Authoritative subspecies diagnosis tool for European honey bees based on ancestry informative SNPs

Momeni, Jamal; Parejo, Melanie; Nielsen, Rasmus Oestergaard; Langa, Jorge; Montes, Iratxe; Papoutsis, Laetitia; Farajzadeh, Leila; Berthou, Christian; Căuia, Eliza; Charrière, Jean-Daniel; Coffey, Mary F.; Costa, Cecília; Dall’Olio, Raffaele; Rúa, Pilar De la; Dražić, Marica Maja; Filipi, Janja; Galea, Thomas; Golubovski, Miroljub; Gregorc, Aleš; Grigoryan, Karina; Hatjina, Fani; Il’yasov, R. S.; Ivanova, Evgeniya; Janashia, Irakli; Kandemi̇r, İrfan; Karatasou, Aikaterini; Kekeçoğlu, Meral; Kezic, Nikola; Matray, Enikö Sz; Mifsud, David; Moosbeckhofer, Rudolf; Николенко, А. Г.; Papachristoforou, Alexandros; Petrov, Plamen; Pinto, M. Alice; Poskryakov, A. V.; Sharipov, A; Siceanu, Adrian; Soysal, M. I.; Uzunov, Aleksandar; Zammit-Mangion, Marion; Vingborg, R. K. K.; Bouga, Maria; Kryger, Per; Meixner, Marina D.; Estonba, Andone

doi:10.1186/s12864-021-07379-7

Cited by 36 publications

(30 citation statements)

References 73 publications

(108 reference statements)

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“…In this study, we used only two colonies of A. m. macedonica; therefore, the results related to this subject should be considered preliminary. The distinctness of A. m. carpatica when compared with A. m. carnica and A. m. macedonica was also confirmed by a recent study based on single-nucleotide polymorphism ( [45], Figure S1). However, in another study based on microsatellites, bees from Romania were similar to those from Slovenia ([44], Figure S3).…”

Section: Discussionsupporting

confidence: 76%

“…Earlier studies of A. m. carpatica were based on wing size and the cubital index (which is a ratio of two wing vein lengths of the cubital cell) [39,40]. Later, it was investigated on the basis of mitochondrial DNA [41][42][43], microsatelites [44] and single-nucleotide polymorphism [45]. A. m. carpatica belongs to Lineage C [2,42,46], and it can be identified using molecular methods [45,47].…”

Section: Introductionmentioning

confidence: 99%

“…Later, it was investigated on the basis of mitochondrial DNA [41][42][43], microsatelites [44] and single-nucleotide polymorphism [45]. A. m. carpatica belongs to Lineage C [2,42,46], and it can be identified using molecular methods [45,47]. It differs from other subspecies not only in morphology but also in physiology [48] and behaviour [40].…”

Section: Introductionmentioning

confidence: 99%

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Historical Changes in Honey Bee Wing Venation in Romania

Tofilski

Căuia²,

Siceanu³

et al. 2021

Insects

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The honey bee (Apis mellifera) is an ecologically and economically important species that provides pollination services to natural and agricultural systems. The biodiversity of the honey bee is being endangered by the mass import of non-native queens. In many locations, it is not clear how the local populations have been affected by hybridisation between native and non-native bees. There is especially little information about temporal changes in hybridisation. In Romania, A. m. carpatica naturally occurs, and earlier studies show that there are two subpopulations separated by the Carpathian Mountains. In this study, we investigated how the arrangement of veins in bees’ wings (venation) has changed in Romanian honey bees in the last four decades. We found that in the contemporary population of Romanian bees, there are still clear differences between the intra- and extra-Carpathian subpopulations, which indicates that natural variation among honey bees is still being preserved. We also found significant differences between bees collected before and after 2000. The observed temporal changes in wing venation are most likely caused by hybridisation between native bees and non-native bees sporadically introduced by beekeepers. In order to facilitate conservation and the monitoring of native Romanian bees, we developed a method facilitating their identification.

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Section: Discussionsupporting

confidence: 76%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Historical Changes in Honey Bee Wing Venation in Romania

Tofilski

Căuia²,

Siceanu³

et al. 2021

Insects

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“…Previous works screened narrower discovery panels, suited to the goals being addressed by the constructed assays. While Momeni, et al 58 screened 14 subspecies to construct a ~ 4 K SNP assay for diagnosing European subspecies, others used discovery panels with less than four subspecies to construct high- to medium-density SNP assays tailored for addressing multiple objectives, including analysis of variation linked to defensive behaviour against V. destructor 59 , 60 genomic selection and breeding 60 , identification of Africanised honey bees 61 , 62 , and inference of C-lineage introgression into M-lineage subspecies 42 , 52 , 63 .…”

Section: Discussionmentioning

confidence: 99%

“…By sampling such an important fraction of the A. mellifera diversity, this discovery panel enabled detection of SNPs with low frequency of the minor allele (average MAF = 0.19), therefore minimizing ascertainment bias 57 . With the exception of the recently published study of Momeni, et al 58 , this is the largest and broadest panel used for SNP discovery in the honey bee. Previous works screened narrower discovery panels, suited to the goals being addressed by the constructed assays.…”

Section: Discussionmentioning

confidence: 99%

A SNP assay for assessing diversity in immune genes in the honey bee (Apis mellifera L.)

Henriques

Lopes

Chejanovsky

et al. 2021

Sci Rep

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With a growing number of parasites and pathogens experiencing large-scale range expansions, monitoring diversity in immune genes of host populations has never been so important because it can inform on the adaptive potential to resist the invaders. Population surveys of immune genes are becoming common in many organisms, yet they are missing in the honey bee (Apis mellifera L.), a key managed pollinator species that has been severely affected by biological invasions. To fill the gap, here we identified single nucleotide polymorphisms (SNPs) in a wide range of honey bee immune genes and developed a medium-density assay targeting a subset of these genes. Using a discovery panel of 123 whole-genomes, representing seven A. mellifera subspecies and three evolutionary lineages, 180 immune genes were scanned for SNPs in exons, introns (< 4 bp from exons), 3’ and 5´UTR, and < 1 kb upstream of the transcription start site. After application of multiple filtering criteria and validation, the final medium-density assay combines 91 quality-proved functional SNPs marking 89 innate immune genes and these can be readily typed using the high-sample-throughput iPLEX MassARRAY system. This medium-density-SNP assay was applied to 156 samples from four countries and the admixture analysis clustered the samples according to their lineage and subspecies, suggesting that honey bee ancestry can be delineated from functional variation. In addition to allowing analysis of immunogenetic variation, this newly-developed SNP assay can be used for inferring genetic structure and admixture in the honey bee.

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Identification of runs of homozygosity in Western honey bees (Apis mellifera) using whole‐genome sequencing data

Gmel

Guichard

Dainat

et al. 2023

Ecology and Evolution

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Runs of homozygosity (ROH) are continuous homozygous segments that arise through the transmission of haplotypes that are identical by descent. The length and distribution of ROH segments provide insights into the genetic diversity of populations and can be associated with selection signatures. Here, we analyzed reconstructed whole‐genome queen genotypes, from a pool‐seq data experiment including 265 Western honeybee colonies from Apis mellifera mellifera and Apis mellifera carnica. Integrating individual ROH patterns and admixture levels in a dynamic population network visualization allowed us to ascertain major differences between the two subspecies. Within A. m. mellifera, we identified well‐defined substructures according to the genetic origin of the queens. Despite the current applied conservation efforts, we pinpointed 79 admixed queens. Genomic inbreeding (FROH) strongly varied within and between the identified subpopulations. Conserved A. m. mellifera from Switzerland had the highest mean FROH (3.39%), while queens originating from a conservation area in France, which were also highly admixed, showed significantly lower FROH (0.45%). The majority of A. m. carnica queens were also highly admixed, except 12 purebred queens with a mean FROH of 2.33%. Within the breed‐specific ROH islands, we identified 14 coding genes for A. m. mellifera and five for A. m. carnica, respectively. Local adaption of A. m. mellifera could be suggested by the identification of genes involved in the response to ultraviolet light (Crh‐BP, Uvop) and body size (Hex70a, Hex70b), while the A. m. carnica specific genes Cpr3 and Cpr4 are most likely associated with the lighter striping pattern, a morphological phenotype expected in this subspecies. We demonstrated that queen genotypes derived from pooled workers are useful tool to unravel the population dynamics in A. mellifera and provide fundamental information to conserve native honey bees.

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Authoritative subspecies diagnosis tool for European honey bees based on ancestry informative SNPs

Cited by 36 publications

References 73 publications

Historical Changes in Honey Bee Wing Venation in Romania

Historical Changes in Honey Bee Wing Venation in Romania

A SNP assay for assessing diversity in immune genes in the honey bee (Apis mellifera L.)

Identification of runs of homozygosity in Western honey bees (Apis mellifera) using whole‐genome sequencing data

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