Monitoring and distribution of kdr and ace-1 mutation variations in Culex pipiens L., 1758 (Diptera: Culicidae) in artificial sites and agricultural fields in the central and eastern Black Sea Region of Türkiye

Year 2022, , 343 - 358, 30.09.2022

Elif Kılıçarslan , Murat Öztürk , Fatih Şaban Beriş , Rıdvan Demirtaş , Muhammet Mustafa Akıner

https://doi.org/10.16970/entoted.1120646

Abstract

Culex pipiens L., 1758 (Diptera: Culicidae) is one of the most important pests and disease vectors in the world. It is of major importance to monitor the development of insecticide resistance in order to effectively control. This study investigated the presence of mutations in specific loci of the Vgsc (kdr L1014F/C) and ace-1 (G119S, F290V) gene, associated with insecticide resistance in Culex pipiens collected from nine provinces in central and eastern Black Sea Region of Türkiye in the 2020 active season. For kdr, L1014F mutation was determined for each region with three different silent mutations for wild and resistant type alleles, while L1014C was not recorded in any of the analyzed populations. For ace-1, substitution F290V was detected at a low frequency in heterozygosity, while G119S was more widespread, in the analyzed populations. For ace-1, G119I (6 populations) and G119A (5 populations) substitution was firstly described. Types of mutations differences related to the resistance between artificial sites and agricultural fields were not significantly different.

Keywords

ace-1 resistance, common house mosquito, insecticide resistance, kdr resistance

Supporting Institution

yok

Project Number

yok

Thanks

This study was a part of PhD thesis of the first author in Recep Tayyip Erdogan University, Institute of Graduate Studies.

Türkiye'nin Orta ve Doğu Karadeniz Bölgesi tarımsal ve yapay alanlarda yayılım gösteren Culex pipiens L., 1758 (Diptera: Culicidae)’te kdr ve ace-1 mutasyon varyasyonlarının izlenmesi ve dağılımı

Abstract

Culex pipiens L., 1758 (Diptera: Culicidae) dünyadaki en önemli ve hastalık vektörü olan türlerden biridir. Efektif bir kontrol yapılabilmesi için insektisitlere karşı gelişen direnci takip etmek büyük öneme sahiptir. Bu çalışmada Türkiye Orta ve Doğu Karadeniz Bölgesi’nde 2020 aktif sezonunda dokuz ilden toplanan Cx. pipiens örneklerinde vgsc (kdr L1014F/C) ve ace-1 (G119S, F290V) spesifik bölgelerinde direnç ile ilgili mutasyonların varlığı araştırılmıştır. kdr için, her bölgede L1014F mutasyonu belirlenirken, yabanıl ve dirençli tip aleller için üç farklı sessiz mutasyon tespit edilirken çalışılan popülasyonların hiçbirinde L1014C mutasyonu saptanmamıştır. ace-1 bölgesi için, çalışılan popülasyonlarda F290V değişimi heterozigot ve düşük oranlarda saptanırken, G119S değişimi daha yaygın bulunmuştur. ace-1 bölgesi için G119I (6 popülasyon) ve G119A (5 popülasyon) değişimleri ilk defa tespit edilmiştir. Dirence neden olan mutasyon tiplerinde yapay ve tarımsal alanlar arasında anlamlı fark bulunamamıştır.

Keywords

ace-1 direnci, ev sivrisineği, insektisit direnci, kdr direnci

Project Number

yok

References

• Akıner, M. M., S. S. Caglar & F. M. Simsek, 2013. Yearly changes of insecticide susceptiblity and possible insecticide resistance mechanisms of Anopheles maculipennis Meigen (Diptera: Culicidae) in Turkey. Acta Tropika, 126 (3): 280-285.
• Akıner, M. M. & E. Ekşi, 2015. Evaluation of insecticide resistance and biochemical mechanisms of Culex pipiens L. in four localities of east and middle mediterranean basin in Turkey. International Journal of Mosquito Research, 2 (3): 39-44.
• Akıner, M. M., M. Öztürk, A. B. Başer, F. Günay, S. Hacıoğlu, A. Brinkmann, N. Emanet, B. Alten, A. Ozkul, A. Nitsch, Y. M. Linton & K. Ergünay, 2019. Arboviral screening of invasive Aedes species in northeastern Turkey: West Nile virus circulation and detection of insect-only viruses. PLoS Neglected Tropical Diseases, 13 (5): e0007334.
• Alout, H., A. Berthomieu, F. Cui, Y. Tan, C. Berticat, C. L. Qiao & M. Weill, 2007a. Different amino-acid substitutions confer insecticide resistance through acetylcholinesterase 1 insensitivity in Culex vishnui and Culex tritaeniorhynchus (Diptera: Culicidae) from China. Journal of Medical Entomology, 44 (1): 463e469.
• Alout, H., A. Berthomieu, A. Hadjivassilis & M. Weill, 2007b. A new amino-acid substitution in acetylcholinesterase 1 confers insecticide resistance to Culex pipiens mosquitoes from Cyprus. Insect Biochemistry & Molecular Biology, 37 (1): 41-47.
• Alout, H., L. Djogbénou, C. Berticat, F. Chandre & M. Weill, 2008. Comparison of Anopheles gambiae and Culex pipiens acetycholinesterase 1 biochemical properties. Biochemistry & Molecular Biology, 150 (3): 271-277.
• Alout, H., P. Labbe, A. Berthomieu, N. Pasteur & M. Weill, 2009. Multiple duplications of the rare ace-1 mutation F290V in Culex pipiens natural populations. Insect Biochemistry & Molecular Biology, 39 (1): 884-891.
• Ari, A., 1972. Studies on activity and ecology of arboviruses in Turkey. Türk Hijyen ve Deneysel Biyoloji Dergisi, 32 (1): 134-143.
• Arich, S., N. Assaid, H. Taki, M. Weill, P. Labbé & M. H. Sarih, 2021. Distribution of insecticide resistance and molecular mechanisms involved in the West Nile vector Culex pipiens in Morocco. Pest Management Science, 77 (3): 1178-1186.
• Awolola, T. S., A. O. Oduola, I. O. Oyewole, J. B. Obansa, C. N. Amajoh, L. L. Koekemoer & M. Coetzee, 2007. Dynamics of knockdown pyrethroid insecticide resistance alleles in a field population of Anopheles gambiae ss in southwestern Nigeria. Journal of Vector Borne Diseases, 44 (3): 181-188.
• Ben Cheikh, R., C. Berticat, A. Berthomieu, N. Pasteur, H. Ben Cheikh & M. Weill, 2014. Genes conferring resistance to organophosphorus insecticides in Culex pipiens (Diptera: Culicidae) from Tunisia. Journal of Medical Entomology, 46 (3): 523-530.
• Bkhache, M., F. Z. Tmimi, O. Charafeddine, C. Faraj, A. B. Faillou & M. H. Sarih, 2016. First report of L1014F-kdr mutation in Culex pipiens complex from Morocco. Parasites & Vectors, 9 (1): 1-7.
• Bkhache, M., F. Z. Tmimi, O. Charafeddine, O. B. Filali, M. Lemrani, P. Labbé & M. H. Sarih, 2019. G119S ace-1 mutation conferring insecticide resistance detected in the Culex pipiens complex in Morocco. Pest Management Science, 75 (1): 286-291.
• Ceianu, C. S., A. Unqureanu, G. Nikolescu, C. Cernescu, L. Nitescu, G. Tardei, A. Petrescu, D. Pitigoi, D. Martin & V. Ciulacu-Purcarea, 2001. West Nile virus surveillance in Romania: 1997-2000. Viral Immunology, 14 (1): 251-262.
• Chandrasiri, P. G. K., S. D. Fernando & B. N. K. De Silva, 2020. Insecticide resistance and molecular characterization of knockdown resistance (kdr) in Culex quinquefasciatus mosquitoes in Sri Lanka. Journal of Vector Ecology, 45 (2): 204-210.
• Colovic, M. B., D. Z. Krstic, T. D. Lazarevic-Pasti, A. M. Bondzic & V. M. Vasic, 2013. Acetylcholinesterase inhibitors: pharmacology and toxicology. Current Neuropharmacology, 11 (3): 315-335.
• Dabire, R. K., M. Namountougou, A. Diabaté, D. D. Soma, J. Bado, H. K. Toé & P. Combary, 2014. Distribution and frequency of kdr mutations within Anopheles gambiae sl populations and first report of the ace-1 G119S mutation in Anopheles arabiensis from Burkina Faso (West Africa). PloS One, 9 (7): e101484.
• Diaz-Badillo, A., B. G. Bolling, G. Perez-Ramirez, C. G. Moore, J. P. Martinez-Munoz, A. A. Padilla-Viveros & M. De Lourdes Munoz, 2011. The distribution of potential West Nile virus vectors, Culex pipiens pipiens and Culex pipiens quinquefasciatus (Diptera: Culicidae), in Mexico City. Parasites & Vectors, 4 (1): 1-12.
• Donnely, M. J., V. Corbel, D. Weetman, C. S. Wilding, M. S. Williamson & W. C. Black, 2009. Does kdr genotype predict insecticide-resistance phenotype in mosquitoes? Trends in Parasitology, 25 (5):213-219.
• Edi, C. V., B. G. Koudou, C. M. Jones, D. Weetman & H. Ranson, 2012. Multiple-insecticide resistance in Anopheles gambiae mosquitoes, Southern Côte d'Ivoire. Emerging Infectious Diseases, 18 (1): 1508-1511.
• EEA, 2018. CORINE Land Cover (CLC), Version 17. (Web page: https://land.copernicus.eu/pan-european/corine-land-cover/clc2018) (Date accessed: March 2022).
• Ergunay, K., F. Gunay, O. E. Kasap, K. Oter, S. Gargari, T. Karaoglu & B. Alten, 2014. Serological, molecular and entomological surveillance demonstrates widespread circulation of West Nile virus in Turkey. PLoS Neglected Tropical Diseases, 8 (7): e3028.
• Grigoraki, L., A. Puggioli, K. Mavridis, V. Douris, M. Montanari, R. Bellini & J. Vontas, 2018. Author correction: striking diflubenzuron resistance in Culex pipiens, the prime vector of West Nile Virus. Scientific Reports, 8 (1): 1-8.
• Hemingway, J., N. J. Hawkes, L. McCarrol & H. Ranson, 2004. The molecular basis insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology, 34 (7): 653-665.
• Kalaycioglu, H., G. Korukluoglu, A. Ozkul, O. Oncul, S. Tosun, O. Karabay & A. B. Altas, 2012. Emergence of West Nile virus infections in humans in Turkey, 2010 to 2011. Euro surveillance, 17 (21): 20182.
• Kasai, S., I. S. Weerashingle & T. Shono, 1998. P450 monooxygenase are an important mechanism of permethrin resistance in Cx. quinquefasciatus Say larvae. Archives Insect Biochemistry & Physiology, 37 (1): 47-56.
• Kioulos, I., A. Kampouraki, E. Morou, G. Skavdis & J. Vontas, 2014. Insecticide resistance status in the major West Nile virus vector Culex pipiens from Greece. Pest Management Science, 70 (4): 623-627.
• Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology & Evolution, 33 (7): 1870-1874.
• Lol, J. C., M. E. Castellanos, K. A. Liebman, A. Lenhart, P. M. Pennington & N. R. Padilla, 2013. Molecular evidence for historical presence of knock-down resistance in Anopheles albimanus, a key malaria vector in Latin America. Parasites & Vectors, 6 (1): 1-7.
• Major, K. M., D. P. Weston, M. J. Lydy, K. E. Huff Hartz, G. A. Wellborn, A. R. Manny & H. C. Poynton, 2020. The G119S ace-1 mutation confers adaptive organophosphate resistance in a nontarget amphipod. Evolutionary Applications, 13 (4): 620-635.
• Marshall, E., 2000. A renewed assault on an old and deadly foe. Science, 290 (1): 428-430.
• Martinet, J. P, H. Ferte, A. B. Faillox, F. Schafner & J. Depaquit, 2019. Mosquitoes of North-Western Europe as Potential Vectors of Arboviruses. A Review, 11 (11): 1059.
• Martinez-Torres, D., F. Chandre, M. S. Williamson, F. Darriet, J. B. Bergé, A. L. Devonshire & D. Pauron, 1998. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae ss. Insect Molecular Biology, 7 (2): 179-184.
• Massouli, E. J., J. L. Sussman, B. P. Doctor, H. Soreq, B. Velan, M. Cygler, R. Rotundo, A. Shafferman, I. Silman & P. Taylor, 1992. “Recommendations for Nomenclature in Cholinesterases, 285-288”. In: Multidisciplinary Approaches to Cholinesterase Functions (Eds. A. Shafferman & B. Velan). Plenum Press, New York, USA, 293 pp.
• Medlock, J., T. Balenghien, B. Alten, V. Versteirt & F. Schaffner, 2018. Field sampling methods for mosquitoes, sandflies, biting midges and ticks: VectorNet project 2014-2018. EFSA Supporting Publications, 15 (6): 1435E.
• Nabeshima, T., A. Mori, T. Kozaki, Y. Iwata, O. Hidoh, S. Harada, S. Kasai, D. W. Severson, Y. Kono & T. Tomita, 2004. An amino acid substitution attributable to insecticide-resistance in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochemical and Biophysical Research Communications, 313 (1): 794e801.
• Osta, M. A., Z. J. Rizk & P. Labbé, 2012. Insecticide resistance to organophosphates in Culex pipiens complex from Lebanon. Parasites & Vectors, 5 (1): 1-6.
• Ozkul A., Y. Yildirim, D. Pinar, A. Akcali, V. Yilmaz & D. Colak, 2006. Serological evidence of West Nile Virus (WNV) in mammalian species in Turkey. Epidemiology & Infection, 134 (4): 826-829.
• Ponce, G., I. P. Sanchez, S. M. García, J. M. Torrado, S. Lozano-Fuentes, B. Lopez-Monroy & A. E. Flores, 2016. First report of L1014F kdr mutation in Culex quinquefasciatus in Mexico. Insect Science, 23 (1): 829- 834.
• Rezza, G., 2014. West Nile virus infections in south-eastern Europe and in the Eastern Mediterranean area. Journal of Microbiology and Infectious Diseases Special Issue, 1 (1): 10-16.
• Rinkevich, F. D., Y. Du & K. Dong, 2013. Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pesticide Biochemistry & Physiology, 106 (3): 93-100.
• Roberts, D. R. & R. G. Andre, 1994. Insecticide resistance issues in vector-borne disease control. American Journal of Tropical Medicine & Hygiene, 5 (1): 21-34.
• Schaffner, F., A. Guy, G. Bernard, H. Jean-Paul, A. Rhaiem & J. Brunhes, 2001. Les moustiques d'Europe: Logiciel d'identification et d'enseignement [The Mosquitoes of Europe: An Identification and Training Program]. Paris (FRA); Montpellier: IRD; EID, 1 CD ROM (Didactiques). ISBN 2-7099-1485-9.
• Scott, J. G., M. H. Yoshimizu & S. Kasai, 2015. Pyrethroid resistance in Culex pipiens mosquitoes. Pesticide Biochemistry & Physiology, 120 (1): 68-76.
• Shi, L., H. Hu, K. Ma, D. Zhou, J. Yu & D. Zhong, 2015. Development of resistance to pyrethroid in Culex pipiens pallens population under different insecticide selection pressures. PLOS Neglected Tropical Diseases, 9 (8): e0003928.
• Smith, J. L. & D. M. Fonseca, 2004. Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: Culicidae). The American Journal of Tropical Medicine & Hygiene, 70 (4): 339-345.
• Taskin, B. G., T. Dogaroglu, S. Kilic, E. Dogac & V. Taskin, 2016. Seasonal dynamics of insecticide resistance, multiple resistance, and morphometric variation in field populations of Culex pipiens. Pesticide Biochemistry & Physiology, 129 (1): 14-27.
• Wang, Z. M., C. X. Li, D. Xing, Y. H. Yu, N. Liu, R. D. Xue, Y. D. Dong & T. Y. Zhao, 2012. Detection and widespread distribution of sodium channel alleles characteristic of insecticide resistance in Culex pipiens complex mosquitoes in China. Medical & Veterinary Entomology, 26 (2): 228-232.
• Wang, Y., W. Yu, H. Shi, Z. Yang & Y. Ma, 2015. Historical survey of the kdr mutations in the populations of Anopheles sinensis in China in 1996-2014. Malaria Journal, 14 (1): 1-10.
• Weill, M. G., K. Lutfalla, F. Mogensen, A. Chandre & C. Berthomieu, 2003. Berticat Comparative genomics: insecticide resistance in mosquito vectors. Nature, 423 (6936): 136-137.
• Weill, M., C. Malcolm, F. Chandre, K. Mogensen, A. Berthomieu & M. Marquine, 2004. The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Molecular Biology, 13 (1): 1-7.
• Whalon, M. E., D. Mota-sanchez & R. M. Hollingworth, 2008. “Analysis of Global Pesticide Resistance in Arthropods, 5-31”. In: Global Pesticide Resistance in Arthropods (Eds. M. E. Whalon, D. Mota-sanchez & R. M. Hallington). CAB international, Cambridge, MA, UK, 166 pp.
• Wirth, M. C. & G. P. Georghiou, 1996. Organophosphate resistance in Culex pipiens from Cyprus. Journal of the American Mosquito Control Association, 12 (1): 112e118.
• Yu, F. H. & W. A. Catterall, 2003. Overview of the voltage-gated sodium channel family. Genome Biology, 4 (3): 1-7.
• Zakhia, R., L. Mousson, M. Vazeille, N. Haddad & A. B. Failloux, 2018. Experimental transmission of West Nile virus and Rift Valley Fever virus by Culex pipiens from Lebanon. PLOS Neglected Tropical Diseases, 12 (1): e0005983.
• Zhong, D., X. Chang, G. Zhou, Z. He, F. Fu, Z. Yan, G. Zhu & T. Xu, 2013. Relationship between knockdown resistance, metabolic detoxification and organismal resistance to pyrethroids in Anopheles sinensis. PLoS One, 8 (2): e55475.