  PubMed  Google Scholar 

  • Bourguet D, Raymond M (1998) The molecular basis of dominance relationships: the case of some recent adaptive genes. J Evol Biol 11:103–122

    Article  Google Scholar 

  • Bouvier JC, Bues R, Boivin T, Boudinhon L, Beslay D, Sauphanor B (2001) Deltamethrin resistance in codling moth: inheritance and number of genes involved. Heredity 87:456–462

    Article  CAS  PubMed  Google Scholar 

  • Chilcutt CF, Tabashnik BE (1995) Evaluation of pesticide resistance and slope of the concentration-mortality line: are they related? J Econ Entomol 88:11–20

    CAS  Google Scholar 

  • Cole LM, Nicholso RA, Casida JE (1993) Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Pestic Biochem Physiol 46:47–54

    Article  CAS  Google Scholar 

  • Deacutis JM, Leichter CA, Gerry AC, Rutz DA, Watson WD, Geden CJ, Scott JG (2006) Susceptibility of field collected house flies to spinosad before and after a season of use. J Agric Urban Entomol 23:105–110

    CAS  Google Scholar 

  • Falconer DS (1989) Introduction to quantitative genetics. Longman, London

    Google Scholar 

  • Ferre J, Van RJ (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47:501–533

    Article  CAS  PubMed  Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University Press, New York

    Google Scholar 

  • Forster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K (2007) Pilot studies on synantropic flies (e.g. Musca, Sarcophaga, Calliphora, Fania, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol Res 101:243–246

    Article  PubMed  Google Scholar 

  • Georghiou GP (1969) Genetics of resistance to insecticides in house flies and mosquitoes. Exp Parasitol 26:224–255

    Article  CAS  PubMed  Google Scholar 

  • Georghiou GP (1983) Management of resistance in arthropods. In: Georghiou GP, Saito T (eds) Pest resistance to pesticides. Plenum, New York, pp 769–792

    Chapter  Google Scholar 

  • Groeters FR, Tabashnik BE (2000) Roles of selection intensity, major genes, and minor genes in evolution of insecticide resistance. J Econ Entomol 93:1580–1587

    Article  CAS  PubMed  Google Scholar 

  • Hainzl D, Cole LM, Casida JE (1998) Mechanisms for selective toxicity of fipronil insecticide and its sulfone metabolite and desulfinyl photoproduct. Chem Res Toxicol 11:1529–1535

    Article  CAS  PubMed  Google Scholar 

  • Heckel DG, Gahan LJ, Liu YB, Tabashnik BE (1999) Genetic mapping of resistance to Bacillus thuringiensis toxins in diamondback moth using biphasic linkage analysis. Proc Natl Acad Sci U S A 96:8373–8377

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoskins WM (1960) Use of the dosage mortality curve in quantitative estimation of insecticide resistance. Entomol Soc Am 2:85–91

    Google Scholar 

  • Ikeda T, Zhao X, Kono Y, Yeh JZ, Narahashi T (2003) Fipronil modulation of glutamate-induced chloride currents in cockroach thoracic ganglion neurons. Neurotoxicology 24:807–815

    Article  CAS  PubMed  Google Scholar 

  • Jiang WH, Han ZJ, Hao ML (2005) Primary study on resistance of rice stem borer (Chilo suppressalis) to fipronil. Chinese J Rice Sci 19:577–579

    CAS  Google Scholar 

  • Kaufman PE, Gerry AC, Rutz DA, Scott JG (2006) Monitoring susceptibility of house flies (Musca domestica L.) in the United States to imidacloprid. J Agric Urban Entomol 23:195–200

    CAS  Google Scholar 

  • Kaufman PE, Nunez SC, Mann RS, Christopher GJ, Scharfa E (2010) Nicotinoid and pyrethroid insecticide resistance in house flies (Diptera: Muscidae) collected from Florida dairies. Pest Manag Sci 66:290–294

    Article  CAS  PubMed  Google Scholar 

  • Kaufman PE, Scott JG, Rutz DA (2001) Monitoring insecticide resistance in house flies (Diptera: Muscidae) from New York dairies. Pest Manag Sci 57:514–521

    Article  CAS  PubMed  Google Scholar 

  • Khan HAA, Shad SA, Akram W (2012) Effect of livestock manures on the fitness of house fly, Musca domestica L. (Diptera: Muscidae). Parasitol Res 111:1165–1171

    Article  PubMed  Google Scholar 

  • Khan HAA, Akram W, Shad SA (2013a) Resistance to conventional insecticides in Pakistani populations of Musca domestica L. (Diptera: Muscidae): a potential ectoparasite of dairy animals. Ecotoxicol 22:522–527

    Article  CAS  Google Scholar 

  • Khan HAA, Akram W, Shad SA, Razaq M, Naeem-Ullah U, Zia K (2013b) A cross sectional survey of knowledge, attitude and practices related to house flies among dairy farmers in Punjab, Pakistan. J Ethnobiol Ethnomed 9:18

    Article  PubMed Central  PubMed  Google Scholar 

  • Khan HAA, Shad SA, Akram W (2013c) Resistance to new chemical insecticides in the house fly Musca domestica L., from dairies in Punjab, Pakistan. Parasitol Res 112:2049–2054

    Article  PubMed  Google Scholar 

  • Kristensen M, Jespersen JB, Knorr M (2004) Cross-resistance potential of fipronil in Musca domestica. Pest Manag Sci 60:894–900

    Article  CAS  PubMed  Google Scholar 

  • Kumar P, Mishra S, Malik A, Satya S (2012) Insecticidal evaluation of essential oils of Citrus sinensis L. (Myrtales: Myrtaceae) against housefly, Musca domestica L. (Diptera: Muscidae). Parasitol Res 110:1929–1936

    Article  PubMed  Google Scholar 

  • Kumar P, Mishra S, Malik A, Satya S (2013) Housefly (Musca domestica L.) control potential of Cymbopogon citratus Stapf. (Poales: Poaceae) essential oil and monoterpenes (citral and 1,8-cineole). Parasitol Res 112:69–76

    Article  PubMed  Google Scholar 

  • Lande R (1981) The minimum number of genes contributing to quantitative variation between and within populations. Genetics 99:541–553

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lecoq M, Balanc G (1998) Field trials of fipronil for control of Rhammatocerus schistocercoides hopper bands in Brazil. Crop Prot 17:105–110

    Article  CAS  Google Scholar 

  • Software LO (2005) POLO for Windows. LeOra Software, Petaluma

    Google Scholar 

  • Litchfield JT, Wilcoxon F (1949) A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 99:99–103

    Google Scholar 

  • Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J Econ Entomol 93:1269–1275

    Article  CAS  PubMed  Google Scholar 

  • Liu N, Yue X (2001) Genetics of pyrethroid resistance in a strain (ALHF) of house flies (Diptera: Muscidae). Pestic Biochem Physiol 70:151–158

    Article  CAS  Google Scholar 

  • Marcon PCRG, Thomas GD, Siegfried BD, Campbell JB, Skoda SR (2003) Resistance status of house flies (Diptera: Muscidae) from southeastern Nebraska beef cattle feedlots to selected insecticides. J Econ Entomol 96:1016–1020

    Article  CAS  PubMed  Google Scholar 

  • McKenzie JA, Anthony G, Parker AG, Janet L, Yen JL (1992) Polygenic and single gene responses to selection for resistance to Diazinon in Lucilia cuprina. Genetics 130:613–620

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mishra S, Kumar P, Malik A, Satya S (2011) Adulticidal and larvicidal activity of Beauveria bassiana and Metarhizium anisopliae against housefly, Musca domestica (Diptera: Muscidae), in laboratory and simulated field bioassays. Parasitol Res 108:1483–1492

    Article  PubMed  Google Scholar 

  • Morey RA, Khandagle AJ (2012) Bioefficacy of essential oils of medicinal plants against housefly, Musca domestica L. Parasitol Res 111:1799–1805

    Article  PubMed  Google Scholar 

  • Roush RT, Daly JC (1990) The role of population genetics in resistance research and management. In: Roush RT, Tabashnik BE (eds) Pesticide Resistance in Arthropods. Chapman and Hall, New York, pp 97–152

    Chapter  Google Scholar 

  • Roush RT, Mckenzie (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361–380

    Article  CAS  PubMed  Google Scholar 

  • Sayyed AH, Attique MNR, Khaliq A, Wright DJ (2005) Inheritance of resistance to deltamethrin in Plutella xylostella (Lepidoptera: Plutellidae) from Pakistan. Pest Manag Sci 61:636–642

    Article  CAS  PubMed  Google Scholar 

  • Sayyed AH, Haward R, Herrero S, Ferre J, Wright DJ (2000) Genetic and biochemical approach for characterisation of resistance to Bacillus thuringiensis toxin Cry1Ac in a field population of the diamondback moth. Appl Environ Microbiol 66:1509–1516

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sayyed AH, Wright DJ (2001) Cross-resistance and inheritance of resistance Cry1Ac toxin in diamondback moth, Plutella xylostella from lowland Malaysia. Pest Manag Sci 57:413–421

    Article  CAS  PubMed  Google Scholar 

  • Sayyed AH, Wright DJ (2004) Fipronil resistance in the diamondback moth (Lepidoptera: Plutellidae): inheritance and number of genes involved. J Econ Entomol 97:2043–2050

    Article  CAS  PubMed  Google Scholar 

  • Scharf ME, Siegfried BD, Meinke LJ, Chandler LD (2000) Fipronil metabolism, oxidative sulfone formation and toxicity among organophosphate- and carbamate-resistant and susceptible western corn rootworm populations. Pest Manag Sci 56:757–766

    Article  CAS  Google Scholar 

  • Scott JG, Alefantis TG, Kaufman PE, Rutz DA (2000) Insecticide resistance in house flies from caged-layer poultry facilities. Pest Manag Sci 56:147–153

    Article  CAS  Google Scholar 

  • Scott JG, Shono T, Georghiou GP (1984) Genetic analysis of permethrin resistance in the house fly, Musca domestica L. Experientia 40:1416–1418

    Article  Google Scholar 

  • Scott JG, Wen Z (1997) Toxicity of fipronil to susceptible and resistant strains of German cockroaches (Dictyoptera: Blattellidae) and house flies (Diptera: Muscidae). J Econ Entomol 90:1152–1156

    CAS  Google Scholar 

  • Shi J, Zhang L, Gao X (2011) Characterisation of spinosad resistance in the house fly Musca domestica (Diptera: Muscidae). Pest Manag Sci 67:335–340

    Article  CAS  PubMed  Google Scholar 

  • Shono T, Kasai S, Kamiya E, Kono Y, Scott JG (2002) Genetics and mechanisms of permethrin resistance in the YPER strain of house fly. Pestic Biochem Physiol 73:27–36

    Article  CAS  Google Scholar 

  • Shono T, Zhang L, Scott JG (2004) Indoxacarb resistance in the house fly, Musca domestica. Pestic Biochem Physiol 80:106–112

    Article  CAS  Google Scholar 

  • Siegfried BD, Spencer T, Marc PCRG (1999) Susceptibility of European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Pyralidae) neonate larvae to fipronil. J Agric Urban Entomol 16:273–278

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, San Francisco

    Google Scholar 

  • Stone BF (1968) A formula for determining degree of dominance in cases of monofactorial inheritance of resistance to chemicals. Bull WHO 38:325–326

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tabashnik BE (1991) Determining the mode of inheritance of pesticide resistance with backcross experiments. J Econ Entomol 84:703–712

    CAS  PubMed  Google Scholar 

  • Tabashnik BE (1992) Resistance risk assessment: realized heritability of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae), tobacco budworm (Lepidoptera: Noctuidae) and Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 85:1551–1559

    Google Scholar 

  • Tang J, Li J, Shao Y, Yang B, Liu Z (2010) Fipronil resistance in the whitebacked planthopper (Sogatella furcifera): possible resistance mechanisms and cross-resistance. Pest Manag Sci 66:121–125

    Article  CAS  PubMed  Google Scholar 

  • Tang JD, Caprio MA, Sheppard DC, Gaydon DM (2002) Genetics and fitness costs of cyromazine resistance in the house fly (Diptera: Muscidae). J Econ Entomol 95:1251–1260

    Article  CAS  PubMed  Google Scholar 

  • Tikar SN, Kumar A, Prasad GB, Prakash S (2009) Temephos-induced resistance in Aedes aegypti and its cross-resistance studies to certain insecticides from India. Parasitol Res 105:57–63

    Article  CAS  PubMed  Google Scholar 

  • 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 90:1254–1258

    CAS  Google Scholar 

  • Wanaratana S, Panyim S, Pakpinyo S (2011) The potential of house flies to act as a vector of avian influenza subtype H5N1 under experimental conditions. Med Vet Entomol 25:58–63

    Article  CAS  PubMed  Google Scholar 

  • Wen Z, Scott JG (1999) Genetic and biochemical mechanisms limiting fipronil toxicity in the LPR strain of house fly, Musca domestica. Pestic Sci 55:988–992

    Article  CAS  Google Scholar 

  • Zhang L, Shi J, Gao X (2008) Inheritance of beta-cypermethrin resistance in the housefly Musca domestica (Diptera: Muscidae). Pest Manag Sci 64:185–190

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors highly thank the Higher Education Commission, Pakistan for providing fund to perform this study.

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The authors declare that there are no conflicts of interest.

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Correspondence to Naeem Abbas or Sarfraz Ali Shad.

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Abbas, N., Khan, H.A.A. & Shad, S.A. Cross-resistance, genetics, and realized heritability of resistance to fipronil in the house fly, Musca domestica (Diptera: Muscidae): a potential vector for disease transmission. Parasitol Res 113, 1343–1352 (2014). https://doi.org/10.1007/s00436-014-3773-4

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