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

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          Abstract

          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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          Most cited references126

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          Immune pathways and defence mechanisms in honey bees Apis mellifera

          Social insects are able to mount both group-level and individual defences against pathogens. Here we focus on individual defences, by presenting a genome-wide analysis of immunity in a social insect, the honey bee Apis mellifera. We present honey bee models for each of four signalling pathways associated with immunity, identifying plausible orthologues for nearly all predicted pathway members. When compared to the sequenced Drosophila and Anopheles genomes, honey bees possess roughly one-third as many genes in 17 gene families implicated in insect immunity. We suggest that an implied reduction in immune flexibility in bees reflects either the strength of social barriers to disease, or a tendency for bees to be attacked by a limited set of highly coevolved pathogens.
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            Diet effects on honeybee immunocompetence.

            The maintenance of the immune system can be costly, and a lack of dietary protein can increase the susceptibility of organisms to disease. However, few studies have investigated the relationship between protein nutrition and immunity in insects. Here, we tested in honeybees (Apis mellifera) whether dietary protein quantity (monofloral pollen) and diet diversity (polyfloral pollen) can shape baseline immunocompetence (IC) by measuring parameters of individual immunity (haemocyte concentration, fat body content and phenoloxidase activity) and glucose oxidase (GOX) activity, which enables bees to sterilize colony and brood food, as a parameter of social immunity. Protein feeding modified both individual and social IC but increases in dietary protein quantity did not enhance IC. However, diet diversity increased IC levels. In particular, polyfloral diets induced higher GOX activity compared with monofloral diets, including protein-richer diets. These results suggest a link between protein nutrition and immunity in honeybees and underscore the critical role of resource availability on pollinator health.
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              Temporal Analysis of the Honey Bee Microbiome Reveals Four Novel Viruses and Seasonal Prevalence of Known Viruses, Nosema, and Crithidia

              Honey bees (Apis mellifera) play a critical role in global food production as pollinators of numerous crops. Recently, honey bee populations in the United States, Canada, and Europe have suffered an unexplained increase in annual losses due to a phenomenon known as Colony Collapse Disorder (CCD). Epidemiological analysis of CCD is confounded by a relative dearth of bee pathogen field studies. To identify what constitutes an abnormal pathophysiological condition in a honey bee colony, it is critical to have characterized the spectrum of exogenous infectious agents in healthy hives over time. We conducted a prospective study of a large scale migratory bee keeping operation using high-frequency sampling paired with comprehensive molecular detection methods, including a custom microarray, qPCR, and ultra deep sequencing. We established seasonal incidence and abundance of known viruses, Nosema sp., Crithidia mellificae, and bacteria. Ultra deep sequence analysis further identified four novel RNA viruses, two of which were the most abundant observed components of the honey bee microbiome (∼1011 viruses per honey bee). Our results demonstrate episodic viral incidence and distinct pathogen patterns between summer and winter time-points. Peak infection of common honey bee viruses and Nosema occurred in the summer, whereas levels of the trypanosomatid Crithidia mellificae and Lake Sinai virus 2, a novel virus, peaked in January.
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                Author and article information

                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                10 April 2020
                April 2020
                : 11
                : 4
                : 239
                Affiliations
                [1 ]Institute of Bee Health, Vetsuisse Faculty, University of Bern, 3003 Bern, Switzerland; orlando.yanez@ 123456vetsuisse.unibe.ch
                [2 ]Agroscope, Swiss Bee Research Center, 3003 Bern, Switzerland
                [3 ]UR Abeilles et Environnement, INRAE, 84914 Avignon, France; anne.dalmon@ 123456inrae.fr
                [4 ]Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, 9000 Ghent, Belgium; Niels.Piot@ 123456UGent.be (N.P.); Guy.Smagghe@ 123456UGent.be (G.S.)
                [5 ]Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, 86069 Ulm, Germany; vincent.doublet@ 123456uni-ulm.de
                [6 ]Department of Microbiology, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo 11600, Uruguay; kantunez03@ 123456gmail.com
                [7 ]Centre for Genome Enabled Biology and Medicine, University of Aberdeen, Aberdeen AB24 3FX, UK; e.m.campbell@ 123456abdn.ac.uk
                [8 ]Environmental Science Research Center (ESRC), Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand; panuwan@ 123456gmail.com
                [9 ]Bee Protection Laboratory (BeeP), Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
                [10 ]Entomology Department, Institute of Plant Protection, The Volcani Center, Rishon Lezion, Tel Aviv 5025001, Israel; ninar@ 123456volcani.agri.gov.il
                [11 ]Laboratory of Bee Diseases, Institute of Veterinary Medicine, Warsaw University of Life Sciences, 02-787 Warsaw, Poland; anna_gajda@ 123456sggw.pl
                [12 ]Bee Research Lab, USDA-ARS, Beltsville, MD 20705, USA; matthew.heerman@ 123456usda.gov
                [13 ]Institute of Biology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany; delphine.panziera@ 123456gmx.com
                [14 ]German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 04103 Leipzig, Germany
                [15 ]Department of Ecology, Swedish University of Agricultural Sciences, 750-07 Uppsala, Sweden; joachim.de.miranda@ 123456slu.se
                Author notes
                Author information
                https://orcid.org/0000-0002-9832-5609
                https://orcid.org/0000-0003-2808-6793
                https://orcid.org/0000-0002-6313-1222
                https://orcid.org/0000-0002-6455-6521
                https://orcid.org/0000-0003-3900-7368
                https://orcid.org/0000-0001-8731-1407
                https://orcid.org/0000-0001-8334-3313
                https://orcid.org/0000-0001-8493-2726
                https://orcid.org/0000-0002-0335-0386
                https://orcid.org/0000-0001-5044-4724
                Article
                insects-11-00239
                10.3390/insects11040239
                7240362
                32290327
                44fb4cdc-daf8-46df-9848-ce61d326d888
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 21 March 2020
                : 08 April 2020
                Categories
                Review

                epidemiology,emerging infectious diseases,pathogens,invasive species,social insects,viruses,honey bee health

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