Oldest Varroa tolerant honey bee population provides insight into the origins of the global decline of honey bees

L E Brettell,S J Martin

doi:10.1038/srep45953

Abstract

The ecto-parasitic mite Varroa destructor has transformed the previously inconsequential Deformed Wing Virus (DWV) into the most important honey bee viral pathogen responsible for the death of millions of colonies worldwide. Naturally, DWV persists as a low level covert infection transmitted between nest-mates. It has long been speculated that Varroa via immunosuppression of the bees, activate a covert infection into an overt one. Here we show that despite Varroa feeding on a population of 20–40 colonies for over 30 years on the remote island of Fernando de Noronha, Brazil no such activation has occurred and DWV loads have remained at borderline levels of detection. This supports the alternative theory that for a new vector borne viral transmission cycle to start, an outbreak of an overt infection must first occur within the host. Therefore, we predict that this honey bee population is a ticking time-bomb, protected by its isolated position and small population size. This unique association between mite and bee persists due to the evolution of low Varroa reproduction rates. So the population is not adapted to tolerate Varroa and DWV, rather the viral quasispecies has simply not yet evolved the necessary mutations to produce a virulent variant.

Highlights

The ecto-parasitic mite Varroa destructor has transformed the previously inconsequential Deformed Wing Virus (DWV) into the most important honey bee viral pathogen responsible for the death of millions of colonies worldwide
DWV was detected in honey bees on Fernando de Noronha using both highly sensitive High resolution melt (HRM) analysis, Agarose Gel Electrophoresis and Sanger sequencing of purified gene fragments in five out of twelve colonies sampled in July 2015, and four out of six sampled in May 2016. qRT-PCR of actin gene fragments showed all samples to contain intact RNA (Ct = 18.15, S.D. = 2.45) (Supplementary Table S1)
DWV loads were at the borderline of detection limits (Fig. 1a, Supplementary Table S1), far below the level where accurate quantification was possible and considerably lower than the positive control, which was a DWV positive, newly emerged bee which had never been parasitised by Varroa, which is considerably lower than what occurs in a mite parasitised bee

Summary

Introduction

The ecto-parasitic mite Varroa destructor has transformed the previously inconsequential Deformed Wing Virus (DWV) into the most important honey bee viral pathogen responsible for the death of millions of colonies worldwide. We show that despite Varroa feeding on a population of 20–40 colonies for over 30 years on the remote island of Fernando de Noronha, Brazil no such activation has occurred and DWV loads have remained at borderline levels of detection This supports the alternative theory that for a new vector borne viral transmission cycle to start, an outbreak of an overt infection must first occur within the host. The two main theories are; the mite’s feeding activity activates covert virus within the host[14,15,16,17] or the mite has to encounter and feed on a bee (adult or brood) which is suffering from an overt infection This allows the feeding mite to become infected with sufficient DWV particles (including virulent variants) that allows the infection to be passed to another bee, establishing a new viral transmission route[1]. Part of this confusion may lie in the fact that many studies focus on immune genes known to be active against bacterial infections, rather than antiviral immunity, which is more complex (e.g. involving virus-derived small interfering RNAs and piwi-interacting RNAs) and currently is poorly understood[22,23]

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