Reversion of susceptibility to insecticides of multiresistant Musca domestica strains in long-term breeding in laboratory conditions

Under laboratory conditions, resistance to insecticides from various chemical classes of several strains of Musca domestica housefly obtained from populations collected at facilities in the Moscow and Kaluga regions was assessed. It has been established that when applied topically, houseflies of both strains are highly resistant to cypermethrin (RR=500–900×), fipronil (RR=46–75×), thiamethoxam and clothianidin (RR=100–333×), fluralaner (RR=300–2100×), susceptible to chlorpyrifos (RR=0.6–1.4×), indoxacarb (RR=0.24–1.46×) and chlorfenapyr (RR=0.25–0.33×). After breeding in an insectarium without an insecticide press for 50–52 generations, the resistance of Kaluga and Krasnogorsk strains decreased to cypermethrin by 3.0 and 8.3 times; to fipronil by 6.0 and 5.3 times, respectively. Susceptibility to chlorpyrifos remained on the same level. In the Kaluga strain resistance to thiamethoxam increased by 1.7 times, to clothianidin by 2.4 times, while in the Krasnogorsk strain, resistance to these neonicotinoids decreased by 6.3 and 5.8 times, respectively. To indoxacarb and chlorfenapyr, the Kaluga strain became more resistant — by 4.2 and 7.6 times, and the Krasnogorsk strain — by 3.0 and 6.4 times. Determination of the susceptibility of strains to these proinsecticides, carried out on flies of 2–3 generations, demonstrated that susceptibility was on several times higher than for the S-NIID strain. After 2 years, the susceptibility of the strains to indoxacarb and chlorfenapyr decreased and approached that of the S-NIID strain. It is suggested that this fact is associated with the initially higher activity of monooxigenases in resistant F3 flies compared to F52. Increased level of monooxigenases in resistant insects leads to the rapid oxidation of the proinsecticide and its transformation into an active metabolite. The mechanisms of resistance of the house fly to insecticides are discussed.

1. Рославцева С.А. Особенности развития и специфичность механизмов резистентности комнатных мух Musca domestica L. к фосфорорганическим инсектицидам / Дисс. на соиск. уч.ст. д.б.н. М: 1975. 353 с.

2. Melo-Santos M.A.V., Varjal-Melo J.J.M., Araujo A.P., Gomes T.C.S., Paiva M.H.S., et al. Resistance to the organophosphate temephos: mechanisms, evolution and reversion in an Aedes aegypti laboratory strain from Brazil // Acta Tropica. 2010. Vol. 113. P. 180-189.

3. Zhang N.N., Liu C.F., Yang F., Dong S.L., Han Z.J. Resistance mechanisms to chlorpyrifos and F392W mutation frequencies in the acetylcholine esterase ace1 allele of field populations of the tobacco whitefly, Bemisia tabaci in China // J. Insect. Sci. 2012. Vol. 12. P. 41.

4. Sial A.A., Brunner J.F. Selection for resistance, reversion towards susceptibility and synergism of chlorantraniliprole and spinetoram in obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae) // Pest Manag. Sci. 2012. Vol. 68. № 3. P. 462-468.

5. Kristensen M., Knorr M., Spencer A.G., Jespersen J.B. Selection and reversion of azamethiphos-resistance in a field population of the housefly Musca domestica (Diptera: Muscidae), and the underlying biochemical mechanisms // J. Econ. Entomol. 2000. Vol. 93. № 6. P. 1788-1795.

6. Kavi L.A., Kaufman P.E., Scott J.G. Genetics and mechanisms of imidacloprid resistance in house flies // Pestic. Biochem. Physiol. 2014. Vol. 109. P. 64-69.

7. Finney D.J. Probit analysis. Cambridge University Press. Cambridge, UK. 1971.

8. Freeman J.C., San Miguel K., Scott J.G. All resistance alleles are not equal: the high fitness cost of super-kdr in the absence of insecticide // Pest. Manag. Sci. 2021. Vol. 77. № 8. P. 3693-3697.

9. Khan H.A., Akram W., Iqbal J., Naeem- Ullah U. Thiamethoxam resistance in the house fly, Musca domestica L.: current status, resistance selection, cross-resistance potential and possible biochemical mechanisms // PLoS One. 2015. Vol. 10. № 5. e0125850.

10. Domingues L.N., Guerrero F.D., Becker M.E., Alison M.W., Foil L.D. Discovery of the Rdl mutation in association with a cyclodiene resistant population of horn flies, Haematobia irritans (Diptera: Muscidae) // Vet. Parasitol. 2013. Vol. 198. № 1-2. P. 172-179.

11. Sheppard C.D., Joyce J.A. Increased susceptibility of pyrethroid-resistant horn flies (Diptera: Muscidae) to chlorfenapyr // J. Econ. Entomol. 1998. Vol. 91. № 2. P. 398–400.

12. Wing K.D., Sacher M., Kagaya Y., Tsurubuchi Y., Mulderig L., et al. Bioactivation and mode of action of the oxadiazine indoxacarb in insects // Crop Protect. 2000. Vol. 19. P. 537–545.

13. Sayyed A.H., Wright D.J. Genetics and evidence for an esterase associated mechanism of resistance to indoxacarb in a field population of diamondback moth (Lepidoptera: Plutellidae) // Pest Manag. Sci. 2006. Vol. 62. P. 1045–1051.

14. Gondhalekar A.D., Nakayasu E.S., Silva I., Cooper B., Scharf M.E. Indoxacarb biotransformation in the German cockroach // Pestic. Biochem. Physiol. 2016. Vol. 134. P. 14-23.

15. Zhang J., Cui L., Xu X., Rui C. Frequency detection of imidacloprid resistance allele in Aphis gossypii field populations by real-time PCR amplification of specific-allele (rtPASA) // Pestic Biochem. Physiol. 2015. Vol. 125. P. 1-7.

16. Xu X., Ding Q., Wang X., Wang R., Ullah F., et al. V101I and R81T mutations in the nicotinic acetylcholine receptor β1 subunit are associated with neonicotinoid resistance in Myzus persicae // Pest Manag. Sci. 2022. Vol. 78. № 4. P. 1500–1507.

17. Sial M.U., Mehmood K., Saeed S., Husain M., Rasool K.G., et al. Neonicotinoid's resistance monitoring, diagnostic mechanisms and cytochrome P450 expression in green peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) // PLoS One. 2022. Vol. 7. № 1. e0261090.

18. Khan H.A., Akram W., Haider M.S. Genetics and mechanism of resistance to deltamethrin in the house fly, Musca domestica L., from Pakistan // Ecotoxicology. 2015. Vol. 24. № 6. P. 1213-1220.

19. Feng X., Li M., Liu N. Carboxylesterase genes in pyrethroid resistant house flies, Musca domestica // Insect Biochem. Mol Biol. 2018. Vol. 92. P. 30-39.

20. Scott J.G. Evolution of resistance to pyrethroid insecticides in Musca domestica // Pest Manag. Sci. 2017. Vol. 73. № 4. P. 716-722.

21. Roca-Acevedo G., Boscaro I., Toloza A.C.. Global pattern of kdr-type alleles in Musca domestica (L.) // Curr. Trop. Med. Rep. 2023. Vol. 10. № 1:1-10.

22. Sun H., Tong K.P., Kasai S., Scott J.G. Overcoming super-knock down resistance (superkdr) mediated resistance: multi-halogenated benzyl pyrethroids are more toxic to super-kdr than kdr house flies // Insect Mol. Biol. 2016. Vol. 25. № 2. P. 126-137.