Decoupling the effects of nutrition, age and behavioral caste on honey bee physiology and immunity

AbstractNutritional stress, and especially a dearth of pollen, is considered an important factor associated with honey bee colony losses. We used pollen-restricted colonies as a model to study the nutritional stress conditions experienced in colonies within intensively cultivated agricultural areas. This model was complemented by the establishment of an experimental design, which allowed us to uncouple the effect of nutrition, behavior and age in colonies of similar size and demography. We used this system to determine the effect of pollen restriction on workers’ behavioral development. Then, we analyzed the effect of nutritional stress, behavior and age on the expression of key physiological genes involved in the regulation of division of labor. Finally, we analyzed the effects of these variables on the expression of immune genes and the titers of honey bee viruses. Our results show that pollen restriction led to an increased number of precocious foragers and this behavioral transition was associated with important changes in the expression of nutritionally regulated physiological genes, immunity and viral titers.Vitellogenin (vg)andmajor royal jelly protein1 (mrjp1)were the most predictive markers of nutrition and behavior. The expression of immune genes was primarily affected by behavior, with higher levels in foragers. Deformed wing virus (DWV) titers were significantly affected by behavior and nutritional status, with higher titer in foragers and increased levels associated with pollen ingestion. Correlation analyses support the predominant effect of behavior on immunity and susceptibility to viral infection, revealing that both immune genes and DWV exhibited strong negative correlations with genes associated with nursing, but positive correlations with genes associated with foraging. Our results provide valuable insights into the physiological mechanisms by which nutritional stress induce precocious foraging and increased susceptibility to viral infections.

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Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera

Insects ◽

10.3390/insects11040239 ◽

2020 ◽

Vol 11 (4) ◽

pp. 239 ◽

Cited By ~ 13

Author(s):

Alexis Beaurepaire ◽

Niels Piot ◽

Vincent Doublet ◽

Karina Antunez ◽

Ewan Campbell ◽

...

Keyword(s):

Apis Mellifera ◽

Honey Bee ◽

High Throughput Sequencing ◽

Temporal Dynamics ◽

Pollination Services ◽

Colony Losses ◽

New Host ◽

Deformed Wing Virus ◽

Bee Colony ◽

Queen Cell

In the past centuries, viruses have benefited from globalization to spread across the globe, infecting new host species and populations. A growing number of viruses have been documented in the western honey bee, Apis mellifera. Several of these contribute significantly to honey bee colony losses. This review synthetizes the knowledge of the diversity and distribution of honey-bee-infecting viruses, including recent data from high-throughput sequencing (HTS). After presenting the diversity of viruses and their corresponding symptoms, we surveyed the scientific literature for the prevalence of these pathogens across the globe. The geographical distribution shows that the most prevalent viruses (deformed wing virus, sacbrood virus, black queen cell virus and acute paralysis complex) are also the most widely distributed. We discuss the ecological drivers that influence the distribution of these pathogens in worldwide honey bee populations. Besides the natural transmission routes and the resulting temporal dynamics, global trade contributes to their dissemination. As recent evidence shows that these viruses are often multihost pathogens, their spread is a risk for both the beekeeping industry and the pollination services provided by managed and wild pollinators.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1523515113 ◽

2016 ◽

Vol 113 (12) ◽

pp. 3203-3208 ◽

Cited By ~ 101

Author(s):

Gennaro Di Prisco ◽

Desiderato Annoscia ◽

Marina Margiotta ◽

Rosalba Ferrara ◽

Paola Varricchio ◽

...

Keyword(s):

Honey Bee ◽

Stress Factors ◽

Colony Losses ◽

Viral Pathogen ◽

Deformed Wing Virus ◽

Mutualistic Symbiosis ◽

Bee Colony ◽

Parasitic Mite ◽

Honey Bee Colony ◽

Honey Bee Colony Losses

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.

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Haemolymph removal by the parasite Varroa destructor can trigger the proliferation of the Deformed Wing Virus in mite infested bees (Apis mellifera), contributing to enhanced pathogen virulence

10.1101/257667 ◽

2018 ◽

Cited By ~ 6

Author(s):

Desiderato Annoscia ◽

Sam P. Brown ◽

Gennaro Di Prisco ◽

Emanuele De Paoli ◽

Simone Del Fabbro ◽

...

Keyword(s):

Honey Bee ◽

Varroa Destructor ◽

Viral Evolution ◽

Colony Losses ◽

Viral Pathogen ◽

Deformed Wing Virus ◽

Bee Colony ◽

Bee Health ◽

Honey Bee Health ◽

Mite Feeding

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.

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RNAseq of Deformed Wing Virus and Other Honey Bee-Associated Viruses in Eight Insect Taxa with or without Varroa Infestation

Viruses ◽

10.3390/v12111229 ◽

2020 ◽

Vol 12 (11) ◽

pp. 1229

Author(s):

Laura E. Brettell ◽

Declan C. Schroeder ◽

Stephen J. Martin

Keyword(s):

Honey Bee ◽

Honey Bees ◽

Large Scale ◽

Sequence Data ◽

Rna Virus ◽

Colony Losses ◽

Deformed Wing Virus ◽

Bee Colony ◽

Parasitic Mite ◽

Insect Populations

The global spread of a parasitic mite (Varroa destructor) has resulted in Deformed wing virus (DWV), a previously rare pathogen, now dominating the viromes in honey bees and contributing to large-scale honey bee colony losses. DWV can be found in diverse insect taxa and has been implicated in spilling over from honey bees into associated (“apiary”) and other (“non-apiary”) insects. Here we generated next generation sequence data from 127 insect samples belonging to diverse taxa collected from Hawaiian islands with and without Varroa to identify whether the mite has indirectly affected the viral landscapes of key insect taxa across bees, wasps, flies and ants. Our data showed that, while Varroa was associated with a dramatic increase in abundance of (predominantly recombinant) DWV in honey bees (and no other honey bee-associated RNA virus), this change was not seen in any other taxa sampled. Honey bees share their environment with other insect populations and exist as a homogenous group, frequently sharing common viruses, albeit at low levels. Our data suggest that the threat of Varroa to increase viral load in an apiary does not automatically translate to an increase in virus load in other insects living in the wider community.

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Clinical signs of deformed wing virus infection are predictive markers for honey bee colony losses

Journal of Invertebrate Pathology ◽

10.1016/j.jip.2012.12.009 ◽

2013 ◽

Vol 112 (3) ◽

pp. 278-280 ◽

Cited By ~ 41

Author(s):

Benjamin Dainat ◽

Peter Neumann

Keyword(s):

Virus Infection ◽

Honey Bee ◽

Clinical Signs ◽

Predictive Markers ◽

Colony Losses ◽

Deformed Wing Virus ◽

Bee Colony ◽

Honey Bee Colony ◽

Honey Bee Colony Losses

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Impact of Chronic Exposure to Sublethal Doses of Glyphosate on Honey Bee Immunity, Gut Microbiota and Infection by Pathogens

Microorganisms ◽

10.3390/microorganisms9040845 ◽

2021 ◽

Vol 9 (4) ◽

pp. 845

Author(s):

Loreley Castelli ◽

Sofía Balbuena ◽

Belén Branchiccela ◽

Pablo Zunino ◽

Joanito Liberti ◽

...

Keyword(s):

Gut Microbiota ◽

Honey Bee ◽

Chronic Exposure ◽

Pollination Services ◽

Deformed Wing Virus ◽

Immune Genes ◽

Bee Health ◽

Honey Bee Health ◽

Sublethal Doses ◽

The Impact

Glyphosate is the most used pesticide around the world. Although different studies have evidenced its negative effect on honey bees, including detrimental impacts on behavior, cognitive, sensory and developmental abilities, its use continues to grow. Recent studies have shown that it also alters the composition of the honey bee gut microbiota. In this study we explored the impact of chronic exposure to sublethal doses of glyphosate on the honey bee gut microbiota and its effects on the immune response, infection by Nosema ceranae and Deformed wing virus (DWV) and honey bee survival. Glyphosate combined with N. ceranae infection altered the structure and composition of the honey bee gut microbiota, for example by decreasing the relative abundance of the core members Snodgrassella alvi and Lactobacillus apis. Glyphosate increased the expression of some immune genes, possibly representing a physiological response to mitigate its negative effects. However, this response was not sufficient to maintain honey bee health, as glyphosate promoted the replication of DWV and decreased the expression of vitellogenin, which were accompanied by a reduced life span. Infection by N. ceranae also alters honey bee immunity although no synergistic effect with glyphosate was observed. These results corroborate previous findings suggesting deleterious effects of widespread use of glyphosate on honey bee health, and they contribute to elucidate the physiological mechanisms underlying a global decline of pollination services.

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Ukraine is Moving Forward from “Undiscovered Honey Land” to Active Participation in International Monitoring of Honey Bee Colony Losses

Bee World ◽

10.1080/0005772x.2018.1554279 ◽

2019 ◽

Vol 96 (2) ◽

pp. 50-54 ◽

Cited By ~ 2

Author(s):

Mariia M. Fedoriak ◽

Per K. Angelstam ◽

Oleksandr M. Kulmanov ◽

Lesia I. Tymochko ◽

Svitlana S. Rudenko ◽

...

Keyword(s):

Honey Bee ◽

Active Participation ◽

Colony Losses ◽

Bee Colony ◽

International Monitoring ◽

Honey Bee Colony ◽

Honey Bee Colony Losses

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Descriptive Analysis of the Varroa Non-Reproduction Trait in Honey Bee Colonies and Association with Other Traits Related to Varroa Resistance

Insects ◽

10.3390/insects11080492 ◽

2020 ◽

Vol 11 (8) ◽

pp. 492 ◽

Cited By ~ 1

Author(s):

Sonia E. Eynard ◽

Christina Sann ◽

Benjamin Basso ◽

Anne-Laure Guirao ◽

Yves Le Conte ◽

...

Keyword(s):

Honey Bee ◽

Empirical Bayes ◽

Descriptive Analysis ◽

Field Studies ◽

Colony Losses ◽

Bee Colony ◽

Bee Health ◽

Honey Bee Health ◽

Varroa Resistance ◽

Resistance Traits

In the current context of worldwide honey bee colony losses, among which the varroa mite plays a major role, the hope to improve honey bee health lies in part in the breeding of varroa resistant colonies. To do so, methods used to evaluate varroa resistance need better understanding. Repeatability and correlations between traits such as mite non-reproduction (MNR), varroa sensitive hygiene (VSH), and hygienic behavior are poorly known, due to practical limitations and to their underlying complexity. We investigate (i) the variability, (ii) the repeatability of the MNR score, and (iii) its correlation with other resistance traits. To reduce the inherent variability of MNR scores, we propose to apply an empirical Bayes correction. In the short-term (ten days), MNR had a modest repeatability of 0.4, whereas in the long-term (a month), it had a low repeatability of 0.2, similar to other resistance traits. Within our dataset, there was no correlation between MNR and VSH. Although MNR is amongst the most popular varroa resistance estimates in field studies, its underlying complex mechanism is not fully understood. Its lack of correlation with better described resistance traits and low repeatability suggest that MNR needs to be interpreted cautiously, especially when used for selection.

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