Journal of Pest Science

, Volume 91, Issue 3, pp 1137–1144 | Cite as

A single mutation is driving resistance to pyrethroids in European populations of the parasitic mite, Varroa destructor

  • Joel González-CabreraEmail author
  • Helen Bumann
  • Sonia Rodríguez-Vargas
  • Peter J. Kennedy
  • Klemens Krieger
  • Gertraut Altreuther
  • Annemarie Hertel
  • Gillian Hertlein
  • Ralf Nauen
  • Martin S. Williamson
Original Paper


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.


Varroa 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.

Supplementary material

10340_2018_968_MOESM1_ESM.tif (3.5 mb)
Fig. S1 Representation of example pyrograms of sequenced European mite samples homozygous for L925 (C/C), heterozygous for L925V (C/G) and homozygous for L925V (G/G) (TIFF 3549 kb)
10340_2018_968_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 12 kb)


  1. 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
  2. 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
  3. Chen YP, Siede R (2007) Honey bee viruses. Adv Virus Res 70:33–80. CrossRefPubMedGoogle Scholar
  4. COLOSS (2016) Losses of honey bee colonies over the 2015/16 winter. Accessed 20 Mar 2018
  5. Davies TGE, Field LM, Usherwood PNR, Williamson MS (2007) DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59:151–162. CrossRefPubMedGoogle Scholar
  6. Dong K, Du Y, Rinkevich F, Nomura Y, Xu P, Wang L, Silver K, Zhorov BS (2014) Molecular biology of insect sodium channels and pyrethroid resistance. Insect Biochem Mol Biol 50C:1–17. CrossRefGoogle Scholar
  7. 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
  8. Elzen PJ, Baxter JR, Spivak M, Wilson WT (2000) Control of Varroa jacobsoni Oud. resistant to fluvalinate and amitraz using coumaphos. Apidologie 31:437–441. CrossRefGoogle Scholar
  9. González-Cabrera J, Davies TGE, Field LM, Kennedy PJ, Williamson MS (2013) An amino acid substitution (L925V) associated with resistance to pyrethroids in Varroa destructor. PLoS ONE 8:e82941. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gracia-Salinas MJ, Ferrer-Dufol M, Latorre-Castro E, Monero-Manera C, Castillo-Hernández JA, Lucientes-Curd J, Peribanez-López MA (2006) Detection of fluvalinate resistance in Varroa destructor in Spanish apiaries. J Apic Res 45:101–105CrossRefGoogle Scholar
  12. Hou C, Chejanovsky N (2014) Acute paralysis viruses of the honey bee. Virol Sin 29:324–326. CrossRefPubMedGoogle Scholar
  13. Hubert J, Nesvorna M, Kamler M, Kopecky J, Tyl J, Titera D, Stara J (2014) Point mutations in the sodium channel gene conferring tau-fluvalinate resistance in Varroa destructor. Pest Manag Sci 70:889–894. CrossRefPubMedGoogle Scholar
  14. 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
  15. 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
  16. Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68:1431–1437. CrossRefPubMedGoogle Scholar
  17. Milani N (1995) The resistance of Varroa-Jacobsoni Oud to pyrethroids—a laboratory assay. Apidologie 26:415–429CrossRefGoogle Scholar
  18. Milani N, Della Vedova G (2002) Decline in the proportion of mites resistant to fluvalinate in a population of Varroa destructor not treated with pyrethroids. Apidologie 33:417–422. CrossRefGoogle Scholar
  19. 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. CrossRefPubMedGoogle Scholar
  20. Mozes-Koch R, Slabezki Y, Efrat H, Kalev H, Kamer Y, Yakobson BA, Dag A (2000) First detection in Israel of fluvalinate resistance in the varroa mite using bioassay and biochemical methods. Exp Appl Acarol 24:35–43. CrossRefGoogle Scholar
  21. O’Reilly AO, Khambay BPS, Williamson MS, Field LM, Wallace BA, Davies TGE (2006) Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochem J 396:255–263. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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. CrossRefPubMedGoogle Scholar
  23. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119. CrossRefPubMedGoogle Scholar
  24. Sammataro D, Untalan P, Guerrero F, Finley J (2005) The resistance of varroa mites (Acari: Varroidae) to acaricides and the presence of esterase. Int J Acarol 31:67–74CrossRefGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. Soderlund DM (2012) Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances. Arch Toxicol 86:165–181. CrossRefPubMedGoogle Scholar
  27. Solignac M, Vautrin D, Pizzo A, Navajas M, Le Conte Y, Cornuet JM (2003) Characterization of microsatellite markers for the apicultural pest Varroa destructor (Acari: Varroidae) and its relatives. Mol Ecol Notes 3:556–559. CrossRefGoogle Scholar
  28. 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. CrossRefGoogle Scholar
  29. Thompson HM, Brown MA, Ball RF, Bew MH (2002) First report of Varroa destructor resistance to pyrethroids in the UK. Apidologie 33:357–366. CrossRefGoogle Scholar
  30. 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. CrossRefPubMedGoogle Scholar
  31. 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. CrossRefPubMedGoogle Scholar
  32. Wang RW, Liu ZQ, Dong K, Elzen PJ, Pettis J, Huang ZY (2002) Association of novel mutations in a sodium channel gene with fluvalinate resistance in the mite, Varroa destructor. J Apic Res 41:17–25CrossRefGoogle Scholar
  33. Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R, Martin SJM, Boots M (2016) Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351:594–597. CrossRefPubMedGoogle Scholar
  34. Yang X, Cox-Foster D (2007) Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134:405–412. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Joel González-Cabrera
    • 1
    Email author
  • Helen Bumann
    • 2
  • Sonia Rodríguez-Vargas
    • 3
  • Peter J. Kennedy
    • 4
  • Klemens Krieger
    • 2
  • Gertraut Altreuther
    • 2
  • Annemarie Hertel
    • 5
  • Gillian Hertlein
    • 5
  • Ralf Nauen
    • 5
  • Martin S. Williamson
    • 6
  1. 1.ERI BIOTECMED, Department of GeneticsUniversitat de ValènciaValenciaSpain
  2. 2.Bayer Animal Health GmbHLeverkusenGermany
  3. 3.Instituto de Agroquímica y Tecnología de Alimentos-CSICValenciaSpain
  4. 4.Environment and Sustainability InstituteUniversity of ExeterPenryn, CornwallUK
  5. 5.Bayer AG, Crop Science DivisionR&D, Pest ControlMonheimGermany
  6. 6.Department of Biointeractions and Crop ProtectionRothamsted ResearchHarpenden, HertfordshireUK

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