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Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye

Year 2026, Volume: 13 Issue: 1, 26 - 34, 14.03.2026
https://doi.org/10.19159/tutad.1821282
https://izlik.org/JA47HW22BL

Abstract

This study aimed to characterize the genetic structure of the honey bee (Apis mellifera L.) population in Ordu Province, Türkiye, using microsatellite markers and to compare it with five regional reference populations. Worker bees were sampled from 50 colonies in 2023 and genotyped at fifteen polymorphic microsatellite loci. Genetic diversity parameters, including allele numbers, heterozygosity levels, polymorphic information content, genetic distances, and molecular variance, were calculated. The Ordu population exhibited high allelic diversity (mean observed allele number= 14.0; mean effective allele number= 9.11) and high marker informativeness (mean polymorphic information content= 0.8276). The mean expected heterozygosity (0.8445) exceeded the observed heterozygosity (0.5920). Pairwise genetic distances between Ordu and other populations ranged from 1.96 to 2.62, indicating marked genetic differentiation. Molecular variance analysis showed that 19.09% of total genetic variation was attributed to differences among populations. Multivariate and clustering analyses consistently demonstrated that the Ordu population formed a distinct genetic cluster. These findings suggest that the Ordu honey bee population represents a regionally differentiated genetic unit within the Anatolian honey bee lineage, emphasizing the importance of regulated queen exchange and region-based conservation strategies.

References

  • Arias, M.C., Silvestre, D., Sheppard, W.S., 2006. Honey bee evolutionary lineages and biogeography. Journal of Apicultural Research, 45(2): 84-90.
  • Bodur, C., Kence, M., Kence, A., 2007. Genetic structure of honey bee (Apis mellifera L.) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research, 46(1): 50-56.
  • Botstein, D., White, R.L., Skolnick, M., Davis, R.W., 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32(3): 314-331.
  • Bouga, M., Alaux, C., Bienkowska, M., Büchler, R., Carreck, N.L., 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, A.M., Siceanu, A., Soland, G., Uzunov, A., Wilde, J., 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50(1): 51-84.
  • Brookfield, J.F., 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology, 5(3): 453-455.
  • Çaglayan, N., Karabag, K., Dursun, I., Yıldız, B.I., Şimşek, A., Sahin, I., Gul, A., Cengiz, M.M., Ilkaya, M., 2025. Microsatellite-based genetic characterisation of honeybee populations from Bingöl. Mediterranean Agricultural Sciences, 38(1): 29-34.
  • Excoffier, L., Laval, G., Schneider, S., 2007. ARLEQUIN (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 23(1): 47-50.
  • Gallai, N., Salles, J.-M., Settele, J., Vaissière, B.E., 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68(3): 810-821.
  • Gebremedhn, H., Hadgu, G., Atsbha, T., 2025. Economic and nutritional value of insect pollination services in Ethiopia. Scientific Reports, 15(1): 35450.
  • Gençer, H.V., Günbey, B., 2020. The morphological characteristics of disinctive honey bee (Apis mellifera L.) genotypes in Black Sea Region. Journal of Animal Science and Products, 3(1): 40-53. (In Turkish).
  • Goulson, D., Nicholls, E., Botías, C., Rotheray, E.L., 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229): 1255957.
  • İvgin Tunca, Ç., 2009. Determination and comparison of genetic variation in honeybee (Apis mellifera L.) populations of Turkey by random amplified polymorphic DNA (RAPD) and microsatellite analyses. Doctoral Dissertation, Middle East Technical University, The Graduate School of Natural and Applied Sciences, Ankara.
  • Kandemir, İ., Kence, A., 1995. Allozyme variability in a central Anatolian honeybee (Apis mellifera L.) population. Apidologie, 26(6): 503-510.
  • Kandemir, İ., Kence, M., Kence, A., 2000. Genetic and morphometric variation in honeybee (Apis mellifera) populations of Turkey. Turkish Journal of Veterinary & Animal Sciences, 24(3): 431-442.
  • Kandemir, İ., Kence, M., Sheppard, W.S., Kence, A., 2006. Mitochondrial DNA variation in honey bee (Apis mellifera L.) populations from Turkey. Journal of Apicultural Research, 45(1): 33-38.
  • Karabağ, K., Tunca, R. İ., Tüten, E., Doğaroğlu, T., 2020. Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers. Turkish Journal of Entomology, 44(3): 333-346.
  • Kekeçoğlu, M., Ünal, E.Ö., Soysal, M.I., 2021. Genetic relationships of Thrace and Yığılca honey bee populations based on microsatellite structure. Turkish Journal of Veterinary & Animal Sciences, 45(6): 999-1009.
  • Kırpık, M.A., Bututakı, Ö., Tanrıkulu, D., 2010. Determining the relative abundance of honey bee (Apis mellifera L.) races in Kars plateau and evaluating some of their characteristics. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16: 277-282. (In Turkish).
  • Kuvancı, A., Cınbırtoğlu, Ş., Gül, A., Akdeniz, G., Eren, İ., Günbey, B., Okuyan, S., Bıyık, S., Aydın, A., Kavak, G., Ayvaz Baykal, G., Güler, A., 2023. Comparative morphological analysis of honey bees (Apis mellifera L.) from the Western and Central Black Sea Region, with emphasis on natural diversity. Bee Studies, 15(1): 25-35.
  • Kükrer, M., 2013. Genetic diversity of honey bee populations in Turkey based on microsatellite markers: A comparison between migratory versus stationary apiaries and isolated regions versus regions open to migratory beekeeping. Master’s Dissertation, Middle East Technical University, The Graduate School of Natural and Applied Sciences, Ankara, Türkiye.
  • Nawrocka, A., Kandemir, İ., Fuchs, S., Tofilski, A., 2018. Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie, 49(5): 545-553.
  • Nei, M., 1972. Genetic distance between populations. The American Naturalist, 106(949): 283-292.
  • Oleksa, A., Tofilski, A., 2015. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of honey bee subspecies. Apidologie, 46(1): 49-60.
  • Özdil, F., Yıldız, M.A., Hall, H.G., 2009. Molecular characterization of Turkish honey bee (Apis mellifera) populations: mtDNA RFLP and sequence results. Apidologie, 40(5): 570-576.
  • Ruttner, F., 1988. Biogeography and Taxonomy of Honeybees. Springer-Verlag, Berlin.
  • Solignac, M., Vautrin, D., Loiseau, A., Mougel, F., Baudry, E., Estoup, A., Garnery, L., Haberl, M., Cornuet, J.M., 2003. Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Molecular Ecology Notes, 3(2): 307-311.
  • Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38(6): 1358-1370.
  • Yıldız, B.İ., Karabağ, K., Bilge, U., GÜL, A., 2025. Explainable artificial intelligence for differentiating honey bee genotypes using morphometrics and SSR markers. Apidologie, 56: 5.
  • Yıldız, B.İ., Tüten, E., Aydın, S., Karaduman Aslan, Y., Çetin, R., Sur, E., Karabağ, K., 2023. A study of whether the genetic variation decreased or not in the protected Caucasian bee, Apis mellifera caucasica Pollmann, 1889 (Hymenoptera: Apidae) population in isolated regions. Turkish Journal of Entomology, 47(3): 271-282.

Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye

Year 2026, Volume: 13 Issue: 1, 26 - 34, 14.03.2026
https://doi.org/10.19159/tutad.1821282
https://izlik.org/JA47HW22BL

Abstract

This study aimed to characterize the genetic structure of the honey bee (Apis mellifera L.) population in Ordu Province, Türkiye, using microsatellite markers and to compare it with five regional reference populations. Worker bees were sampled from 50 colonies in 2023 and genotyped at fifteen polymorphic microsatellite loci. Genetic diversity parameters, including allele numbers, heterozygosity levels, polymorphic information content, genetic distances, and molecular variance, were calculated. The Ordu population exhibited high allelic diversity (mean observed allele number= 14.0; mean effective allele number= 9.11) and high marker informativeness (mean polymorphic information content= 0.8276). The mean expected heterozygosity (0.8445) exceeded the observed heterozygosity (0.5920). Pairwise genetic distances between Ordu and other populations ranged from 1.96 to 2.62, indicating marked genetic differentiation. Molecular variance analysis showed that 19.09% of total genetic variation was attributed to differences among populations. Multivariate and clustering analyses consistently demonstrated that the Ordu population formed a distinct genetic cluster. These findings suggest that the Ordu honey bee population represents a regionally differentiated genetic unit within the Anatolian honey bee lineage, emphasizing the importance of regulated queen exchange and region-based conservation strategies.

References

  • Arias, M.C., Silvestre, D., Sheppard, W.S., 2006. Honey bee evolutionary lineages and biogeography. Journal of Apicultural Research, 45(2): 84-90.
  • Bodur, C., Kence, M., Kence, A., 2007. Genetic structure of honey bee (Apis mellifera L.) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research, 46(1): 50-56.
  • Botstein, D., White, R.L., Skolnick, M., Davis, R.W., 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32(3): 314-331.
  • Bouga, M., Alaux, C., Bienkowska, M., Büchler, R., Carreck, N.L., 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, A.M., Siceanu, A., Soland, G., Uzunov, A., Wilde, J., 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50(1): 51-84.
  • Brookfield, J.F., 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology, 5(3): 453-455.
  • Çaglayan, N., Karabag, K., Dursun, I., Yıldız, B.I., Şimşek, A., Sahin, I., Gul, A., Cengiz, M.M., Ilkaya, M., 2025. Microsatellite-based genetic characterisation of honeybee populations from Bingöl. Mediterranean Agricultural Sciences, 38(1): 29-34.
  • Excoffier, L., Laval, G., Schneider, S., 2007. ARLEQUIN (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 23(1): 47-50.
  • Gallai, N., Salles, J.-M., Settele, J., Vaissière, B.E., 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68(3): 810-821.
  • Gebremedhn, H., Hadgu, G., Atsbha, T., 2025. Economic and nutritional value of insect pollination services in Ethiopia. Scientific Reports, 15(1): 35450.
  • Gençer, H.V., Günbey, B., 2020. The morphological characteristics of disinctive honey bee (Apis mellifera L.) genotypes in Black Sea Region. Journal of Animal Science and Products, 3(1): 40-53. (In Turkish).
  • Goulson, D., Nicholls, E., Botías, C., Rotheray, E.L., 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347(6229): 1255957.
  • İvgin Tunca, Ç., 2009. Determination and comparison of genetic variation in honeybee (Apis mellifera L.) populations of Turkey by random amplified polymorphic DNA (RAPD) and microsatellite analyses. Doctoral Dissertation, Middle East Technical University, The Graduate School of Natural and Applied Sciences, Ankara.
  • Kandemir, İ., Kence, A., 1995. Allozyme variability in a central Anatolian honeybee (Apis mellifera L.) population. Apidologie, 26(6): 503-510.
  • Kandemir, İ., Kence, M., Kence, A., 2000. Genetic and morphometric variation in honeybee (Apis mellifera) populations of Turkey. Turkish Journal of Veterinary & Animal Sciences, 24(3): 431-442.
  • Kandemir, İ., Kence, M., Sheppard, W.S., Kence, A., 2006. Mitochondrial DNA variation in honey bee (Apis mellifera L.) populations from Turkey. Journal of Apicultural Research, 45(1): 33-38.
  • Karabağ, K., Tunca, R. İ., Tüten, E., Doğaroğlu, T., 2020. Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers. Turkish Journal of Entomology, 44(3): 333-346.
  • Kekeçoğlu, M., Ünal, E.Ö., Soysal, M.I., 2021. Genetic relationships of Thrace and Yığılca honey bee populations based on microsatellite structure. Turkish Journal of Veterinary & Animal Sciences, 45(6): 999-1009.
  • Kırpık, M.A., Bututakı, Ö., Tanrıkulu, D., 2010. Determining the relative abundance of honey bee (Apis mellifera L.) races in Kars plateau and evaluating some of their characteristics. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16: 277-282. (In Turkish).
  • Kuvancı, A., Cınbırtoğlu, Ş., Gül, A., Akdeniz, G., Eren, İ., Günbey, B., Okuyan, S., Bıyık, S., Aydın, A., Kavak, G., Ayvaz Baykal, G., Güler, A., 2023. Comparative morphological analysis of honey bees (Apis mellifera L.) from the Western and Central Black Sea Region, with emphasis on natural diversity. Bee Studies, 15(1): 25-35.
  • Kükrer, M., 2013. Genetic diversity of honey bee populations in Turkey based on microsatellite markers: A comparison between migratory versus stationary apiaries and isolated regions versus regions open to migratory beekeeping. Master’s Dissertation, Middle East Technical University, The Graduate School of Natural and Applied Sciences, Ankara, Türkiye.
  • Nawrocka, A., Kandemir, İ., Fuchs, S., Tofilski, A., 2018. Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie, 49(5): 545-553.
  • Nei, M., 1972. Genetic distance between populations. The American Naturalist, 106(949): 283-292.
  • Oleksa, A., Tofilski, A., 2015. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of honey bee subspecies. Apidologie, 46(1): 49-60.
  • Özdil, F., Yıldız, M.A., Hall, H.G., 2009. Molecular characterization of Turkish honey bee (Apis mellifera) populations: mtDNA RFLP and sequence results. Apidologie, 40(5): 570-576.
  • Ruttner, F., 1988. Biogeography and Taxonomy of Honeybees. Springer-Verlag, Berlin.
  • Solignac, M., Vautrin, D., Loiseau, A., Mougel, F., Baudry, E., Estoup, A., Garnery, L., Haberl, M., Cornuet, J.M., 2003. Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Molecular Ecology Notes, 3(2): 307-311.
  • Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38(6): 1358-1370.
  • Yıldız, B.İ., Karabağ, K., Bilge, U., GÜL, A., 2025. Explainable artificial intelligence for differentiating honey bee genotypes using morphometrics and SSR markers. Apidologie, 56: 5.
  • Yıldız, B.İ., Tüten, E., Aydın, S., Karaduman Aslan, Y., Çetin, R., Sur, E., Karabağ, K., 2023. A study of whether the genetic variation decreased or not in the protected Caucasian bee, Apis mellifera caucasica Pollmann, 1889 (Hymenoptera: Apidae) population in isolated regions. Turkish Journal of Entomology, 47(3): 271-282.
There are 29 citations in total.

Details

Primary Language English
Subjects Bee and Silkworm Breeding and Improvement
Journal Section Research Article
Authors

Berkant İsmail Yıldız 0000-0001-8965-6361

Mert Akgün This is me

Zübeyde Sönmez This is me 0000-0002-7701-4510

Akın Çiftçi This is me 0009-0002-0521-5679

Ersin Soydan 0009-0006-8305-9113

Kemal Karabağ 0000-0002-4516-6480

Submission Date November 18, 2025
Acceptance Date March 2, 2026
Publication Date March 14, 2026
DOI https://doi.org/10.19159/tutad.1821282
IZ https://izlik.org/JA47HW22BL
Published in Issue Year 2026 Volume: 13 Issue: 1

Cite

APA Yıldız, B. İ., Akgün, M., Sönmez, Z., Çiftçi, A., Soydan, E., & Karabağ, K. (2026). Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye. Türkiye Tarımsal Araştırmalar Dergisi, 13(1), 26-34. https://doi.org/10.19159/tutad.1821282
AMA 1.Yıldız Bİ, Akgün M, Sönmez Z, Çiftçi A, Soydan E, Karabağ K. Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye. Türkiye Tarımsal Araştırmalar Dergisi. 2026;13(1):26-34. doi:10.19159/tutad.1821282
Chicago Yıldız, Berkant İsmail, Mert Akgün, Zübeyde Sönmez, Akın Çiftçi, Ersin Soydan, and Kemal Karabağ. 2026. “Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye”. Türkiye Tarımsal Araştırmalar Dergisi 13 (1): 26-34. https://doi.org/10.19159/tutad.1821282.
EndNote Yıldız Bİ, Akgün M, Sönmez Z, Çiftçi A, Soydan E, Karabağ K (March 1, 2026) Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye. Türkiye Tarımsal Araştırmalar Dergisi 13 1 26–34.
IEEE [1]B. İ. Yıldız, M. Akgün, Z. Sönmez, A. Çiftçi, E. Soydan, and K. Karabağ, “Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye”, Türkiye Tarımsal Araştırmalar Dergisi, vol. 13, no. 1, pp. 26–34, Mar. 2026, doi: 10.19159/tutad.1821282.
ISNAD Yıldız, Berkant İsmail - Akgün, Mert - Sönmez, Zübeyde - Çiftçi, Akın - Soydan, Ersin - Karabağ, Kemal. “Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye”. Türkiye Tarımsal Araştırmalar Dergisi 13/1 (March 1, 2026): 26-34. https://doi.org/10.19159/tutad.1821282.
JAMA 1.Yıldız Bİ, Akgün M, Sönmez Z, Çiftçi A, Soydan E, Karabağ K. Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye. Türkiye Tarımsal Araştırmalar Dergisi. 2026;13:26–34.
MLA Yıldız, Berkant İsmail, et al. “Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye”. Türkiye Tarımsal Araştırmalar Dergisi, vol. 13, no. 1, Mar. 2026, pp. 26-34, doi:10.19159/tutad.1821282.
Vancouver 1.Berkant İsmail Yıldız, Mert Akgün, Zübeyde Sönmez, Akın Çiftçi, Ersin Soydan, Kemal Karabağ. Microsatellite-Based Genetic Characterization of Honeybees from the Ordu Region, Türkiye. Türkiye Tarımsal Araştırmalar Dergisi. 2026 Mar. 1;13(1):26-34. doi:10.19159/tutad.1821282