Skip to main content
SpringerLink
Log in

Phylogeographic analysis of Apis cerana populations on Hainan Island and southern mainland China, based on mitochondrial DNA sequences

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

The phylogeography of the eastern honeybee (Apis cerana) in southern China is poorly understood. In the present study, we investigated phylogenetic relationships among A. cerana populations on Hainan island and southern mainland China. Analyses were based on the partial cytochrome oxidase subunit 1 gene of mitochondrial DNA and A. cerana samples representing 12 geographic populations. We identified 57 novel haplotypes (GenBank accession numbers: KC175488-KC175544) within our sampled populations and inferred two deeply divergent intraspecific lineages when previously published sequences were included, which could be further divided into six sublineages. We also found a significant phylogeographic structure within lineage A. Our results reveal that A. cerana populations on Hainan island and southern mainland China have undergone a long period of differentiation in isolation followed by historical demographic expansion. Although gene flow now occurs between these locations, gene flow has occurred over comparatively a short time period, and is likely to be the result of anthropogenic effects.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Akaike, H. (1974) A new look at the statistical model identification. IEEE Trans. Autom. Control. 19, 716–723

    Article  Google Scholar 

  • Arias, M.C., Sheppard, W.S. (1996) Molecular phylogenetics of honey bee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequence. Mol Phylogenet Evol 5(3), 557–566

    Article  CAS  PubMed  Google Scholar 

  • Avise, J.C., Arnold, J., Ball, R.M., Bermingham, E., Lamb, T., Neigel, J.E., Reeb, C.A., Saunders, N.C. (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18, 489–522

    Google Scholar 

  • Clarke, K., Oldroyd, B.P., Javier, J., Quezada, E., Rinderer, T.E. (2001) Origin of honeybees (Apis mellifera L.) from the Yucatan peninsula inferred from mitochondrial DNA analysis. Mol. Ecol. 10, 1347–1355

    Article  CAS  PubMed  Google Scholar 

  • Collet, T., Ferreira, K.M., Arias, M.C., Soares, A.E., Del, L.M. (2006) Genetic structure of Africanized honeybee populations (Apis mellifera L.) from Brazil and Uruguay viewed through mitochondrial DNA COI-COII patterns. Heredity 97, 329–335

    Article  CAS  PubMed  Google Scholar 

  • Cornuet, J.M., Garnery, L. (1991) Mitochondrial DNA variability in honeybees and its phylogeographic implications. Apidologie 22, 627–642

    Article  CAS  Google Scholar 

  • Cornuet, J.M., Garnery, L., Solignac, M. (1991) Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics 128, 393–403

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crawford, N.G. (2010) SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Res. 10, 556–557

    Article  Google Scholar 

  • de la Rua, P., Galian, J., Serrano, J., Moritz, R.F. (2001) Genetic structure and distinctness of Apis mellifera L. populations from the Canary Islands. Mol. Ecol. 10, 1733–1742

    Article  PubMed  Google Scholar 

  • de la Rua, P., Simon, U., Tilde, A., Moritz, R., Fuchs, S. (2000) MtDNA variation in Apis cerana populations from the Philippines. Heredity 84, 124–130

    Article  Google Scholar 

  • Excoffier, L., Laval, G., Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. 1, 47–50

    CAS  Google Scholar 

  • Excoffier, L., Smouse, P.E., Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491

    CAS  PubMed Central  PubMed  Google Scholar 

  • Franck, P., Garnery, L., Loiseau, A., Oldroyd, B.P., Hepburn, H.R., Solignac, M., Cornuet, J.M. (2001) Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86, 420–430

    Article  CAS  PubMed  Google Scholar 

  • Fu, Y.X. (1997) Statistical tests of neutrality of mutations agsinst population growth, hitchhiking and background selection. Genetics 147, 915–925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garnery, L., Cornuet, J.M., Solignac, M. (1992) Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol. Ecol. 1, 145–154

    Article  CAS  PubMed  Google Scholar 

  • Henrique, B.F., Waldschmidt, A.M., Campos, L.A.O., Tavares, M.G., Tania, M.F.S. (2010) Phylogeography and historical demography of the neogropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and mitochondrial DNA. Apidologie 41, 534–547

    Article  Google Scholar 

  • Hepburn, H.R., Radloff, S.E., Verma, S., Verma, L.R. (2001) Morphometric analysis of Apis cerana populations in the southern Himalayan region. Apidologie 32, 435–447

    Article  Google Scholar 

  • Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68, 87–112

    Article  Google Scholar 

  • Iiyasov, R.A., Kutuev, I.A., Petukhov, A.V., Poskryakov, A.V., Nikolenko, A.G. (2011) Phylogenetic relationships of dark European honeybees Apis mellifera mellifera L. from the Russian ural and west European populations. J. Apic. Sci. 55, 67–76

    Google Scholar 

  • Kekecoglu, M., Bouga, M., Soysal, M.I., Harizanis, P. (2009) Genetic divergence and phylogenetic relationships of honey bee populations from Turkey using PCR-RFLP's analysis of two mtDNA segments. Bulg. J. Agric. Sci. 15, 589–597

    Google Scholar 

  • Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120

    Article  CAS  PubMed  Google Scholar 

  • Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B: Biol. Sci. 274, 303–313

    Article  Google Scholar 

  • Kremen, C., Williams, N.M., Aizen, M.A., Gemmill-Herren, B., GLebuhn, G., et al. (2007) Pollination and other ecosystem services produced by mobile orgaisms: a conceptual framework for the effects of land use change. Ecol. Lett. 10, 299–314

    Article  PubMed  Google Scholar 

  • Magnus, R., Szalanski, A.L. (2010) Genetic evidence for honey bees (Apis mellifera L.) of middle eastern lineage in the United States. Sociobiology 55, 285–296

    Google Scholar 

  • Moritz, C. (1994) Defining evolutionarily significant units for conservation. Trends Ecol. Evol. 9, 373–374

    Article  CAS  PubMed  Google Scholar 

  • Naderi, S., Rezaei, H.R., Taberlet, P., Zundel, S., Rafat, S.A., Naghash, H.R., Mohamed, A.A.E., Ertugrul, O., Pompanon, F. (2007) Large-scale mitochondrial DNA analysis of the domestic goat reveals six haplogroups with high diversity. PLoS One 2, 1–12

    Article  Google Scholar 

  • Partap, U., Verma, L.R. (1994) Pollination of radish by Apis cerana. J. Apic. Res. 33, 237–241

    Google Scholar 

  • Peng, Y.S., Nasr, M.E., Locke, S.J. (1989) Geographical races of Apis cerana Fabricius in China and their distribution. Review of recent Chinese publications and a preliminary statistical analysis. Apidologie 20, 9–20

    Article  Google Scholar 

  • Posada, D. (2009) Selection of models of DNA evolution with jModelTest. Methods in Mol. Biol. 537, 93–112

    Article  CAS  Google Scholar 

  • Radloff, S.E., Hepburn, C., Hepburn, H.R., Fuchs, S., Hadisoesilo, S., Ken, T., Engel, M.S., Kuznetsov, V. (2010) Population structure and classification of Apis cerana. Apidologie 41, 589–601

    Article  Google Scholar 

  • Radloff, S.E., Hepburn, H.R., Fuchs, S., Otis, G.W., Hadisoesilo, S., Hepburn, C., Ken, T. (2005a) Multivariate morphometric analysis of the Apis cerana populations of oceanic Asia. Apidologie 36, 475–492

    Article  Google Scholar 

  • Radloff, S.E., Hepburn, H.R., Hepburn, C., Fuchs, S., Otis, G.W., et al. (2005b) Multivariate morphometric analysis of Apis cerana of southern mainland Asia. Apidologie 36, 127–139

    Article  Google Scholar 

  • Ronquist, F., Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rozas, J. (2009) DNA sequence polymorphism analysis using DnaSP. Methods in Mol. Biol. 537, 337–350

    Article  CAS  Google Scholar 

  • Rozas, J., Rozas, R. (1995) DnaSP, DNA sequence polymorphism: an interactive program for estimating population genetics parameters from DNA sequence data. Comput. Appl. Biosci. 11, 621–625

    CAS  PubMed  Google Scholar 

  • Ruttner, F. (1988) Biogeography and taxonomy of honeybees. Springer, Berlin

    Book  Google Scholar 

  • Sasaki, M., Ono, M., Asada, S., Yoshida, T. (1991) Oriental orchid (Cymbidium pumilum) attracts drones of the Japanese honeybee (Apis cerana japonica) as pollinators. Experientia 47, 1229–1231

    Article  CAS  PubMed  Google Scholar 

  • Shi, M.C., Chen, C.S., Xu, Q.C., Lin, H.C., Liu, G.M., Wang, H., Wang, F., Yan, J.H. (2002) The role of Qiongzhou Strait in the seasonal variation of the south China sea circulation. J. Phys. Oceanogr. 32, 103–121

    Article  Google Scholar 

  • Sihanuntavong, D., Sittipraneed, S., Klinbunga, S. (1999) Mitochondrial DNA diversity and population structure of the honey bee, Apis cerana, in Thailand. J. Apic. Res. 38, 211–219

    CAS  Google Scholar 

  • Smith, D.R. (2011) Asian honeybees and mitochondrial DNA. In: Hepburn, R., Radloff, S.E. (eds.) Honeybees of Asia, pp. 69–93. Springer, Berlin

    Chapter  Google Scholar 

  • Smith, D.R., Hagen, R.H. (1996) The biogeography of Apis cerana as revealed by mitochondrial DNA sequence data. J. Kansas Entomol. Soc. 69, 294–310

    Google Scholar 

  • Smith, D.R., Villafuerte, L., Otis, G., Palmer, M.R. (2000) Biogeography of Apis cerana F. and A. nigrocincta Smith: insights form mtDNA studies. Apidologie 31, 265–279

    Article  CAS  Google Scholar 

  • Smith, D.R., Warrit, N., Hepburn, H.R. (2004) Apis cerana from Myanmar (Burma): unusual distribution of mitochondrial lineages. Apidologie 35, 637–644

    Article  CAS  Google Scholar 

  • Songram, O., Sittipraneed, S., Klinbunga, S. (2006) Mitochondrial DNA diversity and genetic differentiation of the honeybee (Apis cerana) in Thailand. Biochem. Genet. 44, 256–269

    Article  CAS  PubMed  Google Scholar 

  • Swofford, D.L. (2001) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0. Sinauer, Sunderland, MA

    Google Scholar 

  • Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takahashi, J., Yoshida, T., Takagi, T., Akimoto, S., Woo, K.S., Deowanish, S., Hepburn, R., Nakamura, J., Matsuka, M. (2007) Geographic variation in the Japanese islands of Apis cerana japonica and in A. cerana populations bordering its geographic range. Apidologie 38, 335–340

    Article  CAS  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tan, K., Fuchs, S., Koeniger, N., Ruiguang, Z. (2003) Morphological characterization of Apis cerana in the Yunnan Province of China. Apidologie 34, 553–561

    Article  Google Scholar 

  • Tan, K., Hepburn, H.R., Radloff, S.E., Fuchs, S., Xian, F., Zhang, L.J., Yang, M.X. (2008) Multivariate morphometric analysis of the Apis cerana of China. Apidologie 39, 343–353

    Article  Google Scholar 

  • Tan, K., Meixner, M.D., Fuchs, S., Zhang, X., He, S., Kandemir, I., Sheppard, W.S., Koeniger, N. (2006) Geographic distribution of the eastern honeybee, Apis cerana (Hymenoptera: Apidae), across ecological zones in China: morphological and molecular analyses. Syst. Biodivers. 4, 473–482

    Article  Google Scholar 

  • Tan, K., Warrit, N., Smith, D.R. (2007) Mitochondrial DNA diversity of Chineses Apis cerana. Apidologie 38, 238–246

    Article  CAS  Google Scholar 

  • Tanaka, H., Suka, T., Kahono, S., Samejima, H., Mohamed, M., Roubik, D.W. (2003) Mitochondrial variation and genetic differentiation in honey bees (Apis cerana, A. koschevnikovi and A. dorsata) of Borneo. Tropics 13, 107–117

    Article  Google Scholar 

  • Thompson, J.D., Higgins, D.G., Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tomas, H., Farias, I.P., Crossa, M., Sampaio, I., Porto, J.I.R., Meyer, A. (2005) Population genetic analysis of Arapaima gigas, one of the largest freshwater fishes of the Amazon basin: implications for its conservation. Anim. Conserv. 8, 297–308

    Article  Google Scholar 

  • Verma, L. R., Partap, U. (1993) The Asian hive bee, Apis cerana, as a pollinator in vegetable seed production. International Centre for Integrated Mountain Development (ICIMOD), Nepal.

  • Voris, H.K. (2000) Maps of Pleistocene sea levels in southeast Asia: shorelines, river systems and time durations. J. Biogeogr. 27, 1153–1167

    Article  Google Scholar 

  • Wang, Z.F., Shen, X., Liu, B., Su, J.P., Yonezawa, T., et al. (2010) Phylogeographical analyses of domestic and wild yaks based on mitochondrial DNA: new data and reappraisal. J. Biogeogr. 37, 2332–2344

    Article  Google Scholar 

  • Yang, G.H., Xu, S.Y., Kuang, B.Y., Liu, Y.D. (1986) Subspecific differentiation and distribution of Apis cerana Fab in China. J. Yunnan Agric. Univ. 1, 89–92

    Google Scholar 

  • Zaitoun, S., Hassawi, D.S., Shahrour, W. (2008) Origin of Jordanian honeybees Apis mellifera (Hymenoptera: Apidae) using amplified mitochondrial DNA. Eur. J. Entomol. 105, 41–44

    CAS  Google Scholar 

  • Zayed, A. (2009) Bee genetics and conservaton. Apidologie 40, 237–262

    Article  Google Scholar 

Download references

Acknowledgments

We wish to acknowledge our gratitude to Yuexiong Luo, Zheng Xu, Junjun Hu, and Jinglin Gao for their generous help in sample collection. Heartfelt thanks are extended to Kaixing Qi for his editorial assistance. This study was financially supported by the “National System of Bee Industry and Technology” Program (CARS-45-kxj14)

Author information

Authors and Affiliations

  1. College of Plant Protection, Yunnan Agricultural University, Kunming, 650201, China

    Wenzheng Zhao

  2. Eastern Bee Research Institute, Yunnan Agricultural University, Kunming, 650201, China

    Wenzheng Zhao, Ken Tan, Danyin Zhou, Miao Wang, Chunfu Cheng, Zengyuan Yu & Shaoyu He

  3. College of Animal Science and Technology, Yunnan Agricultural University, Kunming, 650201, China

    Zengyuan Yu & Yongwang Miao

Authors
  1. Wenzheng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ken Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Danyin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Miao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunfu Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zengyuan Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yongwang Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shaoyu He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yongwang Miao or Shaoyu He.

Additional information

Manuscript editor: Marina Meixner

Analyse phylogéographique des populations d'Apis cerana sur l'île de Hainan et dans le sud de la Chine continentale, basée sur les séquences d'ADN mitochondrial

Phylogéographie/ADN mitochondrial/haplotype/flux génétique

Phylogeographische Analyse von Apis cerana Populationen von der Insel Hainan und dem südlichen Festlandchina, auf der Basis von mitochondrialen DNA-Sequenzen Apis cerana/ mitochondriale DNA/Phylogeographie

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

DOC 136 kb

ESM 2

DOC 44 kb

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, W., Tan, K., Zhou, D. et al. Phylogeographic analysis of Apis cerana populations on Hainan Island and southern mainland China, based on mitochondrial DNA sequences. Apidologie 45, 21–33 (2014). https://doi.org/10.1007/s13592-013-0223-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0223-8

Keywords

Search

Navigation