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Genetics and mechanism of resistance to chlorantraniliprole in Musca domestica L. (Diptera: Muscidae)

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Abstract

The house fly, Musca domestica L. is an important mechanical vector of different pathogens of medical and veterinary importance. It is an organism well-known for its ability to develop insecticide resistance. In the current study, we investigated the genetic basis and mechanism of chlorantraniliprole resistance in a field strain of house fly by selecting it artificially in the laboratory with a commercial formulation of chlorantraniliprole (CTPR-SEL). After seven generations of consecutive selection with chlorantraniliprole, CTPR-SEL strain developed a 644-fold resistance compared with the Susceptible strain and a 3-fold resistance compared with the field strain. Reciprocal crossing between the CTPR-SEL and Susceptible homozygous strains revealed an autosomal and incomplete dominant mode of resistance to chlorantraniliprole. A direct test using a monogenic inheritance model based on chi-square analysis revealed that the resistance was governed by more than one gene. Bioassays with synergists indicated that esterases might be involved in the resistance of house fly to chlorantraniliprole. These findings may be helpful to the development of an improved strategy for chlorantraniliprole resistance management in house fly.

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References

  • Abbas N, Khan HAA, Shad SA (2014) 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

    Article  Google Scholar 

  • Abbas N, Ijaz M, Shad SA, Binyameen M (2016) Assessment of resistance risk to fipronil and cross resistance to other insecticides in the Musca domestica L. (Diptera: Muscidae). Vet Parasitol 223:71–76

    Article  CAS  Google Scholar 

  • Abhilash P, Singh N (2009) Pesticide use and application: an Indian scenario. J Hazard Mater 165:1–12

    Article  CAS  Google Scholar 

  • Bentley KS, Fletcher JL, Woodward MD (2010) Chlorantraniliprole: an insecticide of the anthranilic diamide class. In: Krieger R (ed) Hayes’ Handbook of pesticide toxicology (3rd edn). Elsevier, Cambridge, Massachusetts, United States, pp 2231–2242

  • Binns M, Nyrop J (1992) Sampling insect populations for the purpose of IPM decision making. Annu Rev Entomol 37:427–453

    Article  Google Scholar 

  • Bolzan A et al. (2019) Selection and characterization of the inheritance of resistance of Spodoptera frugiperda (Lepidoptera: Noctuidae) to chlorantraniliprole and cross‐resistance to other diamide insecticides. Pest Manag Sci 75:2682–2689

    Article  CAS  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 J-C, Buès R, Boivin T, Boudinhon L, Beslay D, Sauphanor B (2001) Deltamethrin resistance in the codling moth (Lepidoptera: Tortricidae): inheritance and number of genes involved. Heredity 87:456

    Article  CAS  Google Scholar 

  • Busvine J (1957) Inheritance of insecticide resistance in the housefly. B World Health Organ 16:205

    CAS  Google Scholar 

  • Consortium R (2013) Heterogeneity of selection and the evolution of resistance. Trends Ecol Evol 28:110–118

    Article  Google Scholar 

  • Cordova D et al. (2006) Anthranilic diamides: a new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic Biochem Phys 84:196–214

    Article  CAS  Google Scholar 

  • Cordova D et al. (2007) Elucidation of the mode of action of Rynaxypyr®, a selective ryanodine receptor activator. Pesticide Chemistry, Crop Protection, Public Health, and Environmental Safety. Wiley-VCH Verlag GmbH & C, Weinheim Germany, pp 121–126

    Google Scholar 

  • Dubendorfer A, Hediger M, Burghardt G, Bopp D (2003) Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 46:75–79

    Google Scholar 

  • Environmental Protection Agency (2017) Reduced risk and organophosphate alternative decisions for conventional pesticides. United States Environmental Protection Agency. https://www.epa.gov/pesticide-registration/reduced-risk-and-organophosphate-alternative-decisions-conventional

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

    Google Scholar 

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

    Article  Google Scholar 

  • Freeman JC, Ross DH, Scott JG (2019) Insecticide resistance monitoring of house fly populations from the United States. Pesticide Biochem Physiol 158:61–68

    Article  CAS  Google Scholar 

  • Garrood WT, Zimmer CT, Gorman KJ, Nauen R, Bass C, Davies TG (2016) Field‐evolved resistance to imidacloprid and ethiprole in populations of brown planthopper Nilaparvata lugens collected from across South and East Asia. Pest Manag Sci 72:140–149

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Georghiou GP, Taylor CE (1986) Factors influencing the evolution of resistance. Pesticide resistance: strategies and tactics for management. National Academy Press, United States, p 157–169

    Google Scholar 

  • Graczyk TK, Knight R, Gilman RH, Cranfield MR (2001) The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 3:231–235

    Article  CAS  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  Google Scholar 

  • Guo L, Liang P, Zhou X, Gao X (2014) Novel mutations and mutation combinations of ryanodine receptor in a chlorantraniliprole resistant population of Plutella xylostella (L.). Sci Rep-UK 4:6924

    Article  CAS  Google Scholar 

  • Helps J, Paveley N, van den Bosch F (2017) Identifying circumstances under which high insecticide dose increases or decreases resistance selection. J Theor Biol 428:153–167

    Article  CAS  Google Scholar 

  • Hu Z-D et al. (2014) Biochemical mechanism of chlorantraniliprole resistance in the diamondback moth Plutella xylostella Linnaeus. J Integr Agr 13:2452–2459

    Article  CAS  Google Scholar 

  • Jiang W-H, Lu W-P, Guo W-C, Xia Z-H, Fu W-J, Li G-Q (2012) Chlorantraniliprole susceptibility in Leptinotarsa decemlineata in the north Xinjiang Uygur autonomous region in China. J Econ Entomol 105:549–554

    Article  CAS  Google Scholar 

  • Jutsum AR, Heaney SP, Perrin BM, Wege PJ (1998) Pesticide resistance: assessment of risk and the development and implementation of effective management strategies. Pestic Sci 54:435–446

    Article  CAS  Google Scholar 

  • Lahm GP et al. (2005) Insecticidal anthranilic diamides: a new class of potent ryanodine receptor activators. Bioorg Med Chem Lett 15:4898–4906

    Article  CAS  Google Scholar 

  • Lahm GP et al. (2007) Rynaxypyr™: a new insecticidal anthranilic diamide that acts as a potent and selective ryanodine receptor activator. Bioorg Med Chem Lett 17:6274–6279

    Article  CAS  Google Scholar 

  • Lai T, Su J (2011) Assessment of resistance risk in Spodoptera exigua (Hübner)(Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag Sci 67:1468–1472

    Article  CAS  Google Scholar 

  • Lai T, Li J, Su J (2011) Monitoring of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) resistance to chlorantraniliprole in China. Pestic Biochem Phys 101:198–205

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lanner JT, Georgiou DK, Joshi AD, Hamilton SL (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. CSH Perspect Biol 2:a003996

  • Litchfield JJ, Wilcoxon F (1949) A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 96:99–113

    CAS  Google Scholar 

  • Liu Y, Tabashnik BE (1997) Inheritance of resistance to the Bacillus thuringiensis toxin Cry1C in the diamondback moth. Appl Environ Microbiol 63:2218–2223

    Article  CAS  Google Scholar 

  • Mackrill JJ (2012) Ryanodine receptor calcium release channels: an evolutionary perspective. In: Calcium signaling. Springer, New York, United States, pp 159–182

  • McKenzie JA, Batterham P (1994) The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol Evol 9:166–169

    Article  CAS  Google Scholar 

  • Muthusamy R, Vishnupriya M, Shivakumar M (2014) Biochemical mechanism of chlorantraniliprole resistance in Spodoptera litura (Fab)(Lepidoptera: Noctuidae). J Asia Pac Entomol 17:865–869

    Article  CAS  Google Scholar 

  • Ninsin KD, Tanaka T (2005) Synergism and stability of acetamiprid resistance in a laboratory colony of Plutella xylostella. Pest Manag Sci 61:723–727

    Article  CAS  Google Scholar 

  • Phillips J, Graves J, Luttrell R (1989) Insecticide resistance management: relationship to integrated pest management. Pestic Sci 27:459–464

    Article  CAS  Google Scholar 

  • Pimentel D (2009) Pesticides and pest control. In: Integrated pest management: innovation-development process. Springer, United Statments, pp 83–87

  • Robertson J, Preisler H (1992) Pesticide bioassays with arthropods. CRC, Boca Raton, Florida

    Google Scholar 

  • Robertson JL, Jones MM, Olguin E, Alberts B (2017) Bioassays with arthropods. CRC, Boca Raton, Florida

    Book  Google Scholar 

  • Roditakis E et al. (2017) Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Biochem Mol Biol 80:11–20

    CAS  Google Scholar 

  • Rodrigues AC et al. (2015) Life history and biochemical effects of chlorantraniliprole on Chironomus riparius. Sci Total Environ 508:506–513

    Article  CAS  Google Scholar 

  • Roush RT (1989) Designing resistance management programs: how can you choose? Pestic Sci 26:423–441

    Article  CAS  Google Scholar 

  • Roush RT, Combs R, Randolph T, Macdonald J, Hawkins J (1986) Inheritance and effective dominance of pyrethroid resistance in the horn fly (Diptera: Muscidae). J Econ Entomol 79:1178–1182

    Article  CAS  Google Scholar 

  • Roush RT, Daly JC (1990) The role of population genetics in resistance research and management. In: Roush RT, Bruce E (eds) Pesticide resistance in arthropods. Springer, United States, pp 97–152

  • Saha D (2016) Biochemical insecticide resistance in tea pests. Insecticides resistance. InTech, pp 347–-390

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

    Article  CAS  Google Scholar 

  • Scott JG (1990) Investigating mechanisms of insecticide resistance: methods, strategies, and pitfalls. In: Pesticide resistance in arthropods. Springer, United States, p 39–57

  • Shah R, Abbas N, Shad S, Binyamin M (2018) Determination of the genetic and synergistic suppression of a methoxyfenozide-resistant strain of the house fly Musca domestica L. (Diptera: Muscidae). Neotrop Entomol 47:709–715

    Article  CAS  Google Scholar 

  • Shah RM, Shad SA, Abbas N (2015b) Mechanism, stability and fitness cost of resistance to pyriproxyfen in the house fly, Musca domestica L. (Diptera: Muscidae). Pestic Biochem Phys 119:67–73

    Article  CAS  Google Scholar 

  • Shah RM, Abbas N, Shad SA, Sial AA (2015a) Selection, resistance risk assessment, and reversion toward susceptibility of pyriproxyfen in Musca domestica L. Parasitol Res 114:487–494

    Article  Google Scholar 

  • Shah RM, Shad SA (2019) House fly resistance to chlorantraniliprole: cross resistance patterns, stability and associated fitness costs. Pest Manag Sci. https://doi.org/10.1002/ps.5716

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

    Article  CAS  Google Scholar 

  • Sial AA, Brunner JF (2010) Assessment of resistance risk in obliquebanded leafroller (Lepidoptera: Tortricidae) to the reduced-risk insecticides chlorantraniliprole and spinetoram. J Econ Entomol 103:1378–1385

    Article  CAS  Google Scholar 

  • Sial AA, Brunner JF, Garczynski SF (2011) Biochemical characterization of chlorantraniliprole and spinetoram resistance in laboratory-selected oblique banded leafroller Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae). Pestic Biochem Phys 99:274–279

    Article  CAS  Google Scholar 

  • Silva JE, Ribeiro LMDS, Vinasco N, Guedes RNC, Siqueira HÁA (2019) Field-evolved resistance to chlorantraniliprole in the tomato pinworm Tuta absoluta: inheritance, cross-resistance profile, and metabolism. J Pest Sci 92:1421–1431

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry 3rd edition. WH Freeman, San Francisco, CA, USA

    Google Scholar 

  • Steinbach D, Gutbrod O, Lümmen P, Matthiesen S, Schorn C, Nauen R (2015) Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella. Insect Biochem Mol 63:14–22

    Article  CAS  Google Scholar 

  • Strickberger MW (1976) Genetics. Macmillan Publishing Co. Inc, New York, NY, United States

    Google Scholar 

  • Tabashnik B, Croft B (1982) Managing pesticide resistance in crop-arthropod complexes: interactions between biological and operational factors. Environ Entomol 11:1137–1144

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tabashnik BE et al. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. J Econ Entomol 96:1031–1038

    Article  CAS  Google Scholar 

  • Tabashnik BE, Liu Y-B, Finson N, Masson L, Heckel DG (1997) One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proc Natl Acad Sci USA 94:1640–1644

    Article  CAS  Google Scholar 

  • Tabashnik BE, Mota-Sanchez D, Whalon ME, Hollingworth RM, Carrière Y (2014) Defining terms for proactive management of resistance to Bt crops and pesticides. J Econ Entomol 107:496–507

    Article  Google Scholar 

  • Tang JD, Gilboa S, Roush RT, Shelton AM (1997) Inheritance, stability, and lack-of-fitness costs of field-selected resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae) from Florida. J Econ Entomol 90:732–741

    Article  Google Scholar 

  • Troczka B et al. (2012) Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochem Mol 42:873–880

    Article  CAS  Google Scholar 

  • Wang X, Wu Y (2012) High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. J Econ Entomol 105:1019–1023

    Article  CAS  Google Scholar 

  • Wang X, Khakame SK, Ye C, Yang Y, Wu Y (2013) Characterisation of field‐evolved resistance to chlorantraniliprole in the diamondback moth, Plutella xylostella, from China. Pest Manag Sci 69:661–665

    Article  CAS  Google Scholar 

  • Wei Y, Yan R, Zhou Q, Qiao L, Zhu G, Chen M (2019) Monitoring and mechanisms of chlorantraniliprole resistance in Chilo suppressalis (Lepidoptera: Crambidae) in China. J Econ Entomol 112:1348–1353

    Article  CAS  Google Scholar 

  • World Health Organization (2010) International code of conduct on the distribution and use of pesticides: guidelines for the registration of pesticides. World Health Organization

  • Zhu F, Lavine L, O’Neal S, Lavine M, Foss C, Walsh D (2016) Insecticide resistance and management strategies in urban ecosystems. Insects 7:2

    Article  Google Scholar 

  • Zuo Y, Wang H, Xu Y, Huang J, Wu S, Wu Y, Yang Y (2017) CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides. Insect Biochem Mol 89:79–85

    Article  CAS  Google Scholar 

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Acknowledgements

All the authors highly acknowledge the role Mr. Khuram Shahzad in assistance to perform the labor work. We are also cordially thankful to Dr. Naeem Abbas, Assistant Professor, Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Saudi Arabia for technical support.

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RMS and SA designed the experiment; RMS performed the experiment in the supervision of SA. RMS wrote the MS and SA critically reviewed and finalized it.

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Correspondence to Rizwan Mustafa Shah or Sarfraz Ali Shad.

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Shah, R.M., Shad, S.A. Genetics and mechanism of resistance to chlorantraniliprole in Musca domestica L. (Diptera: Muscidae). Ecotoxicology 30, 552–559 (2021). https://doi.org/10.1007/s10646-021-02390-w

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