Taxonomical features of the honey bee Apis mellifera

Taxonomic classification of the honey bee (Apis mellifera) is a complex task caused by a number of factors. Among them are hybridization between subspecies, blurred boundaries of their ranges, imperfect identification methods and intense anthropogenic impact. These factors significantly complicate the classification and systematization of subspecies, which makes the problem relevant for research. The article describes the distribution of 30 subspecies of honey bee in six evolutionary lines (A with sublineages Z, M, C and O with X, Y). The species range covers three regions: Africa (11 subspecies), West Asia and the Middle East (7 subspecies), and Europe (12 subspecies). Particular attention is paid to transitional zones, such as the Mediterranean, where hybridization between different subspecies leads to the formation of populations with intermediate morphometric and genetic characteristics, which complicates their systematization. Beekeeping, as an anthropogenic activity, has a significant impact on the spread of subspecies beyond their natural ranges. An example is the introduction of the Italian honeybee (A. m. ligustica) and the Carniolan honeybee (A. m. carnica) to Northern and Western Europe, which caused genetic mixing with populations of the dark forest honeybee (A. m. mellifera). Modern research methods, such as genome sequencing and fragment analysis of microsatellite loci, allow for a detailed analysis of the evolutionary relationships between subspecies. However, the mechanisms of bee adaptation to various environmental conditions are insufficiently studied. Genetic and morphological characteristics of subspecies play a key role in determining their taxonomic status. To preserve the genetic diversity of bees, it is necessary to reduce anthropogenic impact and control hybridization in border zones. This will preserve the unique genetic lines and adaptive abilities of bees, which is of great importance for the conservation of biodiversity and the development of beekeeping.

1. Ilyasov R.A., Lee M.l., Takahashi J.i., Kwon H.W., Nikolenko A.G., A revision of subspecies structure of western honey bee Apis mellifera, Saudi Journal of Biological Sciences, 2020, Vol. 27, No. 12, pp. 3615–3621, DOI: 10.1016/j.sjbs.2020.08.001.

2. Radloff S.E., Hepburn H.R., Fuchs S., Ecological and morphological differentiation of the honeybees, Apis mellifera Linnaeus (Hymenoptera: Apidae), of West Africa, African Entomology, 1998, Vol. 6, pp. 17–23.

3. Chen C., Liu Z., Pan Q., Chen X., Wang H., Guo H., Liu S., Lu H., Tian S., Li R., Shi W., Genomic analyses reveal demographic history and temperate adaptation of the newly discovered honey bee subspecies Apis mellifera sinisxinyuan n. ssp., Molecular Biology and Evolution, 2016, Vol. 33, No. 5, pp. 1337–1348, DOI: 10.1093/molbev/msw017.

4. Linnaeus C., Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, 1758.

5. Buttel-Reepen H., Mitteilungen aus dem zoologischen museum in Berlin, Berlin, Germany: Springer, 1906, 117 p.

6. Skorikov A.S., Eine neue Basis fur eine Revision der Gattung Apis L., Report of the Bureau of Applied Entomology, 1929, Vol. 4, pp. 249–270.

7. Maa T.C., An inquiry into the systematics of the tribus Apidini or honeybees (Hym.), Treubia, 1953, Vol. 21, pp. 525–640.

8. Ruttner F., Biogeography and taxonomy of honeybees, Berlin, Heidelberg: Springer Berlin Heidelberg, 1988, 284 p.

9. Engel M.S., The taxonomy of recent and fossil honey bees (Hymenoptera, Apidae, Apis), Journal of Hymenoptera Research, 1999, Vol. 8, pp. 165–196.

10. Ruttner F., Tassencourt L., Louveaux J., Biometrical statistical analysis of the geographic variability of Apis mellifera L, Apidologie, 1978, Vol. 9, No. 4, pp. 363–382, DOI: 10.1051/apido:19780408.

11. Smith D.R., Mitochondrial DNA and honeybee biogeography, Diversity in the genus Apis, Boulder, CO: Westview Press. 1991, pp. 131–176.

12. Franck P., Garnery L., Loiseau A., Oldroyd B.P., Hepburn H.R., Solignac M., Cornuet J.M., Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data, Heredity, 2001, Vol. 86, No. 4, pp. 420–430, DOI: 10.1046/j.1365-2540.2001.00842.x.

13. Meixner M.D., Pinto M.A., Bouga M., Kryger P., Ivanova E., Fuchs S., Standard methods for characterising subspecies and ecotypes of Apis mellifera, Journal of Apicultural Research, 2013, Vol. 52, No. 4, pp. 1–28, DOI: 10.3896/IBRA.1.52.4.05.

14. Meixner M.D., Arias M.C., Sheppard W.S., Mitochondrial DNA polymorphisms in honey bee subspecies from Kenya, Apidologie, 2000, Vol. 31, No. 2, pp. 181–190, DOI: 10.1051/apido:2000115.

15. Meixner M.D., Leta M.A., Koeniger N., Fuchs S., The honey bees of Ethiopia represent a new subspecies of Apis mellifera - Apis mellifera simensis n. ssp., Apidologie, 2011, Vol. 42, No. 3, pp. 425–437, DOI: 10.1007/s13592-011-0007-y.

16. Arias M.C., Sheppard W.S., Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data, Molecular Phylogenetics and Evolution, 2005, Vol. 37, No. 1, pp. 25–35, DOI: 10.1016/j.ympev.2005.02.017.

17. Ruttner F., Naturgeschichte der Honigbienen, Munich, Germany: Ehrenwirth, 1992, 455 p.

18. Hepburn H.R., Radloff S.E., Honeybees of Africa. Berlin Heidelberg: Springer, 1998, DOI: 10.1007/978-3-662-03604-4.

19. Dukku U.H., Evaluation of morphometric characters of honeybee (Apis mellifera L.) populations in the Lake Chad Basin in Central Africa, Advances in Entomology, 2016, Vol. 4, No. 2, pp. 75–89, DOI: 10.4236/ae.2016.42009.

20. Cornuet J.M., Garnery L., Mitochondrial DNA variability in honeybees and its phylogeographic implications, Apidologie, 1991, Vol. 22, No. 6, pp. 627–642, DOI: 10.1051/apido:19910606.

21. Franck P., Garnery L., Solignac M., Cornuet J.-M., Molecular confirmation of a fourth lineage in honeybees from the Near East, Apidologie, 2000, Vol. 31, No. 2, pp. 167–180, DOI: 10.1051/apido:2000114.

22. Smith D.R., Brown W.M., Polymorphisms in mitochondrial DNA of European and Africanized honeybees (Apis mellifera), Experientia, 1988, Vol. 44, No. 3, pp. 257–260, DOI: 10.1007/BF01941730.

23. Calfee E., Agra M.N., Palacio M.A., Ramírez S.R., Coop G., Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas, PLoS Genetics, 2020, Vol. 16, No. 10, pp. e1009038, DOI: 10.1371/journal.pgen.1009038.

24. Wragg D., Eynard S.E., Basso B., Canale-Tabet K., Labarthe E., Bouchez O., Bienefeld K., Bieńkowska M., Costa C., Gregorc A., Kryger P., Parejo M., Pinto M.A., Bidanel J.P., Servin B., Le Conte Y., Vignal A., Complex population structure and haplotype patterns in the Western European honey bee from sequencing a large panel of haploid drones, Molecular Ecology Resources, 2022, Vol. 22, No. 8, pp. 3068–3086, DOI: 10.1111/1755-0998.13665.

25. Everitt T., Wallberg A., Christmas M.J., Olsson A., Hoffmann W., Neumann P., Webster M.T., The Genomic Basis of Adaptation to High Elevations in Africanized Honey Bees, Genome Biology and Evolution, 2023, Vol. 15, No. 9, pp. evad157, DOI: 10.1093/gbe/evad157.

26. DuPraw E.J., Non-Linnean taxonomy and the systematics of Honeybees, Systematic Zoology, 1965, Vol. 14, No. 1, pp. 1, DOI: 10.2307/2411899.

27. García C.A.Y., Rodrigues P.J., Tofilski A., Elen D., McCormak G.P., Oleksa A., Henriques D., Ilyasov R., Kartashev A., Bargain C., Fried B., Pinto M.A., Using the Software DeepWings(c) to Classify Honey Bees across Europe through Wing Geometric Morphometrics, Insects, 2022, Vol. 13, No. 12, DOI: 10.3390/insects13121132.

28. Miguel I., Baylac M., Iriondo M., Manzano C., Garnery L., Estonba A., Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch, Apidologie, 2011, Vol. 42, No. 2, pp. 150–161, DOI: 10.1051/apido/2010048.

29. Smith D.R., Glenn T.C., Allozyme polymorphisms in Spanish honeybees (Apis mellifera iberica), Journal of Heredity, 1995, Vol. 86, No. 1, pp. 12–16, DOI: 10.1093/oxfordjournals.jhered.a111518.

30. Sheppard W.S., Berlocher S.H., New allozyme variability in Italian honey bees, Journal of Heredity, 1985, Vol. 76, No. 1, pp. 45–48, DOI: 10.1093/oxfordjournals.jhered.a110016.

31. Sheppard W., Arias M., Grech A., Meixner M., Apis mellifera ruttneri, a new honey bee subspecies from Malta, Apidologie, 1997, Vol. 28, No. 1, pp. 287–293, DOI: 10.1051/apido:19970505.

32. Sheppard W.S., Meixner M.D., Apis mellifera pomonella, a new honey bee subspecies from Central Asia, Apidologie, 2003, Vol. 34, No. 1, pp. 367–375, DOI: 10.1051/apido:2003037.

33. Ivanova E.N., Staykova T.A., Petrov P.P., Allozyme variability in populations of local Bulgarian honey bee, Biotechnology and Biotechnological Equipment, 2010, Vol. 24, No. 2, pp. 371–374, DOI: 10.1080/13102818.2010.10817868.

34. Del Lama M.A., Lobo J.A., Soares A.E.E., Del Lama S.N., Genetic differentiation estimated by isozymic analysis of Africanized honey bee populations from Brazil and from Central America, Apidologie, 1990, Vol. 21, No. 4, pp. 271–280, DOI: 10.1051/apido:19900401.

35. Garnery L., Cornuet J.M., Solignac M., Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis, Molecular Ecology, 1992, Vol. 1, No. 3, pp. 145–154, DOI: 10.1111/j.1365-294X.1992.tb00170.x.

36. Tunca R.I., Kence M., Genetic diversity of honey bee (Apis mellifera L.: Hymenoptera: Apidae) populations in Turkey revealed by RAPD markers, African Journal of Agricultural Research, 2011, Vol. 6, No. 29, pp. 6217–6225, DOI: 10.5897/AJAR10.386.

37. Ilyasov R.A., Youn H.G., Lee M.-l., Kim K.W., Proshchalykin M.Y., Lelej A.S., Takahashi J.-i., Kwon H.W., Phylogenetic relationships of Russian Far-East Apis cerana with other North Asian populations, Journal of Apicultural Science, 2019, Vol. 63, No. 2, pp. 289–314, DOI: 10.2478/jas-2019-0024.

38. Whitfield C.W., Behura S.K., Berlocher S.H., Clark A.G., Johnston J.S., Sheppard W.S., Smith D.R., Suarez A.V., Weaver D., Tsutsui N.D., Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera, Science, 2006, Vol. 314, No. 5799, pp. 642–645, DOI: 10.1126/science.1132772.

39. Pinto M.A., Henriques D., Chávez-Galarza J., Kryger P., Garnery L., van der Zee R., Dahle B., Soland-Reckeweg G., de la Rúa P., Dall’ Olio R., Carreck N.L., Johnston J.S., 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, Vol. 53, No. 23, pp. 269–278, DOI: 10.3896/IBRA.1.53.2.08.

40. Wallberg A., Bunikis I., Pettersson O.V., Mosbech M.B., Childers A.K., Evans J.D., Mikheyev A.S., Robertson H.M., Robinson G.E., Webster M.T., A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosomelength scaffolds, BMC Genomics, 2019, Vol. 20, No. 1, pp. 275, DOI: 10.1186/s12864-019-5642-0.

41. Estoup A., Garnery L., Solignac M., Cornuet J.M., Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models, Genetics, 1995, Vol. 140, No. 2, pp. 679–695, DOI: 10.1093/genetics/140.2.679.

42. Franck P., Garnery L., Solignac M., Cornuet J.M., The origin of west European subspecies of honeybees (Apis mellifera): New insights from microsatellite and mitochondrial data, Evolution, 1998, Vol. 52, No. 4, pp. 1119–1134, DOI: 10.1111/j.1558-5646.1998.tb01839.x.

43. Alburaki M., Bertrand B., Legout H., Moulin S., Alburaki A., Sheppard W.S., Garnery L., A fifth major genetic group among honeybees revealed in Syria, BMC Genetics, 2013, Vol. 14, pp. 117, DOI: 10.1186/1471-2156-14-117.

44. Kandemir I., Kence M., Sheppard W.S., Kence A., Mitochondrial DNA variation in honey bee (Apis mellifera L.) populations from Turkey, Journal of Apicultural Research, 2006, Vol. 45, No. 1, pp. 33–38, DOI: 10.1080/00218839.2006.11101310.

45. Techer M.A., Clemencet J., Simiand C., Preeaduth S., Azali H.A., Reynaud B., Helene D., Large-scale mitochondrial DNA analysis of native honey bee Apis mellifera populations reveals a new African subgroup private to the South West Indian Ocean islands, BMC Genetics, 2017, Vol. 18, No. 1, pp. 53, DOI: 10.1186/s12863-017-0520-8.

46. Kandemir I., Kence M., Kence A., Morphometric and electrophoretic variation in different honeybee (Apis mellifera L.) populations, Turkish Journal of Veterinary and Animal Sciences, 2005, Vol. 29, pp. 885–890.

47. Aumer D., Stolle E., Allsopp M., Mumoki F., Pirk C.W.W., Moritz R.F.A., A Single SNP Turns a Social Honey Bee (Apis mellifera) Worker into a Selfish Parasite, Molecular Biology and Evolution, 2019, Vol. 36, No. 3, pp. 516–526, DOI: 10.1093/molbev/msy232.

48. Garnery L., Franck P., Baudry E., Vautrin D., Cornuet J.-M., Solignac M., Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica). II. Microsatellite loci, Genetics Selection Evolution, 1998, Vol. 30, No. 1, pp. 49–74, DOI: 10.1051/gse:19980703.

49. Kumar Y., Khan M.S., Genetic variability of European honey bee, Apis mellifera in mid hills, plains and tarai region of India, African Journal of Biotechnology, 2014, Vol. 13, No. 8, pp. 916–925, DOI: 10.5897/AJB2013.13142.