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      Costs of insensitive acetylcholinesterase insecticide resistance for the malaria vector Anopheles gambiae homozygous for the G119S mutation

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      Malaria Journal
      BioMed Central

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          Abstract

          Background

          The G119S mutation responsible for insensitive acetylcholinesterase resistance to organophosphate and carbamate insecticides has recently been reported from natural populations of Anopheles gambiae in West Africa. These reports suggest there are costs of resistance associated with this mutation for An. gambiae, especially for homozygous individuals, and these costs could be influential in determining the frequency of carbamate resistance in these populations.

          Methods

          Life-history traits of the AcerKis and Kisumu strains of An. gambiae were compared following the manipulation of larval food availability in three separate experiments conducted in an insecticide-free laboratory environment. These two strains share the same genetic background, but differ in being homozygous for the presence or absence of the G119S mutation at the ace-1 locus, respectively.

          Results

          Pupae of the resistant strain were significantly more likely to die during pupation than those of the susceptible strain. Ages at pupation were significantly earlier for the resistant strain and their dry starved weights were significantly lighter; this difference in weight remained when the two strains were matched for ages at pupation.

          Conclusions

          The main cost of resistance found for An. gambiae mosquitoes homozygous for the G119S mutation was that they were significantly more likely to die during pupation than their susceptible counterparts, and they did so across a range of larval food conditions. Comparing the frequency of G119S in fourth instar larvae and adults emerging from the same populations would provide a way to test whether this cost of resistance is being expressed in natural populations of An. gambiae and influencing the dynamics of this resistance mutation.

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          Most cited references36

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          The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors.

          High insecticide resistance resulting from insensitive acetylcholinesterase (AChE) has emerged in mosquitoes. A single mutation (G119S of the ace-1 gene) explains this high resistance in Culex pipiens and in Anopheles gambiae. In order to provide better documentation of the ace-1 gene and the effect of the G119S mutation, we present a three-dimension structure model of AChE, showing that this unique substitution is localized in the oxyanion hole, explaining the insecticide insensitivity and its interference with the enzyme catalytic functions. As the G119S creates a restriction site, a simple PCR test was devised to detect its presence in both A. gambiae and C. pipiens, two mosquito species belonging to different subfamilies (Culicinae and Anophelinae). It is possibile that this mutation also explains the high resistance found in other mosquitoes, and the present results indicate that the PCR test detects the G119S mutation in the malaria vector A. albimanus. The G119S has thus occurred independently at least four times in mosquitoes and this PCR test is probably of broad applicability within the Culicidae family.
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            Comparative genomics: Insecticide resistance in mosquito vectors.

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              A novel acetylcholinesterase gene in mosquitoes codes for the insecticide target and is non-homologous to the ace gene in Drosophila.

              Acetylcholinesterase (AChE) is the target of two major insecticide families, organophosphates (OPs) and carbamates. AChE insensitivity is a frequent resistance mechanism in insects and responsible mutations in the ace gene were identified in two Diptera, Drosophila melanogaster and Musca domestica. However, for other insects, the ace gene cloned by homology with Drosophila does not code for the insensitive AChE in resistant individuals, indicating the existence of a second ace locus. We identified two AChE loci in the genome of Anopheles gambiae, one (ace-1) being a new locus and the other (ace-2) being homologous to the gene previously described in Drosophila. The gene ace-1 has no obvious homologue in the Drosophila genome and was found in 15 mosquito species investigated. In An. gambiae, ace-1 and ace-2 display 53% similarity at the amino acid level and an overall phylogeny indicates that they probably diverged before the differentiation of insects. Thus, both genes are likely to be present in the majority of insects and the absence of ace-1 in Drosophila is probably due to a secondary loss. In one mosquito (Culex pipiens), ace-1 was found to be tightly linked with insecticide resistance and probably encodes the AChE OP target. These results have important implications for the design of new insecticides, as the target AChE is thus encoded by distinct genes in different insect groups, even within the Diptera: ace-2 in at least the Drosophilidae and Muscidae and ace-1 in at least the Culicidae. Evolutionary scenarios leading to such a peculiar situation are discussed.
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                Author and article information

                Journal
                Malar J
                Malaria Journal
                BioMed Central
                1475-2875
                2010
                13 January 2010
                : 9
                : 12
                Affiliations
                [1 ]Institut Régional de Santé Publique/Université d’Abomey-Calavi, 01 BP 918 Cotonou, Bénin
                [2 ]Lutte contre les Insectes Nuisibles (LIN IRD UR016), 911 Avenue Agropolis, Montpellier 34394, France
                [3 ]Génétique et Evolution des Maladies Infectieuses (GEMI CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France
                Article
                1475-2875-9-12
                10.1186/1475-2875-9-12
                2816975
                20070891
                d3948f97-4300-481e-81cb-b03928084eaf
                Copyright ©2010 Djogbénou et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 4 August 2009
                : 13 January 2010
                Categories
                Research

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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