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Honey bee viruses in the yellow-legged hornet Vespa velutina (Lepelieter 1836): Prevalence, loads, and detection of replicative DWV and LSV forms

Publication . Rodriguez-Flores, Maria Shantal; Lopes, Ana; Diéguez-Antón, Ana; Seijo-Coello, M. Carmen; Pinto, M. Alice

Apiaries in Galicia, northwestern Spain, are currently facing the invasive alien species Vespa velutina, which is well established in the region. The pressure on honey bee colonies is high, resulting in both economic and ecological losses. Honey bee colonies also face the challenge of viruses, which are becoming increasingly diverse. In recent years, honey bee viruses have been spreading across taxonomic groups beyond Apoidea, infecting the Vespoidea superfamily. This cross-species spillover has raised concerns in the scientific community due to the potential risk of viruses spreading in ecosystems. Currently, there is a lack of knowledge on this topic, and further research is needed to address this issue. This study employed qPCR and sequencing to investigate the prevalence, loads, and presence of replicative forms of important honey bee viruses in V. velutina individuals collected from 11 apiaries in Galicia. All V. velutina individuals tested positive for DWV, BQCV, AKI complex (ABPV, KBV, and IAPV), or LSV but not for CBPV. DWV showed the highest prevalence (97.0 %) and loads, with both DWV-A (67.4 %) and DWV-B (32.6 %) being detected. The AKI complex (46.3 %) and LSV (43.3 %) were also common, whereas BQCV (11.9 %) was rarer. LSV is detected for the first time in V. velutina. LSV-2 was the dominant strain (82.1 %), and two less frequent (17.9 %) unknown strains were also detected. All 44 screened V. velutina samples carried the replicative form of DWV, and six of these also carried the replicative form of LSV, raising for the first time the possibility of co-infection in the hornet. The detection of honey bee viruses in V. velutina, and the ability of these viruses to spread to other species, may indicate a potential risk of spillover in the apiaries.

2024Journal article

Open access

Origins, diversity, and adaptive evolution of DWV in the honey bees of the Azores: the impact of the invasive mite Varroa destructor

Publication . Lopes, Ana Rita; Low, Matthew; Martín-Hernández, Raquel; Pinto, M. Alice; Miranda, Joachim

Deformed wing virus (DWV) is a honey bee virus, whose emergence from relative obscurity is driven by the recent host-switch, adaptation, and global dispersal of the ectoparasitic mite Varroa destructor (a highly efficient vector of DWV) to reproduction on honey bees (Apis mellifera). Our study examines how varroa affects the continuing evolution of DWV, using the Azores archipelago, where varroa is present on only three out of the eight Islands, as a natural experimental system for comparing different evolutionary conditions and trajectories. We combined qPCR of 494 honey bee colonies sampled across the archipelago with amplicon deep sequencing to reveal how the DWV genetic landscape is altered by varroa. Two of the varroa-free Islands were also free of DWV, while a further two Islands were intriguingly dominated by the rare DWV-C major variant. The other four Islands, including the three varroa-infested Islands, were dominated by the common DWV-A and DWV-B variants. The varroa-infested Islands had, as expected, an elevated DWV prevalence relative to the uninfested Islands, but not elevated DWV loads, due the relatively high prevalence and loads of DWV-C on the varroa-free Islands. This establishes the Azores as a stable refuge for DWV-C and provides the most convincing evidence to date that at least some major strains of DWV may be capable of not just surviving, but actually thriving in honey bees in the absence of varroa-mediated transmission. We did not detect any change in DWV genetic diversity associated with island varroa status but did find a positive association of DWV diversity with virus load, irrespective of island varroa status.

2024Journal article

Open access

Varroa destructor shapes the unique viral landscapes of the honey bee populations of the Azores archipelago

Publication . Lopes, Ana Rita; Low, Matthew; Martín-Hernández, Raquel; Miranda, Joachim; Pinto, M. Alice

The worldwide dispersal of the ectoparasitic mite Varroa destructor from its Asian origins has fundamentally transformed the relationship of the honey bee (Apis mellifera) with several of its viruses, via changes in transmission and/or host immunosuppression. The extent to which honey bee-virus relationships change after Varroa invasion is poorly understood for most viruses, in part because there are few places in the world with several geographically close but completely isolated honey bee populations that either have, or have not, been exposed long-term to Varroa, allowing for separate ecological, epidemiological, and adaptive relationships to develop between honey bees and their viruses, in relation to the mite's presence or absence. The Azores is one such place, as it contains islands with and without the mite. Here, we combined qPCR with meta-amplicon deep sequencing to uncover the relationship between Varroa presence, and the prevalence, load, diversity, and phylogeographic structure of eight honey bee viruses screened across the archipelago. Four viruses were not detected on any island (ABPV-Acute bee paralysis virus, KBV-Kashmir bee virus, IAPV-Israeli acute bee paralysis virus, BeeMLV-Bee macula-like virus); one (SBV-Sacbrood virus) was detected only on mite-infested islands; one (CBPV-Chronic bee paralysis virus) occurred on some islands, and two (BQCV-Black queen cell virus, LSV-Lake Sinai virus,) were present on every single island. This multi-virus screening builds upon a parallel survey of Deformed wing virus (DWV) strains that uncovered a remarkably heterogeneous viral landscape featuring Varroa-infested islands dominated by DWV-A and -B, Varroa-free islands na & iuml;ve to DWV, and a refuge of the rare DWV-C dominating the easternmost Varroa-free islands. While all four detected viruses investigated here were affected by Varroa for one or two parameters (usually prevalence and/or the Richness component of ASV diversity), the strongest effect was observed for the multi-strain LSV. Varroa unambiguously led to elevated prevalence, load, and diversity (Richness and Shannon Index) of LSV, with these results largely shaped by LSV-2, a major LSV strain. Unprecedented insights into the mite-virus relationship were further gained from implementing a phylogeographic approach. In addition to enabling the identification of a novel LSV strain that dominated the unique viral landscape of the easternmost islands, this approach, in combination with the recovered diversity patterns, strongly suggests that Varroa is driving the evolutionary change of LSV in the Azores. This study greatly advances the current understanding of the effect of Varroa on the epidemiology and adaptive evolution of these less-studied viruses, whose relationship with Varroa has thus far been poorly defined.

2024Journal article

Open access