Negative cross-resistance to chlorfenapyr in pyrethroid-resistance house flies

The purpose of the research is to evaluate the susceptibility to deltamethrin and the pro-insecticide chlorfenapyr in a field population of Musca domestica L. compared to a laboratory strain Lab UF and to clarify a possible mechanism of crossresistance to chlorfenapyr.
Materials and methods. The study was carried out on the adults of the laboratory strain Lab UF and the field population Nik of the housefly M. domestica collected from a livestock farm in the Tyumen region, where pyrethroid insecticides had been used for a long time. The toxicity of the pyrethroid deltamethrin (Delcid, 4%) and the pyrrole chlorfenapyr (Pyrafen EC, 360 g/l) against insects was estimated by the no-choice feeding test. Based on the dose-mortality response, lethal concentrations of insecticides were calculated by the probit analysis and the resistance ratio was determined. To clarify the possible mechanism of cross-resistance to chlorfenapyr in the Nik population of M. domestica, the activity of the main detoxification enzymes was determined depending on sex of the insects. In addition, the presence of the kdr-mutation providing resistance to pyrethroids was assessed by the Sanger sequencing.
Results and discussion. The lethal concentrations of insecticides and the resistance ratios revealed the moderate resistance to deltamethrin and high susceptibility to chlorfenapyr in the field Nik population. A statistically significant increase in the activity of monooxygenases by 2.25–4.36 times, glutathione-S-transferase by 2.02–2.18 times, acetylcholinesterase by 1.45–1.46 times and alpha-naphthyl esterase by 1.41–1.46 times was noted in females and males of the Nik population compared to these parameters of the Lab UF strain. The presence of the kdr-mutation (L1014F) in houseflies of the field population was confirmed by the Sanger sequencing, while the kdr-his mutation (L1014H) was not detected. The results obtained allow us to suggest that resistance to deltamethrin and high susceptibility to chlorfenapyr in the field population of M. domestica are caused by the L1014F mutation and the increased P450 monooxygenase activity. Negative crossresistance can be used to develop insecticidal formulations that reduce the risk of rapid development of insecticidal resistance in M. domestica L.

1. Ben'kovskaya G. V. Principles of Maintenance of Laboratory Insect Lines. Biomika = Biomics. 2017; 9 (1): 24-32. (In Russ.)

2. Davlianidze T. A., Eremina O. Yu. Sanitary and epidemiological significance and resistance to insecticides in the housefly Musca domestica. Vestnik zashchity rastenii = Plant Protection News. 2021; 104 (2): 72-86. (In Russ.) https://doi.org/10.31993/2308-6459-2021-104-2-14984

3. Davlianidze T. A., Eremina O. Yu., Olifer V. V. Resistance to insecticides of housefly Musca domestica in the center of the European part of Russia. Vestnik zashchity rastenii = Plant Protection News. 2022; 105 (3): 114-121. (In Russ.) https://doi.org/10.31993/2308-6459-2022-105-3-15346

4. Eremina O. Yu. Chlorfenapyr is a promising insecticide from the pyrrole group for the control of resistant synanthropic insects. Pest-Menedzhment = Pest Management. 2017; 1 (101): 41-49. (In Russ.)

5. Eremina O. Yu., Lopatina Yu. V. Molecular genetic mechanisms of insecticide resistance in insects. Meditsinskaya parazitologiya i parazitarnye bolezni = Medical parasitology and parasitic diseases. 2017; 4: 44-52. (In Russ.)

6. Sokolyanskaya M. P. Cross-resistance of bitoxibacillin-resistant strains of the housefly Musca domestica. Vestnik zashchity rastenii = Plant Protection News. 2018; 1 (95): 57-60. (In Russ.)

7. Abbas N., Hafez A. M. Alpha-Cypermethrin Resistance in Musca domestica: Resistance Instability, Realized Heritability, Risk Assessment,and Insecticide Cross-Resistance. Insects. 2023; 14: 233. https://doi.org/10.3390/insects14030233

8. Ahmadi E., Khajehali J., Rameshgar F. Evaluation of resistance to permethrin, cypermethrin and deltamethrin in different populations of Musca domestica (L.), collected from the Iranian dairy cattle farms. Journal of Asia-Pacific Entomology. 2020; 23 (2): 277-284. https://doi.org/10.1016/j.aspen.2020.01.014.

9. Basit M. Status of insecticide resistance in Bemisia tabaci: resistance, cross-resistance, stability of resistance, genetics and fitness costs. Phytoparasitica. 2019; 47: 207-225. https://doi.org/10.1007/s12600-019-00722-5

10. Bass C., Jones C. M. Editorial overview: Pests and resistance: Resistance to pesticides in arthropod crop pests and disease vectors: mechanisms, models and tools. Current Opinion in Insect Science. 2018; 27: iv-vii. https://doi.org/10.1016/j.cois.2018.04.009

11. Chien S.-C., Chien S.-C., Su Y.-J. A fatal case of chlorfenapyr poisoning and a review of the literature. Journal of International Medical Research. 2022; 50: 1-7. https://doi.org/10.1177/03000605221121965

12. David M. D. The potential of pro-insecticides for resistance management. Pest Management Science. 2021; 77: 3631-3636. https://doi.org/10.1002/ps.6369

13. De Rouck S., İnak E., Dermauw W., Van Leeuwen T. A review of the molecular mechanisms of acaricide resistance in mites and ticks. Insect Biochemistry and Molecular Biology. 2023; 159: 103981. https://doi.org/10.1016/j.ibmb.2023.103981

14. Freeman J. C., Ross D. H., Scott J. G. Insecticide resistance monitoring of house fly populations from the United States. Pesticide Biochemistry and Physiology. 2019; 158: 61-68. https://doi.org/10.1016/j.pestbp.2019.04.006

15. Huang P., Yan X., Yu B., He X., Lu L., Ren Y. A. Comprehensive Review of the Current Knowledge of Chlorfenapyr: Synthesis, Mode of Action, Resistance, and Environmental Toxicology. Molecules. 2023; 28: 1-18. https://doi.org/10.3390/molecules28227673

16. Khambay B., Carlson G. R., Denholm I., Jacobson R. M. Rapid report: Negative cross-resistance between dihydropyrazole insecticides and pyrethroids in houseflies, Musca domestica. Pest Management Science. 2001; 57 (9): 761-763. https://doi.org/10.1002/ps.381

17. Khan H. A., Akram W., Shad S. A. Genetics, crossresistance and mechanism of resistance to spinosad in a field strain of Musca domestica L. (Diptera: Muscidae). Acta Tropica. 2014; 130: 148-154. https://doi.org/10.1016/j.actatropica.2013.11.006

18. Khan H. A. 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; 10 (5): e0125850. https://doi.org/10.1371/journal.pone.0125850

19. Khan H. A. A. Resistance risk assessment, crossresistance potential and realized heritability of resistance to methomyl in Musca domestica Linnaeus. Ecotoxicology. 2024; 33: 226–234. https://doi.org/10.1007/s10646-024-02742-2

20. Kinareikina A., Silivanova E. Impact of Insecticides at Sublethal Concentrations on the Enzyme Activities in Adult Musca domestica L. Toxics. 2023; 11: 47. https://doi.org/10.3390/toxics11010047

21. Li Q., Huang J., Yuan J. Status and preliminary mechanism of resistance to insecticides in a field strain of housefly (Musca domestica, L). Revista Brasileira de Entomologia. 2018; 62 (4): 311-314. https://doi.org/10.1016/j.rbe.2018.09.003.

22. Liu N., Yue X. Insecticide resistance and crossresistance in the house fly (Diptera: Muscidae). Journal of Economic Entomology. 2000; 93 (4): 1269- 1275. https://doi.org/10.1603/0022-0493-93.4.1269

23. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. Protein measurement with Folin phenol reagent. Journal of Biological Chemistry. 1951; 193 (1): 265-275. https://doi.org/10.1016/s0021-9258(19)52451-6

24. Mekapogu A. R. Finney's probit analysis spreadsheet calculator. 2021; URL: https://probitanalysis.wordpress.com/

25. Pittendrigh B. R., Huesing J. E., Margam V. M., Sun L. Negative Cross Resistance: past present and potential for the future. In book: Insect Resistance Management: Biology, Economics, and Prediction. Publisher: Academic Press Editors: David W. Onstad. 2007; (pp.107-134) https://doi.org/10.1016/b978-012373858-5.50008-3

26. Pittendrigh B. R., Huesing J., Walters K. R., Olds B. P., Steele L. D., Sun L., Gaffney P., Gassmann A. J. Chapter 11 – Negative CrossResistance: History, Present Status, and Emerging Opportunities. In Insect Resistance Management (Second Edition), Editor(s): David W. Onstad, Academic Press, 2014; 373-401. https://doi.org/10.1016/B978-0-12-396955-2.00011-4

27. Pittendrigh B. R., Gaffney P., Murdock L. L. Deterministic modeling of negative crossresistance strategies for use in transgenic host plant resistance. Journal of Theoretical Biology. 2000; 204 (1): 135-150. https://doi.org/10.1006/jtbi.2000.2006

28. Qu R., Zhu J., Li M., Jashenko R., Qiu X. Multiple Genetic Mutations Related to Insecticide Resistance are Detected in Field Kazakhstani House Flies (Muscidae: Diptera). Journal of Medical Entomology. 2021; 58: 2338-2348. https://doi.org/10.1093/jme/tjab110

29. Rodrigues-Silva N., Canuto A. F., Oliveira D. F., Teixeira A. F., Santos-Amaya O. F., Picanço M. C., Pereira E. J. G. Negative cross-resistance between structurally different Bacillus thuringiensis toxins may favor resistance management of soybean looper in transgenic Bt cultivars. Scientific Reports. 2019; 9: 199. https://doi.org/10.1038/s41598-018-35965-5

30. Scott J. G. Evolution of resistance to pyrethroid insecticides in Musca domestica. Pest Management Science. 2017; 73: 716-722. https://doi.org/10.1002/ps.4328

31. Sparks T. C., Crossthwaite A. J., Nauen R., Banba S., Cordova D., Earley F. Ebbinghaus-Kintscher U., Fujioka S., Hirao A., Karmon D., Kennedy R., Nakao T., Popham H. J. R., Salgado V., Watson G. B., Wedel B. J., Wessels F. J. Insecticides, biologics and nematicides: Updates to IRAC’s mode of action classification – a tool for resistance management. Pesticide Biochemistry and Physiology. 2020; 167: 104587. https://doi.org/10.1016/j.pestbp.2020.104587

32. Tchouakui M., Assatse T., Tazokong H. R., Oruni A., Menze B. D., Nguiffo-Nguete D., Mugenzi L. M. J., Kayondo J., Watsenga F., Mzilahowa T., Osae M., Wondji C. S. Detection of a reduced susceptibility to chlorfenapyr in the malaria vector Anopheles gambiae contrasts with full susceptibility in Anopheles funestus across Africa. Scientific Reports. 2023; 13: 1-10. https://doi.org/10.1038/s41598-023-29605-w

33. Wang Q., Rui C., Wang L., Nahiyoon S. A., Huang W., Zhu J., Ji X., Yang Q., Yuan H., Cui L. Field-evolved resistance to 11 insecticides and the mechanisms involved in Helicoverpa armigera (Lepidoptera: Noctuidae). Pest Management Science. 2021; 77: 5086-5095. https://doi.org/10.1002/ps.6548

34. Zhu F., Liu N. Differential expression of CYP6A5 and CYP6A5v2 in pyrethroid-resistant house flies, Musca domestica. Archives of Insect Biochemistry and Physiology. 2008; 67: 107-119. https://doi.org/10.1002/arch.20225

35. Zhu F., Feng J. N., Zhang L., Liu N. Characterization of two novel cytochrome P450 genes in insecticideresistant house-flies. Insect Molecular Biology. 2008; 17: 27-37. https://doi.org/10.1111/j.1365-2583.2008.00777.x