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Viral Co-Infections and Antiviral Immunity in Honey Bees

VIRUSES-BASEL (2023)

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Karen Luisa Haag et al.

Summary: Compared to other types of bees, the effect of diet on the gut microbiome of Neotropical corbiculate bees is not well understood. This study found that there was an increase in gut-associated bacteria in forager bees 2 months before the first symptoms were recorded. Additionally, forager bees showed a decrease in body weight. These changes were linked to diet shifts, specifically the increase in Eucalyptus spp. pollen in the bees' guts. There was also a negative correlation between the amount of Eucalyptus pollen in diets and the abundance of certain bacterial taxa in the gut-associated microbiota.

MICROBIAL ECOLOGY (2023)

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Article Behavioral Sciences

Social immunity in the honey bee: do immune-challenged workers enter enforced or self-imposed exile?

Tarli E. Conroy et al.

Summary: The study shows that immune-challenged honey bees tend to voluntarily leave the hive, while healthy worker bees also actively evict immune-stimulated bees, possibly to limit the spread of pathogens within the colony. Through chemical signals, bees are able to identify and banish sick individuals, demonstrating a form of social immunity in action.

BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY (2022)

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Article Entomology

Warmer winters are associated with lower levels of the cryoprotectant glycerol, a slower decrease in vitellogenin expression and reduced virus infections in winter honeybees

Alberto Prado et al.

Summary: Within the context of climate change, winter temperatures at high latitudes are predicted to rise faster than summer temperatures. This phenomenon is expected to negatively affect the diapause performance and survival of insects, since they largely rely on low temperatures to lower their metabolism and preserve energy. However, some insects like honeybees, remain relatively active during the winter and elevate their metabolic rate to produce endothermic heat when temperatures drop. Warming winters are thus expected to improve overwintering performance of honeybees.

JOURNAL OF INSECT PHYSIOLOGY (2022)

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Article Entomology

Context-Dependent Viral Transgenerational Immune Priming in Honey Bees (Hymenoptera: Apidae)

Sarah Lang et al.

Summary: The study found evidence for viral transgenerational immune priming in honey bees, but it is highly context-dependent based on route of maternal exposure and potentially host genetics or epigenetic factors.

JOURNAL OF INSECT SCIENCE (2022)

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Article Virology

Cold case: The disappearance of Egypt bee virus, a fourth distinct master strain of deformed wing virus linked to honeybee mortality in 1970's Egypt

Joachim R. de Miranda et al.

Summary: In this study, a previously unknown variant of deformed wing virus (DWV-D) was discovered in diseased adult honeybees from Egypt. DWV-D is distinct from the commonly found variants DWV-A and DWV-B, and was not detected in a worldwide selection of honeybee, varroa, and bumblebee samples.

VIROLOGY JOURNAL (2022)

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Article Entomology

Middle-Aged Worker Bees Express Higher Innate Immunity than Young Worker Bees in the Abdomen without the Digestive Tract of Worker Bees Reared in an Incubator

Yi-Wen Lin et al.

Summary: Middle-aged worker bees have higher innate immunity than young worker bees, and raising bees in an incubator can prevent infection from pathogens and parasites.

INSECTS (2022)

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Article Entomology

Analysis of the gut microbiome of susceptible and resistant honeybees (Apis cerana) against sacbrood virus disease

Chaerin Kim et al.

Summary: The global decline in wild bee population, especially the sudden disappearance of millions of managed bees in Korea, has raised concerns. This study found significant differences in the gut bacterial community between resistant and susceptible bees, suggesting that this difference may contribute to disease resistance.

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Comparison of the gut microbiome of sacbrood virus-resistant and -susceptible Apis cerana from South Korea

Bo-Ram Yun et al.

Summary: This study investigated the relationship between the gut microbiome of honey bees and sacbrood disease (SD). It was found that sacbrood virus (SBV)-resistant honey bee strains harbor specific acetic acid bacteria and lactic acid bacteria. SBV infection led to the loss of beneficial bacteria in the honey bee gut, which could affect host nutrition and inhibit honey bee pathogens.

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Article Biochemistry & Molecular Biology

The origin of RNA interference: Adaptive or neutral evolution?

Alessandro Torri et al.

Summary: The origin of RNA interference (RNAi) is usually explained as a defense mechanism, but we propose a neutral evolutionary hypothesis suggesting that RNAi is formed through constructive neutral evolution (CNE) from a prokaryotic antisense RNA gene regulation mechanism. We argue that RNAi was already present in the ancestor of LECA and had a significant impact on eukaryotic genomic architecture and stability.

PLOS BIOLOGY (2022)

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Article Ecology

Epidemiology of a major honey bee pathogen, deformed wing virus: potential worldwide replacement of genotype A by genotype B

Robert J. Paxton et al.

Summary: The honey bee colony losses in temperate regions are largely caused by the transmittance of ectoparasitic mite Varroa destructor and deformed wing virus (DWV), with the rapidly expanding DWV-B potentially replacing the formerly widespread DWV-A. Both genotypes are found in wild bee species, and interference between viral genotypes when co-infecting the same host plays a key role in their epidemiology.

INTERNATIONAL JOURNAL FOR PARASITOLOGY-PARASITES AND WILDLIFE (2022)

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Article Parasitology

Transmission of deformed wing virus between Varroa destructor foundresses, mite offspring and infested honey bees

Vincent Piou et al.

Summary: The study showed a positive correlation between viral loads in bees and mites, with mites carrying multiple DWV variants associated with higher mortality of the infected host. In laboratory conditions, mite infestation increased DWV-B loads and decreased DWV-A loads. Furthermore, viral loads in the mite offspring were more closely correlated with the foundress mites than with the bee hosts in situ.

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Review Virology

Sacbrood Virus: A Growing Threat to Honeybees and Wild Pollinators

Ruike Wei et al.

Summary: This article summarizes the existing knowledge of sacbrood virus (SBV) and addresses the gaps in knowledge within the existing literature, aiming to provide future directions for research and development of management strategies to control the spread of this deadly disease.

VIRUSES-BASEL (2022)

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Article Environmental Sciences

Antibiotics-induced changes in intestinal bacteria result in the sensitivity of honey bee to virus

Yanchun Deng et al.

Summary: Antibiotics are widely used and present in the environment, causing negative impacts on organisms. This study investigated the increased sensitivity of honey bees to viral infection due to antibiotic exposure. The findings showed that antibiotic treatment altered the gut microbiome in bees and promoted their susceptibility to viral infection.

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Review Veterinary Sciences

Bee Stressors from an Immunological Perspective and Strategies to Improve Bee Health

Hesham R. El-Seedi et al.

Summary: This review focuses on the composition of the honeybee immune system and the effects of exposure to stressors on immune competence. Nutrition and phytochemicals play a crucial role in honeybee immunity.

VETERINARY SCIENCES (2022)

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Article Biotechnology & Applied Microbiology

The novel insecticides flupyradifurone and sulfoxaflor do not act synergistically with viral pathogens in reducing honey bee (Apis mellifera) survival but sulfoxaflor modulates host immunocompetence

Yahya Al Naggar et al.

Summary: The study found that common viral pathogens pose a major threat to honey bees, while co-exposure to these novel nACHR insecticides does not significantly exacerbate viral impacts on host survival in the laboratory.

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Deformed wing virus: using reverse genetics to tackle unanswered questions about the most important viral pathogen of honey bees

Luke Woodford et al.

Summary: Deformed wing virus (DWV) is a significant viral pathogen of honey bees, particularly when vectored by mites. The lack of in vitro cell culture has hindered research, but the development of reverse genetic systems has allowed for advancements in studying strain variation, host tropism, and pathogenesis.

FEMS MICROBIOLOGY REVIEWS (2021)

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Article Virology

Direct Evidence for Infection of Varroa destructor Mites with the Bee-Pathogenic Deformed Wing Virus Variant B, but Not Variant A, via Fluorescence In Situ Hybridization Analysis

Sebastian Gisder et al.

Summary: Deformed wing virus (DWV), a bee-pathogenic virus, is spread by the mite Varroa destructor, leading to severe infections in bees. Different variants of DWV exist, and there is debate on whether the mite is a mechanical or biological vector of DWV.

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Article Entomology

Effects of Deformed Wing Virus Infection on Expressions of Immune- and Apoptosis-Related Genes in Western Honeybees (Apis mellifera)

Wannapha Mookhploy et al.

Summary: Deformed wing virus (DWV) affects honeybees by altering immune and apoptosis gene expressions after infection. This may lead to increased mortality rates in infected bees, although wing deformities are not directly correlated with virus levels and immune apoptosis responses.

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Article Biotechnology & Applied Microbiology

Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees (Apis mellifera)

Allyson M. Ray et al.

Summary: The study demonstrated that simulated vector transmission had differential impacts on two closely related viral variants, which could potentially influence viral interactions with the host and showed surprising plasticity in vector-host-viral dynamics.

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Social immunity in honey bees: royal jelly as a vehicle in transferring bacterial pathogen fragments between nestmates

Gyan Harwood et al.

Summary: Social immunity in honey bees involves the transfer of immunological compounds through royal jelly, promoting higher pathogen resistance in offspring. This form of immunity also allows queens to prime their eggs with pathogen fragments, enhancing the embryo's immune system. Consuming pathogen cells induces increased levels of antimicrobial peptides in royal jelly.

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Review Pharmacology & Pharmacy

Propolis antiviral and immunomodulatory activity: a review and perspectives for COVID-19 treatment

Nicolas Ripari et al.

Summary: Propolis is a safe bee-made product with antiviral and immunomodulatory activity. Clinical trials are needed to investigate its effects on individuals with viral diseases, either alone or in combination with antiviral drugs or vaccines. Specific research on the effects of propolis on COVID-19, either in vitro or in infected individuals, should also be conducted to explore its potential as a treatment option.

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Article Biology

Mass-flowering monoculture attracts bees, amplifying parasite prevalence

Hamutahl Cohen et al.

Summary: The study found that mass-flowering crops increase bee abundance, but are also associated with parasite presence. Wild bee abundance is related to parasite presence, but only in areas with low amounts of non-crop flowers. Bee traits related to higher dispersal ability and broader diet are positively correlated with parasite presence.

PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES (2021)

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Review Plant Sciences

siRNA Specificity: RNAi Mechanisms and Strategies to Reduce Off-Target Effects

Julia Neumeier et al.

Summary: SiRNAs and miRNAs function differently in RNAi, with siRNAs directly cleaving target RNAs while miRNAs inhibit translation followed by exonucleolytic decay. However, siRNAs can also lead to miRNA-like off-target effects.

FRONTIERS IN PLANT SCIENCE (2021)

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Article Ecology

Exposure to Inactivated Deformed Wing Virus Leads to Trans-Generational Costs but Not Immune Priming in Honeybees (Apis mellifera)

Matti Leponiemi et al.

Summary: The study found that honeybees may not be able to prime their offspring against a viral pathogen by exposing queens to an inactivated deformed wing virus. However, maternal immune challenge and stress from injection during development can lead to increased costs in offspring, resulting in more deformed wings.

FRONTIERS IN ECOLOGY AND EVOLUTION (2021)

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Article Multidisciplinary Sciences

Honey bees increase social distancing when facing the ectoparasite Varroa destructor

Michelina Pusceddu et al.

Summary: By studying how honey bee colonies respond to parasite intrusion, it was found that bees modify space use and social interactions to increase social distancing between young and old bees, suggesting a previously unreported behavioral strategy in honey bees to limit intracolony parasite transmission.

SCIENCE ADVANCES (2021)

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Article Ecology

The Holobiont as a Key to the Adaptation and Conservation of Wild Bees in the Anthropocene

Kevin Maebe et al.

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Article Agronomy

Nosema Ceranae Interactions with Nosema apis and Black Queen Cell Virus

Anna Maria Gajda et al.

Summary: Research findings indicate that N. ceranae is more pathogenic to A. mellifera than N. apis, and the course of type C nosemosis is more severe, resulting in shorter lifespans for bees. The presence of BQCV exacerbates the disease, making it even more dangerous for bees.

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Article Microbiology

Intra-Colonial Viral Infections in Western Honey Bees (Apis Mellifera)

Loreley Castelli et al.

Summary: RNA viruses, particularly DWV, play a significant role in pollinator losses. This study analyzed DWV variants in Varroa destructor-parasitized pupae, finding that only DWV was detected and its two variants showed significant differences across sampling periods, colonies, and patrilines.

MICROORGANISMS (2021)

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Article Microbiology

The Gut Microbiota Can Provide Viral Tolerance in the Honey Bee

Christopher Dosch et al.

Summary: The study showed that a normal gut microbiota can increase honey bee survival upon viral infection, indicating a positive role of gut microbiota for honey bee health.

MICROORGANISMS (2021)

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Article Biochemistry & Molecular Biology

IAPV-Induced Paralytic Symptoms Associated with Tachypnea via Impaired Tracheal System Function

Yanchun Deng et al.

Summary: The Israeli acute paralysis virus was found to be most abundant in the tracheae of honey bees, positively correlated with viral titers, leading to respiratory failure and typical symptoms of paralysis and trembling. The virus-induced increase in viral loads in the tracheae down-regulates succinate dehydrogenase and cytochrome c oxidase genes, resulting in respiratory distress.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Article Ecology

First come, first served: superinfection exclusion in Deformed wing virus is dependent upon sequence identity and not the order of virus acquisition

Olesya N. Gusachenko et al.

Summary: Deformed wing virus (DWV) is a globally distributed pathogen of honey bees, which when vectored by Varroa destructor can lead to high levels of colony losses. Different DWV types may compete and interact within colonies, with the ability to outcompete existing infections correlated to genetic divergence. Genetic recombination within the DWV genome results in recombinants accounting for a small portion of the population.

ISME JOURNAL (2021)

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Article Multidisciplinary Sciences

Developmental environment shapes honeybee worker response to virus infection

Alexander Walton et al.

Summary: This study manipulated worker developmental nutrition in two ways and found that early life nutritional stress significantly reduced bees' resilience to virus infection and affected the expression of key genes related to immune function. This highlights the importance of considering early life nutritional stress in affecting health-related phenotypes and provides insights into the long-term effects of nutritional stress on honeybee health and its potential interactions with other stressors, such as disease.

SCIENTIFIC REPORTS (2021)

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Article Microbiology

Transcriptome Profiling Reveals a Novel Mechanism of Antiviral Immunity Upon Sacbrood Virus Infection in Honey Bee Larvae (Apis cerana)

Yulong Guo et al.

Summary: This study used high throughput next-generation sequencing technology to investigate host transcriptional responses to CSBV infection in A. cerana larvae, identifying 2,534 differentially expressed genes associated with viral infection. The upregulation of genes involved in host innate immunity pathways and the involvement of the Sirtuin signaling pathway in insects' immune response were notably observed, providing novel insights into molecular mechanisms and immune responses in CSBV infection.

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INSECTS (2021)

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Article Microbiology

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Margaret Steele et al.

Summary: Commensal microbes in animal guts play a role in excluding bacterial pathogens. In honey bees, disruption of the gut microbiota increases susceptibility to the opportunistic pathogen Serratia marcescens, which uses a T6SS to kill competitors in laboratory settings. However, within the bee gut, S. marcescens is rapidly eliminated in the presence of the microbiota and shows limited ability to compete with commensal species, indicating the importance of a healthy gut microbiota in protecting against pathogens.

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High resistance to Sacbrood virus disease in Apis cerana (Hymenoptera: Apidae) colonies selected for superior brood viability and hygienic behavior

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Accumulation and Competition Amongst Deformed Wing Virus Genotypes in Naive Australian Honeybees Provides Insight Into the Increasing Global Prevalence of Genotype B

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Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model

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Review Immunology

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FRONTIERS IN IMMUNOLOGY (2017)

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Hemocyte-mediated phagocytosis differs between honey bee (Apis mellifera) worker castes

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PLOS ONE (2017)

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Virus and dsRNA-triggered transcriptional responses reveal key components of honey bee antiviral defense

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The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss

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Protein nutrition governs within-host race of honey bee pathogens

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DEVELOPMENTAL AND COMPARATIVE IMMUNOLOGY (2017)

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Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies

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Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera)

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A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

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The Iflaviruses Sacbrood virus and Deformed wing virus evoke different transcriptional responses in the honeybee which may facilitate their horizontal or vertical transmission

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In vivo and in vitro infection dynamics of honey bee viruses

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Genetic diversity within honey bee colonies affects pathogen load and relative virus levels in honey bees, Apis mellifera L

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Evidence of the synergistic interaction of honey bee pathogens Nosema ceranae and Deformed wing virus

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Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees

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Parallel Epigenomic and Transcriptomic Responses to Viral Infection in Honey Bees (Apis mellifera)

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CURRENT OPINION IN INSECT SCIENCE (2015)

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Overwintering Is Associated with Reduced Expression of Immune Genes and Higher Susceptibility to Virus Infection in Honey Bees

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Immunogene and viral transcript dynamics during parasitic Varroa destructor mite infection of developing honey bee (Apis mellifera) pupae

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Infection of honey bees with acute bee paralysis virus does not trigger humoral or cellular immune responses

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Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies

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Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila

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Deformed wing virus: replication and viral load in mites (Varroa destructor)

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Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection

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The presence of conifer resin decreases the use of the immune system in wood ants

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Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity

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Review Entomology

The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera)

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In situ hybridization assays for localization of the chronic bee paralysis virus in the honey bee (Apis mellifera) brain

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The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila

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Origins and evolution of eukaryotic RNA interference

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Relish regulates expression of antimicrobial peptide genes in the honeybee, Apis mellifera, shown by RNA interference

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Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination

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Immunogold localization of vitellogenin in the ovaries, hypopharyngeal glands and head fat bodies of honeybee workers, Apis mellifera

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A metagenomic survey of microbes in honey bee colony collapse disorder

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Importance of pollinators in changing landscapes for world crops

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Immune pathways and defence mechanisms in honey bees Apis mellifera

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Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera)

GV Amdam et al.

BEHAVIOURAL BRAIN RESEARCH (2006)

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Reproductive protein protects functionally sterile honey bee workers from oxidative stress

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Trans-generational immune priming in a social insect

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Dicing and slicing - The core machinery of the RNA interference pathway

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Ribo-gnome: The big world of small RNAs

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Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite

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Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2005)

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Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees

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Phenoloxidase activity in Apis mellifera honey bee pupae, and ecdysteroid-dependent expression of the prophenoloxidase mRNA

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Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor

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The damage-response framework of microbial pathogenesis

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2003)

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Nucleopolyhedroviruses of forest and western tent caterpillars: cross-infectivity and evidence for activation of latent virus in high-density field populations

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Inhibition of vitellogenin synthesis in Apis mellifera workers by a juvenile hormone analogue, pyriproxyfen

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