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7. Allele Frequencies of Genetic Variants Associated with Varroa Drone Brood Resistance (DBR) in Apis mellifera Subspecies across the European Continent

Author

Lefebre, Regis, primary, De Smet, Lina, additional, Tehel, Anja, additional, Paxton, Robert J., additional, Bossuyt, Emma, additional, Verbeke, Wim, additional, van Dooremalen, Coby, additional, Ulgezen, Zeynep N., additional, van den Bosch, Trudy, additional, Schaafsma, Famke, additional, Valkenburg, Dirk-Jan, additional, Dall’Olio, Raffaele, additional, Alaux, Cedric, additional, Dezmirean, Daniel S., additional, Giurgiu, Alexandru I., additional, Capela, Nuno, additional, Simões, Sandra, additional, Sousa, José Paulo, additional, Bencsik, Martin, additional, McVeigh, Adam, additional, Ramsey, Michael Thomas, additional, Ahmad, Sausan, additional, Kumar, Tarun, additional, Schäfer, Marc O., additional, Beaurepaire, Alexis L., additional, Moro, Arrigo, additional, Flener, Claude J., additional, Matthijs, Severine, additional, and de Graaf, Dirk C., additional

Published
2024
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9. Cold case: The disappearance of Egypt bee virus, a fourth distinct master strain of deformed wing virus linked to honeybee mortality in 1970’s Egypt

Author

de Miranda, Joachim R., Brettell, Laura E., Chejanovsky, Nor, Childers, Anna K., Dalmon, Anne, Deboutte, Ward, de Graaf, Dirk C., Doublet, Vincent, Gebremedhn, Haftom, Genersch, Elke, Gisder, Sebastian, Granberg, Fredrik, Haddad, Nizar J., Kaden, Rene, Manley, Robyn, Matthijnssens, Jelle, Meeus, Ivan, Migdadi, Hussein, Milbrath, Meghan O., Mondet, Fanny, Remnant, Emily J., Roberts, John M. K., Ryabov, Eugene V., Sela, Noa, Smagghe, Guy, Somanathan, Hema, Wilfert, Lena, Wright, Owen N., Martin, Stephen J., and Ball, Brenda V.

Published
2022
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13. A field realistic model to assess the effects of pesticides residues and adulterants on honey bee gene expression.

Author

El Agrebi, Noëmie, De Smet, Lina, Douny, Caroline, Scippo, Marie-Louise, Svečnjak, Lidija, de Graaf, Dirk C., and Saegerman, Claude

Subjects
HONEYBEES, PESTICIDE residues in food, GENE expression, PESTICIDE pollution, PESTICIDES, GENE expression profiling
Abstract

While studies on the sublethal effects of chemical residues in beeswax on adult honey bees are increasing, the study protocols assessing the impacts on honey bee brood in realistic conditions still need to be investigated. Moreover, little is known about the residue's effect on gene expression in honey bee brood. This study reports the effects of chlorpyriphos-ethyl, acrinathrin and stearin worker pupae exposure through contaminated or adulterated beeswax on the gene expression of some key health indicators, using a novel in vivo realistic model. Larvae were reared in acrinathrin (12.5, 25, 10 and 100 ppb) and chlorpyriphos-ethyl (5, 10, 500 and 5000 ppb) contaminated or stearin adulterated beeswax (3, 4, 5, 6 and 9%) in newly formed colonies to reduce the influence of external factors. On day 11, mortality rates were assessed. Honey bee pupae were extracted from the comb after 19 days of rearing and were analysed for the gene expression profile of four genes involved in the immune response to pathogens and environmental stress factors (Imd, dorsal, domeless and defensin), and two genes involved in detoxifications mechanisms (CYP6AS14 and CYP9Q3). We found no linear relation between the increase in the pesticide concentrations and the brood mortality rates, unlike stearin where an increase in stearin percentage led to an exponential increase in brood mortality. The immune system of pupae raised in acrinathrin contaminated wax was triggered and the expression of CYP6AS14 was significantly upregulated (exposure to 12.5 and 25 ppb). Almost all expression levels of the tested immune and detoxification genes were down-regulated when pupae were exposed to chlorpyrifos-contaminated wax. The exposure to stearin triggered the immune system and detoxification system of the pupae. The identification of substance-specific response factors might ultimately serve to identify molecules that are safer for bees and the ecosystem's health. [ABSTRACT FROM AUTHOR]

Published
2024
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14. Bridging the Gap between Field Experiments and Machine Learning: The EC H2020 B-GOOD Project as a Case Study towards Automated Predictive Health Monitoring of Honey Bee Colonies

Author

van Dooremalen, Coby, primary, Ulgezen, Zeynep N., additional, Dall’Olio, Raffaele, additional, Godeau, Ugoline, additional, Duan, Xiaodong, additional, Sousa, José Paulo, additional, Schäfer, Marc O., additional, Beaurepaire, Alexis, additional, van Gennip, Pim, additional, Schoonman, Marten, additional, Flener, Claude, additional, Matthijs, Severine, additional, Claeys Boúúaert, David, additional, Verbeke, Wim, additional, Freshley, Dana, additional, Valkenburg, Dirk-Jan, additional, van den Bosch, Trudy, additional, Schaafsma, Famke, additional, Peters, Jeroen, additional, Xu, Mang, additional, Le Conte, Yves, additional, Alaux, Cedric, additional, Dalmon, Anne, additional, Paxton, Robert J., additional, Tehel, Anja, additional, Streicher, Tabea, additional, Dezmirean, Daniel S., additional, Giurgiu, Alexandru I., additional, Topping, Christopher J., additional, Williams, James Henty, additional, Capela, Nuno, additional, Lopes, Sara, additional, Alves, Fátima, additional, Alves, Joana, additional, Bica, João, additional, Simões, Sandra, additional, Alves da Silva, António, additional, Castro, Sílvia, additional, Loureiro, João, additional, Horčičková, Eva, additional, Bencsik, Martin, additional, McVeigh, Adam, additional, Kumar, Tarun, additional, Moro, Arrigo, additional, van Delden, April, additional, Ziółkowska, Elżbieta, additional, Filipiak, Michał, additional, Mikołajczyk, Łukasz, additional, Leufgen, Kirsten, additional, De Smet, Lina, additional, and de Graaf, Dirk C., additional

Published
2024
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16. Shift in virus composition in honeybees ( Apis mellifera ) following worldwide invasion by the parasitic mite and virus vector Varroa destructor

Author

Doublet, Vincent, primary, Oddie, Melissa A. Y., additional, Mondet, Fanny, additional, Forsgren, Eva, additional, Dahle, Bjørn, additional, Furuseth-Hansen, Elisabeth, additional, Williams, Geoffrey R., additional, De Smet, Lina, additional, Natsopoulou, Myrsini E., additional, Murray, Tomás E., additional, Semberg, Emilia, additional, Yañez, Orlando, additional, de Graaf, Dirk C., additional, Le Conte, Yves, additional, Neumann, Peter, additional, Rimstad, Espen, additional, Paxton, Robert J., additional, and de Miranda, Joachim R., additional

Published
2024
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21. Characterization of Native Honey Bee Subspecies in Republic of Benin Using Morphometric and Genetic Tools

Author

Amakpe Felicien, De Smet Lina, Brunain Marleen, Jacobs Frans J., Sinsin Brice, and de Graaf Dirk C.

Subjects
apis mellifera, ecotype, republic of benin, subtype, Zoology, QL1-991
Abstract

Morphometric characteristics combined with genetic markers are powerful tools used for determining honey bee subspecies. Bees samples collected from 94 established apiaries distributed throughout all of the Republic of Benin were morphometricaly characterized using seven parameters and the COI-COII regions of mitochondrial DNA were sequenced. Based on the morphometric data the native honey bees could be divided into three distinct ecotypes - the Benino-dry-tropical-ecotype in the north, the Benino-Sudanian-ecotype in the central part and the Benino-Sudano-Guinean-ecotype in the south. The DNA COI-COII regions sequence analyses confirmed that the honey bee population of the Republic of Benin belongs to different mitotypes but do not correspond with the determined ecotypes. We could determine three new haplotypes which missed the P0 segment but the Q region was duplicated or triplicated. Phylogenetic analyses clustered them together in the A evolutionary lineage. In conclusion, morphometric and genetic analysis of the native West African honey bees indicated that each of the different mitotypes was able to adapt to the different ecological conditions in the country by morphometric adjustments.

Published
2018
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24. Trueness and precision of the real-time RT-PCR method for quantifying the chronic bee paralysis virus genome in bee homogenates evaluated by a comparative inter-laboratory study

Author

Schurr, Frank, Cougoule, Nicolas, Rivière, Marie-Pierre, Ribière-Chabert, Magali, Achour, Hamid, Ádám, Dán, Castillo, Carlos, de Graaf, Dirk C., Forsgren, Eva, Granato, Anna, Heinikainen, Sirpa, Jurovčíková, Júlia, Kryger, Per, Manson, Christine, Ménard, Marie-Françoise, Perennes, Stéphane, Schäfer, Marc O., Ibañez, Elena San Miguel, Silva, João, Gajger, Ivana Tlak, Tomkies, Victoria, Toplak, Ivan, Viry, Alain, Zdańska, Dagmara, and Dubois, Eric

Published
2017
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26. Exploring the External Environmental Drivers of Honey Bee Colony Development.

Author

Capela, Nuno, Sarmento, Artur, Simões, Sandra, Lopes, Sara, Castro, Sílvia, Alves da Silva, António, Alves, Joana, Dupont, Yoko L., de Graaf, Dirk C., and Sousa, José Paulo

Subjects
HONEYBEES, BEE colonies, CLIMATE change, AGRICULTURE, SPATIAL variation, BEES
Abstract

Honey bees play an important role in agricultural landscapes by providing pollination services. Throughout the season, colonies increase their population and collect resources from the available flowering plants. Besides internal mechanisms, such as the amount of brood or the availability of bees to perform foraging flights, colonies are also influenced by the climate and the surrounding landscape. Therefore, exposure to different environmental contexts leads to distinct development rates. In this study, we show how colonies develop under three different landscape contexts and explore which external variables (mostly climate and resources availability) influence the colonies' development. We installed three apiaries in three different landscapes in the Iberian Peninsula, with temporal and spatial variation in climatic conditions and resource availability. The availability of resources and their use, as well as the development of colonies throughout the season, were thoroughly investigated. These data were used to take the first step into creating an ecologically relevant landscape by calculating the number of available resources in the landscape at different points in time, based on plants' beekeeping interest as well as nectar and production. Furthermore, climatic variables were transformed into the amount of available foraging minutes that bees had to collect resources, and a theoretical threshold of optimal vs. sub-optimal conditions was also explored. Interestingly, the main drivers of colony development (measured by daily weight increase) were not the same in the tested apiaries, evidencing how colonies are indeed intrinsically connected with the surrounding environmental scenario. Therefore, results from field testing are extremely context-dependent and should be interpreted with caution when being extrapolated to other environmental scenarios. [ABSTRACT FROM AUTHOR]

Published
2023
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32. Virus Prevalence in Egg Samples Collected from Naturally Selected and Traditionally Managed Honey Bee Colonies across Europe

Author

Claeys Bouuaert, David, primary, De Smet, Lina, additional, Brunain, Marleen, additional, Dahle, Bjørn, additional, Blacquière, Tjeerd, additional, Dalmon, Anne, additional, Dezmirean, Daniel, additional, Elen, Dylan, additional, Filipi, Janja, additional, Giurgiu, Alexandru, additional, Gregorc, Aleš, additional, Kefuss, John, additional, Locke, Barbara, additional, de Miranda, Joachim R., additional, Oddie, Melissa, additional, Panziera, Delphine, additional, Parejo, Melanie, additional, Pinto, Maria Alice, additional, and de Graaf, Dirk C., additional

Published
2022
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33. Opportunities and knowledge gaps for EU research and innovation on pollinators

Author

European Research Executive Agency, Tallarico, Tatiana, Brown, Mark, Chauzat, Marie-Pierre, de Graaf, Dirk C., Dupont, Yoko Luise, Kleijn, David, Paxton, Robert, Potts, Simon, Schweiger, Oliver, Settele, Josef, Beaurepaire, Alexis, Boustani, Mira, Bulet, Philippe, Castro, Silvia, de Smet, Lina, Knauer, Anina, Michez, Denis, Neumann, Peter, Reverté Saiz, Sara, Rosa, Paolo, Sousa, José Paulo, Steffan-Dewenter, Ingolf, and Turney, Gail

Published
2023

38. Virus Prevalence in Egg Samples Collected from Naturally Selected and Traditionally Managed Honey Bee Colonies across Europe

Author

Genética, antropología física y fisiología animal, Genetika,antropologia fisikoa eta animalien fisiologia, Claeys Bouuaert, David, De Smet, Lina, Brunain, Marleen, Dahle, Bjørn, Blacquière, Tjeerd, Dalmon, Anne, Dezmirean, Daniel, Elen, Dylan, Filipi, Janja, Giurgiu, Alexandru, Gregorc, Aleš, Kefuss, John, Locke, Barbara, de Miranda, Joachim R., Oddie, Melissa, Panziera, Delphine, Parejo Feuz, Melanie, Pinto, Maria Alice, de Graaf, Dirk C., Genética, antropología física y fisiología animal, Genetika,antropologia fisikoa eta animalien fisiologia, Claeys Bouuaert, David, De Smet, Lina, Brunain, Marleen, Dahle, Bjørn, Blacquière, Tjeerd, Dalmon, Anne, Dezmirean, Daniel, Elen, Dylan, Filipi, Janja, Giurgiu, Alexandru, Gregorc, Aleš, Kefuss, John, Locke, Barbara, de Miranda, Joachim R., Oddie, Melissa, Panziera, Delphine, Parejo Feuz, Melanie, Pinto, Maria Alice, and de Graaf, Dirk C.

Abstract

Monitoring virus infections can be an important selection tool in honey bee breeding. A recent study pointed towards an association between the virus-free status of eggs and an increased virus resistance to deformed wing virus (DWV) at the colony level. In this study, eggs from both naturally surviving and traditionally managed colonies from across Europe were screened for the prevalence of different viruses. Screenings were performed using the phenotyping protocol of the ‘suppressed in ovo virus infection’ trait but with qPCR instead of end-point PCR and a primer set that covers all DWV genotypes. Of the 213 screened samples, 109 were infected with DWV, 54 were infected with black queen cell virus (BQCV), 3 were infected with the sacbrood virus, and 2 were infected with the acute bee paralyses virus. It was demonstrated that incidences of the vertical transmission of DWV were more frequent in naturally surviving than in traditionally managed colonies, although the virus loads in the eggs remained the same. When comparing virus infections with queen age, older queens showed significantly lower infection loads of DWV in both traditionally managed and naturally surviving colonies, as well as reduced DWV infection frequencies in traditionally managed colonies. We determined that the detection frequencies of DWV and BQCV in honey bee eggs were lower in samples obtained in the spring than in those collected in the summer, indicating that vertical transmission may be lower in spring. Together, these patterns in vertical transmission show that honey bee queens have the potential to reduce the degree of vertical transmission over time.

Published
2022

39. Dynamics in vertical transmission of viruses in naturally selected and traditionally managed honey bee colonies across Europe

Author

Claeys Bouuaert, David, De Smet, Lina, Brunain, Marleen, Dahle, Bjorn, Blacquiere, T., Dalmon, Anne, Dezmirean, Daniel, Elen, Dylan, Filipi, Janja, Giurgiu, Alexandru, Gregorc, Aleš, Kefuss, John, Locke, Barbara, de Miranda, Joachim R., Oddie, Melissa, Panziera, D., Parejo, Melanie, Pinto, M.A., de Graaf, Dirk C., Claeys Bouuaert, David, De Smet, Lina, Brunain, Marleen, Dahle, Bjorn, Blacquiere, T., Dalmon, Anne, Dezmirean, Daniel, Elen, Dylan, Filipi, Janja, Giurgiu, Alexandru, Gregorc, Aleš, Kefuss, John, Locke, Barbara, de Miranda, Joachim R., Oddie, Melissa, Panziera, D., Parejo, Melanie, Pinto, M.A., and de Graaf, Dirk C.

Abstract

The ‘suppressed in-ovo virus infection’ trait (SOV) was the first trait applied in honey bee breeding programs aimed to increase resilience to virus infections, a major threat for colony survival. By screening drone eggs for viruses, the SOV trait scores the antiviral resistance of queens and its implications for vertical transmission. In this study, queens from both naturally surviving and traditionally managed colonies from across Europe were screened using a two-fold improved SOV phenotyping protocol. First, a gel-based RT-PCR was replaced by a RT-qPCR. This not only allowed quantification of the infection load but also increased the test sensitivity. Second, a genotype specific primer set was replaced by a primer set that covered all known deformed wing virus (DWV) genotypes, which resulted in higher virus loads and fewer false negative results. It was demonstrated that incidences of vertical transmission of DWV were more frequent in naturally surviving populations than in traditionally managed colonies, although the virus load in the eggs remained the same. Dynamics in vertical transmission were further emphasized when comparing virus infections with queen age. Interestingly, older queens showed significantly lower infection loads of DWV in both traditionally managed and naturally surviving colonies, as well as reduced DWV infection frequencies in traditionally managed colonies when compared with younger queens. Seasonal variation in vertical transmission was found with lower infection frequencies in spring compared to summer for DWV and black queen cell virus. Together, these patterns in vertical transmission suggest an adaptive antiviral response of queens aimed at reducing vertical transmission over time.

Published
2022

40. Virus Prevalence in Egg Samples Collected from Naturally Selected and Traditionally Managed Honey Bee Colonies across Europe

Author

Claeys Bouuaert, David, De Smet, Lina, Brunain, Marleen, Dahle, Bjørn, Blacquière, Tjeerd, Dalmon, Anne, Dezmirean, Daniel, Elen, Dylan, Filipi, Janja, Giurgiu, Alexandru, Gregorc, Aleš, Kefuss, John, Locke, Barbara, De Miranda, Joachim R., Oddie, Melissa, Panziera, Delphine, Parejo, Melanie, Pinto, Maria Alice, De Graaf, Dirk C., Claeys Bouuaert, David, De Smet, Lina, Brunain, Marleen, Dahle, Bjørn, Blacquière, Tjeerd, Dalmon, Anne, Dezmirean, Daniel, Elen, Dylan, Filipi, Janja, Giurgiu, Alexandru, Gregorc, Aleš, Kefuss, John, Locke, Barbara, De Miranda, Joachim R., Oddie, Melissa, Panziera, Delphine, Parejo, Melanie, Pinto, Maria Alice, and De Graaf, Dirk C.

Abstract

Monitoring virus infections can be an important selection tool in honey bee breeding. A recent study pointed towards an association between the virus-free status of eggs and an increased virus resistance to deformed wing virus (DWV) at the colony level. In this study, eggs from both naturally surviving and traditionally managed colonies from across Europe were screened for the prevalence of different viruses. Screenings were performed using the phenotyping protocol of the ‘suppressed in ovo virus infection’ trait but with qPCR instead of end-point PCR and a primer set that covers all DWV genotypes. Of the 213 screened samples, 109 were infected with DWV, 54 were infected with black queen cell virus (BQCV), 3 were infected with the sacbrood virus, and 2 were infected with the acute bee paralyses virus. It was demonstrated that incidences of the vertical transmission of DWV were more frequent in naturally surviving than in traditionally managed colonies, although the virus loads in the eggs remained the same. When comparing virus infections with queen age, older queens showed significantly lower infection loads of DWV in both traditionally managed and naturally surviving colonies, as well as reduced DWV infection frequencies in traditionally managed colonies. We determined that the detection frequencies of DWV and BQCV in honey bee eggs were lower in samples obtained in the spring than in those collected in the summer, indicating that vertical transmission may be lower in spring. Together, these patterns in vertical transmission show that honey bee queens have the potential to reduce the degree of vertical transmission over time.

Published
2022

42. Dynamics in vertical transmission of viruses in naturally selected and traditionally managed honey bee colonies across Europe

Author

Claeys Bouuaert, David, primary, De Smet, Lina, additional, Brunain, Marleen, additional, Dahle, Bjørn, additional, Blacquière, Tjeerd, additional, Dalmon, Anne, additional, Dezmirean, Daniel, additional, Dylan, Elen, additional, Filipi, Janja, additional, Giurgiu, Alexandru, additional, Gregorc, Aleš, additional, Kefuss, John, additional, Locke, Barbara, additional, de Miranda, Joachim R., additional, Oddie, Melissa, additional, Panziera, Delphine, additional, Parejo, Melanie, additional, Pinto, Alice M., additional, and de Graaf, Dirk C., additional

Published
2022
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44. Cold case: The disappearance of Egypt bee virus, a fourth distinct master strain of deformed wing virus linked to honeybee mortality in 1970's Egypt

Author

Rodrigues De Miranda, Joachim, Brettell, Laura E., Chejanovsky, Nor, Childers, Anna K., Dalmon, Anne, Deboutte, Ward, de Graaf, Dirk C., Doublet, Vincent, Gebremedhn, Haftom, Genersch, Elke, Gisder, Sebastian, Granberg, Fredrik, Haddad, Nizar J., Manley, Robyn, Matthijnssens, Jelle, Meeus, Ivan, Migdadi, Hussein, Milbrath, Meghan, Mondet, Fanny, Remnant, Emily J., Roberts, John M. K., Ryabov, Eugene, Sela, Noa, Smagghe, Guy, Somanathan, Hema, Wilfert, Lena, Wright, Owen N., Martin, Stephen J., and Ball, Brenda

Subjects
Ecology
Abstract

In 1977, a sample of diseased adult honeybees (Apis mellifera) from Egypt was found to contain large amounts of a previously unknown virus, Egypt bee virus, which was subsequently shown to be serologically related to deformed wing virus (DWV). By sequencing the original isolate, we demonstrate that Egypt bee virus is in fact a fourth unique, major variant of DWV (DWV-D): more closely related to DWV-C than to either DWV-A or DWV-B. DWV-A and DWV-B are the most common DWV variants worldwide due to their close relationship and transmission by Varroa destructor. However, we could not find any trace of DWV-D in several hundred RNA sequencing libraries from a worldwide selection of honeybee, varroa and bumblebee samples. This means that DWV-D has either become extinct, been replaced by other DWV variants better adapted to varroa-mediated transmission, or persists only in a narrow geographic or host range, isolated from common bee and beekeeping trade routes.

Published
2022

45. Additional file 1 of Cold case: The disappearance of Egypt bee virus, a fourth distinct master strain of deformed wing virus linked to honeybee mortality in 1970’s Egypt

Author

de Miranda, Joachim R., Brettell, Laura E., Chejanovsky, Nor, Childers, Anna K., Dalmon, Anne, Deboutte, Ward, de Graaf, Dirk C., Doublet, Vincent, Gebremedhn, Haftom, Genersch, Elke, Gisder, Sebastian, Granberg, Fredrik, Haddad, Nizar J., Kaden, Rene, Manley, Robyn, Matthijnssens, Jelle, Meeus, Ivan, Migdadi, Hussein, Milbrath, Meghan O., Mondet, Fanny, Remnant, Emily J., Roberts, John M. K., Ryabov, Eugene V., Sela, Noa, Smagghe, Guy, Somanathan, Hema, Wilfert, Lena, Wright, Owen N., Martin, Stephen J., and Ball, Brenda V.

Abstract

Additional file 1: Figure S1. Amplification and sequencing strategy. Figure S2. MENA polymorphisms. Table S1. Primers for amplifying DWV strains. Table S2. Numerical details of the phylogenetic analyses. Table S3. SRA libraries and samples screened for DWV-D.

Published
2022
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47. CSI Pollen: Diversity of Honey Bee Collected Pollen Studied by Citizen Scientists

Author

Brodschneider, Robert, primary, Kalcher-Sommersguter, Elfriede, additional, Kuchling, Sabrina, additional, Dietemann, Vincent, additional, Gray, Alison, additional, Božič, Janko, additional, Briedis, Andrejs, additional, Carreck, Norman L., additional, Chlebo, Robert, additional, Crailsheim, Karl, additional, Coffey, Mary Frances, additional, Dahle, Bjørn, additional, González-Porto, Amelia Virginia, additional, Filipi, Janja, additional, de Graaf, Dirk C., additional, Hatjina, Fani, additional, Ioannidis, Pavlos, additional, Ion, Nicoleta, additional, Jørgensen, Asger Søgaard, additional, Kristiansen, Preben, additional, Lecocq, Antoine, additional, Odoux, Jean-François, additional, Özkirim, Asli, additional, Peterson, Magnus, additional, Podrižnik, Blaž, additional, Rašić, Slađan, additional, Retschnig, Gina, additional, Schiesser, Aygün, additional, Tosi, Simone, additional, Vejsnæs, Flemming, additional, Williams, Geoffrey, additional, and van der Steen, Jozef J.M., additional

Published
2021
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