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Wallberg, Andreas
Publications (10 of 30) Show all publications
Wallberg, A., Bunikis, I., Vinnere, O., Mosbech, M.-B., Childers, A. K., Evans, J. D., . . . Webster, M. T. (2019). A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds. BMC Genomics, 20, Article ID 275.
Open this publication in new window or tab >>A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds
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2019 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 20, article id 275Article in journal (Refereed) Published
Abstract [en]

Background

The ability to generate long sequencing reads and access long-range linkage information is revolutionizing the quality and completeness of genome assemblies. Here we use a hybrid approach that combines data from four genome sequencing and mapping technologies to generate a new genome assembly of the honeybee Apis mellifera. We first generated contigs based on PacBio sequencing libraries, which were then merged with linked-read 10x Chromium data followed by scaffolding using a BioNano optical genome map and a Hi-C chromatin interaction map, complemented by a genetic linkage map.

Results

Each of the assembly steps reduced the number of gaps and incorporated a substantial amount of additional sequence into scaffolds. The new assembly (Amel_HAv3) is significantly more contiguous and complete than the previous one (Amel_4.5), based mainly on Sanger sequencing reads. N50 of contigs is 120-fold higher (5.381 Mbp compared to 0.053 Mbp) and we anchor >98% of the sequence to chromosomes. All of the 16 chromosomes are represented as single scaffolds with an average of three sequence gaps per chromosome. The improvements are largely due to the inclusion of repetitive sequence that was unplaced in previous assemblies. In particular, our assembly is highly contiguous across centromeres and telomeres and includes hundreds of AvaI and AluI repeats associated with these features.

Conclusions

The improved assembly will be of utility for refining gene models, studying genome function, mapping functional genetic variation, identification of structural variants, and comparative genomics.

Place, publisher, year, edition, pages
BMC, 2019
Keywords
Genome assembly, Single-molecule real-time (SMRT) sequencing, Linked-read sequencing, Optical mapping, Hi-C, Telomeres, Centromeres
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-382559 (URN)10.1186/s12864-019-5642-0 (DOI)000464118800001 ()30961563 (PubMedID)
Funder
Swedish Research Council Formas, 2013-722Swedish Research Council, 2014-5096
Note

Andreas Wallberg and Ignas Bunikis contributed equally to this work.

Available from: 2019-05-03 Created: 2019-05-03 Last updated: 2019-05-03Bibliographically approved
Christmas, M. J., Wallberg, A., Bunikis, I., Olsson, A., Wallerman, O. & Webster, M. T. (2019). Chromosomal inversions associated with environmental adaptation in honeybees. Molecular Ecology, 28(6), 1358-1374
Open this publication in new window or tab >>Chromosomal inversions associated with environmental adaptation in honeybees
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 6, p. 1358-1374Article in journal (Refereed) Published
Abstract [en]

Chromosomal inversions can facilitate local adaptation in the presence of gene flow by suppressing recombination between well-adapted native haplotypes and poorly adapted migrant haplotypes. East African mountain populations of the honeybee Apis mellifera are highly divergent from neighbouring lowland populations at two extended regions in the genome, despite high similarity in the rest of the genome, suggesting that these genomic regions harbour inversions governing local adaptation. Here, we utilize a new highly contiguous assembly of the honeybee genome to characterize these regions. Using whole-genome sequencing data from 55 highland and lowland bees, we find that the highland haplotypes at both regions are present at high frequencies in three independent highland populations but extremely rare elsewhere. The boundaries of both divergent regions are characterized by regions of high homology with each other positioned in opposite orientations and contain highly repetitive, long inverted repeats with homology to transposable elements. These regions are likely to represent inversion breakpoints that participate in nonallelic homologous recombination. Using long-read data, we confirm that the lowland samples are contiguous across breakpoint regions. We do not find evidence for disruption of functional sequence by these breakpoints, which suggests that the inversions are likely maintained due to their allelic content conferring local adaptation in highland environments. Finally, we identify a third divergent genomic region, which contains highly divergent segregating haplotypes that also may contain inversion variants under selection. The results add to a growing body of evidence indicating the importance of chromosomal inversions in local adaptation.

Place, publisher, year, edition, pages
WILEY, 2019
Keywords
chromosomal inversion, honeybee, local adaptation, long-read sequencing, nonallelic homologous recombination, structural variation
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-383207 (URN)10.1111/mec.14944 (DOI)000465219200012 ()30431193 (PubMedID)
Funder
Swedish Research Council Formas, 2013-722Swedish Research Council, 2014-5096
Available from: 2019-05-23 Created: 2019-05-23 Last updated: 2019-08-12Bibliographically approved
Jones, J. C., Wallberg, A., Christmas, M., Kapheim, K. M. & Webster, M. T. (2019). Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee. Molecular biology and evolution, 36(10), 2277-2291
Open this publication in new window or tab >>Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee
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2019 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 36, no 10, p. 2277-2291Article in journal (Refereed) Published
Abstract [en]

Social insect genomes exhibit the highest rates of crossing over observed in plants and animals. The evolutionary causes of these extreme rates are unknown. Insight can be gained by comparing recombination rate variation across the genomes of related social and solitary insects. Here, we compare the genomic recombination landscape of the highly social honey bee, Apis mellifera, with the solitary alfalfa leafcutter bee, Megachile rotundata, by analyzing patterns of linkage disequilibrium in population-scale genome sequencing data. We infer that average recombination rates are extremely elevated in A. mellifera compared with M. rotundata. However, our results indicate that similar factors control the distribution of crossovers in the genomes of both species. Recombination rate is significantly reduced in coding regions in both species, with genes inferred to be germline methylated having particularly low rates. Genes with worker-biased patterns of expression in A. mellifera and their orthologs in M. rotundata have higher than average recombination rates in both species, suggesting that selection for higher diversity in genes involved in worker caste functions in social taxa is not the explanation for these elevated rates. Furthermore, we find no evidence that recombination has modulated the efficacy of selection among genes during bee evolution, which does not support the hypothesis that high recombination rates facilitated positive selection for new functions in social insects. Our results indicate that the evolution of sociality in insects likely entailed selection on modifiers that increased recombination rates genome wide, but that the genomic recombination landscape is determined by the same factors.

Keywords
Apis mellifera, Megachile rotundata, Hymenoptera, linkage disequilibrium, recombination, social insect
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-401336 (URN)10.1093/molbev/msz130 (DOI)000501734200016 ()31143942 (PubMedID)
Funder
Swedish Research Council, 2014-5096Swedish Research Council Formas, 2013-722
Available from: 2020-01-07 Created: 2020-01-07 Last updated: 2020-01-17Bibliographically approved
Philippe, H., Poustka, A. J., Chiodin, M., Hoff, K. J., Dessimoz, C., Tomiczek, B., . . . Telford, M. J. (2019). Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria. Current Biology, 29(11), 1818-1826.e6
Open this publication in new window or tab >>Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria
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2019 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 29, no 11, p. 1818-1826.e6Article in journal (Refereed) Published
Abstract [en]

Xenoturbella and the acoelomorph worms (Xenacoe-lomorpha) are simple marine animals with controversial affinities. They have been placed as the sister group of all other bilaterian animals (Nephrozoa hypothesis), implying their simplicity is an ancient characteristic [1, 2]; alternatively, they have been linked to the complex Ambulacraria (echinoderms and hemichordates) in a Glade called the Xenambulacraria [3,5], suggesting their simplicity evolved by reduction from a complex ancestor. The difficulty resolving this problem implies the phylogenetic signal supporting the correct solution is weak and affected by inadequate modeling, creating a misleading non-phylogenetic signal. The idea that the Nephrozoa hypothesis might be an artifact is prompted by the faster molecular evolutionary rate observed within the Acoelomorpha. Unequal rates of evolution are known to result in the systematic artifact of long branch attraction, which would be predicted to result in an attraction between long-branch acoelomorphs and the outgroup, pulling them toward the root [6]. Other biases inadequately accommodated by the models used can also have strong effects, exacerbated in the context of short internal branches and long terminal branches [7]. We have assembled a large and informative dataset to address this problem. Analyses designed to reduce or to emphasize misleading signals show the Nephrozoa hypothesis is supported under conditions expected to exacerbate errors, and the Xenambulacraria hypothesis is preferred in conditions designed to reduce errors. Our reanalyses of two other recently published datasets [1, 2] produce the same result. We conclude that the Xenacoelomorpha are simplified relatives of the Ambulacraria.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-389606 (URN)10.1016/j.cub.2019.04.009 (DOI)000470902000041 ()31104936 (PubMedID)
Funder
EU, European Research Council, ERC-2012-AdG 322790
Available from: 2019-07-23 Created: 2019-07-23 Last updated: 2019-07-23Bibliographically approved
Kawakami, T., Wallberg, A., Olsson, A., Wintermantel, D., de Miranda, J. R., Allsopp, M., . . . Webster, M. T. (2019). Substantial Heritable Variation in Recombination Rate on Multiple Scales in Honeybees and Bumblebees. Genetics, 212(4), 1101-1119
Open this publication in new window or tab >>Substantial Heritable Variation in Recombination Rate on Multiple Scales in Honeybees and Bumblebees
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2019 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 212, no 4, p. 1101-1119Article in journal (Refereed) Published
Abstract [en]

Meiotic recombination shuffles genetic variation and promotes correct segregation of chromosomes. Rates of recombination vary on several scales, both within genomes and between individuals, and this variation is affected by both genetic and environmental factors. Social insects have extremely high rates of recombination, although the evolutionary causes of this are not known. Here, we estimate rates of crossovers and gene conversions in 22 colonies of the honeybee, Apis mellifera, and 9 colonies of the bumblebee, Bombus terrestris, using direct sequencing of 299 haploid drone offspring. We confirm that both species have extremely elevated crossover rates, with higher rates measured in the highly eusocial honeybee than the primitively social bumblebee. There are also significant differences in recombination rate between subspecies of honeybee. There is substantial variation in genome-wide recombination rate between individuals of both A. mellifera and B. terrestris and the distribution of these rates overlap between species. A large proportion of interindividual variation in recombination rate is heritable, which indicates the presence of variation in trans-acting factors that influence recombination genome-wide. We infer that levels of crossover interference are significantly lower in honeybees compared to bumblebees, which may be one mechanism that contributes to higher recombination rates in honeybees. We also find a significant increase in recombination rate with distance from the centromere, mirrored by methylation differences. We detect a strong transmission bias due to GC-biased gene conversion associated with noncrossover gene conversions. Our results shed light on the mechanistic causes of extreme rates of recombination in social insects and the genetic architecture of recombination rate variation.

Place, publisher, year, edition, pages
GENETICS SOCIETY AMERICA, 2019
Keywords
Recombination, honeybee, bumblebee, crossing over, evolution of sociality
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-393827 (URN)10.1534/genetics.119.302008 (DOI)000482224900009 ()31152071 (PubMedID)
Funder
Swedish Research Council, 2014-6325Swedish Research Council, 2014-5096Swedish Research Council, 2018-03896
Available from: 2019-10-02 Created: 2019-10-02 Last updated: 2019-10-02Bibliographically approved
Montero-Mendieta, S., Tan, K., Christmas, M., Olsson, A., Vila, C., Wallberg, A. & Webster, M. T. (2019). The genomic basis of adaptation to high-altitude habitats in the eastern honey bee (Apis cerana). Molecular Ecology, 28(4), 746-760
Open this publication in new window or tab >>The genomic basis of adaptation to high-altitude habitats in the eastern honey bee (Apis cerana)
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 4, p. 746-760Article in journal (Refereed) Published
Abstract [en]

The eastern honey bee (Apis cerana) is of central importance for agriculture in Asia. It has adapted to a wide variety of environmental conditions across its native range in southern and eastern Asia, which includes high-altitude regions. eastern honey bees inhabiting mountains differ morphologically from neighbouring lowland populations and may also exhibit differences in physiology and behaviour. We compared the genomes of 60 eastern honey bees collected from high and low altitudes in Yunnan and Gansu provinces, China, to infer their evolutionary history and to identify candidate genes that may underlie adaptation to high altitude. Using a combination of F-ST-based statistics, long-range haplotype tests and population branch statistics, we identified several regions of the genome that appear to have been under positive selection. These candidate regions were strongly enriched for coding sequences and had high haplotype homozygosity and increased divergence specifically in highland bee populations, suggesting they have been subjected to recent selection in high-altitude habitats. Candidate loci in these genomic regions included genes related to reproduction and feeding behaviour in honey bees. Functional investigation of these candidate loci is necessary to fully understand the mechanisms of adaptation to high-altitude habitats in the eastern honey bee.

Place, publisher, year, edition, pages
WILEY, 2019
Keywords
altitude adaptation, genetic differentiation, honeybees, local adaptation, positive selection, selective sweeps
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-379270 (URN)10.1111/mec.14986 (DOI)000459814500005 ()30576015 (PubMedID)
Funder
Swedish Research Council Formas, 2013-722Swedish Research Council, 2014-5096
Available from: 2019-03-18 Created: 2019-03-18 Last updated: 2019-06-10Bibliographically approved
Buckland-Nicks, J., Lundin, K. & Wallberg, A. (2019). The sperm of Xenacoelomorpha revisited: implications for theevolution of early bilaterians. Zoomorphology, 138(1), 13-27
Open this publication in new window or tab >>The sperm of Xenacoelomorpha revisited: implications for theevolution of early bilaterians
2019 (English)In: Zoomorphology, ISSN 0720-213X, E-ISSN 1432-234X, Vol. 138, no 1, p. 13-27Article in journal (Refereed) Published
Abstract [en]

Sperm structure of the Xenacoelomorpha (Acoelomorpha plus Xenoturbellida) is updated in the light of new discoveries or new interpretations of existing data. Nemertodermatida and Acoela (Acoelomorpha) have introsperm with certain basic features in common, but all acoels lack acrosomes and usually have two flagella with unusual combinations of microtubules, whereas all nemertodermatids have small, simple acrosomes and a typical 9+2 flagellum. Xenoturbellida is currently considered as the sister taxon to Acoelomorpha. Xenoturbella bocki has an aquasperm that has almost nothing in common with the sperm of Acoelomorpha. We argue that the aquasperm ultrastructure of X. bocki has much in common with sperm of hemichordates and to some extent echinoderms, which was previously disputed. Molecular analyses have on the one hand supported a connection with deuterostomes but on the other hand have negated it, suggesting that the closest common ancestor of Xenacoelomorpha is either the Nephrozoa, Deuterostomia or Protostomia. Sperm structure is highly diverse among Xenacoelomorpha, with protostome-like traits in Acoelomorpha and deuterostome-like traits in Xenoturbella. Assuming Xenacoelomorph monophyly and ancestral introsperm in this taxon, however, suggests that the re-expression of the aquasperm form of Xenoturbella, involving some key changes in sperm morphology, is a secondarily derived state that could have occurred through progenetic spermiogenesis with the precocious development of round spermatids to maturity.

Place, publisher, year, edition, pages
SPRINGER, 2019
Keywords
Spermatozoa, Ultrastructure, Nemertodermatida, Acoela, Xenoturbella, Phylogeny, Bilateria
National Category
Biological Systematics
Identifiers
urn:nbn:se:uu:diva-379577 (URN)10.1007/s00435-018-0425-8 (DOI)000459514600002 ()
Available from: 2019-04-12 Created: 2019-04-12 Last updated: 2019-04-12Bibliographically approved
Henriques, D., Parejo, M., Vignal, A., Wragg, D., Wallberg, A., Webster, M. T. & Pinto, M. A. (2018). Developing reduced SNP assays from whole-genome sequence data to estimate introgression in an organism with complex genetic patterns, the Iberian honeybee (Apis mellifera iberiensis). Evolutionary Applications, 11(8), 1270-1282
Open this publication in new window or tab >>Developing reduced SNP assays from whole-genome sequence data to estimate introgression in an organism with complex genetic patterns, the Iberian honeybee (Apis mellifera iberiensis)
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2018 (English)In: Evolutionary Applications, ISSN 1752-4571, E-ISSN 1752-4571, Vol. 11, no 8, p. 1270-1282Article in journal (Refereed) Published
Abstract [en]

The most important managed pollinator, the honeybee (Apis mellifera L.), has been subject to a growing number of threats. In western Europe, one such threat is large-scale introductions of commercial strains (C-lineage ancestry), which is leading to introgressive hybridization and even the local extinction of native honeybee populations (M-lineage ancestry). Here, we developed reduced assays of highly informative SNPs from 176 whole genomes to estimate C-lineage introgression in the most diverse and evolutionarily complex subspecies in Europe, the Iberian honeybee (Apis mellifera iberiensis). We started by evaluating the effects of sample size and sampling a geographically restricted area on the number of highly informative SNPs. We demonstrated that a bias in the number of fixed SNPs (F-ST=1) is introduced when the sample size is small (N10) and when sampling only captures a small fraction of a population's genetic diversity. These results underscore the importance of having a representative sample when developing reliable reduced SNP assays for organisms with complex genetic patterns. We used a training data set to design four independent SNP assays selected from pairwise F-ST between the Iberian and C-lineage honeybees. The designed assays, which were validated in holdout and simulated hybrid data sets, proved to be highly accurate and can be readily used for monitoring populations not only in the native range of A.m.iberiensis in Iberia but also in the introduced range in the Balearic islands, Macaronesia and South America, in a time- and cost-effective manner. While our approach used the Iberian honeybee as model system, it has a high value in a wide range of scenarios for the monitoring and conservation of potentially hybridized domestic and wildlife populations.

Place, publisher, year, edition, pages
WILEY, 2018
Keywords
Apis mellifera iberiensis, fixation index, informative SNPs, reduced SNP assays
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-362481 (URN)10.1111/eva.12623 (DOI)000442210300007 ()30151039 (PubMedID)
Available from: 2018-10-10 Created: 2018-10-10 Last updated: 2018-10-10Bibliographically approved
Henriques, D., Wallberg, A., Chavez-Galarza, J., Johnston, J. S., Webster, M. T. & Alice Pinto, M. (2018). Whole genome SNP-associated signatures of local adaptation in honeybees of the Iberian Peninsula. Scientific Reports, 8, Article ID 11145.
Open this publication in new window or tab >>Whole genome SNP-associated signatures of local adaptation in honeybees of the Iberian Peninsula
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2018 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 11145Article in journal (Refereed) Published
Abstract [en]

The availability of powerful high-throughput genomic tools, combined with genome scans, has helped identifying genes and genetic changes responsible for environmental adaptation in many organisms, including the honeybee. Here, we resequenced 87 whole genomes of the honeybee native to Iberia and used conceptually different selection methods (Sam beta ada, LFMM, PCAdapt, iHs) together with in sillico protein modelling to search for selection footprints along environmental gradients. We found 670 outlier SNPs, most of which associated with precipitation, longitude and latitude. Over 88.7% SNPs laid outside exons and there was a significant enrichment in regions adjacent to exons and UTRs. Enrichment was also detected in exonic regions. Furthermore, in silico protein modelling suggests that several non-synonymous SNPs are likely direct targets of selection, as they lead to amino acid replacements in functionally important sites of proteins. We identified genomic signatures of local adaptation in 140 genes, many of which are putatively implicated in fitness-related functions such as reproduction, immunity, olfaction, lipid biosynthesis and circadian clock. Our genome scan suggests that local adaptation in the Iberian honeybee involves variations in regions that might alter patterns of gene expression and in protein-coding genes, which are promising candidates to underpin adaptive change in the honeybee.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2018
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-361681 (URN)10.1038/s41598-018-29469-5 (DOI)000439550200017 ()30042407 (PubMedID)
Available from: 2018-10-05 Created: 2018-10-05 Last updated: 2018-10-05Bibliographically approved
Nelson, R. M., Wallberg, A., Paulino Simoes, Z. L., Lawson, D. J. & Webster, M. T. (2017). Genomewide analysis of admixture and adaptation in the Africanized honeybee. Molecular Ecology, 26(14), 3603-3617
Open this publication in new window or tab >>Genomewide analysis of admixture and adaptation in the Africanized honeybee
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2017 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 26, no 14, p. 3603-3617Article in journal (Refereed) Published
Abstract [en]

Genetic exchange by hybridization or admixture can make an important contribution to evolution, and introgression of favourable alleles can facilitate adaptation to new environments. A small number of honeybees (Apis mellifera) with African ancestry were introduced to Brazil similar to 60 years ago, which dispersed and hybridized with existing managed populations of European origin, quickly spreading across much of the Americas in an example of a massive biological invasion. Here, we analyse whole-genome sequences of 32 Africanized honeybees sampled from throughout Brazil to study the effect of this process on genome diversity. By comparison with ancestral populations from Europe and Africa, we infer that these samples have 84% African ancestry, with the remainder from western European populations. However, this proportion varies across the genome and we identify signals of positive selection in regions with high European ancestry proportions. These observations are largely driven by one large gene-rich 1.4-Mbp segment on chromosome 11 where European haplotypes are present at a significantly elevated frequency and likely confer an adaptive advantage in the Africanized honeybee population. This region has previously been implicated in reproductive traits and foraging behaviour in worker bees. Finally, by analysing the distribution of ancestry tract lengths in the context of the known time of the admixture event, we are able to infer an average generation time of 2.0 years. Our analysis highlights the processes by which populations of mixed genetic ancestry form and adapt to new environments.

Keywords
adaptation, admixture, Africanized honeybee, biological invasion, introgression, natural selection
National Category
Evolutionary Biology Biochemistry and Molecular Biology Ecology
Identifiers
urn:nbn:se:uu:diva-330033 (URN)10.1111/mec.14122 (DOI)000404618000004 ()
Funder
Swedish Research Council, 2014-5096Swedish Research Council Formas, 2013-722Science for Life Laboratory - a national resource center for high-throughput molecular bioscience, 2014/R2-49Carl Tryggers foundation , CTS14:508
Available from: 2017-09-29 Created: 2017-09-29 Last updated: 2017-09-29Bibliographically approved
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