Skip to main content
SpringerLink
Log in

Reevaluation of honeybee (Apis mellifera) microtaxonomy: a geometric morphometric approach

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

Abstract

In the present study, the microtaxonomy of honeybee (Apis mellifera L.) subspecies was reevaluated based on a geometric morphometric method. Wing images of honeybee subspecies, obtained from the Morphometric Bee Data Bank in Oberursel, Germany, were assigned to four honeybee lineages from the indivudial images, and 40 Cartesian coordinates were obtained. Honeybee lineages were significantly different based on individual and colony consensus average wing shapes of honeybee subspecies (P < 0.001). According to the discriminant function analysis of honeybee lineages, the A lineage and M lineage showed some degree of overlap. Multivariate statistical analysis displayed that Apis mellifera intermissa, a member of M lineage, seemed to belong to the A lineage. In addition, Apis mellifera sicula, a member of C lineage; Apis mellifera sahariensis, a member of M lineage; and Apis mellifera syriaca, a member of O lineage, were located closer to the A lineage rather than to their own lineages. In the previous studies, the results of principal component analysis of morphometric data and the mtDNA analysis of honeybee subspecies supported these subspecific affinities. Thus, geometric morphometric analysis of wing shape could be used as a reliable tool to discriminate among honeybee subspecies and may have advantages over standard morphometry.

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
Figure 2.
Figure 3.
Figure 4.
Figure 5.

Similar content being viewed by others

References

  • Alpatov, W.W. (1929) Biometrical studies on variation and races of the honeybee Apis mellifera L. Rev. Biol. 4, 1–57

    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, 557–566

    Article  PubMed  CAS  Google Scholar 

  • Aytekin, A.M., Terzo, M., Rasmont, P., Çağatay, N. (2007) Landmark based geometric morphometric analysis of wing shape in Sibiricobombus Vogt (Hymenoptera: Apidae: Bombus Latreille). Ann. Soc. Entomol. 43(1), 95–102

    Google Scholar 

  • Bloch, G., Francoy, T.M., Wachtel, I., Panitz-Cohen, N., Fuchs, S., Mazar, A. (2010) Industrial apiculture in the Jordan valley during Biblical times with Anatolian honeybees. PNAS 107(25), 11240–11244

    Article  PubMed  CAS  Google Scholar 

  • Bookstein, F.L. (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York. 435 pp

    Google Scholar 

  • Daly, H.V., Hoelmer, K., Norman, P., Allen, T. (1982) Computer assisted measurement and identification of honey bees. Ann. Entomol. Soc. Am. 75, 591–594

    Google Scholar 

  • De La Riva, J., Le Pont, F., Ali, V., Matias, A., Mollinedo, S., Dujardin, J.P. (2001) Wing geometry as a tool for studying the Lutzomyia longipalpis (Diptera: Psychodidae) complex. Mem. Inst. Oswaldo Cruz 96(8), 1089–1094

    Article  PubMed  Google Scholar 

  • De La Rua, P., Jaffe, R., Dall’Olio, R., Munoz, I., Serrano, J. (2009) Biodiversity, conservation and current threats to European honey bees. Apidologie 40, 263–284

    Article  Google Scholar 

  • Diniz-Filho, J.A.F., Hepburn, H.R., Radloff, S., Fuchs, S. (2000) Spatial analysis of morphometrical variation in African honeybees (Apis mellifera L.) on a continental scale. Apidologie 31, 191–204

    Article  Google Scholar 

  • Engel, M.S. (1999) The taxonomy of recent and fosil honey bees (Hymenoptera: Apidae; Apis). J. Hymenopt. Res. 8, 165–196

    Google Scholar 

  • Franck, P., Garnery, L., Loiseau, A., Solignac, M., Cornuet, J.M. (2000) Molecular confirmation of a fourth lineage in honeybees from Middle-East. Apidologie 31, 167–180

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Francoy, T.M., Wittmann, D., Drauschke, M., Müler, S., Steinhage, V., Bezerra-Laure, M.A.F., De Jong, D., Gonçalves, L.S. (2008) Identification of Africanized honey bees through wing morphometrics: two fast and efficient procedures. Apidologie 39(5), 488–494

    Article  Google Scholar 

  • Francoy, T.M., Wittmann, D., Steinhage, V., Drauschke, M., Müler, S., Cunha, D.R., Nascimento, A.M., Figueiredo, V.L.C., Simões, Z.L.P., De Jong, D., Arias, M.C., Gonçalves, L.S. (2009) Morphometric and genetic changes in a population of Apis mellifera after 34 years of Africanization. Genet. Mol. Res. 8(2), 709–717

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Houle, D., Mezey, J., Galpern, P., Carter, A. (2003) Automated measurement of Drosophila wings. BMC Evol. Biol. 3, 25

    Article  PubMed  Google Scholar 

  • Kandemir, I., Kence, M., Kence, A. (2000) Genetic and morphometric variation in honey bee (Apis mellifera L.) population of Turkey. Apidologie 31, 343–356

    Article  CAS  Google Scholar 

  • Kauhausen-Keller, D., Ruttner, F., Keller, R. (1997) Morphometric studies on the microtaxonomy of the species Apis mellifera L. Apidologie 28, 295–307

    Article  Google Scholar 

  • Miguel, I., Baylac, M., Iriondo, M., Manzano, C., Garnery, L., Estonba, A. (2011) Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie 42, 150–161. doi:10.1051/apido/2010048

    Article  Google Scholar 

  • Monteiro, L.R., Diniz-Filho, J.A.F., Dos Reis, S.F., Araújo, E.D. (2002) Geometric estimates of heritability in biological shape. Evolution 56(3), 563–572

    PubMed  Google Scholar 

  • Palmer, M.R., Smith, D.R., Kaftanoglu, O. (2000) Turkish honeybees: genetic variation and evidence for a fourth lineage of Apis mellifera mtDNA. J. Hered. 91, 42–46

    Article  PubMed  CAS  Google Scholar 

  • Pretorius, E. (2005) Using geometrics to investigate wing dimorphism in males and females Hymenoptera—a case study based on the genus Tachysphex Kohl (Hymenoptera: Sphecidae: Larrinae). Aust. J. Entomol. 44, 113–121

    Article  Google Scholar 

  • Pretorius, E., Scholtz, C.H. (2001) Geometric morphometrics and the analysis of higher taxa: a case study based on the metendosternite of the Scarabaeoidea (Coleoptera). Biol. J. Linn. Soc. 74, 35–50

    Google Scholar 

  • Rohlf F.J. (2004) NTSYS-PC, Numerical Taxonomy and Multivariate Analysis System, version 2.2. Department of Ecology and Evolution, State University of New York, Exeter Software, Stony Brook, New York.

  • Rohlf F.J. (2008a) tpsUtil, version 1.40. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.

  • Rohlf F.J. (2008b) tpsDIG, version 2.11. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.

  • Rohlf, F.J., Marcus, L.F. (1993) A revolution in morphometrics. Trends Ecol. Evol. 8, 129–132

    Article  Google Scholar 

  • Ruttner, F. (1988) Biogeography and taxonomy of honeybees, p. 284. Springer, Berlin, Heildelberg

    Google Scholar 

  • Ruttner, F. (1992) Naturgeschichte der honigbienen. Ehrenwirth, München, 357 pp.

  • Ruttner, F., Elmi, P.M., Fuchs, S. (2000) Ecoclines in the Near East along 36° N latitude in Apis mellifera L. Apidologie 31, 157–165

    Article  Google Scholar 

  • Sadeghi, S., Adriaens, D., Dumont, H.J. (2009) Geometric morphometric analysis of wing shape variation in ten European populations of Calopteryx splendens (Harris, 1782) (Zygoptera: Odonata). Odonatologica 38(4), 343–360

    Google Scholar 

  • Schachter-Broide, J., Dujardin, J.-P., Kitron, U., Gürtler, R.E. (2004) Spatial structure of Triatoma infestans (Hemiptera, Reduviidae) populations from Northwestern Argentina using wing geometric morphometry. J. Med. Entomol. 14(4), 643–649

    Google Scholar 

  • Schneider, S.S., Leamy, L.J., Lewis, L.A., De Grandi-Hoffman, G. (2003) The influence of hybridization between African and European honeybees, Apis mellifera, on asymmetries in wing size and shape. Evolution 57(10), 2350–2364

    PubMed  CAS  Google Scholar 

  • Sheppard, W.S., Meixner, M.D. (2003) Apis mellifera pomonella, a new honey bee subspecies from Central Asia. Apidologie 34, 367–375

    Article  Google Scholar 

  • Sheppard, W.S., Smith, D.R. (2000) Identification of African-derived bees in the Americas: a survey of methods. Ann. Entomol. Soc. Am. 93, 159–176

    Article  CAS  Google Scholar 

  • Sheppard, W.S., Arias, M.C., Meixner, M.D., Grech, A. (1997) Apis mellifera ruttneri, a new honey bee subspecies from Malta. Apidologie 28, 287–293

    Article  Google Scholar 

  • Slice, D.E. (2002) Morpheus, For morphometric research software. Department of Biomedical Engineering, Wake Forest University School of Medicine, Winston, Salem

    Google Scholar 

  • Smith, D.R. (1991) Mitochondrial DNA and honeybee biogeography. In: Smith, D.R. (ed.) Diversity in genus Apis, pp. 131–176. Westview Press, Oxford

    Google Scholar 

  • Smith, D.R., Slaymaker, A., Palmer, M., Kaftanoglu, O. (1997) Turkish honeybees belong to the east Mediterranean mitochondrial lineage. Apidologie 28, 269–274

    Article  CAS  Google Scholar 

  • Tofilski, A. (2008) Using geometric morphometrics and standard morphometry to discriminate three honeybee subspecies. Apidologie 39(5), 558–563

    Article  Google Scholar 

  • 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. (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314, 642–645

    Article  PubMed  CAS  Google Scholar 

  • Zelditch, M.L., Swiderski, D.L., Sheets, H.D., Fink, W.L. (2004) Geometric morphometrics for biologists: a primer. Elsevier Academic, New York. 443 pp

    Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the Institut für Bienenkunde in Oberursel, Germany, for the use of reference samples. We thank W.S. Sheppard and two anonymous referees for editorial comments on the manuscript. This study was supported by TUBITAK-TBAG 107 T154 grant to IK.

Ré-évaluation de la microtaxonomie de l’abeille Apis mellifera par une approche de morphométrie géométrique

Apis mellifera / morphométrie géométrique / sous-espèce / élément du paysage / analyse fonctionnelle discriminante

Re-evaluation der Mikrotaxonomie der Honigbienen ( Apis mellifera ) Ein geometrisch-morphometrischer Ansatz

Apis mellifera / geometrisch-morphometrisch / Landmarken / Unterarten / Diskriminanzfunktionsanalyse

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ankara University, Tandoğan, 06100, Ankara, Turkey

    İrfan Kandemir & Ayça Özkan

  2. Institut für Bienenkunde (Polytechnische Gesellschaft), Fachbereich Biowissenschaften der J.W. Goethe-Universität Frankfurt am Main, Karl-von-Frisch-Weg 2, 61440, Oberursel, Germany

    Stefan Fuchs

Authors
  1. İrfan Kandemir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ayça Özkan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stefan Fuchs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to İrfan Kandemir.

Additional information

Manuscript editor: Stan Schneider

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kandemir, İ., Özkan, A. & Fuchs, S. Reevaluation of honeybee (Apis mellifera) microtaxonomy: a geometric morphometric approach. Apidologie 42, 618–627 (2011). https://doi.org/10.1007/s13592-011-0063-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-011-0063-3

Keywords

Search

Navigation