Mutations associated with pyrethroid resistance in Varroa mite, a parasite of honey bees, are widespread across the United States

Abstract

BACKGROUND: Managed honey bees are key pollinators of many crops and play an essential role in the United States food production. For more than ten years, beekeepers in the United States have been reporting high rates of colony losses. One of the drivers of these losses is the parasitic mite Varroa destructor. Maintaining healthy honey bee colonies in the United States is dependent on a successful control of this mite. The pyrethroid tau-fluvalinate (Apistan®) was among the first synthetic varroacides registered in the United States. With over 20 years of use, mites resistant to Apistan® have emerged, and so it is unsurprising that treatment failures have been reported. Resistance to tau-fluvalinate in US mite populations is associated with point mutations at position 925 of the voltage-gated sodium channel.RESULTS: Here, we have generated a distribution map of pyrethroid resistance alleles in Varroa samples collected from US apiaries in 2016 and 2017, using a high throughput allelic discrimination assay based on TaqMan®. Our results evidence that knockdown resistance (kdr)-type mutations are widely distributed in Varroa populations across the country showing high variability among apiaries. We used these data to predict the phenotype of the mites in the case of treatments with pyrethroids. CONCLUSION: We highlight the relevance of monitoring the resistance in mite populations to achieve an efficient control of this pest. We also put forward the benefits of implementing this methodology to provide data for designing pest management programs aiming to control Varroa.

Pyrethroid target-site resistance mutations in populations of the honey bee parasite Varroa destructor (Acari: Varroidae) from Flanders, Belgium

“…However, based on our questionnaire, it appears that most of the surveyed Flemish beekeepers refrain from pyrethroid use, and apply organic acids or thymol instead. The L925I genotype was detected in one population and has until now been recorded for mites from the USA (González-Cabrera et al 2016;Millán-Leiva et al 2021a), Greece (Alissandrakis et al 2017;Millán-Leiva et al 2021a) and its neighboring country Turkey (Koc et al 2021). This leucine to isoleucine (L925I) substitution is proposed to have evolved via the methionine (L925M) 'stopover' (L [CTG] → M [ATG] → I [ATA]) (Millán-Leiva et al 2021b).…”

“…Many cases of leucine to valine substitution at this position (L925V) in V. destructor populations have been reported in the UK (González-Cabrera et al 2013), the Czech Republic (Hubert et al 2014), Greece (Alissandrakis et al 2017) and Turkey (Koc et al 2021). The substitution to isoleucine (L925I) has been reported in Greece (Alissandrakis et al 2017), Turkey (Koc et al 2021) and the USA (Millán-Leiva et al 2021a), whereas the substitution to methionine (L925M) has been recorded in the USA (Millán-Leiva et al 2021a), Japan (Ogihara et al 2021) and the Canary Islands archipelago (Spain) (Millán-Leiva et al 2021b). The occurrence of these target site mutations in Varroa mites found in bee populations in Flanders (the northern region of Belgium) remains poorly studied.…”

An Insight Into the microRNA Profile of the Ectoparasitic Mite Varroa destructor (Acari: Varroidae), the Primary Vector of Honey Bee Deformed Wing Virus

“…The pyrethroid tau-fluvalinate (Apistan ® ) was one of the first synthetic varroacides registered in the United States, and pyrethroid-resistant Varroa is a major challenge in controlling this mite. Pyrethroid-resistant Varroa are associated with point mutations in the voltage-gated sodium channel gene at position 925 ( Millán-Leiva et al., 2021 ). Further dissection of these mechanisms might provide a fruitful means to overcome pyrethroid resistance in Varroa .…”

Frontiers in effective control of problem parasites in beekeeping

“…One contributor to this is the evolution of resistance to highly selective acaricides by varroa populations. The biomolecular bases for resistance or susceptibility to numerous approved acaricides have recently been described; namely, resistance to the pyrethroid tau-fluvalinate is associated with specific site point mutations on the gene encoding the varroa voltage-gated sodium channel ( Millán-Leiva et al, 2021 ), coumaphos resistance is linked to loss-of-function mutations in varroa cytochrome-P450 genes ( Vlogiannitis et al, 2021 ), and the target molecule of amitraz leading to its differential toxicity to varroa and honey bees appears to be the octopamine receptor ( Guo et al, 2021 ). Understanding resistance evolution in varroa is thus a frontier making rapid gains in the field; one likely future frontier is understand cross-resistance, or antagonistic susceptibility, of varroa to different acaricides based on mutations such as those recently characterized, as well as the broader costs of resistance in this system.…”