Identification and geographical distribution of pyrethroid resistance mutations in the poultry red mite Dermanyssus gallinae.

Dermanyssus diagnostics poultry red mite pyrethroid resistance resistance origin and spread

Journal

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

Informations de publication

Date de publication:
Jan 2020
Historique:
received: 16 05 2019
revised: 18 07 2019
accepted: 22 07 2019
pubmed: 11 8 2019
medline: 18 3 2020
entrez: 11 8 2019
Statut: ppublish

Résumé

The poultry red mite (PRM) Dermanyssus gallinae is the most common ectoparasite on poultry and causes high economic losses in poultry farming worldwide. Pyrethroid acaricides have been widely used for its control and, consequently, pyrethroid resistance has arisen. In this study we aim to investigate the occurrence of resistance and study the geographical distribution of pyrethroid resistance mutations across PRM populations in Europe. Full dose-response contact bioassays revealed very high levels of resistance against several pyrethroids (α-cypermethrin, fluvalinate, and cyfluthrin) in two PRM populations from Greece, compared to a susceptible reference strain. Resistance was associated with mutations in the gene encoding the target site of pyrethroids, the voltage-gated sodium channel (VGSC). Mutations, M918L and L925V in domain IIS4-S5 and F1534L in domain IIIS6, were found at positions known to play a role in pyrethroid resistance in other arthropod species. Subsequent screening by sequencing VGSC gene fragments IIS4-S5 and IIIS6 revealed the presence and distribution of these mutations in many European populations. In some populations, we identified additional or different mutations including M918V/T, L925M, T929I, I936F, and F1538L. The latter mutation is a possible alternative for F1538I that has been previously associated with pyrethroid resistance in other Acari species. We report very high levels of pyrethroid resistance in PRM populations from Greece, as well as the identification and geographical distribution of 10 pyrethroid resistance mutations in PRM populations across Europe. Our results draw attention to the need for an evidence-based implementation of PRM control, taking acaricide resistance management into consideration. © 2019 Society of Chemical Industry.

Sections du résumé

BACKGROUND BACKGROUND
The poultry red mite (PRM) Dermanyssus gallinae is the most common ectoparasite on poultry and causes high economic losses in poultry farming worldwide. Pyrethroid acaricides have been widely used for its control and, consequently, pyrethroid resistance has arisen. In this study we aim to investigate the occurrence of resistance and study the geographical distribution of pyrethroid resistance mutations across PRM populations in Europe.
RESULTS RESULTS
Full dose-response contact bioassays revealed very high levels of resistance against several pyrethroids (α-cypermethrin, fluvalinate, and cyfluthrin) in two PRM populations from Greece, compared to a susceptible reference strain. Resistance was associated with mutations in the gene encoding the target site of pyrethroids, the voltage-gated sodium channel (VGSC). Mutations, M918L and L925V in domain IIS4-S5 and F1534L in domain IIIS6, were found at positions known to play a role in pyrethroid resistance in other arthropod species. Subsequent screening by sequencing VGSC gene fragments IIS4-S5 and IIIS6 revealed the presence and distribution of these mutations in many European populations. In some populations, we identified additional or different mutations including M918V/T, L925M, T929I, I936F, and F1538L. The latter mutation is a possible alternative for F1538I that has been previously associated with pyrethroid resistance in other Acari species.
CONCLUSION CONCLUSIONS
We report very high levels of pyrethroid resistance in PRM populations from Greece, as well as the identification and geographical distribution of 10 pyrethroid resistance mutations in PRM populations across Europe. Our results draw attention to the need for an evidence-based implementation of PRM control, taking acaricide resistance management into consideration. © 2019 Society of Chemical Industry.

Identifiants

pubmed: 31400055
doi: 10.1002/ps.5582
doi:

Substances chimiques

Pyrethrins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

125-133

Subventions

Organisme : European Union's Horizon 2020 research and innovation program
ID : 773 902-SuperPests
Organisme : European Union's Horizon 2020 research and innovation program
ID : 772 026-POLYADAPT
Organisme : Research Foundation Flanders (FWO)
ID : G053815N
Organisme : Research Foundation Flanders (FWO)
ID : G009312N

Informations de copyright

© 2019 Society of Chemical Industry.

Références

Abbas RZ, Colwell DD, Iqbal Z and Khan A, Acaricidal drug resistance in poultry red mite (Dermanyssus gallinae) and approaches to its management. Worlds Poult Sci J 70:113-124 (2014).
Tomley FM and Sparagano O, Spotlight on avian pathology: red mite, a serious emergent problem in layer hens. Avian Pathol 47:533-535 (2018).
Sigognault Flochlay A, Thomas E and Sparagano O, Poultry red mite (Dermanyssus gallinae) infestation: a broad impact parasitological disease that still remains a significant challenge for the egg-laying industry in Europe. Parasit Vectors 10:4-9 (2017).
Mul M, Fact Sheet: The Poultry Red Mite, Dermanyssus gallinae (De Geer, 1778) A Small Pest That Packs a Big Punch. Wagening UR, Wageningen, The Netherlands (2013).
Arsenopoulos K, Agelou A, and Papadopoulos H, Dermanyssus gallinae - a ghost ectoparasite for Greek laying hen industry: Results of a preliminary study, in 4th Panhellenic Conf Vet Product Anim Food Hyg, Volos, Greece (2017).
Pugliese N, Circella E, Marino M, De Virgilio C, Cocciolo G, Lozito P et al., Circulation dynamics of Salmonella enterica subsp. enterica ser. Gallinarum biovar Gallinarum in a poultry farm infested by Dermanyssus gallinae. Med Vet Entomol 33:162-170 (2019).
Sparagano OAE, George DR, Harrington DWJ and Giangaspero A, Significance and control of the poultry red mite, Dermanyssus gallinae. Annu Rev Entomol 59:447-466 (2014).
Thomas E, Chiquet M, Sander B, Zschiesche E and Flochlay AS, Field efficacy and safety of fluralaner solution for administration in drinking water for the treatment of poultry red mite (Dermanyssus gallinae) infestations in commercial flocks in Europe. Parasit Vectors 10:1-9 (2017).
Gassel M, Wolf C, Noack S, Williams H and Ilg T, The novel isoxazoline ectoparasiticide fluralaner: selective inhibition of arthropod γ-aminobutyric acid- and l-glutamate-gated chloride channels and insecticidal/acaricidal activity. Insect Biochem Mol Biol 45:111-124 (2014).
Genchi C, Traldi G and Hubert H, Efficacia della flumetrina (Bayticol, Bayer) nel controllo dell' acaro rosso, Dermanyssus gallinae, De Geer 1778 [dei polli]. Arch Vet Ital 35:125-128 (1984).
Marangi M, Cafiero MA, Capelli G, Camarda A, Sparagano OAE and Giangaspero A, Evaluation of the poultry red mite, Dermanyssus gallinae (Acari: Dermanyssidae) susceptibility to some acaricides in field populations from Italy. Exp Appl Acarol 48:11-18 (2009).
Zeman P and Železný J, The susceptibility of the poultry red mite, Dermanyssus gallinae (De Geer, 1778), to some acaricides under laboratory conditions. Exp Appl Acarol 1:17-22 (1985).
Beugnet F, Chauve C, Gauthey M and Beert L, Resistance of the red poultry mite to pyrethroids in France. Vet Rec 140:577-579 (1997).
Nordenfors H, Höglund J, Tauson R and Chirico J, Effect of permethrin impregnated plastic strips on Dermanyssus gallinae in loose-housing systems for laying hens. Vet Parasitol 102:121-131 (2001).
Zdybel J, Karamon J and Cencek T, In vitro effectiveness of selected acaricides against red poultry mites (Dermanyssus gallinae, De Geer, 1778) isolated from laying hen battery cage farms localised in different regions of Poland. Bull Vet Inst Pulawy 55:411-416 (2011).
Marangi M, Morelli V, Pati S, Camarda A, Cafiero MA and Giangaspero A, Acaricide residues in laying hens naturally infested by red mite Dermanyssus gallinae. PLoS One 7:3-8 (2012).
Van Leeuwen T and Tirry L, Esterase-mediated bifenthrin resistance in a multiresistant strain of the two-spotted spider mite, Tetranychus urticae. Pest Manag Sci 63:150-156 (2007).
Ay R and Gürkan MO, Resistance to bifenthrin and resistance mechanisms of different strains of the two-spotted spider mite (Tetranychus urticae) from Turkey. Phytoparasitica 33:237-244 (2005).
Dong K, Du Y, Rinkevich F, Nomura Y, Xu P, Wang L et al., Molecular biology of insect sodium channels and pyrethroid resistance. Insect Biochem Mol Biol 50:1-17 (2014).
Van Leeuwen T and Dermauw W, The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annu Rev Entomol 61:475-498 (2016).
Tan J, Liu Z, Wang R, Huang ZY, Chen AC, Gurevitz M et al., Identification of amino acid residues in the insect sodium channel critical for pyrethroid binding. Mol Pharmacol 67:513-522 (2005).
Tsagkarakou A, Van Leeuwen T, Khajehali J, Ilias A, Grispou M, Williamson MS et al., Identification of pyrethroid resistance associated mutations in the Para sodium channel of the two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Insect Mol Biol 18:583-593 (2009).
Riga M, Bajda S, Themistokleous C, Papadaki S, Palzewicz M, Dermauw W et al., The relative contribution of target-site mutations in complex acaricide resistant phenotypes as assessed by marker assisted backcrossing in Tetranychus urticae. Sci Rep 7:9202 (2017).
He H, Chen AC, Davey RB, Ivie GW and George JE, Identification of a point mutation in the para-type sodium channel gene from a pyrethroid-resistant cattle tick. Biochem Biophys Res Commun 261:558-561 (1999).
Nyoni BN, Gorman K, Mzilahowa T, Williamson MS, Navajas M, Field LM et al., Pyrethroid resistance in the tomato red spider mite, Tetranychus evansi, is associated with mutation of the para-type sodium channel. Pest Manag Sci 67:891-897 (2011).
Wu M, Adesanya AW, Morales MA, Walsh DB, Lavine LC, Lavine MD et al., Multiple acaricide resistance and underlying mechanisms in Tetranychus urticae on hops. J Pest Sci 92:543-555 (2018).
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:e0005625 (2017).
Burgess STG, Bartley K, Nunn F, Wright HW, Hughes M, Gemmell M et al., Draft genome assembly of the poultry red mite, Dermanyssus gallinae. Microbiol Resour Announc 7:e01221-e01218 (2018).
Schicht S, Qi W, Poveda L and Strube C, Whole transcriptome analysis of the poultry red mite Dermanyssus gallinae (De Geer, 1778). Parasitology 141:336-346 (2014).
Hall TA, BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/ NT. Nucleic Acids Symp Ser 41:95-98 (1999).
Du Y, Garden DP, Wang L, Zhorov BS and Dong K, Identification of new batrachotoxin-sensing residues in segment IIIS6 of the sodium channel. J Biol Chem 286:13151-13160 (2011).
Rinkevich FD, Du Y and Dong K, Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 106:93-100 (2013).
Panini M, Anaclerio M, Puggioni V, Stagnati L, Nauen R and Mazzoni E, Presence and impact of allelic variations of two alternative s-kdr mutations, M918T and M918L, in the voltage-gated sodium channel of the green peach aphid Myzus persicae. Pest Manag Sci 71:878-884 (2014).
Karatolos N, Gorman K, Williamson MS and Denholm I, Mutations in the sodium channel associated with pyrethroid resistance in the greenhouse whitefly, Trialeurodes vaporariorum. Pest Manag Sci 68:834-838 (2012).
Major KM, Weston DP, Lydy MJ, Wellborn GA and Poynton HC, Unintentional exposure to terrestrial pesticides drives widespread and predictable evolution of resistance in freshwater crustaceans. Evol Appl 11:748-761 (2018).
Bothorel S, Robert C, Ruck L and Julien Carpezat A, Resistance to pyrethroid insecticides in cabbage stem flea beetle (Psylliodes chrysocephala) and rape winter stem weevil (Ceutorhynchus picitarsis) populations in France, in Proceedings of the IOBC-WPRS Work Group “Integrated Control Oilseed Crop”. Darmstadt: IOBC-WPRS, Zagreb, Croatia (2018).
Kapantaidaki DE, Sadikoglou E, Tsakireli D, Kampanis V, Stavrakaki M, Schorn C et al., Insecticide resistance in Trialeurodes vaporariorum populations and novel diagnostics for kdr mutations. Pest Manag Sci 74:59-69 (2017).
Kawada H, Higa Y, Komagata O, Kasai S, Tomita T, Nguyen TY et al., Widespread distribution of a newly found point mutation in voltage-gated sodium channel in pyrethroid-resistant Aedes aegypti populations in Vietnam. PLoS Negl Trop Dis 3:e527 (2009).
Kasai S, Ng LC, Lam-Phua SG, Tang CS, Itokawa K, Komagata O et al., First detection of a putative knockdown resistance gene in major mosquito vector, Aedes albopictus. Jpn J Infect Dis 64:217-221 (2011).
Hu Z, Du Y, Nomura Y and Dong K, A sodium channel mutation identified in Aedes aegypti selectively reduces cockroach sodium channel sensitivity to type I, but not type II pyrethroids. Insect Biochem Mol Biol 41:9-13 (2011).
González-Cabrera J, Bumann H, Rodríguez-Vargas S, Kennedy PJ, Krieger K, Altreuther G et al., A single mutation is driving resistance to pyrethroids in European populations of the parasitic mite, Varroa destructor. J Pest Sci 91:1137-1144 (2018).
Stara J, Pekar S, Nesvorna M, Kamler M, Doskocil I and Hubert J, Spatio-temporal dynamics of Varroa destructor resistance to tau-fluvalinate in Czechia, associated with L925V sodium channel point mutation. Pest Manag Sci 75:1287-1294 (2018).
Alissandrakis E, Ilias A and Tsagkarakou A, Pyrethroid target site resistance in Greek populations of the honey bee parasite Varroa destructor (Acari: Varroidae). J Apic Res 56:625-630 (2017).
Balvín O and Booth W, Distribution and frequency of pyrethroid resistance-associated mutations in host lineages of the bed bug (Hemiptera: Cimicidae) across Europe. J Med Entomol 55:923-928 (2018).
Morgan JAT, Corley SW, Jackson LA, Lew-Tabor AE, Moolhuijzen PM and Jonsson NN, Identification of a mutation in the para-sodium channel gene of the cattle tick Rhipicephalus (Boophilus) microplus associated with resistance to synthetic pyrethroid acaricides. Int J Parasitol 39:775-779 (2009).
Wrzesin B, Czerwoniec A and Wieczorek P, A survey of pyrethroid-resistant populations of Meligethes aeneus F. in Poland indicates the incidence of numerous substitutions in the pyrethroid target site of voltage-sensitive sodium channels in individual beetles. Insect Mol Biol 23:682-693 (2014).
Vais H, Williamson MS, Devonshire AL and Usherwood PNR, The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. Pest Manag Sci 57:877-888 (2001).
Usherwood PNR, Davies TGE, Mellor IR, O′Reilly AO, Peng F, Vais H et al., Mutations in DIIS5 and the DIIS4-S5 linker of Drosophila melanogaster sodium channel define binding domains for pyrethroids and DDT. FEBS Lett 581:5485-5492 (2007).
Haddi K, Valbon WR, Viteri Jumbo LO, de Oliveira LO, Guedes RNC and Oliveira EE, Diversity and convergence of mechanisms involved in pyrethroid resistance in the stored grain weevils, Sitophilus spp. Sci Rep 8:1-15 (2018).
Sparagano OAE and Giangaspero A, Parasitism in Egg Production Systems: The Role of the Red Mite (Dermanyssus gallinae), Improving the Safety and Quality of Eggs and Egg Products: Egg Chemistry, Production and Consumption. Woodhead Publishing Limited, Cambridge, UK, pp. 394-414 (2011).
Grigoraki L, Pipini D, Labbé P, Chaskopoulou A, Weill M and Vontas J, Carboxylesterase gene amplifications associated with insecticide resistance in Aedes albopictus: geographical distribution and evolutionary origin. PLoS Negl Trop Dis 11:e0005533 (2017).

Auteurs

Evangelia Katsavou (E)

Department of Crop Science, Agricultural University of Athens, Athens, Greece.

Spyros Vlogiannitis (S)

Department of Crop Science, Agricultural University of Athens, Athens, Greece.

Eleanor Karp-Tatham (E)

Department of Pathobiology and Population Sciences, The Royal Veterinary College, University of London, North Mymms, Hertfordshire, UK.

Damer P Blake (DP)

Department of Pathobiology and Population Sciences, The Royal Veterinary College, University of London, North Mymms, Hertfordshire, UK.

Aris Ilias (A)

Institute of Molecular Biology & Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece.

Christina Strube (C)

Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Buenteweg 17, Hannover, Germany.

Ilias Kioulos (I)

Department of Crop Science, Agricultural University of Athens, Athens, Greece.

Wannes Dermauw (W)

Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.

Thomas Van Leeuwen (T)

Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.

John Vontas (J)

Department of Crop Science, Agricultural University of Athens, Athens, Greece.
Institute of Molecular Biology & Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece.

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