Shift in virus composition in honeybees ( Apis mellifera ) following worldwide invasion by the parasitic mite and virus vector Varroa destructor

Abstract

Invasive vectors can induce dramatic changes in disease epidemiology. While viral emergence following geographical range expansion of a vector is well known, the influence a vector can have at the level of the host's pathobiome is less well understood. Taking advantage of the formerly heterogeneous spatial distribution of the ectoparasitic mite Varroa destructor that acts as potent virus vector among honeybees Apis mellifera , we investigated the impact of its recent global spread on the viral community of honeybees in a retrospective study of historical samples. We hypothesized that the vector has had an effect on the epidemiology of several bee viruses, potentially altering their transmissibility and/or virulence, and consequently their prevalence, abundance, or both. To test this, we quantified the prevalence and loads of 14 viruses from honeybee samples collected in mite-free and mite-infested populations in four independent geographical regions. The presence of the mite dramatically increased the prevalence and load of deformed wing virus, a cause of unsustainably high colony losses. In addition, several other viruses became more prevalent or were found at higher load in mite-infested areas, including viruses not known to be actively varroa-transmitted, but which may increase opportunistically in varroa-parasitized bees.

Caught in the act: the invasion of a viral vector changes viral prevalence and titre in native honeybees and bumblebees

“…In varroa-free populations, common honeybee pathogens, including DWV, frequently occur at low prevalence with low viral titres [ 21 , 23 , 25 , 27 , 36 ] or are mostly absent, such as in Australia [ 29 ]. The rapid and dramatic increase in DWV frequency and titre in the honeybee’s native community following the Ushant invasion highlights the importance of varroa control and mirrors the effects observed in non-native populations in New Zealand [ 21 ] and Hawai’i [ 27 ], and fits with the long-term pattern observed in European islands [ 25 ].…”

“…The re-emergence of DWV and its global spread followed varroa's host switch to western honeybees [8,18]. In addition, there are multiple other honeybee viral pathogens that are vectored by varroa [19] and that have also been shown to increase in prevalence in the presence of this vector, such as acute bee paralysis virus (ABPV), black queen cell virus (BQCV) and slow bee paralysis virus (SBPV) [19][20][21][22][23]. Although varroa uniquely parasitizes honeybees, its effect as a vector is not limited to honeybees.…”

Selection and Multiplexing of Reverse Transcription–Quantitative PCR Tests Targeting Relevant Honeybee Viral Pathogens

“…The primers and probe systems previously described for the detection of honeybee viral pathogens ABPV, BQCV, DWVA, DWVB, CPBV and SBV [25,26,29,[31][32][33][34][35][36][37][38][39] were tested for their specificity and inclusivity by BLASTN (https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 27 April 2024) against 500 database entries. Those matching the highest number of sequences of the target virus were selected for use in one-step RT-qPCR tests with TaqMan probes.…”

“…ABPV, DWVA and DWVB are transmitted by V. destructor [ 2 ]. Moreover, it was reported that V. destructor mite presence was significantly associated with a higher prevalence of BQCV, CBPV and SBV [ 26 ].…”

“…The RT-qPCR-based methods available for the detection of ABPV, BQCV, CBPV, DWVA, DWVB and SBV are singleplex tests that use Sybr Green [ 25 , 26 , 29 , 31 , 32 , 34 , 35 , 36 , 37 , 38 ] or fluorescent-probe-based detection [ 33 , 39 , 40 , 41 , 42 ], but only two of these have been validated [ 6 , 40 ].…”