Impact of selection regime and introgression on deltamethrin resistance in the arbovirus vector Aedes aegypti - a comparative study between contrasted situations in New Caledonia and French Guiana.


Journal

Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744

Informations de publication

Date de publication:
Dec 2021
Historique:
received: 09 08 2021
accepted: 16 08 2021
pubmed: 17 8 2021
medline: 12 11 2021
entrez: 16 8 2021
Statut: ppublish

Résumé

Pyrethroid insecticides such as deltamethrin have been massively used against Aedes aegypti leading to the spread of resistance alleles worldwide. In an insecticide resistance management context, we evaluated the temporal dynamics of deltamethrin resistance using two distinct populations carrying resistant alleles at different frequencies. Three different scenarios were followed: a continuous selection, a full release of selection, or a repeated introgression with susceptible individuals. The responses of each population to these selection regimes were measured across five generations by bioassays and by monitoring the frequency of knockdown resistance (kdr) mutations and the transcription levels and copy number variations of key detoxification enzymes. Knockdown resistance mutations, overexpression and copy number variations of detoxification enzymes as a mechanism of metabolic resistance to deltamethrin was found and maintained under selection across generations. On comparison, the release of insecticide pressure for five generations did not affect resistance levels and resistance marker frequencies. However, introgressing susceptible alleles drastically reduced deltamethrin resistance in only three generations. The present study confirmed that strategies consisting to stop deltamethrin spraying are likely to fail when the frequencies of resistant alleles are too high and the fitness cost associated to resistance is low. In dead-end situations like in French Guiana where alternative insecticides are not available, alternative control strategies may provide a high benefit for vector control, particularly if they favor the introgression of susceptible alleles in natural populations. © 2021 Society of Chemical Industry.

Sections du résumé

BACKGROUND BACKGROUND
Pyrethroid insecticides such as deltamethrin have been massively used against Aedes aegypti leading to the spread of resistance alleles worldwide. In an insecticide resistance management context, we evaluated the temporal dynamics of deltamethrin resistance using two distinct populations carrying resistant alleles at different frequencies. Three different scenarios were followed: a continuous selection, a full release of selection, or a repeated introgression with susceptible individuals. The responses of each population to these selection regimes were measured across five generations by bioassays and by monitoring the frequency of knockdown resistance (kdr) mutations and the transcription levels and copy number variations of key detoxification enzymes.
RESULTS RESULTS
Knockdown resistance mutations, overexpression and copy number variations of detoxification enzymes as a mechanism of metabolic resistance to deltamethrin was found and maintained under selection across generations. On comparison, the release of insecticide pressure for five generations did not affect resistance levels and resistance marker frequencies. However, introgressing susceptible alleles drastically reduced deltamethrin resistance in only three generations.
CONCLUSION CONCLUSIONS
The present study confirmed that strategies consisting to stop deltamethrin spraying are likely to fail when the frequencies of resistant alleles are too high and the fitness cost associated to resistance is low. In dead-end situations like in French Guiana where alternative insecticides are not available, alternative control strategies may provide a high benefit for vector control, particularly if they favor the introgression of susceptible alleles in natural populations. © 2021 Society of Chemical Industry.

Identifiants

pubmed: 34398490
doi: 10.1002/ps.6602
doi:

Substances chimiques

Insecticides 0
Nitriles 0
Pyrethrins 0
decamethrin 2JTS8R821G

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5589-5598

Subventions

Organisme : Agence Nationale de Sécurité Sanitaire de l'Alimentation, de l'Environnement et du Travail
Organisme : European Union's Horizon 2020
Organisme : ZIKAlliance

Informations de copyright

© 2021 Society of Chemical Industry.

Références

Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I et al., Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis 11:1-20 (2017).
Dusfour I, Vontas J, David JP, Weetman D, Fonseca DM, Corbel V et al., Management of insecticide resistance in the major Aedes vectors of arboviruses: advances and challenges. PLoS Negl Trop Dis 13:1-22 (2019).
Smith LB, Kasai S and Scott JG, Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pestic Biochem Physiol 133:1-12 (2016).
Cattel J, Faucon F, Le Péron B, Sherpa S, Monchal M, Grillet L et al., Combining genetic crosses and pool targeted DNA-seq for untangling genomic variations associated with resistance to multiple insecticides in the mosquito Aedes aegypti. Evol Appl 13:303-317 (2020).
Faucon F, Dusfour I, Gaude T, Navratil V, Boyer F, Chandre F et al., Unravelling genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing. Genome Res 25:1347-1359 (2015).
Faucon F, Gaude T, Dusfour I, Navratil V, Corbel V, Juntarajumnong W et al., In the hunt for genomic markers of metabolic resistance to pyrethroids in the mosquito Aedes aegypti: an integrated next-generation sequencing approach. PLoS Negl Trop Dis 11:e0005526 (2017).
García GP, Flores AE, Fernández-Salas I, Saavedra-Rodríguez K, Reyes-Solis G, Lozano-Fuentes S et al., Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México. PLoS Negl Trop Dis 3:e531 (2009).
Mallet J and Porter P, Preventing insect adaptation to insect-resistant crops: are seed mixtures or refugia the best strategy? Proc R Soc Lond B Biol Sci 250:165-169 (1992).
Martins AJ, Ribeiro CDEM, Bellinato DF, Peixoto AA, Valle D and JBP L, Effect of insecticide resistance on development, longevity and reproduction of field or laboratory selected Aedes aegypti populations. PLoS One 7:1-9 (2012).
Grossman MK, Uc-Puc V, Rodriguez J, Cutler DJ, Morran LT, Manrique-Saide P et al., Restoration of pyrethroid susceptibility in a highly resistant Aedes aegypti population. Biol Lett 14:20180022 (2018).
Brito LP, Linss JGB, Lima-Camara TN, Belinato TA, Peixoto AA, Lima JBP et al., Assessing the effects of Aedes aegypti kdr mutations on pyrethroid resistance and its fitness cost. PLoS One 8:e60878 (2013).
Alvarez-Gonzalez LC, Briceño A, Ponce-Garcia G, Villanueva-Segura OK, Davila-Barboza JA, Lopez-Monroy B et al., Assessing the effect of selection with deltamethrin on biological parameters and detoxifying enzymes in Aedes aegypti (L.). Pest Manag Sci 73:2287-2293 (2017).
Ffrench-Constant RH and Bass C, Does resistance really carry a fitness cost? Curr Opin Insect Sci 21:39-46 (2017).
Kliot A and Ghanim M, Fitness costs associated with insecticide resistance. Pest Manag Sci 68:1431-1437 (2012).
Dusfour I, Zorrilla P, Guidez A, Issaly J, Girod R, Guillaumot L et al., Deltamethrin resistance mechanisms in Aedes aegypti populations from three French overseas territories worldwide. PLoS Negl Trop Dis 9:1-17 (2015).
WHO. Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets. (2006).
Collins F, Drumm ML, Cole JL, Lockwood WK, Woude GF and Vande IMC, Construction of a general human chromosome jumping library, with application to cystic fibrosis. Science 235:1046-1049 (1987).
Saavedra-Rodriguez K, Urdaneta-Marquez L, Rajatileka S, Moulton M, Flores AE, Fernandez-Salas I et al., A mutation in the voltage-gated sodium channel gene associated with pyrethroid resistance in Latin American Aedes aegypti. Insect Mol Biol 16:785-798 (2007).
Pfaffl MW, A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45-e45, 445 (2001).
Guidez A, Pocquet N, Restrepo J, Mathieu L, Gaborit P, Issaly J et al., Spatiotemporal multiple insecticide resistance in Aedes aegypti populations in French Guiana: need for alternative vector control. Mem Inst Oswaldo Cruz 115 (2020).
Salgueiro P, Restrepo-Zabaleta J, Costa M, Galardo AKR, Pinto J, Gaborit P et al., Liaisons dangereuses: cross-border gene flow and dispersal of insecticide resistance-associated genes in the mosquito Aedes aegypti from Brazil and French Guiana. Mem Inst Oswaldo Cruz 114 (2019).
Haddi K, Tomé HVV, Du Y, Valbon WR, Nomura Y, Martins GF et al., Detection of a new pyrethroid resistance mutation (V410L) in the sodium channel of Aedes aegypti: a potential challenge for mosquito control. Sci Rep 7:1-9 (2017).
Plernsub S, Saingamsook J, Yanola J, Lumjuan N, Tippawangkosol P, Sukontason K et al., Additive effect of knockdown resistance mutations, S989P, V1016G and F1534C, in a heterozygous genotype conferring pyrethroid resistance in Aedes aegypti in Thailand. Parasit Vectors 9:1-7 (2016).
Bariami V, Jones CM, Poupardin R, Vontas J and Ranson H, Gene amplification, abc transporters and cytochrome p450s: unraveling the molecular basis of pyrethroid resistance in the dengue vector, aedes aegypti. PLoS Negl Trop Dis 6:e1692 (2012).
Kasai S, Komagata O, Itokawa K, Shono T, Ng LC, Kobayashi M et al., Mechanisms of pyrethroid resistance in the dengue mosquito vector, Aedes aegypti: target site insensitivity, penetration, and metabolism. PLoS Negl Trop Dis 8:e2948 (2014).
Reid WR, Thornton A, Pridgeon JW, Becnel JJ, Tang F, Estep A et al., Transcriptional analysis of four family 4 P450s in a Puerto Rico strain of Aedes aegypti (Diptera: Culicidae) compared with an Orlando strain and their possible functional roles in permethrin resistance. J Med Entomol 51:605-615 (2014).
Marcombe S, Poupardin R, Darriet F, Reynaud S, Bonnet J, Strode C et al., Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 10:1-14 (2009).
Saavedra-Rodriguez K, Flores-Suarez A, Fernandez-Salas I, Strode C, Ranson H, Hemingway J et al., Transcription of detoxification genes following permethrin selection in the mosquito Aedes aegypti. Insect Mol Biol 1:233-245 (2012).
Strode C, Wondji CS, David JP, Hawkes NJ, Lumjuan N, Nelson DR et al., Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem Mol Biol 38:113-123 (2008).
Calvez E, Guillaumot L, Millet L, Marie J, Bossin H, Rama V et al., Genetic diversity and phylogeny of Aedes aegypti, the main arbovirus vector in the pacific. PLoS Negl Trop Dis 10:1-17 (2016).
Lucas ER, Miles A, Harding NJ, Clarkson CS, Mara K, Lawniczak N et al., Whole genome sequencing reveals high complexity of copy number variation at insecticide resistance loci in malaria mosquitoes. Genome Res 29:1250-1261 (2018).
Cattel J, Haberkorn C, Laporte F, Gaude T, Cumer T, Renaud J et al., A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti from genomic characterization to high-throughput field detection. Evol Appl 14:1009-1022 (2021).
Diniz DFA, De Melo-Santos MAV, Santos EMDM, Beserra EB, Helvecio E, De Carvalho-Leandro D et al., Fitness cost in field and laboratory Aedes aegypti populations associated with resistance to the insecticide temephos. Parasit Vectors 8:1-15 (2015).
Bisset JA, Rodríguez MM, Piedra LA, Cruz M, Gutiérrez G and Ruiz A, Reversal of resistance to the larvicide temephos in an Aedes aegypti (Diptera: Culicidae) laboratory strain from Cuba. J Med Entomol 57:801-806 (2020).
Assogba BS, Djogbénou LS, Milesi P, Berthomieu A, Perez J, Ayala D et al., An ace-1 gene duplication resorbs the fitness cost associated with resistance in Anopheles gambiae, the main malaria mosquito. Sci Rep 5:1-12 (2015).
Saingamsook J, Yanola J, Lumjuan N, Walton C and Somboon P, Investigation of relative development and reproductivity fitness cost in three insecticide-resistant strains of Aedes aegypti from Thailand. Insects 10:1-16 (2019).

Auteurs

Julien Cattel (J)

Laboratoire d'Ecologie Alpine (LECA), UMR 5553 CNRS - Université Grenoble-Alpes, Grenoble, France.
Symbiosis Technologies for Insect Control (SymbioTIC), Plateforme de Recherche Cyroi, Sainte-Clotilde, La Réunion.

Marine Minier (M)

Institut Pasteur de Nouvelle-Calédonie (IPNC), Nouméa, Nouvelle-Calédonie.

Nausicaa Habchi-Hanriot (N)

Vectopôle Amazonien Emile Abonnenc, Institut Pasteur de la Guyane, Cayenne, French Guiana.
ARS La Réunion, Sainte-Clotilde, La Réunion.

Morgane Pol (M)

Institut Pasteur de Nouvelle-Calédonie (IPNC), Nouméa, Nouvelle-Calédonie.

Frederic Faucon (F)

Laboratoire d'Ecologie Alpine (LECA), UMR 5553 CNRS - Université Grenoble-Alpes, Grenoble, France.

Thierry Gaude (T)

Laboratoire d'Ecologie Alpine (LECA), UMR 5553 CNRS - Université Grenoble-Alpes, Grenoble, France.

Pascal Gaborit (P)

Vectopôle Amazonien Emile Abonnenc, Institut Pasteur de la Guyane, Cayenne, French Guiana.

Jean Issaly (J)

Vectopôle Amazonien Emile Abonnenc, Institut Pasteur de la Guyane, Cayenne, French Guiana.

Emma Ferrero (E)

Vectopôle Amazonien Emile Abonnenc, Institut Pasteur de la Guyane, Cayenne, French Guiana.
Ynsect, Damparis, France.

Fabrice Chandre (F)

MIVEGEC, UMR IRD 224-CNRS 5290, Université de Montpellier, Montpellier, France.

Nicolas Pocquet (N)

Institut Pasteur de Nouvelle-Calédonie (IPNC), Nouméa, Nouvelle-Calédonie.

Jean-Philippe David (JP)

Laboratoire d'Ecologie Alpine (LECA), UMR 5553 CNRS - Université Grenoble-Alpes, Grenoble, France.

Isabelle Dusfour (I)

MIVEGEC, UMR IRD 224-CNRS 5290, Université de Montpellier, Montpellier, France.
Département de Santé Globale, Institut Pasteur, Paris, France.
MIVEGEC, UMR IRD 224-CNRS 5290-Université de Montpellier, Montpellier, France.

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