Browsing by Author "McCormack, Grace P."
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- An unprecedented large-scale survey of honey bee mitochondrial diversity in Europe: c-lineage dominance and the need for conservation effortsPublication . Li, Fernanda; Costa, Maíra; Lopes, Ana Rita; Gonçalves, Telma; Henriques, Dora; Quaresma, Andreia; Yadró Garcia, Carlos A.; Albo, Alexandre; Blažytė-Čereškienė, Laima; Brodschneider, Robert; Brusbardis, Valters; Carreck, Norman L.; Charistos, Leonidas; Chlebo, Robert; Coffey, Mary F.; Dahle, Bjørn; Danneels, Ellen; Dobrescu, Constantin; Dupleix-Marchal, Anna; Filipi, Janja; Gajda, Anna; Gratzer, Kristina; Groeneveld, Linn Fenna; Hatjina, Fani; Johannesen, Jes; Kolasa, Michal; Körmendy-Rácz, János; Kovačić, Marin; Kristiansen, Preben; Martikkala, Maritta; McCormack, Grace P.; Martín-Hernández, Raquel; Pavlov, Borce; Pietropaoli, Marco; Poirot, Benjamin; Radev, Zheko; Raudmets, Aivar; René-Douarre, Vincent; Roessink, Ivo; Škerl, Maja Ivana Smodiš; Soland-Reckeweg, Gabriele; Titera, Dalibor; Steen, Jozef van der; Varnava, Andri; Vejsnæs, Flemming; Webster, Matthew T.; Fedoriak, Mariia M.; Zarochentseva, Oksana; Graaf, Dirk C.; Pinto, M. AliceEurope is home to ten Apis mellifera subspecies, which belong to three mitochondrial lineages: the Western European (M), Eastern European (C), and African (A). However, the long-standing human-mediated movement of queens, primarily of C-lineage ancestry, has threatened the genetic integrity of many of these native subspecies through introgression and replacement. This has led to the establishment of conservation programs to recover the native lines in some European countries. The maternally-inherited mitochondrial DNA (mtDNA), particularly the highly polymorphic intergenic region tRNAleu-cox2, has been the marker of choice for assessing honey bee variation and introgression at large geographical scales. Herein, we will show the results of the tRNAleu-cox2 variation obtained from over 1200 colonies sampled across the range of the ten subspecies and covering 33 European countries. These revealed that apart from a few countries (Portugal, Spain, and Ireland) and isolated protected populations, European populations are predominantly dominated by C-lineage haplotypes, and many native subspecies exhibit a signature of C-derived introgression. In conclusion, this unprecedented survey of honey bee diversity across Europe underscores the concerning dominance of C-lineage genetic variation, highlighting the urgent need for strategic conservation efforts to preserve the native genetic diversity of Apis mellifera.
- Applying a SNP-based tool for conservation of wild and managed black bees in IrelandPublication . Browne, Keith A.; Henriques, Dora; Pinto, M. Alice; Native Irish Honey Bee Society; McCormack, Grace P.Apis mellifera mellifera (Amm) is threatened over much of its natural range. However, in Ireland microsatellite and mitochondrial data have shown that a significant population of this subspecies exists in pure form and is spread over a large geographical region on the Island. Black bees have been managed and protected by beekeepers on the island, some of whom formed the Native Irish Honeybee Society (NIHBS)in 2012 and a breeding programme was initiated for Amm in 2014/2015. The application of a SNP panel that detects hybridization between M and C lineages clearly supports other data showing that the majority of beekeepers included in the breeding programme indeed have bees with very low to no introgression from the C lineage. Furthermore, SNP data has also been applied to the first feral bee colonies located in Ireland subsequent to the introduction of Varroa. Here we will present on the use of molecular data as an aid to manage and conserve honeybees in Ireland, and to elucidate patterns in colour variation and honeybee subspecies purity in wild and managed bees with a view towards improving conservation approaches in the face of a potential hybridization threat.
- Applying molecular tools for conservation of wild and managed black bees in IrelandPublication . Browne, Keith A.; Henriques, Dora; Hassett, Jack; Geary, Michael; Moore, E.; Pinto, M. Alice; Native Irish Honey Bee Society; McCormack, Grace P.Apis mellifera mellifera (black bees) is threatened over much of its natural range. However, in Ireland microsatellite and mitochondrial data have shown that a significant population of this subspecies exists in pure form and spread over a large geographical region on the Island. Black bees have been managed and protected by beekeepers on the island, some of who formed the Native Irish Honeybee Society in 2012. The application of a SNP panel that detects hybridization between M and C lineages clearly supports other data in that the majority of beekeepers included who purported to keep black bees indeed have bees that show very low to no introgression from the C lineage. Furthermore, SNP data has also been applied to the first feral bee colonies located in Ireland subsequent to the introduction of Varroa. Long considered extinct, feral bees sampled to date show high levels of A. m. mellifera purity using SNPs. Here we will present this data and also discuss the use of this SNP panel to elucidate patterns in colour variation and honeybee subspecies purity in wild and managed bees towards improving conservation approaches in the face of potential hybridization threat.
- Can introgression in M-lineage honey bees be detected by abdominal colour patterns?Publication . Henriques, Dora; Lopes, Ana; Ferrari, Roberto; Neves, Cátia J.; Quaresma, Andreia; Browne, Keith A.; McCormack, Grace P.; Pinto, M. AliceHoney bee abdominal pigmentation is one of the most recognisable traits and it is often used by beekeepers as an indicator of M-lineage subspecies purity. However, this approach may negatively impact population diversity and is futile if there is no association between tergite colour patterns and the genetic background. To assess whether this trait can be used as a proxy for introgression proportions in M-lineage subspecies, we genotyped, with highly informative SNP assays, A. m. mellifera and A. m. iberiensis individuals displaying four different colour phenotypes. The SNP data detected highly introgressed bees exhibiting a black phenotype and, at the same time, pure or marginally introgressed bees with yellow banding patterns, in both subspecies. Despite these observations, contrary to A. m. iberiensis , in A. m. mellifera , introgression proportions revealed to be a significant predictor of abdominal pigmentation. Therefore, abdominal pigmentation could be used by A. m. mellifera conservationists to guide colony selection when genetic tools are unavailable.
- Conservation of European M-lineage honey bees using abdominal colour as an indicator of subspecies purity has pitfallsPublication . Henriques, Dora; Lopes, Ana; Ferrari, Roberto; Neves, Cátia J.; Quaresma, Andreia; Browne, Keith A.; McCormack, Grace P.; Pinto, M. AliceThere are 31 honey bee (Apis mellifera) recognized subspecies, which have been grouped into four main lineages. Two of these lineages occur naturally in Europe: M in western and northern Europe and C in southeastern Europe. In Europe, M-lineage groups only two subspecies, Apis mellifera mellifera and Apis mellifera iberiensis, both being black in colour. C-Lineage groups have instead eight subspecies, including one of the beekeepers-favored and phenotypically distinct, the yellow Apis mellifera ligustica from Italy. M-lineage honey bees’ distribution has been changing and in some countries, the native bee is being replaced or hybridised with C-lineage subspecies. Honey bee abdominal pigmentation is one of the most recognisable traits and it has been used by beekeepers as an indicator of subspecies identity. However, this approach may negatively impact population diversity and is futile if there is no association between tergite colour patterns and genetic background. To test this approach, we calculated the introgression level of A. m. mellifera (N=162) and A. m. iberiensis individuals (N=559) with different colour phenotypes and from a wide geographical range using informative SNPs. In this study, many A. m. mellifera samples showed high levels of C-lineage introgression. The individuals collected in Iberia were revealed to be pure. Introgressed A. m. iberiensis individuals were all from the Azores, where a high frequency of C-lineage mitotypes exists in several islands. Our results showed that for both subspecies, it is not possible to directly identify introgressed individuals from observed colour patterns, as we found black honey bees with a considerable amount of introgression and honey bees with yellow banding that were pure or marginally introgressed. With this study, we hope to increase awareness among stakeholders of the need to use other tools to select honey bees for conservation and breeding purposes.
- 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.
- High sample throughput genotyping for estimating C-lineage introgression in the dark honeybee: an accurate and cost-effective SNP-based toolPublication . Henriques, Dora; Browne, Keith A.; Barnett, Mark W.; Parejo, Melanie; Kryger, Per; Freeman, Tom C.; Muñoz, Irene; Garnery, Lionel; Highet, Fiona; Jonhston, J. Spencer; McCormack, Grace P.; Pinto, M. AliceThe natural distribution of the honeybee (Apis mellifera L.) has been changed by humans in recent decades to such an extent that the formerly widest-spread European subspecies, Apis mellifera mellifera, is threatened by extinction through introgression from highly divergent commercial strains in large tracts of its range. Conservation efforts for A. m. mellifera are underway in multiple European countries requiring reliable and cost-efficient molecular tools to identify purebred colonies. Here, we developed four ancestry-informative SNP assays for high sample throughput genotyping using the iPLEX Mass Array system. Our customized assays were tested on DNA from individual and pooled, haploid and diploid honeybee samples extracted from different tissues using a diverse range of protocols. The assays had a high genotyping success rate and yielded accurate genotypes. Performance assessed against whole-genome data showed that individual assays behaved well, although the most accurate introgression estimates were obtained for the four assays combined (117 SNPs). The best compromise between accuracy and genotyping costs was achieved when combining two assays (62 SNPs). We provide a ready-to-use cost-effective tool for accurate molecular identification and estimation of introgression levels to more effectively monitor and manage A. m. mellifera conservatories.
- High sample throughput genotyping for estimating C-lineage introgression in the dark honeybee: An accurate and cost-effective SNP-based toolPublication . Henriques, Dora; Browne, Keith A.; Barnett, Mark W.; Parejo, Melanie; Kryger, Per; Freeman, Tom C.; Muñoz, Irene; Garnery, Lionel; Highet, Fiona; Johnston, J. Spencer; McCormack, Grace P.; Pinto, M. AliceThe natural distribution of the honeybee (Apis mellifera L.) has been changed by humans in recent decades to such an extent that the formerly widest-spread European subspecies, Apis mellifera mellifera, is threatened by extinction through introgression from highly divergent commercial strains in large tracts of its range. Conservation efforts for A. m. mellifera are underway in multiple European countries requiring reliable and cost-efficient molecular tools to identify purebred colonies. Here, we developed four ancestry-informative SNP assays for high sample throughput genotyping using the iPLEX Mass Array system. Our customized assays were tested on DNA from individual and pooled, haploid and diploid honeybee samples extracted from different tissues using a diverse range of protocols. The assays had a high genotyping success rate and yielded accurate genotypes. Performance assessed against whole-genome data showed that individual assays behaved well, although the most accurate introgression estimates were obtained for the four assays combined (117 SNPs). The best compromise between accuracy and genotyping costs was achieved when combining two assays (62 SNPs). We provide a ready-to-use cost-effective tool for accurate molecular identification and estimation o
- Investigation of free-living honey bee colonies in IrelandPublication . Browne, Keith A.; Hassett, Jack; Geary, Michael; Moore, Elizabeth; Henriques, Dora; Soland-Reckeweg, Gabriele; Ferrari, Roberto; Mac Loughlin, Eoin; O’Brien, Elizabeth; O’Driscoll, Saoirse; Young, Philip; Pinto, M. Alice; McCormack, Grace P.Apis mellifera mellifera (Linnaeus), the Western European honey bee, is considered extinct in the wild over most of its range due largely to hybridisation and replacement by other subspecies, parasitism by Varroa destructor, habitat loss, and effects from agricultural pesticides. The purity of the subspecies within the managed cohort is also at risk over much of its range. Here, we investigated if honey bee colonies inhabited locations outside of the apiaries. In those we located, we explored how long the colony persisted and we investigated the genotypes of the bees using multiple markers. We show here that unmanaged free-living honey bee colonies are present and widespread in Ireland, inhabiting a mixture of nesting habitats with some colonies persisting naturally and unaided over multiple years. Molecular data including mitochondrial, microsatellite, and SNPs evidence indicate that the free-living population sampled is largely comprised of pure A. m. mellifera. Finally, we discuss the implications of conserving free-living A. m. mellifera in Ireland and its possible role in improving the fitness of the managed population both in Ireland and the rest of its European range.
- Investigations into unmanaged honey bee survivor colonies in IrelandPublication . Browne, Keith A.; Henriques, Dora; Hassett, Jack; Geary, Michael; Moore, E.; Pinto, M. Alice; McCormack, Grace P.Unmanaged honey bee colonies of local ecotype surviving without human intervention are likely to form a valuable genetic resource for the sustainability of managed apiaries as well conservation of threatened subspecies. In Ireland, following the Isle of Wight disease (which devastated honey bee colonies at the beginning of the 20th century) and subsequent hybridisation with C lineage bees, there has been a general acceptance by government agencies, scientists, and many beekeepers that no Apis mellifera mellifera (Amm) colonies persisted in the wild. However, sporadic reports were received in 2014/2015 of the existence of unmanaged honey bee colonies. Given that Ireland’s human population is low in density with only 32 persons per square km in some rural areas and only approximately 3000 registered beekeepers, many of whom are reported to not favour purchasing imported bees, it is feasible that honeybees could have naturally adapted to introduced pathogens such as Varroa destructor. We initiated an investigation into the state of unmanaged honey bee colonies and in 2016 we launched a nationwide request through press and social media seeking locations of unmanaged colonies which realised over 170 replies in a short time period. We found that unmanaged colonies have utilised a wide variety of both natural and artificial cavities and survived unaided for periods reported to be from three to over 20 years. Given the difficulty in confirming the authenticity of these timings the survival of individual colonies has been monitored since 2016. Sixty-two of the colonies were sampled and a combined approach using mitochondrial, microsatellite and single nucleotide polymorphism (SNP) genotyping has shown the majority to be pure Apis mellifera mellifera and forming an integral part of the previously described pure Amm population in Ireland. This data, along with survival records for >2 years, and details of surrounding habitat and health of the unmanaged colonies, will be presented.