Modern methods of assessing the taxonomic affiliation of honeybee colonies

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Abstract

At least 30 subspecies of the honeybee Apis mellifera L. were formed allopatrically during the evolution, which spreaded throughout all Africa, Europe and West Asia. The dark forest bee Apis mellifera mellifera is the only and most valuable subspecies for the Northern and Western Europe countries, adapted to productive living in the hard-continental climate of Eurasia. In the past 100 years, natural geographical isolation of subspecies has been disrupted as a result of a human activities. Mass transportations of honeybee colonies beyond the boundaries of their area have been threatened of loss the identity of gene pool of subspecies as a result of hybridization. Preservation of the gene pool of subspecies is possible only when controlling the transportation of honeybee colonies using the methods of identification of taxonomic affiliation of honeybee colonies. Now, dozens of methods have been developed to identify the taxonomic affiliation of honeybee's colony, which are based on the variability of body parts, allozyme loci, mitochondrial DNA loci, microsatellite nuclear loci, sites of single nucleotide polymorphism (SNP). The variability of microsatellite loci and the single nucleotide polymorphism sites have shown the greatest informativeness in identification of the taxonomic affiliation of honeybee's colony.

About the authors

Rustem A. Ilyasov

Institute of Biochemistry and Genetics (IBG)

Author for correspondence.
Email: apismell@hotmail.com
ORCID iD: 0000-0003-2445-4739
SPIN-code: 8302-8152
http://ibg.anrb.ru

Doctor of the sciences, Senior Researcher of Laboratory of Insects’ Biochemistry and Adaptiveness

Russian Federation, 71 Prospect Oktyabrya, IBG, Ufa, 450054

Aleksandr V. Poskryakov

Institute of Biochemistry and Genetics (IBG)

Email: possash@yandex.ru
SPIN-code: 3920-9579
http://ibg.anrb.ru

Ph.D., Senior Researcher of Laboratory of Insects’ Biochemistry and Adaptiveness

Russian Federation, 71 Prospect Oktyabrya, IBG, Ufa, 450054

Aleksei G. Nikolenko

Institute of Biochemistry and Genetics (IBG)

Email: a-nikolenko@yandex.ru
SPIN-code: 1014-4653
http://ibg.anrb.ru

Doctor of the sciences, Professor, Head of Laboratory of Insects’ Biochemistry and Adaptiveness

Russian Federation, 71 Prospect Oktyabrya, IBG, Ufa, 450054

References

  1. Бородачев А.В., Бородачева В.Т. Хозяйственная ценность межпородных помесей // Пчеловодство. – 1982. – № 9. – С. 13–15. [Borodachev AV, Borodacheva VT. Economic value of honeybee crossbreeds. Russian Journal of Beekeeping “Pchelovodstvo”. 1982;(9):13-15. (In Russ.)]
  2. Jensen AB, Palmer KA, Boomsma JJ, Pedersen BV. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology. 2005;14(1):93-106. doi: 10.1111/j.1365-294X.2004.02399.x.
  3. Ruttner F. Biogeography and Taxonomy of Honey bees. Berlin, Heidelberg: Springer-Verlag; 1988.
  4. Ильясов Р.А., Поскряков А.В., Петухов А.В., Николенко А.Г. Локальные популяции Apis mellifera mellifera L. на Урале // Генетика. – 2007. – Т. 43. – № 6. – С. 855–858. [Ilyasov RA, Petukhov AV, Poskryakov AV, Nikolenko AG. Local honeybee (Apis mellifera mellifera L.) populations in the Urals. Russian Journal of Genetics. 2007;43(6):709-711. (In Russ.)]. doi: 10.1134/S1022795407060166.
  5. Ильясов Р.А., Поскряков А.В., Петухов А.В., Николенко А.Г. Новый подход к классификации митотипов темной лесной пчелы Apis mellifera mellifera и иберийской пчелы Apis mellifera iberiensis // Генетика. – 2016. – Т. 52. – № 3. – С. 320–331. doi: 10.7868/S0016675816020053. [Ilyasov RA, Poskryakov AV, Petukhov AV, Nikolenko AG. New approach to the mitotype classification in black honeybee Apis mellifera mellifera and Iberian honeybee Apis mellifera iberiensis. Russian Journal of Genetics. 2016;52(3):281-291. (In Russ.)]. doi: 10.1134/S1022795416020058.
  6. Franck P, Garnery L, Celebrano G, et al. Hybrid origins of honeybees from Italy (Apis mellifera ligustica) and Sicily (A. m. sicula). Molecular Ecology. 2000;9(7):907-21. doi: 10.1046/j.1365-294X.2000.00945.x.
  7. Ильясов Р.А., Поскряков А.В., Николенко А.Г. Митохондриальная ДНК в изучении популяций пчел на Урале // Материалы межрегионального совещания энтомологов Сибири и Дальнего Востока. – Новосибирск, 2006. – С. 72–74. [Ilyasov R, Posryakov A, Nikolenko AG. Mitochondrial DNA in the study of bee populations in the Urals. In Materials of interregional meeting of entomologists of Siberia and the Far East (conference proceedings). Novosibirsk; 2006. P. 72-74. (In Russ.)]
  8. Smith DR. Mitochondrial DNA and honeybee biogeography. In: Smith DR, editor. Diversity in the genus Apis. Boulder, CO: Westview Press; 1991. P. 131-176.
  9. Whitfield CW, Behura SK, Berlocher SH, et al. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science. 2006;314(5799):642-5. doi: 10.1126/science.1132772.
  10. Wallberg A, Han F, Wellhagen G. A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. Nature Genetics. 2014;46:1081-1088.
  11. Harpur B, Chapman N, Krimus L, et al. Assessing patterns of admixture and ancestry in Canadian honey bees. Insectes Sociaux. 2015;62(4):479-489. doi: 10.1007/s00040-015-0427-1.
  12. Алпатов В.В. Породы медоносной пчелы и их использование в сельском хозяйстве. – М.: Московское общество испытателей природы, 1948. – 183 с. [Alpatov VV. Honeybee species and their use in agriculture. Moscow: Moscow Society of Naturalists; 1948. (In Russ.)]
  13. Бояршинов Б.Д., Коробов Н.В., Шураков А.И., и др. В Камском Приуралье // Пчеловодство. – 2001. – № 5. – С. 16–18. [Boyarshinov BD, Korobov NV, Shurakov AI, et al. In the Kama Pre-Urals. Russian Journal of Beekeeping “Pchelovodstvo”. 2001;(5):16-18. (In Russ.)]
  14. Сафиуллин Р.Р. Племенные ресурсы среднерусских пчел Республики Татарстан // Пчеловодство. – 2013. – № 3. – С. 8–9. [Safiullin RR. Tribal resources of the Dark forest bees of the Republic of Tatarstan. Russian Journal of Beekeeping “Pchelovodstvo”. 2013;(3):8-9. (In Russ.)]
  15. Саттаров В.Н., Туктаров В.Р., Борисов И.М., и др. Некоторые аспекты оценки морфометрических признаков медоносной пчелы // Пчеловодство. – 2010. – № 7. – С. 10–11. [Sattarov VN, Tuktarov VR, Borisov IM, et al. Some aspects of assessing the morphometric features of a honey bee. Russian Journal of Beekeeping “Pchelovodstvo”. 2010;(7):10-11. (In Russ.)]
  16. Колбина Л.М., Непейвода С.Н., Ильясов Р.А., и др. Использование морфологических и молекулярно-генетических методов для исследования Apis mellifera // Аграрная наука Евро-Северо-Востока. – 2007. – Т. 2. – № 10. – С. 57–58. [Kolbina LM, Nepeivoda SN, Ilyasov RA, et al. The morphological and molecular genetic methods applied in the researching of Apis mellifera. Agricultural Science of the Euro-North-East. 2007;2(10):57-58. (In Russ.)]
  17. Bookstein FL. Morphometric Tools for Landmark Data, Geometry and Biology. NY, USA: Cambridge University Press; 1991.
  18. Kandemir I, Ozkan A, Fuchs S. Reevaluation of honeybee (Apis mellifera) microtaxonomy: A geometric morphometric approach. Apidologie. 2011;42(5):618-627. doi: 10.1007/s13592-011-0063-3.
  19. Miguel I, Baylac M, Iriondo M, et al. Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie. 2011;42(2):150-161. doi: 10.1051/apido/2010048.
  20. Янбаев Ю.А., Косарев М.Н., Бахтиярова Р.М., Николенко А.Г. Генетические аспекты сохранения биологического разнообразия. – Уфа: БГУ, 2000. – 108 с. [Yanbaev YA, Kosarev MN, Bakhtiyarova RM, Nikolenko AG. Genetic aspects of conservation of biological diversity. Ufa: BSU; 2000. (In Russ.)]
  21. Талипов А.Н., Янбаев Ю.А., Юмагужин Ф.Г. Морфологическая и генетическая изменчивость пчелы медоносной (Apis mellifera mellifera L.) в Башкирском Зауралье. – Уфа: РИО Башкирского государственного университета, 2007. – 110 с. [Talipov AN, Yanbaev YA, Yumaguzhin FG. Morphological and genetic variability of the honey bee (Apis mellifera mellifera L.) in the Bashkir Post-Urals. Ufa: RIO of Bashkir State University; 2007. (In Russ.)]
  22. Smith DR, Glenn TC. Allozyme polymorphisms in Spanish honeybees (Apis mellifera iberica). Journal of Heredity. 1995;86(1):12-16.
  23. Sheppard WS, Berlocher SH. New allozyme variability in Italian honey bees. Journal of Heredity. 1985;76:45-8.
  24. Ivanova E, Staykova T, Petrov P. Allozyme variability in populations of local Bulgarian honey bee. Biotechnology and Biotechnological Equipment. 2010;24(2):371-4.
  25. Del Lama MA, Lobo JA, Soares AEE, Del Lama SN. Genetic differentiation estimated by isozymic analysis of Africanized honey bee populations from Brazil and from Central America. Apidologie. 1990;21:271-280.
  26. Cornuet JM, Piry S, Luikart G, et al. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics. 1999;153:1989-2000.
  27. Gartside DF. Similar allozyme polymorphism in honeybees (Apis mellifera) from different continents. Experientia. 1980;36:649-650.
  28. Lobo JA, Del Lama MA, Mestriner MA. Population differentiation and racial admixture in the Africanized honey bee (Apis mellifera L.). Evolution. 1989;43:794-802.
  29. Sylvester HA. Biochemical genetics. In: Rinderer T, editor. Bee genetics and breeding; Orlando, Florida: Academic Press.; 1986. P. 177-203.
  30. Ashokan KV. Molecular phylogenetic study on Apis mellifera subspecies inferred from cytochrome oxidase I. Indian Journal of Fundamental and Applied Life Sciences. 2011;1(4):193-202.
  31. Arias MC, Sheppard WS. Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution. 2005;37(1):25-35. doi: 10.1016/j.ympev.2005.02.017.
  32. Garnery L, Franck P, Baudry E, et al. Genetic biodiversity of the West European honeybee (Apis mellifera mellifera and Apis mellifera iberica). II. Mitochondrial DNA. Genetics, Selection and Evolution. 1998;30:31-47.
  33. Никоноров Ю.М., Беньковская Г.В., Поскряков А.В., и др. Использование метода ПЦР для контроля чистопородности пчелосемей Apis mellifera mellifera L. в условиях Южного Урала // Генетика. – 1998. – Т. 34. – № 11. – С. 1574–1577. [Nikonorov IM, Ben’kovskaya GV, Poskryakov AV, et al. Use of a PCR method for controlling pure-breeding of honeybees Apis mellifera mellifera L. in the southern Urals. Russian Journal of Genetics. 1998;34(11):1574-1577. (In Russ.)]
  34. Stevanovic J, Stanimirovic Z, Radakovic M, Kovacevic SR. Biogeographic Study of the Honey Bee (Apis mellifera L.) from Serbia, Bosnia and Herzegovina and Republic of Macedonia Based on Mitochondrial DNA Analyses. Russian Journal of Genetics. 2010;46(5):603-9. doi: 10.1134/S1022795410050145.
  35. Hall HG, Smith DR. Distinguishing African and European honey bee matrilines using amplified mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America. 1991;88:4548-4552.
  36. Nielsen DJ, Ebert PR, Page RE, et al. Improved polymerase chain reaction-based mitochondrial genotype assay for identification of the Africanized honey bee (Hymenoptera: Apidae). Annals of Entomological Society of America. 2000;93:1-6.
  37. Crozier YC, Koulianos S, Crozier RH. An improved test for Africanized honeybee mitochondrial DNA. Experientia. 1991;47(9):968-969. doi: 10.1007/BF01929894.
  38. Cánovas F, De la Rúa P, Serrano J, Galián J. Geographical patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). Journal of Zoological Systematics and Evolutionary Research. 2008;46(1):24-30. doi: 10.1111/j.1439-0469.2007.00435.x.
  39. Clarke KE, Rinderer TE, Franck P, et al. The Africanization of honey bees (Apis mellifera L.) of the Yucatan: a study of a massive hybridization event across time. Evolution. 2002;56(7):1462-1474.
  40. Collet T, Ferreira KM, Arias MC, et al. Genetic structure of Africanized honey bee populations (Apis mellifera L.) from Brazil and Uruguay viewed through mitochondrial DNA COI-COII patterns. Heredity. 2006;97:329-335. doi: 10.1038/sj.hdy.6800875.
  41. Munoz I, Henriques D, Johnston JS, et al. Reduced SNP panels for genetic identification and introgression analysis in the dark honey bee (Apis mellifera mellifera). PLoS ONE. 2015;10(4): e0124365. doi: 10.1371/journal.pone.0124365.
  42. Estoup A, Garnery L, Solignac M, Cornuet JM. Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics. 1995;140:679-695.
  43. Solignac M, Vautrin D, Pizzo A, et al. Characterization of microsatellite markers for the apicultural pest Varroa destructor (Acari: Varroidae) and its relatives. Molecular Ecology Notes. 2003;3(4):556-559. doi: 10.1046/j.1471-8286.2003.00510.x.
  44. Островерхова Н.В., Конусова О.Л., Кучер А.Н., и др. Генетическое разнообразие локуса COI–COII мтДНК медоносной пчелы Apis mellifera L. в Томской области // Генетика. – 2015. – Т. 51. – № 1. – С. 89–100. [Ostroverkhova NV, Konusova OL, Kucher AN, et al. Genetic diversity of the locus COI–COII of mitochondrial DNA in honeybee populations (Apis mellifera L.) from the Tomsk region. Russian Journal of Genetics. 2015;51(1):80-90. (In Russ.)]. doi: 10.7868/S0016675815010105.
  45. Форнара М.С. Характеристика аллелофонда и дифференциация пород и популяций медоносной пчелы с использованием микросателлитов: Автореф. дис. … канд. биол. наук. – Дубровицы, 2012. – С. 19. [Fornara MS. Characteristics of allelefund and differentiation of breeds and populations of honey bees using microsatellites. [dissertation] Dubrovitsy: State University of the Russian Academy of Agricultural Sciences; 2012. P. 19. (In Russ.)]
  46. Каскинова М.Д., Ильясов Р.А., Поскряков А.В., Николенко А.Г. Анализ генетической структуры популяций медоносной пчелы (Apis mellifera L.) // Генетика. – 2015. – Т. 51. – № 10. – С. 1199–1202. [Kaskinova MD, Ilyasov RA, Poskryakov AV, Nikolenko AG. Analysis of the genetic structure of honeybee (Apis mellifera L.) populations. Russian Journal of Genetics. 2015;51(10):1033-1035. (In Russ.)]. doi: 10.1134/S1022795415100075.
  47. Зиновьева Н.А., Кривцов Н.И., Форнара М.С. Микросателлиты как инструмент для оценки динамики аллелофонда при создании приокского типа среднерусской породы медоносной пчелы Apis mellifera L. // Сельскохозяйственная биология. – 2011. – № 6. – С. 75–79. [Zinovieva NA, Krivtsov NI, Fornara MS. Microsatellites as a tool for assessing the dynamics of the allele fund when creating the Prioksky type of the Central Russian breed of honey bee Apis mellifera L. Agricultural Biology. 2011;(6):75-79. (In Russ.)]
  48. Калашников А.Е. Изучение дифференциации отечественных популяций медоносной пчелы Apis mellifera и их инфицированности РНК-содержащими вирусами с помощью молекулярно-генетических методов: Автореф. дис. … канд. биол. наук. – Дубровицы, 2013. – С. 21. [Kalashnikov AE. Study of the differentiation of domestic populations of honey bee Apis mellifera and their infection with RNA-containing viruses using molecular genetic methods. [dissertation] Dubrovitsy: State University of the Russian Academy of Agricultural Sciences; 2013. P. 21. (In Russ.)]
  49. Soland-Reckeweg G, Heckel G, Neumann P, et al. Gene flow in admixed populations and implications for the conservation of the Western honeybee, Apis mellifera. Journal of Insect Conservation. 2009;13:317-28. doi: 10.1007/s10841-008-9175-0.
  50. Oleksa A, Chybicki I, Tofilski A, Burczyk J. Nuclear and mitochondrial patterns of introgression into native dark bees (Apis mellifera mellifera) in Poland. Journal of Apicultural Research. 2011;50(2):116-129. doi: 10.3896/IBRA.1.50.2.03.
  51. De la Rúa P, Galián J, Pedersen BV, Serrano J. Molecular characterization and population structure of Apis mellifera from Madeira and the Azores. Apidologie. 2006;37:699-708.
  52. Evans JD, Schwarz RS, Chen YP, et al. Standard methods for molecular research in Apis mellifera. Journal of Apicultural Research. 2013;52(4):1-56. doi: 10.3896/IBRA.1.52.4.11.
  53. Brumfield RT, Beerli P, Nickerson DA, Edwards SV. The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology and Evolution. 2003;18:249-256.
  54. Sobrino B, Brion M, Carracedo A. SNPs in forensic genetics: a review on SNP typing methodologies. Forensic Science International. 2005;154(2-3):181-194.
  55. Pinto MA, Henriques D, Ch’avez-Galarza J, et al. Genetic integrity of the Dark European honey bee (Apis mellifera mellifera) from protected populations: a genome-wide assessment using SNPs and mtDNA sequence data. Journal of Apicultural Research. 2014;53(2):269-278. doi: 10.3896/IBRA.1.53.2.08.
  56. Ильясов Р.А., Поскряков А.В., Николенко А.Г. Новые SNP маркеры в гене вителлогенина VG медоносной пчелы для идентификации Аpis mellifera mellifera L. // Генетика. – 2015. – Т. 51. – № 2. – С. 194–199. doi: 10.7868/S0016675815020083. [Ilyasov RA, Poskryakov AV, Nikolenko AG. New SNP markers of the honeybee vitellogenin gene (VG) used for identification of subspecies Apis mellifera mellifera L. Russian Journal of Genetics. 2015;51(2):163-168. (In Russ.)]. doi: 10.1134/S1022795415020088.
  57. Ильясов, Р. А. Поскряков А.В., Николенко А.Г. Семь генов митохондриального генома, позволяющие дифференцировать подвиды медоносной пчелы Apis mellifera // Генетика. – 2016. – Т. 52. – № 9. – С. 1–9. doi: 10.7868/S001667581609006X. [Ilyasov RA, Poskryakov AV, Nikolenko AG. Seven genes of mitochondrial genome enabling differentiation of honeybee subspecies Apis mellifera. Russian Journal of Genetics. 2016;52(10):1062-1070. (In Russ.)]. doi: 10.1134/S1022795416090064.

Supplementary files

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2. Fig. 1. Differentiation of honeybee subspecies on wing venation pattern by the method of discriminant analysis DAWINO. The points of connection of veins are numbered. FH – wing width, FL – wing length

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3. Fig. 2. Electrophoretic pattern of polymorphic allozyme locus of Malate dehydrogenase MDH in honeybees. FF, SS and FS – genotypes are composed of fast F and slow S alleles

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4. Fig. 3. Amplifed fragments lengths polymorphism of the locus COI-COII mtDNA. Q, PQ, PQQ, PQQQ – variants of DNA sequences, containing a different number of fragments P and Q

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5. Fig. 4. Electrophoretic pattern of variable microsatellite locus A113 in honeybees. 12, 13, 14, 23, 24 – genotypes are composed of 1, 2, 3, 4 alleles

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Copyright (c) 2017 Ilyasov R.A., Poskryakov A.V., Nikolenko A.G.

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