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

2019 ◽  
Vol 286 (1901) ◽  
pp. 20190331 ◽  
Author(s):  
Desiderato Annoscia ◽  
Sam P. Brown ◽  
Gennaro Di Prisco ◽  
Emanuele De Paoli ◽  
Simone Del Fabbro ◽  
...  

The association between the deformed wing virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honeybee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, particularly, the causes of viral proliferation in mite-infested bees. Here, we develop and test a novel hypothesis that mite feeding destabilizes viral immune control through the removal of both virus and immune effectors, triggering uncontrolled viral replication. Our hypothesis is grounded on the predator–prey theory developed by Volterra, which predicts prey proliferation when both predators and preys are constantly removed from the system. Consistent with this hypothesis, we show that the experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. By contrast, we do not find consistent support for alternative proposed mechanisms of viral expansion via mite immune suppression or within-host viral evolution. Our results suggest that haemolymph removal plays an important role in the enhanced pathogen virulence observed in the presence of feeding Varroa mites. Overall, these results provide a new model for the mechanisms driving pathogen–parasite interactions in bees, which ultimately underpin honeybee health decline and colony losses.

2018 ◽  
Author(s):  
Desiderato Annoscia ◽  
Sam P. Brown ◽  
Gennaro Di Prisco ◽  
Emanuele De Paoli ◽  
Simone Del Fabbro ◽  
...  

AbstractThe association between the Deformed Wing Virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honey bee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, in particular, the causes of viral proliferation in mite infested bees.Here we develop and test a novel hypothesis - grounded in ecological predator-prey theory - that mite feeding destabilizes viral immune control through the removal of both viral ‘prey’ and immune ‘predators’, triggering uncontrolled viral replication. Consistent with this hypothesis, we show that experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. In contrast, we find no support for alternative proposed mechanisms of viral expansion via mite immune-suppression or within-host viral evolution.Overall, these results provide a new model for the mechanisms driving pathogen-parasite interactions in bees, which ultimately underpin honey bee health decline and colony losses.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Francisco Posada-Florez ◽  
Zachary S. Lamas ◽  
David J. Hawthorne ◽  
Yanping Chen ◽  
Jay D. Evans ◽  
...  

AbstractTransmission routes impact pathogen virulence and genetics, therefore comprehensive knowledge of these routes and their contribution to pathogen circulation is essential for understanding host–pathogen interactions and designing control strategies. Deformed wing virus (DWV), a principal viral pathogen of honey bees associated with increased honey bee mortality and colony losses, became highly virulent with the spread of its vector, the ectoparasitic mite Varroa destructor. Reproduction of Varroa mites occurs in capped brood cells and mite-infested pupae from these cells usually have high levels of DWV. The removal of mite-infested pupae by worker bees, Varroa Sensitive Hygiene (VSH), leads to cannibalization of pupae with high DWV loads, thereby offering an alternative route for virus transmission. We used genetically tagged DWV to investigate virus transmission to and between worker bees following pupal cannibalisation under experimental conditions. We demonstrated that cannibalization of DWV-infected pupae resulted in high levels of this virus in worker bees and that the acquired virus was then transmitted between bees via trophallaxis, allowing circulation of Varroa-vectored DWV variants without the mites. Despite the known benefits of hygienic behaviour, it is possible that higher levels of VSH activity may result in increased transmission of DWV via cannibalism and trophallaxis.


2016 ◽  
Vol 113 (12) ◽  
pp. 3203-3208 ◽  
Author(s):  
Gennaro Di Prisco ◽  
Desiderato Annoscia ◽  
Marina Margiotta ◽  
Rosalba Ferrara ◽  
Paola Varricchio ◽  
...  

Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite–virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.


2020 ◽  
Author(s):  
Francisco Posada-Florez ◽  
Zachary Lamas ◽  
David Hawthorne ◽  
Yanping Chen ◽  
Jay Evans ◽  
...  

Abstract Transmission routes impact pathogen virulence and genetics, therefore comprehensive knowledge of these routes and their contribution to pathogen circulation is essential for understanding host-pathogen interactions and designing control strategies. Deformed wing virus (DWV), a principal viral pathogen of honey bees associated with increased honey bee mortality and colony losses, became highly virulent with the spread of its vector, the ectoparasitic mite Varroa destructor. Reproduction of Varroa mites occurs in capped brood cells and mite-infested pupae from these cells usually have high levels of DWV. The removal of mite-infested pupae by worker bees, Varroa Sensitive Hygiene (VSH), leads to cannibalization of pupae with high DWV loads, thereby offering an alternative route for virus transmission. We used genetically tagged DWV to investigate virus transmission to and between worker bees following pupal cannibalisation under experimental conditions. We demonstrated that cannibalization of DWV-infected pupae resulted in high levels of this virus in worker bees and that the acquired virus was then transmitted between bees via trophallaxis, allowing circulation of Varroa-vectored DWV variants without the mites. Despite the known benefits of hygienic behaviour, it is possible that higher levels of VSH activity may result in increased transmission of DWV via cannibalism and trophallaxis.


2020 ◽  
Author(s):  
Francisco Posada-Florez ◽  
Zachary S. Lamas ◽  
David J. Hawthorne ◽  
Yanping Chen ◽  
Jay D. Evans ◽  
...  

AbstractTransmission routes impact pathogen virulence and genetics, therefore comprehensive knowledge of these routes and their contribution to pathogen circulation is essential for understanding host-pathogen interactions and designing control strategies. Deformed wing virus (DWV), a principal viral pathogen of honey bees associated with increased honey bee mortality and colony losses, became highly virulent with the spread of its vector, the ectoparasitic mite Varroa destructor. Reproduction of Varroa mites occurs in capped brood cells and mite-infested pupae from these cells usually have high levels of DWV. The removal of mite-infested pupae by worker bees, Varroa Sensitive Hygiene (VSH), leads to cannibalization of pupae with high DWV loads, thereby offering an alternative route for virus transmission. We used genetically tagged DWV to investigate virus transmission to and between worker bees following pupal cannibalisation under experimental conditions. We demonstrated that cannibalization of DWV-infected pupae resulted in high levels of this virus in worker bees and that the acquired virus was then transmitted between bees via trophallaxis, allowing circulation of Varroa-vectored DWV variants without the mites. Despite the known benefits of hygienic behaviour, it is possible that higher levels of VSH activity may result in increased transmission of DWV via cannibalism and trophallaxis.


2011 ◽  
Vol 78 (4) ◽  
pp. 981-987 ◽  
Author(s):  
Benjamin Dainat ◽  
Jay D. Evans ◽  
Yan Ping Chen ◽  
Laurent Gauthier ◽  
Peter Neumann

ABSTRACTElevated winter losses of managed honeybee colonies are a major concern, but the underlying mechanisms remain controversial. Among the suspects are the parasitic miteVarroa destructor, the microsporidianNosema ceranae, and associated viruses. Here we hypothesize that pathogens reduce the life expectancy of winter bees, thereby constituting a proximate mechanism for colony losses. A monitoring of colonies was performed over 6 months in Switzerland from summer 2007 to winter 2007/2008. Individual dead workers were collected daily and quantitatively analyzed for deformed wing virus (DWV), acute bee paralysis virus (ABPV),N. ceranae, and expression levels of thevitellogeningene as a biomarker for honeybee longevity. Workers from colonies that failed to survive winter had a reduced life span beginning in late fall, were more likely to be infected with DWV, and had higher DWV loads. Colony levels of infection with the parasitic miteVarroa destructorand individual infections with DWV were also associated with reduced honeybee life expectancy. In sharp contrast, the level ofN. ceranaeinfection was not correlated with longevity. In addition,vitellogeningene expression was significantly positively correlated with ABPV andN. ceranaeloads. The findings strongly suggest thatV. destructorand DWV (but neitherN. ceranaenor ABPV) reduce the life span of winter bees, thereby constituting a parsimonious possible mechanism for honeybee colony losses.


2021 ◽  
Vol 9 ◽  
Author(s):  
Matti Leponiemi ◽  
Gro V. Amdam ◽  
Dalial Freitak

Pathogens are identified as one of the major drivers behind the honeybee colony losses, as well as one of the reasons for the reported declines in terrestrial insect abundances in recent decades. To fight infections, animals rely on their immune system. The immune system of many invertebrates can be primed by exposure to a pathogen, so that upon further exposure the animal is better protected. The protective priming effect can even extend to the next generation, but the species capable of priming the immune system of their offspring are still being investigated. Here we studied whether honeybees could prime their offspring against a viral pathogen, by challenging honeybee queens orally with an inactivated deformed wing virus (DWV), one of the most devastating honeybee viruses. The offspring were then infected by viral injection. The effects of immune priming were assayed by measuring viral loads and two typical symptoms of the virus, pupal mortality, and abnormal wing phenotype. We saw a low amount of wing deformities and low pupal mortality. While no clear priming effect against the virus was seen, we found that the maternal immune challenge, when combined with the stress caused by an injection during development, manifested in costs in the offspring, leading to an increased number of deformed wings.


2020 ◽  
Vol 7 (4) ◽  
pp. 159
Author(s):  
Julia Dittes ◽  
Heike Aupperle-Lellbach ◽  
Marc O. Schäfer ◽  
Christoph K. W. Mülling ◽  
Ilka U. Emmerich

Veterinarians are educated in prevention, diagnosis and treatment of diseases in various vertebrate species. As they are familiar with multifactorial health problems in single animals as well as in herd health management, their knowledge and skills can be beneficial for the beekeepers and honeybee health. However, in education and in practice, honeybees are not a common species for most veterinarians and the typical veterinary diagnostic methods such as blood sampling or auscultation are not applicable to the superorganism honeybee. Honeybee colonies may be affected by various biotic and abiotic factors. Among the infectious agents, RNA-viruses build the largest group, causing covert and overt infections in honeybee colonies which may lead to colony losses. Veterinarians could and should play a more substantial role in managing honeybee health—not limited to cases of notifiable diseases and official hygiene controls. This review discusses the veterinary diagnostic approach to adult bee examination with a special focus on diagnosis and differential diagnosis of the common virus diseases Acute Bee Paralysis Virus (ABPV)-Kashmir Bee Virus (KBV)-Israeli Acute Paralysis Virus (IAPV)-Complex, Chronic Bee Paralysis Virus (CBPV) and Deformed Wing Virus (DWV), as well as coinfections like Varroa spp. and Nosema spp.


Viruses ◽  
2020 ◽  
Vol 12 (5) ◽  
pp. 575 ◽  
Author(s):  
John M. K. Roberts ◽  
Nelson Simbiken ◽  
Chris Dale ◽  
Joel Armstrong ◽  
Denis L. Anderson

The global spread of the parasitic mite Varroa destructor has emphasized the significance of viruses as pathogens of honey bee (Apis mellifera) populations. In particular, the association of deformed wing virus (DWV) with V. destructor and its devastating effect on honey bee colonies has led to that virus now becoming one of the most well-studied insect viruses. However, there has been no opportunity to examine the effects of Varroa mites without the influence of DWV. In Papua New Guinea (PNG), the sister species, V. jacobsoni, has emerged through a host-shift to reproduce on the local A. mellifera population. After initial colony losses, beekeepers have maintained colonies without chemicals for more than a decade, suggesting that this bee population has an unknown mite tolerance mechanism. Using high throughput sequencing (HTS) and target PCR detection, we investigated whether the viral landscape of the PNG honey bee population is the underlying factor responsible for mite tolerance. We found A. mellifera and A. cerana from PNG and nearby Solomon Islands were predominantly infected by sacbrood virus (SBV), black queen cell virus (BQCV) and Lake Sinai viruses (LSV), with no evidence for any DWV strains. V. jacobsoni was infected by several viral homologs to recently discovered V. destructor viruses, but Varroa jacobsoni rhabdovirus-1 (ARV-1 homolog) was the only virus detected in both mites and honey bees. We conclude from these findings that A. mellifera in PNG may tolerate V. jacobsoni because the damage from parasitism is significantly reduced without DWV. This study also provides further evidence that DWV does not exist as a covert infection in all honey bee populations, and remaining free of this serious viral pathogen can have important implications for bee health outcomes in the face of Varroa.


Author(s):  
F. Nazzi ◽  
D. Annoscia ◽  
E. Caprio ◽  
G. Di Prisco ◽  
F. Pennacchio

The decline of honeybee colonies and their eventual collapse is a widespread phenomenon in the Northern hemisphere of the globe, which severely limits the beekeeping industry. This dramatic event is associated with an enhanced impact of parasites and pathogens on honeybees, which is indicative of reduced immunocompetence. The parasitic mite Varroa destructor and the vectored viral pathogens appear to play a key-role in the induction of this complex syndrome. In particular, the Deformed Wing Virus (DWV) is widespread and is now considered, along with Varroa, one of the major causes of bee colony losses. Several lines of evidence indicate that this mite/DWV association severely affects the immune system of honeybees and makes them more sensitive to the action of other stress factors. The molecular mechanisms underpinning these complex interactions are currently being investigated and the emerging information has allowed the development of a new functional model, describing how different stress factors may synergistically concur in the induction of bee immune alteration and health decline. This provides a new logical framework in which to interpret the proposed multifactorial origin of bee colony losses and sets the stage for a more comprehensive and integrated analysis of the effect that multiple stress agents may have on honeybees.


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