Skip to main content
Log in

Apis mellifera evolutionary lineages in Northern Africa: Libya, where orient meets occident

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

The distribution of various evolutionary lineages of Apis mellifera subspecies in Africa is still controversial. We sampled honeybees from eight coastal locations and three Saharan oases in Libya and analyzed mtDNA variability with restriction fragment length polymorphisms and the sequence of the tRNAleu-cox2 intergenic region. Haplotypes belonging to the oriental O evolutionary lineage, including four which are newly described, were detected in all investigated locations. Haplotypes belonging to the European M lineage were rarely detected, probably reflecting the effect of sporadic importations. Honeybees belonging to the A lineage were detected in Al Aziziyah and Zlitan close to the Tunisian border. The distribution of the O lineage extends westward up to the border between Libya and Tunisia, a contact area between the O and A lineages. Various Libyan honeybee populations in Saharan oases are characterized by novel and unique haplotypes (O4, O5, O5′ and O5″). These might be natural relic populations that became isolated when the North African Sahara desert was still grassland (0.126–0.168 Myr ago).

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arias M. and 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 

  • Bandelt H.J., Forster P. and Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37–48

    PubMed  CAS  Google Scholar 

  • Boore J.L. 2001. Mitochondrial gene arrangement source guide, version 6.1 (available at http://www.uniulm.de/fileadmin/website_uni_ulm/iui.inst.190/Forschung/Projekte/GENESIS/MGA_Guide.pdf)

  • Cánovas F., De la Rúa P., Serrano J. and Galián J. 2008. Geographic patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). J. Zool. Syst. Evol. Res. 46: 24–30

    Google Scholar 

  • Clarke K.E., Rinderer T.E., Franck P., Quezada-Euán J.G. and Oldroyd B.P. 2002. The Africanization of honey bees (Apis mellifera L.) of the Yucatan: a study of a massive hybridization event across time. Evolution 56: 1462–1474

    PubMed  CAS  Google Scholar 

  • Dall′Olio R., Marino A., Lodesani M. and Moritz R.F.A. 2007. Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie 38: 207–217

    Article  Google Scholar 

  • De la Rúa P., Serrano J. and Galián J. 1998. Mitochondrial DNA variability in the Canary Islands honeybees (Apis mellifera L.). Mol. Ecol. 7: 1543–1547

    Article  Google Scholar 

  • De la Rúa, P., Galián J., Serrano J. and Moritz R.F.A. 2001. Genetic structure and distinctness of Apis mellifera L. populations from the Canary Islands. Mol. Ecol. 10: 1733–1742

    Article  Google Scholar 

  • De la Rúa P., Galián J., Serrano J. and Moritz R.F.A. 2002. Microsatellite analysis of non-migratory colonies of Apis mellifera iberica from south eastern Spain. J. Zool. Syst. Evol. Res. 40:164–168

    Article  Google Scholar 

  • De la Rúa P., Galián J., Pedersen B.V. and Serrano J. 2006. Molecular characterization and population structure of Apis mellifera from Madeira and the Azores. Apidologie 37: 699–708

    Article  Google Scholar 

  • El Banby M.A. 1977. Biometrical studies on the local honeybee of the Libyan Arab People’s Socialist Jamachiriya. Proc. Int. Beekeep. Congr. 26: 269

    Google Scholar 

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

    Google Scholar 

  • Forster P., Torroni A., Renfrew C. and Röhl A. 2001. Phylogenetic star contraction applied to Asian and Papuan mtDNA evolution. Mol. Biol. Evol. 18: 1864–1881

    PubMed  CAS  Google Scholar 

  • Franck P., Garnery L., Solignac M. and Cornuet J.M. 1998. The origin of west European subspecies of honeybees (Apis mellifera): New insights from microsatellite and mitochondrial data. Evolution 52: 1119–1134

    Article  CAS  Google Scholar 

  • Franck P., Garnery L., Celebrano G. and Solignac M. 2000a. Hybrid origins of honeybees from Italy (Apis mellifera ligustica) and Sicily (A. m. sicula). Mol. Ecol. 9: 907–921

    Article  PubMed  CAS  Google Scholar 

  • Franck P., Garnery L., Solignac M. and Cornuet J.M. 2000b. Molecular confirmation of a fourth lineage in honeybees from the Near East. Apidologie 31: 167–180

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Garnery L., Solignac M., Celebrano G. and Cornuet J.M. 1993. A simple test using restricted PCR amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia 49: 1016–1021

    Article  CAS  Google Scholar 

  • Garnery L., Mosshine E.H., Oldroyd B.P. and Cornuet J.M. 1995. Mitochondrial DNA variation in Moroccan and Spanish honey bee populations. Mol. Ecol. 4: 465–471

    Article  CAS  Google Scholar 

  • Garnery L., Franck P., Baudry E., Vautrin D., Cornuet J.M. and Solignac M. 1998. Genetic biodiversity of the West European honeybee (Apis mellifera mellifera and Apis mellifera iberica). II. Microsatellite loci. Genet. Sel. Evol. 30: 49–74

    Article  Google Scholar 

  • Hepburn H.R. and Radloff S.E. 1998. Honeybees of Africa. Springer Verlag, Berlin. 370 p

    Google Scholar 

  • Hicheri K. and Bouderbala M. 1969. Tunisian apiculture. Proc. Int. Beekeep. Congr. 22: 440–443

    Google Scholar 

  • Jensen A.B., Palmer K.A., Boomsma J.J. and Pedersen B.V. 2005. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Mol. Ecol. 14: 93–106

    Article  PubMed  Google Scholar 

  • Kandemir I., Kence M., Sheppard W.S. and Kence A. 2006. Mitochondrial DNA variation in honey bee (Apis mellifera L.) populations from Turkey. J. Apic. Res. 45: 33–38

    CAS  Google Scholar 

  • Kraus F.B., Franck P. and Vandame R. 2007. Asymmetric introgression of African genes in honeybee populations (Apis mellifera L.) in Central Mexico. Heredity 99: 233–240

    Article  PubMed  CAS  Google Scholar 

  • Lebdigrissa K., Msadda K., Cornuet J.M. and Fresnaye J. 1991. The influence of European Honeybees introduced in Tunisia on the Tunisian breed Apis mellifera. Landbouwtijdschrift 44: 631–636

    Google Scholar 

  • Miguel I., Iriondo M., Garnery L., Sheppard W.S. and Estonba A. 2007. Gene flow within the M evolutionary lineage of Apis mellifera: role of the Pyrenees, isolation by distance and post-glacial re-colonization routes in the Western Europe. Apidologie 38: 141–155

    Article  CAS  Google Scholar 

  • Moritz R.F.A., Kraus F.B., Kryger P. and Crewe R.M. 2007. The size of wild honeybee populations (Apis mellifera) and its implications for the conservation of honeybees. J. Insect. Conserv. 11: 391–397

    Article  Google Scholar 

  • Moritz R.F.A., Dietemann V. and Crewe R.M. 2008. Determining colony densities in wild honeybee populations (Apis mellifera) with linked microsatellite DNA markers. J. Insect Conserv. 12: 455–459

    Article  Google Scholar 

  • Palmer M.R., Smith D.R. and Kaftanoğlu 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 

  • Polzin T. and Daneschmand S.V. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Oper. Res. Lett. 31: 12–20

    Article  Google Scholar 

  • Rozas J., Sánchez-Del Barrio J.C., Messeguer X. and Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Ruttner F. 1988. Biogeography and Taxonomy of Honey Bees. Springer, Heidelberg, New York. 284 pp

    Google Scholar 

  • Second G. 1974. L’apiculture dans les pays d’Afrique du nord. Bull. Tech. Apic. 1: 7–28

    Google Scholar 

  • Shaibi T., Lattorf H.M.G. and Moritz R.F.A. 2008. A microsatellite toolkit for studying population structure in Apis mellifera. Mol. Ecol. Resources 8: 1034–1036

    Article  CAS  Google Scholar 

  • Shaibi T., Fuchs S. and Moritz R.F.A. 2009. Morphological study of honeybees (Apis mellifera) from Libya. Apidologie 40: 97–105

    Article  Google Scholar 

  • Sheppard W.S. and Meixner M.D. 2003. Apis mellifera pomonella, a new honey bee subspecies from the Tien Shan mountains of Central Asia. Apidologie 34: 367–375

    Article  Google Scholar 

  • Smith D.R. and Glenn T.C. 1995. Allozyme polymorphisms in Spanish honeybees (Apis mellifera iberiensis). J. Hered. 86: 12–16

    PubMed  CAS  Google Scholar 

  • Smith D.R., Slaymaker A., Palmer M. and Kaftanoglu O. 1997. Turkish honey bees belong to the east Mediterranean mitochondrial lineage. Apidologie 28: 269–274

    Article  CAS  Google Scholar 

  • Szabo B.J., Haynes C.V. and Maxwell T.A. 1995. Ages of Quaternary pluvial episodes determined by uranium series and radiocarbon dating of lacustrine deposits of Eastern Sahara. Palaeogeogr. Palaeoclimatol. Palaeoecol. 113: 227–242

    Article  Google Scholar 

  • Tamura K., Dudley J., Nei M. and Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Walsh P.S., Metzgar D.A. and Higuchi R. 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513

    PubMed  CAS  Google Scholar 

  • Williams J.L. 1987. Wind-directed pheromone trap for drone honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 80: 532–536

    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. and 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 

Download references

Acknowledgments

We thank Mustafa El-Fituri for his help in collecting samples. This work is financed by the Ministry of High Education of Libya (TS) and the EU Commission DG Research (Strategic Research Project FOOD-CT-2006-022568 BEE SHOP) (RFAM). PDR and IM are supported by the programs “Ramón y Cajal” and “Formación del Personal Universitario” of the Spanish Ministry of Science and Innovation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Shaibi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shaibi, T., Muñoz, I., Dall′Olio, R. et al. Apis mellifera evolutionary lineages in Northern Africa: Libya, where orient meets occident. Insect. Soc. 56, 293–300 (2009). https://doi.org/10.1007/s00040-009-0023-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-009-0023-3

Keywords

Navigation