Focal distribution of diflubenzuron resistance mutations in Culex pipiens mosquitoes from Northern Italy is associated with the history of insecticide applications

Authors: PORRETTA, D - UNIVERSITY OF ROME SAPIENZA; FOTAKIS, E - AGRICULTURAL UNIVERSITY OF ATHENS; MASTRANTONIO, V - UNIVERSITY OF ROME SAPIENZA; CHASKOPOULOU, ALEXANDRA - EUROPEAN BIOLOGICAL CONTROL LABORATORY (EBCL); MICHAELAKIS, A - BENAKI PHYTOPATHOLOGICAL INSTITUTE; KIOULOS, I - AGRICULTURAL UNIVERSITY OF ATHENS; WEILL, M - NATIONAL COUNCIL FOR SCIENTIFIC RESEARCH-CNRS; URBANELLI, S - UNIVERSITY OF ROME SAPIENZA; VONTAS, J - AGRICULTURAL UNIVERSITY OF ATHENS; BELLINI, R - CAA G NICOLI

Submitted to: ACTA TROPICA
Publication Type: Review Article
Publication Acceptance Date: 2/22/2019
Publication Date: 5/1/2019
Citation: Porretta, D., Fotakis, E.A., Mastrantonio, V., Chaskopoulou, A., Michaelakis, A., Kioulos, I., Weill, M., Urbanelli, S., Vontas, J., Bellini, R. 2019. Focal distribution of diflubenzuron resistance mutations in Culex pipiens mosquitoes from Northern Italy is associated with the history of insecticide applications. ACTA TROPICA. 193:106-112. https://doi.org/10.1016/j.actatropica.2019.02.024.
DOI: https://doi.org/10.1016/j.actatropica.2019.02.024

Interpretive Summary: An understanding of the environmental factors affecting the response of insect pests to insecticides is pivotal to better manage resistance and design effective pest control strategies. Here we showed that the selection pressures from intense agricultural applications of diflubenzuron, a very widely used insecticide chemistry, accounted for the high mutation frequencies observed in the Cx. pipiens mosquitoes (West Nile virus vectors) in Italy. No mutations were detected in mosquitoes from Greece and France, where the agricultural use of diflubenzuron was less intense. Our study supports the hypothesis that the use of insecticides in agriculture can contribute to the selection of resistance in vector populations. Monitoring of mosquito vectors for possible insecticide resistant alleles in multiple geographical regions and environmental settings is needed for the development of appropriate Insecticide Resistance Management strategies and public health protection. Furthermore, with very limited chemistries available in both vector control and agriculture, it becomes increasingly important to invest in the development of new insecticidal groups with novel modes of action or/and alternative vector management technologies that will help to expand the currently very limited vector control toolbox.

Technical Abstract: Insecticide resistance is a major threat for vector control and prevention of mosquito borne diseases. In the Culex pipiens mosquitoes, resistance against diflubenzuron (DFB) was detected in Ravenna (Emilia-Romagna region, Northern Italy), in 2015. The resistant phenotypes were associated with two mutations, I1043M and I1043L, at the amino acid 1043 of the chitin synthase gene. In this study, we monitored the presence, frequency and geographical distribution of the DFB resistant mutations in Cx. pipiens populations from Northern Italy, and in populations from Greece and France. In the Emilia-Romagna region, the resistant mutations were detected in 20 out of the 30 populations analysed, reaching allelic frequencies over 70%. The presence and distribution of the resistance mutations was highly focal, with a clear pattern of increasing resistant allelic frequencies moving from the Western towards the Eastern provinces of Emilia-Romagna. Contrary to Italy, DFB resistant alleles were not detected in the Cx. pipiens mosquitoes sampled from Greece and France. Following statistical, literature and bibliographical database analyses on the history of DFB insecticide use in the study areas, we suggest that the selection pressures from the intense agricultural DFB applications occurring throughout the ’80-‘90s against orchard pests, followed, from 2000 onwards by mosquito control DFB applications, may account for the high mutation frequencies observed in the Cx. pipiens populations of the Eastern provinces of Emilia-Romagna. The findings are of major concern for public health in Italy and Europe, as DFB remains a very important insecticide used for controlling arbovirus mosquito vectors, where alternative larvicides are extremely limited.