Interaction of Varroa destructor and Sublethal Clothianidin Doses during the Larval Stage on Subsequent Adult Honey Bee (Apis mellifera L.) Health, Cellular Immunity, Deformed Wing Virus Levels and Differential Gene Expression

Honeybees (Apis mellifera L.) are exposed to many parasites, but little is known about interactions with abiotic stressors on their health, particularly when affected as larvae. Larvae were exposed singly and in combination to the parasitic mite Varroa destructor and three sublethal doses of the neonicotinoid insecticide clothianidin to evaluate their effects on survivorship, weight, haemocyte counts, deformed wing virus (DWV) levels and gene expression of the adult bees that subsequently developed. Clothianidin significantly reduced bee weight at the highest dose and was associated with an increase in haemocyte counts at the lowest dose, whereas V. destructor parasitism increased DWV levels, reduced bee emergence, lowered weight and reduced haemocyte counts. An interaction between the two stressors was observed for weight at emergence. Among the differentially expressed genes (DEGs), V. destructor infestation resulted in broader down-regulatory effects related to immunity that was often shared with the combined stressors, while clothianidin resulted in a broader up-regulatory effect more related to central metabolic pathways that was often shared with the combined stressors. Parasites and abiotic stressors can have complex interactions, including additive effects on reduced weight, number of up-regulated DEGs and biological pathways associated with metabolism.

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

BMC Genomics ◽

10.1186/1471-2164-9-301 ◽

2008 ◽

Vol 9 (1) ◽

pp. 301 ◽

Cited By ~ 115

Author(s):

M Navajas ◽

A Migeon ◽

C Alaux ◽

ML Martin-Magniette ◽

GE Robinson ◽

...

Keyword(s):

Gene Expression ◽

Apis Mellifera ◽

Honey Bee ◽

Differential Gene Expression ◽

Varroa Destructor ◽

Differential Gene

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Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection

Journal of Insect Physiology ◽

10.1016/j.jinsphys.2010.03.019 ◽

2010 ◽

Vol 56 (9) ◽

pp. 1207-1218 ◽

Cited By ~ 27

Author(s):

Yi Zhang ◽

Xuejiao Liu ◽

Wenqing Zhang ◽

Richou Han

Keyword(s):

Gene Expression ◽

Apis Mellifera ◽

Differential Gene Expression ◽

Honey Bees ◽

Varroa Destructor ◽

Differential Gene

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Detection and phylogenetic analysis of deformed wing virus (DWV) in honey bees, Apis mellifera L. and parasitic mite, Varroa destructor Anderson and Trueman (Acari: Varroidae)

Systematic and Applied Acarology ◽

10.11158/saa.26.6.13 ◽

2021 ◽

Author(s):

Amin Shojaei ◽

Mohammad Khanjani ◽

Alireza Nourian ◽

Pezhman Mahmoodi

Keyword(s):

Genetic Diversity ◽

Apis Mellifera ◽

Varroa Destructor ◽

Viral Infections ◽

Structural Protein ◽

Deformed Wing Virus ◽

Reverse Transcription Pcr ◽

Geographical Regions ◽

Parasitic Mite ◽

Virus Strains

Deformed wing virus is one of the most common viral infections in honeybee populations around the world. In this study, a total of 30 apiaries located in different geographical regions of Hamedan, Iran were analyzed for the presence of deformed wing virus on capped larvae and workers of the honeybee, Apis mellifera (Hym: Apidae), as well as the parasitic mite, Varroa destructor (Acari: Varroidae), using reverse-transcription PCR. Two target sequences within the putative VP1, VP4, and VP2 structural-protein genes and the RNA helicase enzyme gene, were selected for amplification and sequencing. According to the results, 36.6% of apiaries were found to be infected with deformed wing virus, including 8, 0, and 3 positive samples on capped larvae and workers, and Varroa mites, respectively. Four strains of the virus obtained from honeybees and mites were selected for analysis of genetic diversity and phylogenetic relationships with other sequences deposited in GenBank. The results showed a high degree of similarity between the virus strains in honeybee and Varroa mite. The phylogenetic results highlight the higher suitability of non-structural in comparison with structural proteins for genetic diversity and phylogenetic studies of deformed wing virus strains.

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The Combined Effects of Varroa destructor Parasitism and Exposure to Neonicotinoids Affects Honey Bee (Apis mellifera L.) Memory and Gene Expression

Biology ◽

10.3390/biology9090237 ◽

2020 ◽

Vol 9 (9) ◽

pp. 237

Author(s):

Nuria Morfin ◽

Paul H. Goodwin ◽

Ernesto Guzman-Novoa

Keyword(s):

Apis Mellifera ◽

Honey Bees ◽

Varroa Destructor ◽

Combined Effects ◽

Proboscis Extension Response ◽

Neural Genes ◽

Abiotic Stressors ◽

Neural Processes ◽

Parasitic Mite ◽

Colony Survival

Honey bees (Apis mellifera L.) are exposed biotic and abiotic stressors but little is known about their combined effect and impact on neural processes such as learning and memory, which could affect behaviours that are important for individual and colony survival. This study measured memory with the proboscis extension response (PER) assay as well as the expression of neural genes in bees chronically exposed to three different sublethal doses of the insecticide clothianidin and/or the parasitic mite Varroa destructor. The proportion of bees that positively responded to PER at 24 and 48 h post-training (hpt) was significantly reduced when exposed to clothianidin. V. destructor parasitism reduced the proportion of bees that responded to PER at 48 hpt. Combined effects between the lowest clothianidin dose and V. destructor for the proportion of bees that responded to PER were found at 24 hpt. Clothianidin, V. destructor and their combination differentially affected the expression of the neural-related genes, AmNrx-1 (neurexin), AmNlg-1 (neuroligin), and AmAChE-2 (acetylcholinesterase). Different doses of clothianidin down-regulated or up-regulated the genes, whereas V. destructor tended to have a down-regulatory effect. It appears that clothianidin and V. destructor affected neural processes in honey bees through different mechanisms.

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Neonicotinoid Clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation

Nature Communications ◽

10.1038/s41467-020-19715-8 ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Desiderato Annoscia ◽

Gennaro Di Prisco ◽

Andrea Becchimanzi ◽

Emilio Caprio ◽

Davide Frizzera ◽

...

Keyword(s):

Immune Responses ◽

Honey Bee ◽

Honey Bees ◽

Varroa Destructor ◽

Negative Impact ◽

Asymptomatic Infection ◽

Varroa Mite ◽

Deformed Wing Virus ◽

Synergistic Interactions ◽

Parasitic Mite

AbstractThe neonicotinoid Clothianidin has a negative impact on NF-κB signaling and on immune responses controlled by this transcription factor, which can boost the proliferation of honey bee parasites and pathogens. This effect has been well documented for the replication of deformed wing virus (DWV) induced by Clothianidin in honey bees bearing an asymptomatic infection. Here, we conduct infestation experiments of treated bees to show that the immune-suppression exerted by Clothianidin is associated with an enhanced fertility of the parasitic mite Varroa destructor, as a possible consequence of a higher feeding efficiency. A conceptual model is proposed to describe the synergistic interactions among different stress agents acting on honey bees.

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Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor

Ecology and Evolution ◽

10.1002/ece3.17 ◽

2011 ◽

Vol 1 (4) ◽

pp. 451-458 ◽

Cited By ~ 35

Author(s):

Dieter Behrens ◽

Qiang Huang ◽

Cornelia Geßner ◽

Peter Rosenkranz ◽

Eva Frey ◽

...

Keyword(s):

Apis Mellifera ◽

Honey Bee ◽

Varroa Destructor ◽

Parasitic Mite

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Biology and Management of Varroa destructor (Mesostigmata: Varroidae) in Apis mellifera (Hymenoptera: Apidae) Colonies

Journal of Integrated Pest Management ◽

10.1093/jipm/pmz036 ◽

2020 ◽

Vol 11 (1) ◽

Cited By ~ 2

Author(s):

Morgan A Roth ◽

James M Wilson ◽

Keith R Tignor ◽

Aaron D Gross

Keyword(s):

Apis Mellifera ◽

Honey Bee ◽

Varroa Destructor ◽

Sampling Methods ◽

Apis Cerana ◽

Varroa Mite ◽

Resistance Development ◽

Deformed Wing Virus ◽

The Past ◽

Asian Honey Bee

Abstract Varroa mite (Varroa destructor Anderson and Trueman) infestation of European honey bee (Apis mellifera L.) colonies has been a growing cause of international concern among beekeepers throughout the last 50 yr. Varroa destructor spread from the Asian honey bee (Apis cerana Fabricius [Hymenoptera: Apidae]) to A. mellifera populations in Europe in the 1970s, and subsequently traveled to the Americas. In addition to causing damage through feeding upon lipids of larval and adult bees, V. destructor also facilitates the spread of several viruses, with deformed wing virus being most prevalent. Several sampling methods have been developed for estimating infestation levels of A. mellifera colonies, and acaricide treatments have been implemented. However, overuse of synthetic acaricides in the past has led to widespread acaricide resistant V. destructor populations. The application of Integrated Pest Management (IPM) techniques is a more recent development in V. destructor control and is suggested to be more effective than only using pesticides, thereby posing fewer threats to A. mellifera colonies. When using IPM methods, informed management decisions are made based upon sampling, and cultural and mechanical controls are implemented prior to use of acaricide treatments. If acaricides are deemed necessary, they are rotated based on their mode of action, thus avoiding V. destructor resistance development.

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New Viruses from the Ectoparasite Mite Varroa destructor Infesting Apis mellifera and Apis cerana

Viruses ◽

10.3390/v11020094 ◽

2019 ◽

Vol 11 (2) ◽

pp. 94 ◽

Cited By ~ 11

Author(s):

Sofia Levin ◽

Noa Sela ◽

Tal Erez ◽

David Nestel ◽

Jeffery Pettis ◽

...

Keyword(s):

Apis Mellifera ◽

Varroa Destructor ◽

Rna Virus ◽

Apis Cerana ◽

Virus Genome ◽

Deformed Wing Virus ◽

Viral Loads ◽

Short Period ◽

Honeybee Subspecies ◽

Colony Survival

Varroa destructor is an ectoparasitic mite of Asian or Eastern honeybees Apis cerana (A. cerana) which has become a serious threat to European subspecies of Western honeybees Apis mellifera (A. mellifera) within the last century. V. destructor and its vectored honeybee viruses became serious threats for colony survival. This is a short period for pathogen- and host-populations to adapt. To look for possible variation in the composition of viral populations we performed RNA metagenomic analysis of the Western honeybee subspecies A. m. ligustica, A. m. syriaca, A. m. intermissa, and A. cerana and their respective V. destructor mites. The analysis revealed two novel viruses: Varroa orthomyxovirus-1 (VOV-1) in A. mellifera and V. destructor and a Hubei like-virga virus-14 homolog in V. destructor. VOV-1 was more prevalent in V. destructor than in A. mellifera and we found evidence for viral replication in both hosts. Interestingly, we found differences in viral loads of A. cerana and their V. destructor, A. m. intermissa, and its V. destructor showed partial similarity, while A. m. ligustica and A. m. syriaca and their varroa where very similar. Deformed wing virus exhibited 82.20%, 99.20%, 97.90%, and 0.76% of total viral reads in A. m. ligustica, A. m. syriaca, A. m. intermissa, and A. cerana, respectively. This is the first report of a complete segmented-single-stranded negative-sense RNA virus genome in honeybees and V. destructor mites.

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