CYP6 P450 Enzymes and ACE-1 Duplication Produce Extreme and Multiple Insecticide Resistance in the Malaria Mosquito Anopheles gambiae
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{"title"=>"CYP6 P450 Enzymes and ACE-1 Duplication Produce Extreme and Multiple Insecticide Resistance in the Malaria Mosquito Anopheles gambiae", "type"=>"journal", "authors"=>[{"first_name"=>"Constant V.", "last_name"=>"Edi", "scopus_author_id"=>"53866421000"}, {"first_name"=>"Luc", "last_name"=>"Djogbénou", "scopus_author_id"=>"16177411600"}, {"first_name"=>"Adam M.", "last_name"=>"Jenkins", "scopus_author_id"=>"54410617300"}, {"first_name"=>"Kimberly", "last_name"=>"Regna", "scopus_author_id"=>"54411096500"}, {"first_name"=>"Marc A T", "last_name"=>"Muskavitch", "scopus_author_id"=>"7003652999"}, {"first_name"=>"Rodolphe", "last_name"=>"Poupardin", "scopus_author_id"=>"23767621800"}, {"first_name"=>"Christopher M.", "last_name"=>"Jones", "scopus_author_id"=>"55249513100"}, {"first_name"=>"John", "last_name"=>"Essandoh", "scopus_author_id"=>"55916908800"}, {"first_name"=>"Guillaume K.", "last_name"=>"Kétoh", "scopus_author_id"=>"14062104300"}, {"first_name"=>"Mark J I", "last_name"=>"Paine", "scopus_author_id"=>"7005943158"}, {"first_name"=>"Benjamin G.", "last_name"=>"Koudou", "scopus_author_id"=>"15848378000"}, {"first_name"=>"Martin J.", "last_name"=>"Donnelly", "scopus_author_id"=>"7102824979"}, {"first_name"=>"Hilary", "last_name"=>"Ranson", "scopus_author_id"=>"6603762935"}, {"first_name"=>"David", "last_name"=>"Weetman", "scopus_author_id"=>"57188535266"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"372738205", "sgr"=>"84897374261", "issn"=>"15537404", "pmid"=>"24651294", "scopus"=>"2-s2.0-84897374261", "doi"=>"10.1371/journal.pgen.1004236", "isbn"=>"1553-7390"}, "id"=>"61128936-8c38-3a20-ad2a-76f8d15da34f", "abstract"=>"Malaria control relies heavily on pyrethroid insecticides, to which susceptibility is declining in Anopheles mosquitoes. To combat pyrethroid resistance, application of alternative insecticides is advocated for indoor residual spraying (IRS), and carbamates are increasingly important. Emergence of a very strong carbamate resistance phenotype in Anopheles gambiae from Tiassalé, Côte d'Ivoire, West Africa, is therefore a potentially major operational challenge, particularly because these malaria vectors now exhibit resistance to multiple insecticide classes. We investigated the genetic basis of resistance to the most commonly-applied carbamate, bendiocarb, in An. gambiae from Tiassalé. Geographically-replicated whole genome microarray experiments identified elevated P450 enzyme expression as associated with bendiocarb resistance, most notably genes from the CYP6 subfamily. P450s were further implicated in resistance phenotypes by induction of significantly elevated mortality to bendiocarb by the synergist piperonyl butoxide (PBO), which also enhanced the action of pyrethroids and an organophosphate. CYP6P3 and especially CYP6M2 produced bendiocarb resistance via transgenic expression in Drosophila in addition to pyrethroid resistance for both genes, and DDT resistance for CYP6M2 expression. CYP6M2 can thus cause resistance to three distinct classes of insecticide although the biochemical mechanism for carbamates is unclear because, in contrast to CYP6P3, recombinant CYP6M2 did not metabolise bendiocarb in vitro. Strongly bendiocarb resistant mosquitoes also displayed elevated expression of the acetylcholinesterase ACE-1 gene, arising at least in part from gene duplication, which confers a survival advantage to carriers of additional copies of resistant ACE-1 G119S alleles. Our results are alarming for vector-based malaria control. Extreme carbamate resistance in Tiassalé An. gambiae results from coupling of over-expressed target site allelic variants with heightened CYP6 P450 expression, which also provides resistance across contrasting insecticides. Mosquito populations displaying such a diverse basis of extreme and cross-resistance are likely to be unresponsive to standard insecticide resistance management practices.", "link"=>"http://www.mendeley.com/research/cyp6-p450-enzymes-ace1-duplication-produce-extreme-multiple-insecticide-resistance-malaria-mosquito", "reader_count"=>147, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>8, "Librarian"=>1, "Student > Doctoral Student"=>7, "Researcher"=>29, "Student > Ph. D. Student"=>35, "Student > Postgraduate"=>12, "Student > Master"=>25, "Other"=>7, "Student > Bachelor"=>9, "Lecturer"=>5, "Professor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>8, "Librarian"=>1, "Student > Doctoral Student"=>7, "Researcher"=>29, "Student > Ph. D. Student"=>35, "Student > Postgraduate"=>12, "Student > Master"=>25, "Other"=>7, "Student > Bachelor"=>9, "Lecturer"=>5, "Professor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>29, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>90, "Medicine and Dentistry"=>10, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Social Sciences"=>5, "Computer Science"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>5}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>90}, "Computer Science"=>{"Computer Science"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>29}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>4, "Ghana"=>1, "Switzerland"=>1, "Portugal"=>1}, "group_count"=>12}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1429295"], "description"=>"<p>Plots show: (A). Log<sub>2</sub>-transformed fold-changes (FC) plotted against -log<sub>10</sub> transformed q-values (multiple-testing-corrected probabilities) for bendiocarb-selected Tiassalé samples versus the average of the three susceptible populations; (B) Comparison of Kovié FC against Tiassalé-selected FC for probes significant in both experiments. For genes represented by multiple probes, numbers in parentheses indicate the number of probes significant/total.</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "overexpressed", "susceptible", "bendiocarb", "resistant", "samples"], "article_id"=>969229, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g002", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_significantly_overexpressed_relative_to_susceptible_samples_in_A_Tiassal_233_bendiocarb_resistant_samples_in_Exp1_and_B_both_Tiassal_233_and_Kovi_233_samples_/969229", "title"=>"Genes significantly overexpressed (relative to susceptible samples) in (A) Tiassalé bendiocarb resistant samples in Exp1, and (B). both Tiassalé and Kovié samples.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429294"], "description"=>"<p>Arrows indicate pairwise comparisons with direction indicating an increasing level of bendiocarb resistance, which was used to predict the expected direction of differential gene expression (only solid arrows were used to determine significance). Coloured boxes indicate samples resistant to bendiocarb; the red box indicates the only bendiocarb-selected sample. In Exp2 (C) microarray probes were considered significantly differentially expressed in resistant samples if: (i) each sus <i>vs.</i> res comparisons showed a consistent direction of expression as predicted by arrow direction; and (ii) each sus <i>vs.</i> res comparison yielded corrected P<0.05. In Exp1 (A, B) an additional criteria for significance was applied to increase specificity of results to the bendiocarb phenotype: (iii) fold-change for each Tiassalé-selected <i>vs.</i> sus comparison must be more extreme than the corresponding Tiassalé <i>vs.</i> sus comparison. Overall significance required significance in both Exp1 and Exp2.</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases"], "article_id"=>969228, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Microarray_experimental_design_/969228", "title"=>"Microarray experimental design.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429302"], "description"=>"<p>LC<sub>50</sub> estimates (µg) and 95% confidence limits are shown, in bold type where Act5C test line LC<sub>50</sub>s are significantly greater than CyO controls.</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "transformed", "expressing", "exposed", "pyrethroids", "permethrin"], "article_id"=>969236, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.t001", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Survival_of_transformed_D_melanogaster_expressing_CYP6M2_and_CYP6P3_exposed_to_the_pyrethroids_permethrin_and_deltamethrin_and_for_CYP6M2_also_DDT_/969236", "title"=>"Survival of transformed <i>D. melanogaster</i> expressing <i>CYP6M2</i> and <i>CYP6P3</i> exposed to the pyrethroids permethrin and deltamethrin, and for <i>CYP6M2</i> also DDT.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429299"], "description"=>"<p>In both plots, which show the effect of (A) incubation time and (B) enzyme concentration, points show the mean of three replicates (following subtraction of no-NADPH negative control values) ± one standard error.</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "metabolism", "bendiocarb", "recombinant", "cyp6p3"], "article_id"=>969233, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g005", "stats"=>{"downloads"=>3, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vitro_metabolism_of_bendiocarb_by_recombinant_CYP6P3_expressed_in_E_coli_/969233", "title"=>"<i>In vitro</i> metabolism of bendiocarb by recombinant CYP6P3 expressed in <i>E. coli</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429297"], "description"=>"<p>Bars show mean fold changes relative to the bendiocarb and organophosphate susceptible Okyereko population. Asterisks indicate significant over-expression. Expression differences between pairs of populations are significant where error bars do not overlap. N = 5 biological replicates except for Tia_sel (N = 3).</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases"], "article_id"=>969231, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_qRT_PCR_expression_analysis_of_candidate_genes_/969231", "title"=>"qRT-PCR expression analysis of candidate genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429298"], "description"=>"<p>Boxes show interquartile ranges with median lines and whiskers (error bars) show 95<sup>th</sup> percentiles for test (Act5C driver) or control (CyO) lines following exposure to 0.1 µg bendiocarb. Note that whiskers and median lines coincident with interquartile limits are not visible. Individual points falling outside percentiles are marked as dots. Mann-Whitney tests: ***P<0.001; *P<0.05.</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "transgenic", "expressing", "gambiae"], "article_id"=>969232, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g004", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Survival_of_transgenic_Drosophila_expressing_An_gambiae_Cyp6M2_or_CYP6P3_in_the_presence_of_bendiocarb_/969232", "title"=>"Survival of transgenic <i>Drosophila</i> expressing <i>An. gambiae Cyp6M2</i> or <i>CYP6P3</i> in the presence of bendiocarb.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429304", "https://ndownloader.figshare.com/files/1429305", "https://ndownloader.figshare.com/files/1429306", "https://ndownloader.figshare.com/files/1429307", "https://ndownloader.figshare.com/files/1429308", "https://ndownloader.figshare.com/files/1429309", "https://ndownloader.figshare.com/files/1429310", "https://ndownloader.figshare.com/files/1429311", "https://ndownloader.figshare.com/files/1429312", "https://ndownloader.figshare.com/files/1429313", "https://ndownloader.figshare.com/files/1429314", "https://ndownloader.figshare.com/files/1429315", "https://ndownloader.figshare.com/files/1429316"], "description"=>"<div><p>Malaria control relies heavily on pyrethroid insecticides, to which susceptibility is declining in <i>Anopheles</i> mosquitoes. To combat pyrethroid resistance, application of alternative insecticides is advocated for indoor residual spraying (IRS), and carbamates are increasingly important. Emergence of a very strong carbamate resistance phenotype in <i>Anopheles gambiae</i> from Tiassalé, Côte d'Ivoire, West Africa, is therefore a potentially major operational challenge, particularly because these malaria vectors now exhibit resistance to multiple insecticide classes. We investigated the genetic basis of resistance to the most commonly-applied carbamate, bendiocarb, in <i>An. gambiae</i> from Tiassalé. Geographically-replicated whole genome microarray experiments identified elevated P450 enzyme expression as associated with bendiocarb resistance, most notably genes from the CYP6 subfamily. P450s were further implicated in resistance phenotypes by induction of significantly elevated mortality to bendiocarb by the synergist piperonyl butoxide (PBO), which also enhanced the action of pyrethroids and an organophosphate. <i>CYP6P3</i> and especially <i>CYP6M2</i> produced bendiocarb resistance via transgenic expression in <i>Drosophila</i> in addition to pyrethroid resistance for both genes, and DDT resistance for <i>CYP6M2</i> expression. CYP6M2 can thus cause resistance to three distinct classes of insecticide although the biochemical mechanism for carbamates is unclear because, in contrast to CYP6P3, recombinant CYP6M2 did not metabolise bendiocarb <i>in vitro</i>. Strongly bendiocarb resistant mosquitoes also displayed elevated expression of the acetylcholinesterase <i>ACE-1</i> gene, arising at least in part from gene duplication, which confers a survival advantage to carriers of additional copies of resistant <i>ACE-1</i> G119S alleles. Our results are alarming for vector-based malaria control. Extreme carbamate resistance in Tiassalé <i>An. gambiae</i> results from coupling of over-expressed target site allelic variants with heightened CYP6 P450 expression, which also provides resistance across contrasting insecticides. Mosquito populations displaying such a diverse basis of extreme and cross-resistance are likely to be unresponsive to standard insecticide resistance management practices.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "cyp6", "p450", "enzymes", "duplication", "insecticide", "malaria", "mosquito"], "article_id"=>969238, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004236.s001", "https://dx.doi.org/10.1371/journal.pgen.1004236.s002", "https://dx.doi.org/10.1371/journal.pgen.1004236.s003", "https://dx.doi.org/10.1371/journal.pgen.1004236.s004", "https://dx.doi.org/10.1371/journal.pgen.1004236.s005", "https://dx.doi.org/10.1371/journal.pgen.1004236.s006", "https://dx.doi.org/10.1371/journal.pgen.1004236.s007", "https://dx.doi.org/10.1371/journal.pgen.1004236.s008", "https://dx.doi.org/10.1371/journal.pgen.1004236.s009", "https://dx.doi.org/10.1371/journal.pgen.1004236.s010", "https://dx.doi.org/10.1371/journal.pgen.1004236.s011", "https://dx.doi.org/10.1371/journal.pgen.1004236.s012", "https://dx.doi.org/10.1371/journal.pgen.1004236.s013"], "stats"=>{"downloads"=>15, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/CYP6_P450_Enzymes_and_ACE_1_Duplication_Produce_Extreme_and_Multiple_Insecticide_Resistance_in_the_Malaria_Mosquito_Anopheles_gambiae_/969238", "title"=>"CYP6 P450 Enzymes and <i>ACE-1</i> Duplication Produce Extreme and Multiple Insecticide Resistance in the Malaria Mosquito <i>Anopheles gambiae</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429301"], "description"=>"<p>A. <i>ACE-1</i> G119S TaqMan genotyping scatterplot of females exposed to bendiocarb, following PBO synergist exposure. Filled dots are genotypes called, unfilled are those excluded owing to ambiguous position. The line illustrates a 1∶1 Glycine (G): Serine (S) allele balance. Triangles are controls: S/S = mutant (resistant) allele homozygote; G/G = wild type (susceptible) allele homozygote. The line illustrates a 1∶1 Gly∶Ser allele balance. The dashed circle illustrates heterozygous genotypes. B. <i>Ace-1</i> genomic DNA copy number ratio of survivors and dead (N = 16 each) from the heterozygote genotype cluster. Bars show mean ΔΔ<i>CT</i> values relative to a standard susceptible laboratory strain (Kisumu) following normalisation against reference genes; error bars are 95% confidence intervals. In both plots blue denotes bioassay survivors and red denotes dead.</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "allelic", "bendiocarb"], "article_id"=>969235, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g007", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Role_of_target_site_allelic_variation_and_copy_number_variation_in_bendiocarb_resistance_/969235", "title"=>"Role of target site allelic variation and copy number variation in bendiocarb resistance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/1429300"], "description"=>"<p>Bars are mean mortalities from four replicate bioassays (N = 25 each), with 95% binomial confidence limits. Odds ratios are shown above bars and represent the odds of mortality with PBO pre-exposure, compared to the odds of mortality with insecticide alone (data from the two seasons are pooled). *P≪0.001; <sup>NS</sup>not significant (×<sup>2</sup>-test).</p>", "links"=>[], "tags"=>["Evolutionary biology", "genetics", "gene expression", "Genetic mutation", "Infectious diseases", "phenotypes", "seasons", "synergist"], "article_id"=>969234, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Constant V. Edi", "Luc Djogbénou", "Adam M. Jenkins", "Kimberly Regna", "Marc A. T. Muskavitch", "Rodolphe Poupardin", "Christopher M. Jones", "John Essandoh", "Guillaume K. Kétoh", "Mark J. I. Paine", "Benjamin G. Koudou", "Martin J. Donnelly", "Hilary Ranson", "David Weetman"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004236.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Insecticide_resistance_phenotypes_from_dry_blue_and_wet_red_seasons_with_and_without_the_synergist_PBO_/969234", "title"=>"Insecticide resistance phenotypes from dry (blue) and wet (red) seasons with and without the synergist PBO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-20 04:24:29"}

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