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- First detection of Nosema ceranae in honey bees (Apis mellifera L.) of the Macaronesian archipelago of MadeiraPublication . Lopes, Ana; Martín-Hernández, Raquel; Higes, Mariano; Segura, Sara K.; Henriques, Dora; Pinto, M. AliceThe Microsporidia Nosema ceranae is an invasive pathogen affecting honey bee health, particularly in warm climates. In this study, N. ceranae was detected for the first time in honey bees (Apis mellifera L.) of the Madeira archipelago, indicating that this pathogen is now spreading across the entire Macaronesia. Nosema apis was not detected, and the high prevalence (67.7%) of N. ceranae indicates its dominance over N. apis.
- Projeto BEEHAPPY: sanidade da abelha melífera (Apis mellifera L.) dos Açores: comparação dos padrões epidemiológicos num laboratório natural únicoPublication . Pinto, M. Alice; Henriques, Dora; Rodrigues, Pedro João; Miranda, Joachim; Martín-Hernández, Raquel; Amaral, Joana S.O BEEHAPPY é um projeto financiado pela Fundação para a Ciência e a Tecnologia (FCT), é coordenado pelo CIMO e envolve uma equipa de 16 especialistas multidisciplinares provenientes de várias instituições nacionais (CIMO-Centro de Investigação de Montanha, REQUIMTE-Rede de Química e Tecnologia, CEDRI -Centro de Investigação em Digitalização e Robótica Inteligente) e estrangeiras (SLU-Swedish University of Agricultural Sciences, CIAPA-IRIAF- Centro de Investigación Apícola y Agroambiental- Instituto Regional de Investigación y Desarrollo Agralimentario y Forestal, INIA-Peru- Instituto Nacional de Innovación Agraria). O BEEHAPPY centra-se nas populações de abelha dos Açores e tem como principais objectivos (i) o estudo da interação entre a abelha e as suas principais doenças (viroses e Nosemose) e (ii) o desenvolvimento de ferramentas com vista a identificar as populações de abelha (ferramenta informática) e avaliar a autenticidade do mel dos Açores (ferramenta molecular), o qual apresenta um grande potencial comercial. Para se atingirem tais objetivos, irão ser executadas 10 tarefas dedicadas à abelha (Tarefas 1, 4, 5, 6, 7, 8, 9), patogénios (Tarefas 1, 2, 3) e mel (Tarefa 10; Figura 1).
- Epidemiology of the microsporidium nosema ceranae in four mediterranean countriesPublication . Jabal-Uriel, Clara; Barrios, Laura; Bonjour-Dalmon, Anne; Caspi-Yona, Shiran; Chejanovsky, Nor; Erez, Tal; Henriques, Dora; Higes, Mariano; Le Conte, Yves; Lopes, Ana; Meana, Aranzazu; Alice Pinto, M.; Teixeira, Amílcar; Reyes-Carreño, Maritza; Soroker, Victoria; Martín-Hernández, RaquelNosema ceranae is a highly prevalent intracellular parasite of honey bees’ midgut worldwide. This Microsporidium was monitored during a long-term study to evaluate the infection at apiary and intra-colony levels in six apiaries in four Mediterranean countries (France, Israel, Portugal, and Spain). Parameters on colony strength, honey production, beekeeping management, and climate were also recorded. Except for São Miguel (Azores, Portugal), all apiaries were positive for N. ceranae, with the lowest prevalence in mainland France and the highest intra-colony infection in Israel. A negative correlation between intra-colony infection and colony strength was observed in Spain and mainland Portugal. In these two apiaries, the queen replacement also influenced the infection levels. The highest colony losses occurred in mainland France and Spain, although they did not correlate with the Nosema infection levels, as parasitism was low in France and high in Spain. These results suggest that both the effects and the level of N. ceranae infection depends on location and beekeeping conditions. Further studies on host-parasite coevolution, and perhaps the interactions with other pathogens and the role of honey bee genetics, could assist in understanding the difference between nosemosis disease and infection, to develop appropriate strategies for its control.
- Standard methods and good practices in Apis honey bee omics researchPublication . Techer, Maeva A.; Chakrabarti, Priyadarshini; Caesar, Lílian; Eynard, Sonia E.; Farrell, M. Catherine; Foster, Leonard J.; Gorrochategui-Ortega, June; Henriques, Dora; Li-Byarlay, Hongmei; Morré, Jeffrey T.; Newton, Irene L. G.; Parejo, Melanie; Pinto, M. Alice; Vignal, Alain; Zarraonaindia, Iratxe; McAfee, AlisonIn the past decades, COLOSS members have joined forces multiple times to develop and condense standard methods related to research on honey bees, their pests, pathogens, and colony products. This led to the publication of four open-access BEEBOOK volumes that have been utilized by researchers worldwide. Among the chapters, “Standard methods for molecular research in Apis mellifera,” written by Evans and collaborators in 2013, has been a cornerstone for the standardization of honey bee molecular studies. However, since sequencing technologies and analyzing algorithms have made tremendous progress, many described methods require updating. In parallel, other Apis species’ genomes have now been sequenced, thus opening new research avenues in a comparative framework. In this chapter, we add to the methods previously covered by Evans et al. in 2013 and provide updated methodology where necessary, including worked examples and bioinformatic analysis pipe-lines. We also cover topics which were not previously covered in depth, such as sequencing ancient samples, population genomics, proteomics, and sampling honey bee colony products for microbiome studies, among others. Our hope is for this to become a lasting resource for honey bee scientists as the field continues to advance.
- Genomic DNA extraction from honey bee (Apis mellifera) queen spermathecal contentPublication . Yadró, Carlos A.; Lopes, Ana Rita; Henriques, Dora; Musin, Eduard; Wegener, Jakob; Pinto, M. AliceGenetic analysis of the honey bee spermathecal content can be particularly useful to provide an estimate of the genetic diversity and purity of the surrounding populations. Here we compared the concentration and quality of DNA extracted from queen spermatheca using four commercial kits to determine the best method to obtain DNA suitable for single nucleotide polymorphism genotyping by next-generation sequencing. The four kits were tested with different adjustments in the lysis incubation time, use of RNA-carrier, elution conditions and number of re-elutions. Only the use of QIAamp DNA Microkit with 3 h of lysis incubation, the addition of RNA-carrier and multiple re-elutions produced a DNA concentration over the required threshold.
- Maternal diversity patterns of Ibero-Atlantic populations reveal further complexity of Iberian honeybeesPublication . Pinto, M. Alice; Henriques, Dora; Neto, Margarida; Guedes, Helena; Muñoz, Irene; Azevedo, João; De la Rúa, PilarDissecting complex diversity patterns typically exhibited by organisms of hybrid zones is among the greatest challenges in evolutionary biology. This has been a long-standing goal of numerous Iberian honeybee studies. Herein, we further contribute to this goal by a fine-scale maternal survey of the Portuguese honeybee populations. In addition to confirm a predicted African ancestry of Portuguese populations and negligible levels of C-lineage introgression, our fine-scale survey revealed unparalleled levels of African maternal diversity and a remarkable north–south cline formed by African haplotypes of distinct ancestry. This survey further highlights the distinctiveness of Apis mellifera iberiensis by showing the existence of highly contrasting diversity patterns between the Atlantic and Mediterranean populations. Our findings further support an ancient natural invasion of the Iberian Peninsula possibly by Apis mellifera intermissa and also by Apis mellifera sahariensis. Protecting this African legacy is of unquestionable importance, especially with Iberia becoming warmer and dryer.
- DNA-based methods as a powerful tool for the entomological authentication of honeyPublication . Honrado, Mónica; Quaresma, Andreia; Lopes, Ana; Pinto, M. Alice; Henriques, Dora; Amaral, Joana S.Honey is a food widely consumed worldwide and much appreciated for its nutritional, organoleptic and health properties. However, it is also considered one of the food products most prone to be adulterated in the EU. Up until now, honey authenticity addressed mainly the issue of sugars addition and botanical origin. Still, increased attention has recently been paid to honey entomological origin as it also relates to its geographical origin since honeybees carrying mitochondrial DNA (mtDNA) of distinct ancestries can be found across Europe. While in Portugal mtDNA of the autochthonous subspecies Apis mellifera iberiensis belongs to the African (A) lineage, in the northeastern part of Iberia African mitotypes are replaced by mitotypes of western European (M-lineage) ancestry. The native distribution of the M-lineage A. m. mellifera expands from the Pyrenees to Scandinavia and from the British Isles to the Ural Mountains while the C-lineage A. m. ligustica and A. m. carnica subspecies are naturally found in the Apennine and Balkan peninsulas, respectively [1]. Also, certain honeys holding the protected designation of origin (PDO) label should be produced by autochthonous A. mellifera subspecies, as mentioned in their EU geographical indications register.
- Padrões de diversidade genética da abelha ibérica (Apis mellifera iberiensis): implicações para a conservação e melhoramentoPublication . Pinto, M. Alice; Chávez-Galarza, Julio; Henriques, Dora; Johnston, J. Spencer; De la Rúa, Pilar; Patton, John C.; Costa, Filipe Oliveira; Azevedo, JoãoA conservação da diversidade genética das populações locais de abelhas é fundamental à sustentabilidade da actividade apícola. Em primeiro lugar, porque a diversidade genética é a matéria-prima sobre a qual a selecção (natural ou artificial) actua, permitindo a adaptação das abelhas às cada vez mais rápidas alterações ambientais (pesticidas, novos patogénios e parasitas) e às exigências de uma actividade apícola cada vez mais competitiva. Em segundo lugar, porque a perda de diversidade genética pode conduzir à consanguinidade e à redução do valor adaptativo das colónias podendo-se traduzir em perdas de produtividade e menor resistência aos parasitas e patogénios, entre outros efeitos. Nesta comunicação apresentaremos os avanços científicos mais importantes sobre os padrões de diversidade genética da abelha ibérica alcançados pelo grupo de investigação do CIMO em colaboração com a Universidad de Murcia, University of Purdue e Texas A&M University. Para além da colecção de abelha ibérica temos também analisado amostras de outras origens geográficas incluindo norte e leste da Europa e norte de África. As mais de 3000 amostras têm vindo a ser analisadas usando marcadores mitocondriais e nucleares (“single nucleotide polymorphism”, SNPs), através da aplicação das mais avançadas ferramentas moleculares e analíticas. Esta apresentação centrar-se-á principalmente na abelha ibérica onde abordaremos (i) o padrão geográfico de diversidade mitocondrial e nuclear, (ii) os resultados do scan genómico que revelam as regiões do genoma que emitem um forte sinal de selecção e que parecem estar envolvidas na adaptação da abelha ibérica ao meio ambiente, (iii) o grau de introgressão de A.m. ligustica e A.m. carnica no genoma da abelha ibérica e comparação com os resultados que obtivemos para a A.m. mellifera. Este estudo constitui a mais recente e completa caracterização genética da abelha ibérica proporcionando informação de base que pode ser útil em programas de melhoramento e conservação da abelha ibérica.
- DeepWings: a machine learning tool for identification of honey bee subspeciesPublication . Ariel Yadró, Carlos; Rodrigues, Pedro João; Adam, Tofilski; Elen, Dylan; McCormack, Grace P.; Henriques, Dora; Pinto, M. AliceDeepWings© is a software that uses Machine Learning for fully automated identification of Apis mellifera subspecies based on wing geometric morphometrics (WGM). Here, we examined the performance of DeepWings© under realistic conditions by processing 14,782 wing images with varying quality and produced by different operators. These images represented 2,593 colonies covering the native ranges of A. m. iberiensis (Portugal, Spain and historical introduction in the Azores), A. m. mellifera (Belgium, France, Ireland, Poland, Russia, Sweden, Switzerland, UK) and A. m. carnica (Croatia, Hungary, Romania). The classification probability obtained for the colonies was contrasted with the endemic subspecies distribution. Additionally, the association between WGM classification and that inferred from microsatellites and SNPs was evaluated for 1,214 colonies. As much as 94.4% of the wings were accepted and classified by DeepWings©. In the Iberian honey bee native range, 92,6% of the colonies were classified as A. m. iberiensis with a median probability of 91.88 (IQR = 22.52). In the Azores, 85.7% of colonies were classified as A. m. iberiensis, with a median probability of 84.16 (32.40). In the Dark honey bee native range, 41.1 % of the colonies were classified as A. m mellifera with a median probability of 99.36 (8.02). The low percentage of colonies matching the native subspecies was mainly due to the low values registered in Avignon (20.0%), Poland (32.9%), and Wales (41.2%). In contrast, most of the colonies analyzed in other locations of the native range of A. m. mellifera matched this subspecies: Belgium (100.0%), Groix (63.9%), Ouessant (72.7%), Ireland (78.0%), Russia (96.2%), Sweden (84.2%) and Switzerland (55.6%). In the colonies from Croatia, Hungary, and Romania, 88.0% of the samples were classified as A. m. carnica, with a median probability of 98.49 (6.76). The association between WGM and molecular data was highly significant but not very strong (Spearman r = 0.31, p < 0.0001). A good agreement between morphological and molecular methods was registered in samples originating from highly conserved M-lineage populations whereas in populations with historical records of foreign queen importations the agreement was weaker. In general, DeepWings© showed good performance when tested under realistic conditions. It is a valuable tool that can be used not only for honey bee breeding and conservation but also for research purposes.
- COI Metabarcoding as a Novel Approach for Assessing the Honey Bee Source of European HoneyPublication . Honrado, Mónica; Quaresma, Andreia; Henriques, Dora; Pinto, M. Alice; Amaral, Joana S.Honey is a widely consumed food product frequently subjected to adulteration, with the mislabeling of its botanical or geographical origin being one of the most common practices. Determining the entomological origin of honey is particularly challenging but of high relevance for ensuring its authenticity, especially for products with protected designation of origin (PDO) labels. This study presents a novel DNA metabarcoding approach targeting a highly informative 406 bp fragment of the cytochrome c oxidase I (COI) gene to differentiate among the three major mitochondrial lineages (A, M, and C) of honey bees (Apis mellifera L.) native to Europe. The target region was selected based on the calculated fixation index (FST), which is frequently used in Population Genetics as a measure of differentiation between populations. The approach was validated with 11 honey samples of known entomological origin and applied to 44 commercial honeys from 13 countries. The approach demonstrated high sensitivity, accurately identifying the entomological origin of honey, including samples produced by honey bees of varying ancestries, which could not be resolved by previous methods based on real-time PCR coupled with high-resolution melting (PCR-HRM) analysis. The results demonstrate the effectiveness of COI metabarcoding in verifying honey authenticity and highlight the predominance of C-lineage honey bees in the production of commercial honeys from northwestern Europe. This finding suggests a limited presence of the native M-lineage ancestry, underscoring the need for conservation efforts.