Varroa destructor is an ectoparasitic mite of Asian or Eastern honeybees Apis cerana (A. cerana) which has become a serious threat to European subspecies of Western honeybees Apis mellifera (A. mellifera) within the last century. V. destructor and its vectored honeybee viruses became serious threats for colony survival. This is a short period for pathogen- and host-populations to adapt. To look for possible variation in the composition of viral populations we performed RNA metagenomic analysis of the Western honeybee subspecies A. m. ligustica, A. m. syriaca, A. m. intermissa, and A. cerana and their respective V. destructor mites. The analysis revealed two novel viruses: Varroa orthomyxovirus-1 (VOV-1) in A. mellifera and V. destructor and a Hubei like-virga virus-14 homolog in V. destructor. VOV-1 was more prevalent in V. destructor than in A. mellifera and we found evidence for viral replication in both hosts. Interestingly, we found differences in viral loads of A. cerana and their V. destructor, A. m. intermissa, and its V. destructor showed partial similarity, while A. m. ligustica and A. m. syriaca and their varroa where very similar. Deformed wing virus exhibited 82.20%, 99.20%, 97.90%, and 0.76% of total viral reads in A. m. ligustica, A. m. syriaca, A. m. intermissa, and A. cerana, respectively. This is the first report of a complete segmented-single-stranded negative-sense RNA virus genome in honeybees and V. destructor mites.
The viral ecology of bee communities is complex, where viruses are readily shared among co-foraging bee species. Additionally, in honey bees (Apis mellifera), many viruses are transmitted – and their impacts exacerbated – by the parasitic Varroa destructor mite. Thus far, the viruses found to be shared across bee species and transmitted by V. destructor mites are positive-sense single-stranded RNA viruses. Recently, a negative-sense RNA enveloped virus, Apis rhabdovirus-1 (ARV-1), was found in A. mellifera honey bees in Africa, Europe, and islands in the Pacific. Here, we describe the identification – using a metagenomics approach – of ARV-1 in two bee species (A. mellifera and Bombus impatiens) and in V. destructor mites from populations collected in the United States and Israel. We confirmed the presence of ARV-1 in pools of A. mellifera, B. impatiens, and V. destructor from Israeli and U.S. populations by RT-PCR and found that it can reach high titers in individual honey bees and mites (107–108 viral genomic copies per individual). To estimate the prevalence of ARV-1 in honey bee populations, we screened 104 honey bee colonies across Israel, with 21 testing ARV-1-positive. Tagged-primer-mediated RT-PCR analysis detected the presence of the positive-sense ARV-1 RNA in A. mellifera and V. destructor, indicating that ARV-1 replicates in both hosts. This is the first report of the presence of ARV-1 in B. impatiens and of the replication of a rhabdovirus in A. mellifera and V. destructor. Our data suggest that Varroa mites could act as an ARV-1 vector; however, the presence of ARV-1 in B. impatiens (which are not parasitized by Varroa) suggests that it may not require the mite for transmission and ARV-1 may be shared among co-foraging bee species. Given that ARV-1 is found in non-Apis bee species, and because “ARV” is used for the Adelaide River virus, we propose that this virus should be called bee rhabdovirus 1 and abbreviated BRV-1. These results greatly expand our understanding of the diversity of viruses that can infect bee communities, though further analysis is required to determine how infection with this virus impacts these different hosts.
Bees are important plant pollinators in agricultural and natural ecosystems. High average annual losses of honey bee (Apis mellifera) colonies in some parts of the world, and regional population declines of some mining bee species (Andrena spp.), are attributed to multiple factors including habitat loss, lack of quality forage, insecticide exposure, and pathogens, including viruses. While research has primarily focused on viruses in honey bees, many of these viruses have a broad host range. It is therefore important to apply a community level approach in studying the epidemiology of bee viruses. We utilized high-throughput sequencing to evaluate viral diversity and viral sharing in sympatric, co-foraging bees in the context of habitat type. Variants of four common viruses (i.e., black queen cell virus, deformed wing virus, Lake Sinai virus 2, and Lake Sinai virus NE) were identified in honey bee and mining bee samples, and the high degree of nucleotide identity in the virus consensus sequences obtained from both taxa indicates virus sharing. We discovered a unique bipartite + ssRNA Tombo-like virus, Andrena-associated bee virus-1 (AnBV-1). AnBV-1 infects mining bees, honey bees, and primary honey bee pupal cells maintained in culture. AnBV-1 prevalence and abundance was greater in mining bees than in honey bees. Statistical modeling that examined the roles of ecological factors, including floral diversity and abundance, indicated that AnBV-1 infection prevalence in honey bees was greater in habitats with low floral diversity and abundance, and that interspecific virus transmission is strongly modulated by the floral community in the habitat. These results suggest that land management strategies that aim to enhance floral diversity and abundance may reduce AnBV-1 spread between co-foraging bees.
Plants of Eruca sativa Mill. (Brassicaceae) from desert and Mediterranean populations in Israel differ in flower color and size. In the desert habitat, the population has higher abundance of flowers with cream color and longer petals, whereas in the Mediterranean habitat, the population has higher abundance of flowers with yellow and shorter petals. Choice experiments with honey bee foragers (Apis mellifera Linn., Apidae, Hymenoptera), the main pollinator in the natural habitat in Israel, confirmed that they are more attracted to the yellow flower morph than to the cream one. A proboscis extension response test indicated that honey bees are able to discriminate between flower scents of the desert and Mediterranean populations. Considering the advantage of plants of the yellow morph in attracting pollinators, we further tested in a common garden experiment whether these possess higher fitness than plants of the desert population. Indeed, a significant association was found between flower color and fruit set, and seed mass. In general, our results provide evidence for ecotypic differentiation between populations imposed by pollinators. The advantage of the yellow color morph in attracting pollinators may explain its dominance among plants of the Mediterranean population. We discuss why the cream color morph may be dominant in the desert habitat, considering the possibility of different pollinators, tradeoffs between traits, or pleiotropy.
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