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Insecticide resistance is mediated by multiple mechanisms in recently introduced Aedes aegypti from Madeira Island (Portugal)

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Seixas, Goncalo, Grigoraki, Linda, Weetman, David ORCID: https://orcid.org/0000-0002-5820-1388, Vincente, Jose Luis, Silva, Ana Clara, Pinto, Joao, Vontas, John and Sousa, Carla Alexandra (2017) 'Insecticide resistance is mediated by multiple mechanisms in recently introduced Aedes aegypti from Madeira Island (Portugal)'. PLoS Neglected Tropical Diseases, Vol 11, Issue 7, e0005799.

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Abstract

Background

Aedes aegypti is a major mosquito vector of arboviruses, including dengue, chikungunya and Zika. In 2005, Ae. aegypti was identified for the first time in Madeira Island. Despite an initial insecticide-based vector control program, the species expanded throughout the Southern coast of the island, suggesting the presence of insecticide resistance. Here, we characterized the insecticide resistance status and the underlying mechanisms of two populations of Ae. aegypti from Madeira Island, Funchal and Paúl do Mar.

Methodology/Principal findings
WHO susceptibility bioassays indicated resistance to cyfluthrin, permethrin, fenitrothion and bendiocarb. Use of synergists significantly increased mortality rates, and biochemical assays indicated elevated activities of detoxification enzymes, suggesting the importance of metabolic resistance. Microarray-based transcriptome analysis detected significant upregulation in both populations of nine cytochrome P450 oxidase genes (including four known pyrethroid metabolizing enzymes), the organophosphate metabolizer CCEae3a, Glutathione-S-transferases, and multiple putative cuticle proteins. Genotyping of knockdown resistance loci linked to pyrethroid resistance revealed fixation of the 1534C mutation, and presence with moderate frequencies of the V1016I mutation in each population.

Conclusions/Significance
Significant resistance to three major insecticide classes (pyrethroid, carbamate and organophosphate) is present in Ae. aegypti from Madeira Island, and appears to be mediated by multiple mechanisms. Implementation of appropriate resistance management strategies including rotation of insecticides with alternative modes of action, and methods other than chemical-based vector control are strongly advised to delay or reverse the spread of resistance and achieve efficient control.

Author summary
Aedes aegypti is the major mosquito vector of dengue, chikungunya and Zika worldwide. After its introduction in Madeira, it took a few years for the first dengue outbreak to occur in the region. Control strategies rely mostly on the use of insecticides but their efficiency is often being hampered by the ability of mosquitoes to resist to the compounds used. In fact, previous vector control programs using insecticides failed to eradicate, or even, to limit the spread of Ae. aegypti in Funchal, and now, the mosquito is widely distributed throughout the southern coast of the island. Bioassays to determine insecticide susceptibility profiles were carried-out in two populations of Madeira Island and the molecular mechanisms underlying the observed insecticide resistance phenotype were investigated. Transcription levels of detoxification genes were analysed, and screenings for kdr mutations, V1016I and F1534C, associated with pyrethroid resistance were performed. Our study showed the up-regulation of several detoxification genes of multiple enzyme families associated with metabolic resistance, and the presence of the two kdr mutations, with the F1534C being fixed. Another suggested mechanism probably involved in the resistance phenotype is cuticle thickening, as several cuticle genes were found overexpressed. This study reinforces the importance of alternative control strategies to suppress Ae. aegypti population and thus reduce the likelihood of arbovirus transmission in the region.

Item Type: Article
Subjects: QX Parasitology > Insects. Other Parasites > QX 510 Mosquitoes
QX Parasitology > Insects. Other Parasites > QX 525 Aedes
QX Parasitology > Insects. Other Parasites > QX 600 Insect control. Tick control
WA Public Health > Preventive Medicine > WA 240 Disinfection. Disinfestation. Pesticides (including diseases caused by)
WC Communicable Diseases > Tropical and Parasitic Diseases > WC 765 Prevention and control
Faculty: Department: Biological Sciences > Vector Biology Department
Digital Object Identifer (DOI): https://doi.org/10.1371/journal.pntd.0005799
Depositing User: Stacy Murtagh
Date Deposited: 07 Aug 2017 15:39
Last Modified: 22 Sep 2017 14:29
URI: http://archive.lstmed.ac.uk/id/eprint/7433

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