A single mutation is driving resistance to pyrethroids in European populations of the parasitic mite, Varroa destructor
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Varroa destructor is one of the major contributors to the significant losses of Western honey bee colonies worldwide. The synthetic pyrethroids tau-fluvalinate and flumethrin were very popular among beekeepers to control levels of parasitism until reports of therapeutic failures increased during the early 1990s. Three different mutations at position 925 of the V. destructor voltage-gated sodium channel have been associated with the resistance to these compounds. Resistant mites collected in the UK and in the Czech Republic showed only a substitution of leucine to valine (L925V), while those collected in the USA carried alternative mutations to isoleucine (L925I) or methionine (L925M). Here, we have used high-throughput genotyping assays to investigate the distribution of resistance mutations across Europe. Our data show that the mutation L925V is present in most of the European countries tested, albeit with an uneven distribution. We also show new evidence for the significant correlation of the mutation with resistance and conclude that it is likely that resistant mites have a reduced fitness. The implications for integrated management of the parasite are discussed.
KeywordsVarroa mite Real-time PCR Pyrosequencing Acaricides Target-site resistance Voltage-gated sodium channel Pyrethroids
The authors thank the beekeepers and beekeepers associations that provided many of the samples used in this study. Spanish samples were provided by Dr. Aranzazu Meana, Miguel Llorens (Universidad Complutense de Madrid), Mariano Higes (Centro Apícola Marchamalo) and Fernando Calatayud (Asociación de Defensa Sanitaria, ApiADS, Montroi), Austrian samples were provided by Rudolf Moosbeckhofer (Austrian Agency for Health & Food Safety).
Joel González-Cabrera was supported by the Spanish Ministry of Economy and Competitiveness, Ramón y Cajal Program (RYC-2013-13834). The work at the Universitat de València was funded by a grant from the Spanish Ministry of Economy and Competitiveness (CGL2015‐65025‐R, MINECO/FEDER, UE) and by Bayer Animal Health GmbH, Leverkusen, Germany. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the United Kingdom.
Compliance with ethical standards
Conflict of interest
Klemens Krieger, Helen Bumann and Gertraut Altreuther are employees of Bayer Animal Health GmbH, Leverkusen, Germany, and received support in the form of salary. Annemarie Hertel, Gillian Hertlein and Ralf Nauen are employees of Bayer AG, Crop Science Division, R&D, Pest Control, Monheim, Germany, and received support in the form of salary. Joel González-Cabrera is not an employee of Bayer, but part of the work performed at the Universitat de València was supported by a grant from Bayer Animal Health GmbH. There are no more competing interests to declare.
- Bak B, Wilde J, Siuda M (2012) Characteristics of north-eastern population of Varroa destructor resistant to synthetic pyrethroids. Med Weter 68:603–606Google Scholar
- Baxter JR, Ellis MD, Wilson WT (2000) Field evaluation of Apistan and five candidate compounds for parasitic mite control in honey bees. Am Bee J 140:898–900Google Scholar
- COLOSS (2016) Losses of honey bee colonies over the 2015/16 winter. http://www.coloss.org/core-projects/data-honey-bee-colony-losses-winter-2015-16.pdf. Accessed 20 Mar 2018
- Elzen PJ, Eischen FA, Baxter JB, Pettis J, Elzen GW, Wilson WT (1998) Fluvalinate resistance in Varroa jacobsoni from several geographic locations. Am Bee J 138:674–676Google Scholar
- González-Cabrera J, Rodríguez-Vargas S, Davies TG, Field LM, Schmehl D, Ellis JD, Krieger K, Williamson MS (2016) Novel Mutations in the voltage-gated sodium channel of pyrethroid-resistant Varroa destructor populations from the Southeastern USA. PLoS ONE 11:e0155332. https://doi.org/10.1371/journal.pone.0155332 CrossRefPubMedPubMedCentralGoogle Scholar
- IPBES (2016) Summary for policymakers of the assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. In: Potts SG, Imperatriz-Fonseca VL, Ngo HT, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Settele J, Vanbergen AJ, Aizen MA, Cunningham SA, Eardley C, Freitas BM, Gallai N, Kevan PG, Kovács-Hostyánszki A, Kwapong PK, Li J, Li X, Martins DJ, Nates-Parra G, Pettis JS, Rader R, Viana BF (eds) Secretariat of the intergovernmental science-policy platform on biodiversity and ecosystem services. IPBES, BonnGoogle Scholar
- Kim W, Lee M, Han S, Park K, Choi J, Kim J, Choi Y, Jeong G, Koh Y (2009) A geographical polymorphism in a Voltage-Gated Sodium Channel gene in the mite, Varroa destructor, from Korea. Korean J Apic 24:159–165Google Scholar
- Morgan JAT, Corley SW, Jackson LA, Lew-Tabor AE, Moolhuijzen PM, Jonsson NN (2009) 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. https://doi.org/10.1016/j.ijpara.2008.12.006 CrossRefPubMedGoogle Scholar
- O’Reilly AO, Williamson MS, González-Cabrera J, Turberg A, Field LM, Wallace BA, Davies TG (2014) Predictive 3D modelling of the interactions of pyrethroids with the voltage-gated sodium channels of ticks and mites. Pest Manag Sci 70:369–377. https://doi.org/10.1002/ps.3561 CrossRefPubMedGoogle Scholar
- Seitz N, Traynor KS, Steinhauer N, Rennich K, Wilson ME, Ellis JD, Rose R, Tarpy DR, Sagili RR, Caron DM, Delaplane KS, Rangel J, Lee K, Baylis K, Wilkes JT, Skinner JA, Pettis JS, vanEngelsdorp D (2016) A national survey of managed honey bee 2014–2015 annual colony losses in the USA. J Apic Res 54:292–304. https://doi.org/10.1080/00218839.2016.1153294 CrossRefGoogle Scholar
- Solignac M, Cornuet JM, Vautrin D, Le Conte Y, Anderson D, Evans J, Cros-Arteil S, Navajas M (2005) The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honeybee (Apis mellifera), are two partly isolated clones. Proc R Soc B Biol Sci 272:411–419. https://doi.org/10.1098/rspb.2004.2853 CrossRefGoogle Scholar
- Troczka B, Zimmer CT, Elias J, Schorn C, Bass C, Davies TG, Field LM, Williamson MS, Slater R, Nauen R (2012) Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochem Mol Biol 42:873–880. https://doi.org/10.1016/j.ibmb.2012.09.001 CrossRefPubMedGoogle Scholar
- Voudouris C, Kati AN, Sadikoglou E, Williamson M, Skouras PJ, Dimotsiou O, Georgiou S, Fenton B, Skavdis G, Margaritopoulos JT (2016) Insecticide resistance status of Myzus persicae in Greece: long-term surveys and new diagnostics for resistance mechanisms. Pest Manag Sci 72:671–683. https://doi.org/10.1002/ps.4036 CrossRefPubMedGoogle Scholar