scholarly journals Multi-host viruses in Argentine ants and honey bees: Increased viral disease in honey bees is associated with Argentine ants

2021 ◽  
Author(s):  
◽  
Jana Dobelmann

<p><b>Emerging infectious diseases threaten public health, livestock economies, and wildlife. Human-mediated species introductions can alter host and pathogen communities that shape the dynamics of infectious diseases. Several RNA viruses that have been linked to population declines in wild pollinators and losses of managed honey bees have been detected in multiple other species and are suspected to circulate within insect communities. Yet, we lack an understanding of how disease dynamics are affected by the introduction of novel species. These introduced species include invasive ants, which can disturb honey bees and become a pest in apiaries. The Argentine ant (Linepithema humile) is a globally successful invader that has been observed to attack bees and multiple bee-associated viruses have been detected in this ant species.</b></p> <p>Here, I studied interactions between Argentine ants and European honey bees (Apis mellifera) and how these interactions affect viral dynamics in beehives. I first tested a range of pollinators and associated insects for RNA viruses that are pathogenic to honey bees. Bee-associated viruses showed evidence for active viral replication in several pollinator species but also in species that cohabit in beehives such as ants, spiders, and cockroaches. Using phylogenetic analyses, I found that viral transmission within communities was shaped by geographic origin rather than being restricted by species barriers. Next, I used a longitudinal field study to test whether Argentine ant presence affected pathogen infections and survival in beehives. Argentine ants tested positive for three bee-associated viruses even before beehives were moved into ant-infested sites. Increased levels of deformed wing virus in beehives in autumn were associated with ant presence, although hive mortality was not affected by ants over the duration of this experiment. I used RNA sequencing on a subset of honey bee samples collected during autumn to study the RNA virome and identify transcriptomic responses associated with ant presence. Twelve RNA viruses were found in beehives, among those, three plant-associated viruses and an unclassified RNA virus that had not previously been observed in honey bees. Deformed wing virus showed the highest viral titres in most hives, but was only marginally affected by ant presence. Sacbrood virus and tomato ringspot virus levels were increased in hives with ants, however, both viruses are not known to infect Argentine ants and the plant-associated tomato ringspot virus seems unlikely to affect bee health.</p> <p>Lastly, I tested the feasibility of controlling Argentine ants in apiaries using a novel pest control strategy. RNA interference is a conserved cellular gene regulation mechanism that could be used to silence specific genes in ants. Using double-stranded RNA (dsRNA) to silence two immune-related genes in Argentine ants was expected to increase pathogen susceptibility, which could then lead to higher pathogen levels that reduce ant numbers. My results indicated that no consistent immune silencing could be achieved in the field. Immune gene expression changes were observed, but pathogen titres were not affected, and ant numbers stayed high. Argentine ant control using a conventional insecticide significantly increased bee survival, whereas many hives in the dsRNA and control group abandoned their hives due to ant attacks. Although population control was not successful using the two Argentine ant-specific dsRNAs, insights into ant immunity and ant-bee interactions could improve the development of novel control strategies.</p> <p>Bee-associated viruses have repeatedly been detected in ant species, yet, this is one of the first studies to investigate whether ants affect viral dynamics in honey bees. I showed that invasive Argentine ants are associated with increases in viral pathogens in honey bees. The mechanisms by which ants affect bee disease are unknown, although there is some evidence for ants transmitting viruses or causing stress responses in bees that affect immunity. The findings of this thesis highlight the risk of invasive ant species disrupting pollination services. New and environmentally-friendly methods to control invasive species are urgently needed to improve bee health and limit the spread of invasive ants, such as Argentine ants. The high prevalence of bee-associated viruses and viral diversity in ants suggests that pathogens that are suitable for population control might be present in ant populations, although risks of spillovers into other species need to be carefully considered.</p>

2021 ◽  
Author(s):  
◽  
Jana Dobelmann

<p><b>Emerging infectious diseases threaten public health, livestock economies, and wildlife. Human-mediated species introductions can alter host and pathogen communities that shape the dynamics of infectious diseases. Several RNA viruses that have been linked to population declines in wild pollinators and losses of managed honey bees have been detected in multiple other species and are suspected to circulate within insect communities. Yet, we lack an understanding of how disease dynamics are affected by the introduction of novel species. These introduced species include invasive ants, which can disturb honey bees and become a pest in apiaries. The Argentine ant (Linepithema humile) is a globally successful invader that has been observed to attack bees and multiple bee-associated viruses have been detected in this ant species.</b></p> <p>Here, I studied interactions between Argentine ants and European honey bees (Apis mellifera) and how these interactions affect viral dynamics in beehives. I first tested a range of pollinators and associated insects for RNA viruses that are pathogenic to honey bees. Bee-associated viruses showed evidence for active viral replication in several pollinator species but also in species that cohabit in beehives such as ants, spiders, and cockroaches. Using phylogenetic analyses, I found that viral transmission within communities was shaped by geographic origin rather than being restricted by species barriers. Next, I used a longitudinal field study to test whether Argentine ant presence affected pathogen infections and survival in beehives. Argentine ants tested positive for three bee-associated viruses even before beehives were moved into ant-infested sites. Increased levels of deformed wing virus in beehives in autumn were associated with ant presence, although hive mortality was not affected by ants over the duration of this experiment. I used RNA sequencing on a subset of honey bee samples collected during autumn to study the RNA virome and identify transcriptomic responses associated with ant presence. Twelve RNA viruses were found in beehives, among those, three plant-associated viruses and an unclassified RNA virus that had not previously been observed in honey bees. Deformed wing virus showed the highest viral titres in most hives, but was only marginally affected by ant presence. Sacbrood virus and tomato ringspot virus levels were increased in hives with ants, however, both viruses are not known to infect Argentine ants and the plant-associated tomato ringspot virus seems unlikely to affect bee health.</p> <p>Lastly, I tested the feasibility of controlling Argentine ants in apiaries using a novel pest control strategy. RNA interference is a conserved cellular gene regulation mechanism that could be used to silence specific genes in ants. Using double-stranded RNA (dsRNA) to silence two immune-related genes in Argentine ants was expected to increase pathogen susceptibility, which could then lead to higher pathogen levels that reduce ant numbers. My results indicated that no consistent immune silencing could be achieved in the field. Immune gene expression changes were observed, but pathogen titres were not affected, and ant numbers stayed high. Argentine ant control using a conventional insecticide significantly increased bee survival, whereas many hives in the dsRNA and control group abandoned their hives due to ant attacks. Although population control was not successful using the two Argentine ant-specific dsRNAs, insights into ant immunity and ant-bee interactions could improve the development of novel control strategies.</p> <p>Bee-associated viruses have repeatedly been detected in ant species, yet, this is one of the first studies to investigate whether ants affect viral dynamics in honey bees. I showed that invasive Argentine ants are associated with increases in viral pathogens in honey bees. The mechanisms by which ants affect bee disease are unknown, although there is some evidence for ants transmitting viruses or causing stress responses in bees that affect immunity. The findings of this thesis highlight the risk of invasive ant species disrupting pollination services. New and environmentally-friendly methods to control invasive species are urgently needed to improve bee health and limit the spread of invasive ants, such as Argentine ants. The high prevalence of bee-associated viruses and viral diversity in ants suggests that pathogens that are suitable for population control might be present in ant populations, although risks of spillovers into other species need to be carefully considered.</p>


2015 ◽  
Vol 11 (9) ◽  
pp. 20150610 ◽  
Author(s):  
Alexandra Sébastien ◽  
Philip J. Lester ◽  
Richard J. Hall ◽  
Jing Wang ◽  
Nicole E. Moore ◽  
...  

When exotic animal species invade new environments they also bring an often unknown microbial diversity, including pathogens. We describe a novel and widely distributed virus in one of the most globally widespread, abundant and damaging invasive ants (Argentine ants, Linepithema humile ). The Linepithema humile virus 1 is a dicistrovirus, a viral family including species known to cause widespread arthropod disease. It was detected in samples from Argentina, Australia and New Zealand. Argentine ants in New Zealand were also infected with a strain of Deformed wing virus common to local hymenopteran species, which is a major pathogen widely associated with honeybee mortality. Evidence for active replication of viral RNA was apparent for both viruses. Our results suggest co-introduction and exchange of pathogens within local hymenopteran communities. These viral species may contribute to the collapse of Argentine ant populations and offer new options for the control of a globally widespread invader.


2019 ◽  
Vol 56 (4) ◽  
pp. 636-641 ◽  
Author(s):  
Roman V. Koziy ◽  
Sarah C. Wood ◽  
Ivanna V. Kozii ◽  
Claire Janse van Rensburg ◽  
Igor Moshynskyy ◽  
...  

Deformed wing virus (DWV) is a single-stranded RNA virus of honey bees ( Apis mellifera L.) transmitted by the parasitic mite Varroa destructor. Although DWV represents a major threat to honey bee health worldwide, the pathological basis of DWV infection is not well documented. The objective of this study was to investigate clinicopathological and histological aspects of natural DWV infection in honey bee workers. Emergence of worker honey bees was observed in 5 colonies that were clinically affected with DWV and the newly emerged bees were collected for histopathology. DWV-affected bees were 2 times slower to emerge and had 30% higher mortality compared to clinically normal bees. Hypopharyngeal glands in bees with DWV were hypoplastic, with fewer intracytoplasmic secretory vesicles; cells affected by apoptosis were observed more frequently. Mandibular glands were hypoplastic and were lined by cuboidal epithelium in severely affected bees compared to tall columnar epithelium in nonaffected bees. The DWV load was on average 1.7 × 106 times higher ( P < .001) in the severely affected workers compared to aged-matched sister honey bee workers that were not affected by deformed wing disease based on gross examination. Thus, DWV infection is associated with prolonged emergence, increased mortality during emergence, and hypoplasia of hypopharyngeal and mandibular glands in newly emerged worker honey bees in addition to previously reported deformed wing abnormalities.


2017 ◽  
Vol 91 (16) ◽  
Author(s):  
Emily J. Remnant ◽  
Mang Shi ◽  
Gabriele Buchmann ◽  
Tjeerd Blacquière ◽  
Edward C. Holmes ◽  
...  

ABSTRACT Understanding the diversity and consequences of viruses present in honey bees is critical for maintaining pollinator health and managing the spread of disease. The viral landscape of honey bees (Apis mellifera) has changed dramatically since the emergence of the parasitic mite Varroa destructor, which increased the spread of virulent variants of viruses such as deformed wing virus. Previous genomic studies have focused on colonies suffering from infections by Varroa and virulent viruses, which could mask other viral species present in honey bees, resulting in a distorted view of viral diversity. To capture the viral diversity within colonies that are exposed to mites but do not suffer the ultimate consequences of the infestation, we examined populations of honey bees that have evolved naturally or have been selected for resistance to Varroa. This analysis revealed seven novel viruses isolated from honey bees sampled globally, including the first identification of negative-sense RNA viruses in honey bees. Notably, two rhabdoviruses were present in three geographically diverse locations and were also present in Varroa mites parasitizing the bees. To characterize the antiviral response, we performed deep sequencing of small RNA populations in honey bees and mites. This provided evidence of a Dicer-mediated immune response in honey bees, while the viral small RNA profile in Varroa mites was novel and distinct from the response observed in bees. Overall, we show that viral diversity in honey bee colonies is greater than previously thought, which encourages additional studies of the bee virome on a global scale and which may ultimately improve disease management. IMPORTANCE Honey bee populations have become increasingly susceptible to colony losses due to pathogenic viruses spread by parasitic Varroa mites. To date, 24 viruses have been described in honey bees, with most belonging to the order Picornavirales. Collapsing Varroa-infected colonies are often overwhelmed with high levels of picornaviruses. To examine the underlying viral diversity in honey bees, we employed viral metatranscriptomics analyses on three geographically diverse Varroa-resistant populations from Europe, Africa, and the Pacific. We describe seven novel viruses from a range of diverse viral families, including two viruses that are present in all three locations. In honey bees, small RNA sequences indicate that these viruses are processed by Dicer and the RNA interference pathway, whereas Varroa mites produce strikingly novel small RNA patterns. This work increases the number and diversity of known honey bee viruses and will ultimately contribute to improved disease management in our most important agricultural pollinator.


2021 ◽  
Vol 11 (22) ◽  
pp. 10732
Author(s):  
Dawn L. Boncristiani ◽  
James P. Tauber ◽  
Evan C. Palmer-Young ◽  
Lianfei Cao ◽  
William Collins ◽  
...  

Western honey bees (Apis mellifera), a cornerstone to crop pollination in the U.S., are faced with an onslaught of challenges from diseases caused by parasites, pathogens, and pests that affect this economically valuable pollinator. Natural products (NPs), produced by living organisms, including plants and microorganisms, can support health and combat disease in animals. NPs include both native extracts and individual compounds that can reduce disease impacts by supporting immunity or directly inhibiting pathogens, pests, and parasites. Herein, we describe the screening of NPs in laboratory cage studies for their effects on honey bee disease prevention and control. Depending on the expected activity of compounds, we measured varied responses, including viral levels, honey bee immune responses, and symbiotic bacteria loads. Of the NPs screened, several compounds demonstrated beneficial activities in honey bees by reducing levels of the critical honey bee virus deformed wing virus (DWV-A and-B), positively impacting the gut microbiome or stimulating honey bee immune responses. Investigations of the medicinal properties of NPs in honey bees will contribute to a better understanding of their potential to support honey bee immunity to fight off pests and pathogens and promote increased overall honey bee health. These investigations will also shed light on the ecological interactions between pollinators and specific floral food sources.


2021 ◽  
Author(s):  
◽  
Alexandra Sébastien

<p>Invasive species can lead to major economic and ecological issues. For this reason, biological controls are being developed in order to help with invasive species population management. Pathogenic bacteria and viruses offer good biological control opportunities as both micro-organisms have played a role in natural population declines. However, beneficial bacteria and viruses associated with the targeted invasive species may interfere with biological controls, by protecting their hosts from infections. Previous knowledge on both pathogenic and beneficial bacteria and viruses present in invasive species may then support the development of an active and efficient biological control.  The Argentine ant, Linepithema humile, is a South American invasive ant species that has successfully spread over five continents. The ants were introduced to New Zealand after a complex invasion path, from Argentina their home range to Europe, then to Australia and finally to New Zealand. In their new environments, invasive Argentine ants affect species diversity and can cause agricultural losses. In the absence of any biological controls, the Argentine ant population is controlled by chemical sprays and poison baits. Management of these invasive ants in New Zealand is estimated to cost NZ$ 60 million a year. The Argentine ant population in New Zealand was reported to have unexpectedly declined. It was hypothesised that pathogens were the cause of this population collapse.  In this study, bacteria and viruses present in the invasive ants were investigated using 454 sequencing and Illumina sequencing for future developments of possible biological controls for the Argentine ants, and a better understanding of the observed population decline in New Zealand. Bacterial diversity present in Argentine ants either declined or diminished along the invasion pathway. At the same time, the invasive ants maintained a core of nine bacteria genera, including Lactobacillus and Gluconobacter, two bacterial genera with members known for their beneficial associations with honey bees. The presence of these core bacteria may have participated in the success of Argentine ants in their new environments. In the laboratory, the use of ampicillin and gentamicin antibiotics on the ants increased bacterial diversity present in the ants. Furthermore, ampicillin, kanamycin and spectinomycin antibiotic treatments increased ant survival but did not affect the ant fitness or intra-species aggressiveness. Only spectinomycin treated ants presented a higher level of inter-species aggressiveness. Bacterial diversity may play an important role in the ant health and at length population dynamics.  Finally, Argentine ants are the hosts of two viruses: the Deformed wing virus (DWV) involved in colony collapse disorder in honey bees, and Linepithema humile virus 1 (LHUV-1), a new virus related to DWV. Both viruses actively replicate within the ants, indicating a possible reservoir role of the ants. However, the effects of the viruses on the ants are not yet known. Further viral infection in the laboratory under different stress conditions and / or antibiotic treatment will give an insight in the role played by these viruses in the observed population collapse of Argentine ants in New Zealand. LHUV-1 may offer a possibility in the development of the first biological control for Argentine ants, depending on its specificity and its effects.  This dissertation provides a first insight in the core bacteria as well as potential harmful viruses present in Argentine ants. These bacteria and viruses may play a role in the ant population dynamics. Invasive species may co-introduce harmful pathogens with them, and participate to the spread of local ones. The pathogens may affect both invasive ants and native species population dynamics.</p>


2022 ◽  
Author(s):  
Xuye Yuan ◽  
Tatsuhiko Kadowaki

Deformed wing virus (DWV) is the most prevalent Iflavirus that is infecting honey bees worldwide. However, the mechanisms of its infection and replication in host cells are poorly understood. In this study, we analyzed the structure and function of DWV 3C protease (3Cpro), which is necessary for the cleavage of the polyprotein to synthesize mature viral proteins. We found that the 3Cpros of DWV and picornaviruses share common enzymatic properties, including sensitivity to the same inhibitors, such as rupintrivir. The predicted structure of DWV 3Cpro by AlphaFold2, the predicted rupintrivir binding domain, and the protease activities of mutant proteins revealed that it has a Cys-His-Asn catalytic triad. Moreover, 3Cpros of other Iflaviruses and Dicistrovirus appear to contain Asn, Ser, Asp, or Glu as the third residue of the catalytic triad, suggesting diversity in insect RNA viruses. Both precursor 3Cpro with RNA-dependent RNA polymerase and mature 3Cpro are present in DWV-infected cells, suggesting that they may have different enzymatic properties and functions. DWV 3Cpro is the first 3Cpro characterized among insect RNA viruses, and our study uncovered both the common and unique characteristics among 3Cpros of Picornavirales. Furthermore, the specific inhibitors of DWV 3Cpro could be used to control DWV infection in honey bees.


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.


2021 ◽  
Vol 9 (4) ◽  
pp. 871
Author(s):  
Christopher Dosch ◽  
Anja Manigk ◽  
Tabea Streicher ◽  
Anja Tehel ◽  
Robert J. Paxton ◽  
...  

Adult honey bees host a remarkably consistent gut microbial community that is thought to benefit host health and provide protection against parasites and pathogens. Currently, however, we lack experimental evidence for the causal role of the gut microbiota in protecting the Western honey bees (Apis mellifera) against their viral pathogens. Here we set out to fill this knowledge gap by investigating how the gut microbiota modulates the virulence of a major honey bee viral pathogen, deformed wing virus (DWV). We found that, upon oral virus exposure, honey bee survival was significantly increased in bees with an experimentally established normal gut microbiota compared to control bees with a perturbed (dysbiotic) gut microbiota. Interestingly, viral titers were similar in bees with normal gut microbiota and dysbiotic bees, pointing to higher viral tolerance in bees with normal gut microbiota. Taken together, our results provide evidence for a positive role of the gut microbiota for honey bee fitness upon viral infection. We hypothesize that environmental stressors altering honey bee gut microbiota composition, e.g., antibiotics in beekeeping or pesticides in modern agriculture, could interact synergistically with pathogens, leading to negative effects on honey bee health and the epidemiology and impact of their viruses.


Viruses ◽  
2020 ◽  
Vol 12 (8) ◽  
pp. 890
Author(s):  
Severine Matthijs ◽  
Valérie De Waele ◽  
Valerie Vandenberge ◽  
Bénédicte Verhoeven ◽  
Jacqueline Evers ◽  
...  

The health of honey bees is threatened by multiple factors, including viruses and parasites. We screened 557 honey bee (Apis mellifera) colonies from 155 beekeepers distributed all over Belgium to determine the prevalence of seven widespread viruses and two parasites (Varroa sp. and Nosema sp.). Deformed wing virus B (DWV-B), black queen cell virus (BQCV), and sacbrood virus (SBV) were highly prevalent and detected by real-time RT-PCR in more than 95% of the colonies. Acute bee paralysis virus (ABPV), chronic bee paralysis virus (CBPV) and deformed wing virus A (DWV-A) were prevalent to a lower extent (between 18 and 29%). Most viruses were only present at low or moderate viral loads. Nevertheless, about 50% of the colonies harbored at least one virus at high viral load (>107 genome copies/bee). Varroa mites and Nosema sp. were found in 81.5% and 59.7% of the honey bee colonies, respectively, and all Nosema were identified as Nosema ceranae by real time PCR. Interestingly, we found a significant correlation between the number of Varroa mites and DWV-B viral load. To determine the combined effect of these and other factors on honey bee health in Belgium, a follow up of colonies over multiple years is necessary.


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