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Adapted tolerance to virus infections in four geographically distinct Varroa destructor-resistant honeybee populations.

ABSTRACT: The ectoparasitic mite, Varroa destructor, is unarguably the leading cause of honeybee (Apis mellifera) mortality worldwide through its role as a vector for lethal viruses, in particular, strains of the Deformed wing virus (DWV) and Acute bee paralysis virus (ABPV) complexes. Several honeybee populations across Europe have well-documented adaptations of mite-resistant traits but little is known about host adaptations towards the virus infections vectored by the mite. The aim of this study was to assess and compare the possible contribution of adapted virus tolerance and/or resistance to the enhanced survival of four well-documented mite-resistant honeybee populations from Norway, Sweden, The Netherlands and France, in relation to unselected mite-susceptible honeybees. Caged adult bees and laboratory reared larvae, from colonies of these four populations, were inoculated with DWV and ABPV in a series of feeding infection experiments, while control groups received virus-free food. Virus infections were monitored using RT-qPCR assays in individuals sampled over a time course. In both adults and larvae the DWV and ABPV infection dynamics were nearly identical in all groups, but all mite-resistant honeybee populations had significantly higher survival rates compared to the mite-susceptible honeybees. These results suggest that adapted virus tolerance is an important component of survival mechanisms.

SUBMITTER: Locke B

PROVIDER: S-EPMC8196020 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Honey bees play important roles in pollination for many crops and wild plants, but have been facing great threats posed by various pathogens and parasites. Among them, Varroa destructor, an obligate ectoparasite of honey bees, is considered the most damaging. Within the last century, V. destructor shifted from the original host, the Asian honey bee Apis cerana to the new host, the European honey bee A. mellifera. However, the reproduction of Varroa mites, especially of different haplotypes in the two hosts, is still largely unknown. In this study, we first investigated the existing Varroa haplotypes in local colonies in southern China, and then compared the reproduction of different haplotypes on the worker brood of both the original and new hosts by artificial inoculation. We confirmed that there are two haplotypes of V. destructor in southern China, one is the Korea haplotype and the other is the China haplotype, and the two types parasitized different honey bee species. Although Varroa females from A. mellifera (Korea haplotype) are able to reproduce on the worker brood of both honey bee species, they showed better reproductive performance in the new host A. mellifera with significantly higher fecundity (number of offspring per mother mite) and reproductive rate (number of adult daughters per mother mite), suggesting that this parasite gains higher fitness after host shift. The data further showed that a short stay of Varroa females inside the A. cerana worker cells decreased their fecundity and especially the reproductive rate in a time-dependent manner, suggesting that the A. cerana worker cells may inhibit Varroa reproduction. In contrast, Varroa mites derived from A. cerana colonies (China haplotype) were entirely sterile in A. mellifera worker cells during two sequential inoculations, while the control mites from A. mellifera colonies (Korea haplotype) reproduced normally. In addition, all the infertile mites were found to defecate on the abdomen of bee pupae. We have revealed that two haplotypes of V. destructor exhibit differential reproduction on the worker brood of the original and new host honey bees, providing novel insights into the diversity and complexity of the reproduction of V. destructor.

Project description:BACKGROUND:The parasite Varroa destructor represents a significant threat to honeybee colonies. Indeed, development of Varroa infestation within colonies, if left untreated, often leads to the death of the colony. Although its impact on bees has been extensively studied, less is known about its biology and the functional processes governing its adult life cycle and adaptation to its host. We therefore developed a full life cycle transcriptomic catalogue in adult Varroa females and included pairwise comparisons with males, artificially-reared and non-reproducing females (10 life cycle stages and conditions in total). RESULTS:Extensive remodeling of the Varroa transcriptome was observed, with an upregulation of energetic and chitin metabolic processes during the initial and final phases of the life cycle (e.g. phoretic and post-oviposition stages), whereas during reproductive stages in brood cells genes showing functions related to transcriptional regulation were overexpressed. Several neurotransmitter and neuropeptide receptors involved in behavioural regulation, as well as active compounds of salivary glands, were also expressed at a higher level outside the reproductive stages. No difference was detected between artificially-reared phoretic females and their counterparts in colonies, or between females who failed to reproduce and females who successfully reproduced, indicating that phoretic individuals can be reared outside host colonies without impacting their physiology and that mechanisms underlying reproductive failure occur before oogenesis. CONCLUSIONS:We discuss how these new findings reveal the remarkable adaptation of Varroa to its host biology and notably to the switch from living on adults to reproducing in sealed brood cells. By spanning the entire adult life cycle, our work captures the dynamic changes in the parasite gene expression and serves as a unique resource for deciphering Varroa biology and identifying new targets for mite control.

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Adapted tolerance to virus infections in four geographically distinct Varroa destructor-resistant honeybee populations.

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