Abstract
Mitochondrial DNA sequence variation can be used to infer honeybee evolutionary relationships. In this study, DNA sequence diversity of the mitochondrial 16s rDNA region was investigated in 112 honeybees from 15 populations in Turkey, which is mainly populated with Apis mellifera anatoliaca, A. m. caucasica, and A. m. meda. The study revealed 11 haplotypes for this segment, with 13 variable sites and nine parsimony informative sites. The haplotypes were not discriminated according to their geographical locations in a neighbor-joining dendrogram based on 16s rDNA sequences available in Genbank, but all the haplotypes obtained in this study are clustered with published haplotypes such as A. mellifera TAS (AF214666) and A. m. ligustica (EF116868) and with some unpublished Genbank records (HQ318928, HQ318934, and HQ318938). This study expands the knowledge of the mitochondrial 16s rDNA region, and it presents the first comprehensive sequence analysis of this region in Turkish honeybees.
Similar content being viewed by others
References
Adl MBF, Gençer HV, Fıratlı Ç, Bahreini R (2007) Morphometric characterization of Iranian (Apis mellifera meda), Central Anatolian (Apis mellifera anatoliaca) and Caucasian (Apis mellifera caucasica) honey bee populations. J Apicult Res 46:225–231
Arias MC, Sheppard WS (1996) Molecular phylogenetics of honey bee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequence. Mol Phylogenet Evol 5:557–566
Asal S, Kocabas S, Elmacı C, Yıldız MA (1995) Enzyme polymorphism in honey bee (Apis mellifera L.) from Anatolia. Turk J Zool 19:153–156
Bouga M, Harizanis PC, Kilias G, Alahiotis S (2005) Genetic divergence and phylogenetic relationships of honey bee Apis mellifera (Hymenoptera: Apidae) populations from Greece and Cyprus using PCR-RFLP analysis of three mtDNA segments. Apidologie 36:335–344
Bouga M, Alaux C, Bienkowska M, Büchler R, Carreck NL, Cauia E, Chlebo R, Dahle B, Dall’olio R, De La Rúa P, Gregorc A, Ivanova E, Kence A, Kence M, Kezic N, Kiprijanovska H, Kozmus P, Kryger P, Le Conte Y, Lodesani M, Murilhas AM, Siceanu A, Soland G, Uzunov A, Wilde J (2011) A review of methods for discrimination of honey bee populations as applied to European beekeeping. J Apicult Res 50:51–84
Collet T, Arias MC, Del Lama MA (2007) 16S mtDNA variation in Apis mellifera detected by PCR-RFLP. Apidologie 38:47–54
Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133:97–117
De la Rúa P, Serrano J, Galián J (2002) Biodiversity of Apis mellifera populations from Tenerife (Canary Islands) and hybridization with East European races. Biodivers Conserv 11:59–67
De la Rúa P, Hernández-Garcia R, Pedersen BV, Galián J, Serrano J (2004) Molecular diversity of honeybee Apis mellifera iberica L. (Hymenoptera: Apidae) from western Andalusia. Arch Zootec 53:195–203
Franck P, Garnery L, Solignac M, Cornuet J-M (2000) Molecular confirmation of a fourth lineage in honeybees from the Near East. Apidologie 31:167–180
Franck P, Garnery L, Loiseau A, Oldroyd BP, Hepburn HR, Solignac M, Cornuet J-M (2001) Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86:420–430
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
Garnery L, Solignac M, Celebrano G, Cornuet J-M (1993) A simple test using restricted PCR amplified mitochondrial DNA to study the genetic structure of Apis mellifera. Experientia 49:1016–1021
Gençer HV, Fıratlı Ç (1999) Morphological characteristics of the Central Anatolian (A. m. anatoliaca) and Caucasian (A. m. caucasica) honey bees. Turk J Vet A Anim Sci 23(Suppl 1):107–113
Hall HG (1990) Parental analysis of introgressive hybridization between African and European honeybees using nuclear DNA RFLPs. Genetics 125:611–621
Hall HG, Smith DR (1991) Distinguishing African and European honeybee matrilines using amplified mitochondrial DNA. Proc Natl Acad Sci USA 88:4548–4552
Kandemir I, Kence M, Sheppard WS, Kence A (2006) Mitochondrial DNA variation in honey bee (Apis mellifera L.) populations from Turkey. J Apicult Res Bee World 45(1):33–38
Kauhausen-Keller D, Ruttner F, Keller R (1997) Morphometric studies on the microtaxonomy of the species Apis mellifera L. Apidologie 28:295–307
Kekeçoglu M, Bouga Soysal MI M, Harizanis P (2009) Genetic divergence and phylogenetic relationships of honey bee populations from Turkey using PCR-RFLP analysis of two mtDNA segments. Bulgar J Agric Sci 15:589–597
Magnus R, Szalanski AL (2010) Genetic evidence for honey bees (Apis mellifera L.) of middle eastern lineage in the United States. Sociobiology 55:285–296
Marino A, Sabatini AG, Carpana E, Mantovani B (2002) Analysis of mitochondrial genes NDH2, CO1 and 16S for the characterization of Apis mellifera populations. Insects Soc Life 4:87–92
Martimianakis S, Klossa-Kilia E, Bouga M, Kilias G (2011) Phylogenetic relationships of Greek Apis mellifera subspecies based on sequencing of mtDNA segments (COI and ND5). J Apicult Res 50(1):42–50
Muňoz I, Dall’Olio R, Lodesani M, De la Rúa P (2009) Population genetic structure of coastal Croatian honeybees (Apis mellifera carnica). Apidologie 40:617–626
Özdil F, Yıldız MA, Hall HG (2009a) Molecular characterization of Turkish honey bee populations (Apis mellifera L.) inferred from mitochondrial DNA RFLP and sequence results. Apidologie 40(5):570–576
Özdil F, Fakhri B, Meydan H, Yıldız MA, Hall HG (2009b) Mitochondrial DNA variation in the CoxI-CoxII intergenic region among Turkish and Iranian honey bees (Apis mellifera L.). Biochem Genet 47:717–721
Özdil F, Aytekin I, Ilhan F, Boztepe S (2012) Genetic variation in Turkish honeybees (Apis mellifera anatoliaca, A. m. caucasica, A. m. meda) inferred from RFLP analysis of three mtDNA segments (16S rDNA-COI-ND5). Eur J Entomol 109(2):161–167
Palmer MR, Smith DR, Kaftanoğlu O (2000) Turkish honeybees: genetic variation and evidence for a fourth lineage of Apis mellifera mtDNA. J Hered 91:42–46
Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin, p 284
Smith DR, Slaymaker A, Palmer M, Kaftanoğlu O (1997) Turkish honeybees belong to the east Mediterranean mitochondrial lineage. Apidologie 28:269–274
Stevanovic J, Stanimirovic Z, Radakovic M, Kovacevic RS (2010) Biogeographic study of the honey bee (Apis mellifera L.) from Serbia, Bosnia and Herzegovina and Republic of Macedonia based on mitochondrial DNA analyses. Russ J Genet 46:603–609
Sušnik S, Kozmus P, Poklukar J, Meglić V (2004) Molecular characterization of indigenous Apis mellifera carnica in Slovenia. Apidologie 35:623–636
Szalanski AL, Magnus RM (2010) Mitochondrial DNA characterization of Africanized honey bee (Apis mellifera L.) populations from the USA. J Apicult Res Bee World 49:177–185
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
Tanaka H, Roubik DW, Kato M, Liew F, Gunsalam G (2001) Phylogenetic position of Apis nuluensis of northern Borneo and phylogeography of A. cerana as inferred from mitochondrial DNA sequences. Insect Soc 48:44–51
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Yıldız MA, Asal S (1996) General protein (P-3) polymorphism in honey bee (Apis mellifera L.) from Centeral Anatolia. Turk J Vet Anim Sci 20:379–381
Acknowledgments
The authors would like to thank Prof. Dr. Mehmet Ali Yildiz (Ankara University, Faculty of Agriculture) for providing insight and guidance during various phases of this project. We also thank the anonymous reviewers for their comments on an earlier version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Özdil, F., Ilhan, F. Diversity of Apis mellifera Subspecies from Turkey Revealed by Sequence Analysis of Mitochondrial 16s rDNA Region. Biochem Genet 50, 748–760 (2012). https://doi.org/10.1007/s10528-012-9517-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10528-012-9517-1