Skip to main content
SpringerLink
Log in

Genetic Properties and Evolution of Asian Honey Bee Apis cerana ussuriensis from Primorsky Krai, Russia

  • ANIMAL GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Apis cerana ussuriensis Ilyasov et al., 2019 is the northernmost subspecies of the Asian honey bee A. cerana Fabricius, 1793, common in the forests of Primorsky krai and Khabarovsk krai as far as 47°54′ N. Genetic studies of this subspecies are of great interest for science and apiculture, since all its adaptive traits were formed under the influence of the natural environment without human interference. We sequenced and annotated the complete mitochondrial DNA (mtDNA) sequences of bees of subspecies Apis cerana ussuriensis Ilyasov et al., 2019 (GenBank accession number AP018450) from Primorsky krai and Apis cerana koreana Ilyasov et al., 2019 (AP018431) from South Korea, as well as six exons of the nuclear DNA (nDNA) vitellogenin VG E2–E7 gene of bee subspecies A. c. ussuriensis, A. c. koreana, A. c. japonica Radoszkowski, 1887, A. c. cerana, and A. c. indica Fabricius, 1798. Cluster analysis of the mtDNA and the nDNA VG gene sequences showed the division of bees into two groups, the southern subspecies A. c. indica and the northern subspecies A. c. ussuriensis, A. c. koreana, A. c. japonica, and A. c. cerana. On the basis of the genetic divergence, we showed that subspecies A. c. ussuriensis was genetically closer to subspecies A. c. japonica, A. c. koreana, and A. c. cerana than to subspecies A. c. indica. Values of genetic divergence (0.80–8.00%) and Jukes–Cantor genetic distance (0.005–0.100) for mtDNA and nDNA VG gene between subspecies A. c. ussuriensis, A. c. koreana, A. c. japonica, A. c. cerana, and A. c. indica are within the range of intraspecific differences between insect subspecies. The estimated time of the emergence of the A. cerana subspecies is from two to one million years ago.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Ruttner, F., Breeding Techniques and Selection for Breeding of the Honeybee, Derby, UK: British Isles Bee Breeders Association, 1988.

    Google Scholar 

  2. Proshchalykin, M.Yu., Novomodnyi, E.V., Bezborodov, V.G., and Koshkin, E.S., The first modern findings of a wax bee Apis cerana Fabricius, 1793 (Hymenoptera, Apidae) in Khabarovsk Krai, Evras. Entomol. Zh., 2014, vol. 13, no. 3, pp. 295—298.

    Google Scholar 

  3. Kuznetsov, V.N., Kitaiskaya voskovaya pchela Apis cerana cerana F. (Hymenoptera, Apidae) na Dal’nem Vostoke Rossii (Chinese Wax Bee, Apis cerana cerana F. (Hymenoptera, Apidae) in the Russian Far East), Moscow: KMK, 2005.

  4. Behura, S.K., Analysis of nuclear copies of mitochondrial sequences in honeybee (Apis mellifera) genome, Mol. Biol. Evol., 2007, vol. 24, no. 7, pp. 1492—1505. https://doi.org/10.1093/molbev/msm068

    Article  CAS  PubMed  Google Scholar 

  5. Choi, Y.S., Lee, M.Y., Hong, I.P., et al., Occurrence of sacbrood virus in Korean apiaries from Apis cerana (Hymenoptera: Apidae), J. Apic., 2010, vol. 25, no. 3, pp. 187—191.

    Google Scholar 

  6. Koetz, A.H., Ecology, behaviour and control of Apis cerana with a focus on relevance to the Australian incursion, Insects, 2013, vol. 4, no. 4, pp. 558—592. https://doi.org/10.3390/insects4040558

    Article  PubMed  PubMed Central  Google Scholar 

  7. Vung, N., Lee, M.-L., Lee, M.-Y., et al., Breeding and selection for resistance to sacbrood virus for Apis cerana, J. Apic., 2017, vol. 32, pp. 345—352. https://doi.org/10.17519/apiculture.2017.11.32.4.345

    Article  Google Scholar 

  8. Pesenko, Yu.A., Lelei, A.S., Radchenko, V.G., and Filatkin, G.N., Chinese wax bee Apis cerana cerana F. (Hymenoptera, Apidae) in the Soviet Far East, Entomol. Obozr., 1989, vol. 68, no. 3, pp. 527—548.

    Google Scholar 

  9. Zhuang, D., New subspecies of Apis cerana (in Chinese), Southwest China J. Agric. Sci., 1989, vol. 2, pp. 61—65.

    Google Scholar 

  10. Zhen-Ming, J., Yang, G., Huang, S., et al., The advancement of beekeeping science and technology in China, Honeybees in Mountain Agriculture, Verma, L.R., Ed., New Delhi: Oxford and IBH Publ., 1992.

    Google Scholar 

  11. Diniz-Filho, J.A.F., Malapsina, O., and Pignata, M.I.B., Geographic variation in Apis cerana indica F.: a spatial autocorrelation analysis of morphometric patterns, J. Apic. Res., 1993, vol. 32, pp. 65—72. https://doi.org/10.1080/00218839.1993.11101289

    Article  Google Scholar 

  12. Engel, M.S., The taxonomy of recent and fossil honey bees (Hymenoptera, Apidae, Apis), J. Hymenoptera Res., 1999, vol. 8, no. 2, pp. 165—196. https://doi.org/10.1007/978-1-4614-4960-718

    Article  Google Scholar 

  13. Sugawara, M., Feral colonies of Japanese honey bees, Apis cerana japonica and their life history: 2. Natural nests and swarming, Mitsubachi Kagaku (Honeybee Sci.), 2000, vol. 21, no. 1, pp. 35—39.

    Google Scholar 

  14. Hepburn, H.R., Smith, D.R., Radloff, S.E., and Otis, G.W., Infraspecific categories of Apis cerana: morphometric, allozymal and mtDNA diversity, Apidologie, 2001, vol. 32, no. 1, pp. 3—23. https://doi.org/10.1051/apido:2001108

    Article  CAS  Google Scholar 

  15. Takahashi, J. and Yoshida, T., The origin of Japanese honey bee Apis cerana japonica inferred from mitochondrial DNA, Mitsubachi Kagaku (Honeybee Sci.), 2003, vol. 24, no. 2, pp. 71—76.

    CAS  Google Scholar 

  16. Radloff, S.E., Hepburn, C., Hepburn, R.H., et al., Population structure and classification of Apis cerana, Apidologie, 2010, vol. 41, no. 6, pp. 589—601. https://doi.org/10.1051/apido/2010008

    Article  Google Scholar 

  17. Takahashi, J., Wakamiya, T., Kiyoshi, T., et al., The complete mitochondrial genome of the Japanese honeybee, Apis cerana japonica (Insecta: Hymenoptera: Apidae), Mitochondrial DNA, Part B, 2016, vol. 1, no. 1, pp. 156—157. https://doi.org/10.1080/23802359.2016.1144108

    Article  Google Scholar 

  18. Ilyasov, R.A., Park, J., Takahashi, J., and Kwon, H.W., Phylogenetic uniqueness of honeybee Apis cerana from the Korean peninsula inferred from the mitochondrial, nuclear, and morphological data, J. Apic. Sci., 2018, vol. 62, no. 2, pp. 189—214. https://doi.org/10.2478/Jas-2018-0018

    Article  CAS  Google Scholar 

  19. Ilyasov, R.A., Han, G.Y., Lee, M.L., et al., Phylogenetic relationships of Russian Far-East Apis cerana with other north Asian populations, J. Apic. Sci., 2019, vol. 63, no. 2, pp. 297—322. https://doi.org/10.2478/JAS-2019-0024

    Article  Google Scholar 

  20. Cornuet, J.-M., Garnery, L., and Solignac, M., Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA, Genetics, 1991, vol. 128, no. 2, pp. 393—403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Garnery, L., Cornuet, J.-M., and Solignac, M., Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis, Mol. Ecol., 1992, vol. 1, no. 3, pp. 145—154. https://doi.org/10.1111/j.1365-294x.1992.tb00170.x

    Article  CAS  PubMed  Google Scholar 

  22. Garnery, L., Mosshine, E.H., Oldroyd, B.P., and Cornuet, J.-M., Mitochondrial DNA variation in Moroccan and Spanish honey bee populations, Mol. Ecol., 1995, vol. 4, pp. 465—472. https://doi.org/10.1111/j.1365-294X.1995.tb00240.x

    Article  CAS  Google Scholar 

  23. Arias, M.C. and Sheppard, W.S., Molecular phylogenetics of honey bee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequence, Mol. Phylogenet. Evol., 1996, vol. 5, no. 3, pp. 557—566. https://doi.org/10.1006/mpev.1996.0050

    Article  CAS  PubMed  Google Scholar 

  24. Songrarn, O., Sittipraneed, S., and Klinbunga, S., Mitochondrial DNA diversity and genetic differentiation of the honeybee (Apis cerana) in Thailand, Biochem. Genet., 2006, vol. 44, nos. 5—6, pp. 256—269. https://doi.org/10.1007/s10528-006-9030-5

    Article  CAS  Google Scholar 

  25. Tan, H.W., Liu, G.H., Dong, X., et al., The complete mitochondrial genome of the Asiatic cavity-nesting honeybee Apis cerana (Hymenoptera: Apidae), PLoS One, 2011, vol. 6, no. 8. e23008. https://doi.org/10.1371/journal.pone.0023008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kent, C.F., Issa, A., Bunting, A.C., and Zayed, A., Adaptive evolution of a key gene affecting queen and worker traits in the honey bee, Apis mellifera, Mol. Ecol., 2011, vol. 20, no. 24, pp. 5226—5235. https://doi.org/10.1111/j.1365-294X.2011.05299.x

    Article  CAS  PubMed  Google Scholar 

  27. Bernt, M., Donath, A., Jühling, F., et al., MITOS: improved de novo metazoan mitochondrial genome annotation, Mol. Phylogenet. Evol., 2013, vol. 69, no. 2, pp. 313—319. https://doi.org/10.1016/j.ympev.2012.08.023

    Article  PubMed  Google Scholar 

  28. Lowe, T.M. and Eddy, S.R., tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence, Nucleic Acids. Res., 1997, vol. 25, no. 5, pp. 955—964. https://doi.org/10.1093/nar/25.5.0955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sanger, F., Nicklen, S., and Coulson, A.R., DNA sequencing with chain-terminating inhibitors, Proc. Natl. Acad. Sci. U.S.A., 1977, vol. 74, no. 12, pp. 5463—5467. https://doi.org/10.1073/pnas.74.12.5463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jukes, T.H. and Cantor, C.R., Evolution of protein molecules, in Mammalian Protein Metabolism, Munro, H.N., Ed., New York: Acad. Press, 1969, pp. 21—132.

    Google Scholar 

  31. Tamura, K., Battistuzzi, F.U., Billing-Ross, P., et al., Estimating divergence times in large molecular phylogenies, Proc. Natl. Acad. Sci. U.S.A., 2012, vol. 109, no. 47, pp. 19333—19338. https://doi.org/10.1073/pnas.1213199109

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, New York: Oxford Univ. Press, 2000.

    Google Scholar 

  33. Kumar, S., Stecher, G., and Tamura, K., MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870—1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Saitou, N. and Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, no. 4, pp. 406—425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  35. Tamura, K. and Nei, M., Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees, Mol. Biol. Evol., 1993, vol. 10, no. 3, pp. 512—526. https://doi.org/10.1093/oxfordjournals.molbev.a040023

    Article  CAS  PubMed  Google Scholar 

  36. Crozier, R.H. and Crozier, Y.C., The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization, Genetics, 1993, vol. 133, no. 1, pp. 97—117. https://doi.org/10.1111/j.1365-2583.1993.tb00131.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Okuyama, H., Tingek, S., and Takahashi, J., The complete mitochondrial genome of the cavity-nesting honeybee, Apis cerana (Insecta: Hymenoptera: Apidae) from Borneo, Mitochondrial DNA, Part B, 2017, vol. 2, no. 2, pp. 475—476. https://doi.org/10.1080/23802359.2017.1361344

    Article  Google Scholar 

  38. Kent, C.F., Minaei, S., Harpur, B.A., and Zayed, A., Recombination is associated with the evolution of genome structure and worker behavior in honey bees, Proc. Natl. Acad. Sci. U.S.A., 2012, vol. 109, no. 44, pp. 18012—18017. https://doi.org/10.1073/pnas.1208094109

    Article  PubMed  PubMed Central  Google Scholar 

  39. Lee, J.Y., Wang, A.R., Choi, Y.S., et al., Mitochondrial DNA variations in Korean Apis cerana (Hymenoptera: Apidae) and development of another potential marker, Apidologie, 2016, vol. 47, no. 1, pp. 123—134. https://doi.org/10.1007/s13592-015-0381-y

    Article  Google Scholar 

  40. Tan, Y.D., Wan, C.L., Zhu, Y.F., et al., An amplified fragment length polymorphism map of the silkworm, Genetics, 2001, vol. 157, no. 3, pp. 1277—1284.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Smith, C.R., Smith, C.D., Robertson, H.M., et al., Draft genome of the red harvester ant Pogonomyrmex barbatus, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, no. 14, pp. 5667—5672. https://doi.org/10.1073/pnas.1007901108

    Article  PubMed  PubMed Central  Google Scholar 

  42. Tian, D., Wang, Q., Zhang, P., et al., Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes, Nature, 2008, vol. 455, no. 7209, pp. 105—108. https://doi.org/10.1038/nature07175

    Article  CAS  PubMed  Google Scholar 

  43. McDonald, M.J., Wang, W.C., Huang, H.D., and Leu, J.Y., Clusters of nucleotide substitutions and insertion/deletion mutations are associated with repeat sequences, PLoS Biol., 2011, vol. 9, no. 6. e1000622. https://doi.org/10.1371/journal.pbio.1000622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Koren, A., Polak, P., Nemesh, J., et al., Differential relationship of DNA replication timing to different forms of human mutation and variation, Am. J. Hum. Genet., 2012, vol. 91, no. 6, pp. 1033—1040. https://doi.org/10.1016/j.ajhg.2012.10.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Seplyarskiy, V.B., Kharchenko, P., Kondrashov, A.S., and Bazykin, G.A., Heterogeneity of the transition/transversion ratio in Drosophila and Hominidae genomes, Mol. Biol. Evol., 2012, vol. 29, no. 8, pp. 1943—1955. https://doi.org/10.1093/molbev/mss071

    Article  CAS  PubMed  Google Scholar 

  46. Han, T., Lee, W., Lee, S., et al., Reassessment of species diversity of the subfamily Denticollinae (Coleoptera: Elateridae) through DNA barcoding, PLoS One, 2016, vol. 11, no. 2. e0148602. https://doi.org/10.1371/journal.pone.0148602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Eimanifar, A., Kimball, R.T., Braun, E.L., et al., The complete mitochondrial genome of the Egyptian honey bee, Apis mellifera lamarckii (Insecta: Hymenoptera: Apidae), Mitochondrial DNA, Part B, 2017, vol. 2, no. 1, pp. 270—272. https://doi.org/10.1080/23802359.2017.1325343

    Article  Google Scholar 

  48. DeSalle, R., Freedman, T., Prager, E.M., and Wilson, A.C., Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila, J. Mol. Evol., 1987, vol. 26, nos. 1—2, pp. 157—164. https://doi.org/10.1007/BF02111289

    Article  CAS  PubMed  Google Scholar 

  49. Johns, G.C. and Avise, J.C., A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene, Mol. Biol. Evol., 1998, vol. 15, pp. 1481—1490. https://doi.org/10.1093/oxfordjournals.molbev.a025875

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

We are grateful to Dr. Hisashi Okuyama for the assistance with sequencing as well as the e-ASIA JRP (The East Asia Science and Innovation Area Joint Research Program) Foundation for support in the implementation of the project (https://www.the-easia.org).

Funding

The present study was supported by the government assignment (registration no. AAAA-A21-121011990120-7) (IR), by the Russian Foundation for Basic Research (no. 19-54-70002 e-Asia_t) (NA)), and by the postdoctoral research programs of Incheon National University 2019 (IR).

Author information

Authors and Affiliations

  1. Ufa Federal Research Center, Institute of Biochemistry and Genetics, Russian Academy of Sciences, 450054, Ufa, Russia

    R. A. Ilyasov & A. G. Nikolenko

  2. Division of Life Sciences, Major of Biological Sciences, Incheon National University, Convergence Research Center for Insect Vectors, Incheon National University, 22012, Incheon, Korea

    R. A. Ilyasov, G. Y. Han, M. L. Lee, K. W. Kim, J. H. Park & H. W. Kwon

  3. Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences, 690022, Vladivostok, Russia

    M. Y. Proshchalykin & A. S. Lelej

  4. 3BIGS CO. LTD., 18454, Hwaseong-si, Korea

    J. H. Park

  5. Faculty of Life Sciences, Kyoto Sangyo University, 603-8555, Kyoto, Japan

    J. I. Takahashi

Authors
  1. R. A. Ilyasov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Y. Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. L. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. W. Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Y. Proshchalykin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. S. Lelej
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. H. Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. I. Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. H. W. Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. A. G. Nikolenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to R. A. Ilyasov or H. W. Kwon.

Ethics declarations

Conflict of interest. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by A. Lisenkova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ilyasov, R.A., Han, G.Y., Lee, M.L. et al. Genetic Properties and Evolution of Asian Honey Bee Apis cerana ussuriensis from Primorsky Krai, Russia. Russ J Genet 57, 568–581 (2021). https://doi.org/10.1134/S1022795421050033

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795421050033

Keywords:

Search

Navigation