Mutations associated with pyrethroid resistance in the honey bee parasite Varroa destructor evolved as a series of parallel and sequential events

Managed honey bees have suffered severe seasonal losses for most of the past 30 years, while at the same time there is a growing need for food crop pollination. Parasitism by Varroa destructor plays a key role in explaining these losses as this parasite directly damages honey bees by feeding on them and by vectoring an array of viruses while doing so. Pyrethroids like tau-fluvalinate and flumethrin are among the few acaricides that may control Varroa mites in honey bee colonies. However, their intensive use has led to the evolution of resistance in many locations. Knockdown resistance (kdr-type) in Varroa destructor is associated with point mutations that change the amino acid at position 925 in the para-type voltage-gated sodium channel (VGSC) from leucine to valine, methionine or isoleucine. In order to assess the evolution of resistant mutations, we genotyped a region of the VGSC from V. destructor samples collected worldwide. Our phylogenetic analysis supports the hypothesis of independent origin for resistant alleles in Europe and the USA, and a close relation between L925M and L925I alleles. Our data also suggest that uncontrolled trading of parasitised honey bees might be an important route for spreading resistant alleles overseas. The substitution M918L, associated with pyrethroid resistance in other species, is reported here for the first time in V. destructor, in conjunction with L925V in mites from Spain. The implications of these evolutionary and dispersal processes for Varroa mite management are discussed.