Special Issue "Antiviral Defense in Invertebrates"

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Insect Viruses".

Deadline for manuscript submissions: closed (5 February 2018).

Special Issue Editor

Dr. Michelle Flenniken
E-Mail Website
Guest Editor
Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT, USA
Interests: honey bee host pathogen interactions; ssRNA viruses; honey bees; honey bee pathogens; antiviral defense; dsRNA triggered immune responses; Lake Sinai viruses; Potato virus Y (PVY)-host interactions

Special Issue Information

Dear Colleagues,

Invertebrate organisms include vectors of human viruses (mosquitos), model organisms (fruit fly), pollinators (honey bees and bumble bees), plant virus vectors (aphids), and commercially valuable aquatic species (oysters and shrimp) that play important roles in shaping in ecosystems throughout the world. Like all organisms, invertebrates are infected by viruses and have, in turn, evolved strategies to limit virus infection. Invertebrate antiviral defense involves canonical immune signalling cascades (e.g., JAK/STAT, Toll, Imd), heat shock responses, apoptosis, and dsRNA-triggered responses including the sequence-specific RNA interference mechanism and a less well characterized, non-sequence specific dsRNA mediated response.

This Special Issue of Viruses features articles written by prominent researchers in the field of invertebrate immunology. The goal of this compilation is to better understand the similarities and differences in antiviral responses mounted by invertebrates, while recognizing that some of what is learned is unique to specific virus–host pairs. Interesting parallels can be drawn between invertebrate and vertebrate antiviral responses and in some cases homologous genes that play similar roles in a wide range of organisms have been identified. Together the articles in this issue serve as a foundation for future studies aimed at further elucidating the molecular mechanism of invertebrate antiviral defense.

Dr. Michelle Flenniken
Guest Editor

Manuscript Submission Information

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Keywords

  • antiviral defense
  • RNAi
  • invertebrate
  • Drosophila
  • honey bee
  • mosquito
  • innate immunity
  • cell mediated immunity
  • PAMP
  • VAMP

Published Papers (13 papers)

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Editorial

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Editorial
Antiviral Defense in Invertebrates
Viruses 2018, 10(8), 403; https://0-doi-org.brum.beds.ac.uk/10.3390/v10080403 - 31 Jul 2018
Cited by 2 | Viewed by 1346
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)

Research

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Article
The C-Type Lectin Domain Gene Family in Aedes aegypti and Their Role in Arbovirus Infection
Viruses 2018, 10(7), 367; https://0-doi-org.brum.beds.ac.uk/10.3390/v10070367 - 12 Jul 2018
Cited by 14 | Viewed by 2114
Abstract
Several medically important flaviviruses that are transmitted by mosquitoes have been shown to bind to the C-type lectin fold that is present in either vertebrate or invertebrate proteins. While in some cases this interaction is part of a neutralizing anti-viral immune response, many [...] Read more.
Several medically important flaviviruses that are transmitted by mosquitoes have been shown to bind to the C-type lectin fold that is present in either vertebrate or invertebrate proteins. While in some cases this interaction is part of a neutralizing anti-viral immune response, many reports have implicated this as critical for successful virus entry. Despite the establishment of mosquito C-type lectin domain containing proteins (CTLDcps) as known host factors in assisting the infectious process for flaviviruses, little is known about the structural characteristics of these proteins and their relationships to each other. In this report, we describe the manual annotation and structural characterization of 52 Aedes aegypti CTLDcps. Using existing RNAseq data, we establish that these genes can be subdivided into two classes: those highly conserved with expression primarily in development (embryo/early larvae) and those with no clear orthologs with expression primarily in late larvae/pupae or adults. The latter group contained all CTLDcps that are regulated by the Toll/Imd immune pathways, all known microbiome-regulating CTLDcps, and almost all CTLDcps that are implicated as flavivirus host factors in A. aegypti. Finally, we attempt to synthesize results from multiple conflicting gene expression profiling experiments in terms of how flavivirus infection changes steady-state levels of mRNA encoding CTLDcps. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Article
piRNA Profiling of Dengue Virus Type 2-Infected Asian Tiger Mosquito and Midgut Tissues
Viruses 2018, 10(4), 213; https://0-doi-org.brum.beds.ac.uk/10.3390/v10040213 - 22 Apr 2018
Cited by 25 | Viewed by 3099
Abstract
The Asian tiger mosquito, Aedes albopictus, is a competent vector for the majority of arboviruses. The mosquito innate immune response is a primary determinant for arthropod-borne virus transmission, and the midgut is the first barrier to pathogen transmission. Mosquito antiviral immunity is [...] Read more.
The Asian tiger mosquito, Aedes albopictus, is a competent vector for the majority of arboviruses. The mosquito innate immune response is a primary determinant for arthropod-borne virus transmission, and the midgut is the first barrier to pathogen transmission. Mosquito antiviral immunity is primarily mediated by the small interfering RNA pathway. However, the roles that the P-element induced wimpy testis (PIWI)-interacting RNA (piRNA) pathway play in antiviral immunity in Ae. albopictus and its midgut still need further exploration. This study aimed to explore the profiles of both viral-derived and host-originated piRNAs in the whole body and midgut infected with Dengue virus 2 (DENV-2) in Ae. albopictus, and to elucidate gene expression profile differences of the PIWI protein family between adult females and their midguts. A deep sequencing-based method was used to identify and analyze small non-coding RNAs, especially the piRNA profiles in DENV-2-infected Ae. albopictus and its midgut. The top-ranked, differentially-expressed piRNAs were further validated using Stem-loop qRT-PCR. Bioinformatics analyses and reverse-transcription PCR (RT-PCR) methods were used to detect PIWI protein family members, and their expression profiles. DENV-2 derived piRNAs (vpiRNA, 24–30 nts) were observed in both infected Ae. albopictus and its midgut; however, only vpiRNA in the whole-body library had a weak preference for adenine at position 10 (10A) in the sense molecules as a feature of secondary piRNA. These vpiRNAs were not equally distributed, instead they were derived from a few specific regions of the genome, especially several hot spots, and displayed an obvious positive strand bias. We refer to the differentially expressed host piRNAs after DENV infection as virus-induced host endogenous piRNAs (vepiRNAs). However, we found that vepiRNAs were abundant in mosquito whole-body tissue, but deficient in the midgut. A total of eleven PIWI family genes were identified in Ae. albopictus; however, only AalPiwi5–7 and AalAgo3(1–2) were readily detected in the midgut. The characteristics of piRNAs in DENV-2-infected Ae. albopictus adult females were similar to those previously described for flavivirus infections but were not observed in the midgut. The reduced levels of vepiRNAs and incomplete expression of PIWI pathway genes in midgut samples from DENV-2-infected Ae. albopictus suggests that viral regulation of host piRNAs may not be an important factor in the midgut. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Article
Baculovirus PTP2 Functions as a Pro-Apoptotic Protein
Viruses 2018, 10(4), 181; https://0-doi-org.brum.beds.ac.uk/10.3390/v10040181 - 07 Apr 2018
Cited by 4 | Viewed by 2311
Abstract
The family Baculoviridae encompasses a large number of invertebrate viruses, mainly infecting caterpillars of the order Lepidoptera. The baculovirus Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) induces physiological and behavioral changes in its host Spodoptera exigua, as well as immunological responses, which may affect [...] Read more.
The family Baculoviridae encompasses a large number of invertebrate viruses, mainly infecting caterpillars of the order Lepidoptera. The baculovirus Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) induces physiological and behavioral changes in its host Spodoptera exigua, as well as immunological responses, which may affect virus transmission. Here we show that the SeMNPV-encoded protein tyrosine phosphatase 2 (PTP2) induces mild apoptosis in Spodoptera frugiperda (Sf) 21 cells upon transient expression. Transient expression of a catalytic-site mutant of ptp2 did not lead to apoptosis, indicating that the phosphatase activity of PTP2 is needed to induce apoptosis. We also found that the caspase level (indicator of apoptosis) was higher in cells transfected with the ptp2 gene than in cells transfected with the catalytic mutant. Adding a caspase inhibitor reduced the level of ptp2-induced apoptosis. Moreover, deletion of the ptp2 gene from the viral genome prevented the induction of apoptosis in S. exigua hemocytes. The virus titer and virulence indices (the viral infectivity and the time to death) were not affected by deletion of the ptp2 gene. However, the viral occlusion body yield from S. exigua larvae infected with the mutant virus lacking the ptp2 gene was much lower than the yield from larvae infected with the wild-type (WT) virus. We hypothesize that the observed pro-apoptotic effects of PTP2 are the result of PTP2-mediated immune suppression in larvae, which consequently leads to higher viral occlusion body yields. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Article
Identification of Secreted Proteins Involved in Nonspecific dsRNA-Mediated Lutzomyia longipalpis LL5 Cell Antiviral Response
Viruses 2018, 10(1), 43; https://0-doi-org.brum.beds.ac.uk/10.3390/v10010043 - 18 Jan 2018
Cited by 6 | Viewed by 2637
Abstract
Hematophagous insects transmit infectious diseases. Sand flies are vectors of leishmaniasis, but can also transmit viruses. We have been studying immune responses of Lutzomyia longipalpis, the main vector of visceral leishmaniasis in the Americas. We identified a non-specific antiviral response in L. [...] Read more.
Hematophagous insects transmit infectious diseases. Sand flies are vectors of leishmaniasis, but can also transmit viruses. We have been studying immune responses of Lutzomyia longipalpis, the main vector of visceral leishmaniasis in the Americas. We identified a non-specific antiviral response in L. longipalpis LL5 embryonic cells when treated with non-specific double-stranded RNAs (dsRNAs). This response is reminiscent of interferon response in mammals. We are investigating putative effectors for this antiviral response. Secreted molecules have been implicated in immune responses, including interferon-related responses. We conducted a mass spectrometry analysis of conditioned medium from LL5 cells 24 and 48 h after dsRNA or mock treatment. We identified 304 proteins. At 24 h, 19 proteins had an abundance equal or greater than 2-fold change, while the levels of 17 proteins were reduced when compared to control cells. At the 48 h time point, these numbers were 33 and 71, respectively. The two most abundant secreted peptides at 24 h in the dsRNA-transfected group were phospholipid scramblase, an interferon-inducible protein that mediates antiviral activity, and forskolin-binding protein (FKBP), a member of the immunophilin family, which mediates the effect of immunosuppressive drugs. The transcription profile of most candidates did not follow the pattern of secreted protein abundance. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Article
ABC Assay: Method Development and Application to Quantify the Role of Three DWV Master Variants in Overwinter Colony Losses of European Honey Bees
Viruses 2017, 9(11), 314; https://0-doi-org.brum.beds.ac.uk/10.3390/v9110314 - 27 Oct 2017
Cited by 43 | Viewed by 3813
Abstract
Deformed wing virus (DWV) is one of the most prevalent honey bee viral pathogens in the world. Typical of many RNA viruses, DWV is a quasi-species, which is comprised of a large number of different variants, currently consisting of three master variants: Type [...] Read more.
Deformed wing virus (DWV) is one of the most prevalent honey bee viral pathogens in the world. Typical of many RNA viruses, DWV is a quasi-species, which is comprised of a large number of different variants, currently consisting of three master variants: Type A, B, and C. Little is known about the impact of each variant or combinations of variants upon the biology of individual hosts. Therefore, we have developed a new set of master variant-specific DWV primers and a set of standards that allow for the quantification of each of the master variants. Competitive reverse transcriptase polymerase chain reaction (RT-PCR) experimental design confirms that each new DWV primer set is specific to the retrospective master variant. The sensitivity of the ABC assay is dependent on whether DNA or RNA is used as the template and whether other master variants are present in the sample. Comparison of the overall proportions of each master variant within a sample of known diversity, as confirmed by next-generation sequence (NGS) data, validates the efficiency of the ABC assay. The ABC assay was used on archived material from a Devon overwintering colony loss (OCL) 2006–2007 study; further implicating DWV type A and, for the first time, possibly C in the untimely collapse of honey bee colonies. Moreover, in this study DWV type B was not associated with OCL. The use of the ABC assay will allow researchers to quickly and cost effectively pre-screen for the presence of DWV master variants in honey bees. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Review

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Review
Honey Bee and Bumble Bee Antiviral Defense
Viruses 2018, 10(8), 395; https://0-doi-org.brum.beds.ac.uk/10.3390/v10080395 - 27 Jul 2018
Cited by 27 | Viewed by 4442
Abstract
Bees are important plant pollinators in both natural and agricultural ecosystems. Managed and wild bees have experienced high average annual colony losses, population declines, and local extinctions in many geographic regions. Multiple factors, including virus infections, impact bee health and longevity. The majority [...] Read more.
Bees are important plant pollinators in both natural and agricultural ecosystems. Managed and wild bees have experienced high average annual colony losses, population declines, and local extinctions in many geographic regions. Multiple factors, including virus infections, impact bee health and longevity. The majority of bee-infecting viruses are positive-sense single-stranded RNA viruses. Bee-infecting viruses often cause asymptomatic infections but may also cause paralysis, deformity or death. The severity of infection is governed by bee host immune responses and influenced by additional biotic and abiotic factors. Herein, we highlight studies that have contributed to the current understanding of antiviral defense in bees, including the Western honey bee (Apis mellifera), the Eastern honey bee (Apis cerana) and bumble bee species (Bombus spp.). Bee antiviral defense mechanisms include RNA interference (RNAi), endocytosis, melanization, encapsulation, autophagy and conserved immune pathways including Jak/STAT (Janus kinase/signal transducer and activator of transcription), JNK (c-Jun N-terminal kinase), MAPK (mitogen-activated protein kinases) and the NF-κB mediated Toll and Imd (immune deficiency) pathways. Studies in Dipteran insects, including the model organism Drosophila melanogaster and pathogen-transmitting mosquitos, provide the framework for understanding bee antiviral defense. However, there are notable differences such as the more prominent role of a non-sequence specific, dsRNA-triggered, virus limiting response in honey bees and bumble bees. This virus-limiting response in bees is akin to pathways in a range of organisms including other invertebrates (i.e., oysters, shrimp and sand flies), as well as the mammalian interferon response. Current and future research aimed at elucidating bee antiviral defense mechanisms may lead to development of strategies that mitigate bee losses, while expanding our understanding of insect antiviral defense and the potential evolutionary relationship between sociality and immune function. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Review
miRNAs in Insects Infected by Animal and Plant Viruses
Viruses 2018, 10(7), 354; https://0-doi-org.brum.beds.ac.uk/10.3390/v10070354 - 03 Jul 2018
Cited by 8 | Viewed by 2774
Abstract
Viruses vectored by insects cause severe medical and agricultural burdens. The process of virus infection of insects regulates and is regulated by a complex interplay of biomolecules including the small, non-coding microRNAs (miRNAs). Considered an anomaly upon its discovery only around 25 years [...] Read more.
Viruses vectored by insects cause severe medical and agricultural burdens. The process of virus infection of insects regulates and is regulated by a complex interplay of biomolecules including the small, non-coding microRNAs (miRNAs). Considered an anomaly upon its discovery only around 25 years ago, miRNAs as a class have challenged the molecular central dogma which essentially typifies RNAs as just intermediaries in the flow of information from DNA to protein. miRNAs are now known to be common modulators or fine-tuners of gene expression. While recent years has seen an increased emphasis on understanding the role of miRNAs in host-virus associations, existing literature on the interaction between insects and their arthropod-borne viruses (arboviruses) is largely restricted to miRNA abundance profiling. Here we analyse the commonalities and contrasts between miRNA abundance profiles with different host-arbovirus combinations and outline a suggested pipeline and criteria for functional analysis of the contribution of miRNAs to the insect vector-virus interaction. Finally, we discuss the potential use of the model organism, Drosophila melanogaster, in complementing research on the role of miRNAs in insect vector-virus interaction. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Review
Defense Mechanisms against Viral Infection in Drosophila: RNAi and Non-RNAi
Viruses 2018, 10(5), 230; https://0-doi-org.brum.beds.ac.uk/10.3390/v10050230 - 01 May 2018
Cited by 32 | Viewed by 3466
Abstract
RNAi is considered a major antiviral defense mechanism in insects, but its relative importance as compared to other antiviral pathways has not been evaluated comprehensively. Here, it is attempted to give an overview of the antiviral defense mechanisms in Drosophila that involve both [...] Read more.
RNAi is considered a major antiviral defense mechanism in insects, but its relative importance as compared to other antiviral pathways has not been evaluated comprehensively. Here, it is attempted to give an overview of the antiviral defense mechanisms in Drosophila that involve both RNAi and non-RNAi. While RNAi is considered important in most viral infections, many other pathways can exist that confer antiviral resistance. It is noted that very few direct recognition mechanisms of virus infections have been identified in Drosophila and that the activation of immune pathways may be accomplished indirectly through cell damage incurred by viral replication. In several cases, protection against viral infection can be obtained in RNAi mutants by non-RNAi mechanisms, confirming the variability of the RNAi defense mechanism according to the type of infection and the physiological status of the host. This analysis is aimed at more systematically investigating the relative contribution of RNAi in the antiviral response and more specifically, to ask whether RNAi efficiency is affected when other defense mechanisms predominate. While Drosophila can function as a useful model, this issue may be more critical for economically important insects that are either controlled (agricultural pests and vectors of diseases) or protected from parasite infection (beneficial insects as bees) by RNAi products. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
Review
Conflict in the Intracellular Lives of Endosymbionts and Viruses: A Mechanistic Look at Wolbachia-Mediated Pathogen-blocking
Viruses 2018, 10(4), 141; https://0-doi-org.brum.beds.ac.uk/10.3390/v10040141 - 21 Mar 2018
Cited by 45 | Viewed by 4417
Abstract
At the forefront of vector control efforts are strategies that leverage host-microbe associations to reduce vectorial capacity. The most promising of these efforts employs Wolbachia, a maternally transmitted endosymbiotic bacterium naturally found in 40% of insects. Wolbachia can spread through a population [...] Read more.
At the forefront of vector control efforts are strategies that leverage host-microbe associations to reduce vectorial capacity. The most promising of these efforts employs Wolbachia, a maternally transmitted endosymbiotic bacterium naturally found in 40% of insects. Wolbachia can spread through a population of insects while simultaneously inhibiting the replication of viruses within its host. Despite successes in using Wolbachia-transfected mosquitoes to limit dengue, Zika, and chikungunya transmission, the mechanisms behind pathogen-blocking have not been fully characterized. Firstly, we discuss how Wolbachia and viruses both require specific host-derived structures, compounds, and processes to initiate and maintain infection. There is significant overlap in these requirements, and infection with either microbe often manifests as cellular stress, which may be a key component of Wolbachia’s anti-viral effect. Secondly, we discuss the current understanding of pathogen-blocking through this lens of cellular stress and develop a comprehensive view of how the lives of Wolbachia and viruses are fundamentally in conflict with each other. A thorough understanding of the genetic and cellular determinants of pathogen-blocking will significantly enhance the ability of vector control programs to deploy and maintain effective Wolbachia-mediated control measures. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Review
Antiviral Defense and Innate Immune Memory in the Oyster
Viruses 2018, 10(3), 133; https://0-doi-org.brum.beds.ac.uk/10.3390/v10030133 - 16 Mar 2018
Cited by 33 | Viewed by 3485
Abstract
The Pacific oyster, Crassostrea gigas, is becoming a valuable model for investigating antiviral defense in the Lophotrochozoa superphylum. In the past five years, improvements to laboratory-based experimental infection protocols using Ostreid herpesvirus I (OsHV-1) from naturally infected C. gigas combined with next-generation [...] Read more.
The Pacific oyster, Crassostrea gigas, is becoming a valuable model for investigating antiviral defense in the Lophotrochozoa superphylum. In the past five years, improvements to laboratory-based experimental infection protocols using Ostreid herpesvirus I (OsHV-1) from naturally infected C. gigas combined with next-generation sequencing techniques has revealed that oysters have a complex antiviral response involving the activation of all major innate immune pathways. Experimental evidence indicates C. gigas utilizes an interferon-like response to limit OsHV-1 replication and spread. Oysters injected with a viral mimic (polyI:C) develop resistance to OsHV-1. Improved survival following polyI:C injection was found later in life (within-generational immune priming) and in the next generation (multi-generational immune priming). These studies indicate that the oyster’s antiviral defense system exhibits a form of innate immune-memory. An important priority is to identify the molecular mechanisms responsible for this phenomenon. This knowledge will motivate the development of practical and cost-effective treatments for improving oyster health in aquaculture. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Review
Natural Variation in Resistance to Virus Infection in Dipteran Insects
Viruses 2018, 10(3), 118; https://0-doi-org.brum.beds.ac.uk/10.3390/v10030118 - 09 Mar 2018
Cited by 37 | Viewed by 5379
Abstract
The power and ease of Drosophila genetics and the medical relevance of mosquito-transmitted viruses have made dipterans important model organisms in antiviral immunology. Studies of virus–host interactions at the molecular and population levels have illuminated determinants of resistance to virus infection. Here, we [...] Read more.
The power and ease of Drosophila genetics and the medical relevance of mosquito-transmitted viruses have made dipterans important model organisms in antiviral immunology. Studies of virus–host interactions at the molecular and population levels have illuminated determinants of resistance to virus infection. Here, we review the sources and nature of variation in antiviral immunity and virus susceptibility in model dipteran insects, specifically the fruit fly Drosophila melanogaster and vector mosquitoes of the genera Aedes and Culex. We first discuss antiviral immune mechanisms and describe the virus-specificity of these responses. In the following sections, we review genetic and microbiota-dependent variation in antiviral immunity. In the final sections, we explore less well-studied sources of variation, including abiotic factors, sexual dimorphism, infection history, and endogenous viral elements. We borrow from work on other pathogen types and non-dipteran species when it parallels or complements studies in dipterans. Understanding natural variation in virus–host interactions may lead to the identification of novel restriction factors and immune mechanisms and shed light on the molecular determinants of vector competence. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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Other

Opinion
Honey Bee Antiviral Immune Barriers as Affected by Multiple Stress Factors: A Novel Paradigm to Interpret Colony Health Decline and Collapse
Viruses 2018, 10(4), 159; https://0-doi-org.brum.beds.ac.uk/10.3390/v10040159 - 30 Mar 2018
Cited by 29 | Viewed by 2424
Abstract
Any attempt to outline a logical framework in which to interpret the honey bee health decline and its contribution to elevated colony losses should recognize the importance of the multifactorial nature of the responsible syndrome and provide a functional model as a basis [...] Read more.
Any attempt to outline a logical framework in which to interpret the honey bee health decline and its contribution to elevated colony losses should recognize the importance of the multifactorial nature of the responsible syndrome and provide a functional model as a basis for defining and testing working hypotheses. We propose that covert infections by deformed wing virus (DWV) represent a sword of Damocles permanently threatening the survival of honey bee colonies and suggest that any factor affecting the honey bee’s antiviral defenses can turn this pathogen into a killer. Here we discuss the available experimental evidence in the framework of a model based on honey bee immune competence as affected by multiple stress factors that is proposed as a conceptual tool for analyzing bee mortality and its underlying mechanisms. Full article
(This article belongs to the Special Issue Antiviral Defense in Invertebrates)
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