Araştırma Makalesi
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Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers

Yıl 2020, Cilt: 44 Sayı: 3, 333 - 346, 01.09.2020
https://doi.org/10.16970/entoted.678808

Öz

Turkey, having three phytogeographical floristic regions, is a natural bridge among three continents. A lot of subspecies and ecotypes of honey bees have been reported within Turkey. However, hybridization due to informal cultivation and uncontrolled migratory beekeeping practices are thought to affect the genetic diversity of local honey bee populations, and this may result the loss of allele combinations resulting from long evolutionary processes. Numerous identification and conservation studies on honey bee subspecies have been conducted in many countries to determine the loss of genetic variability. On this basis, genetic causes and phylogenetic relationships of four common honey bee subspecies [Apis mellifera anatoliaca Maa, 1953, Apis mellifera carnica Pollmann, 1879, Apis mellifera caucasica Pollmann, 1889, Apis mellifera syriaca Skorikov, 1829 (Hymenoptera: Apidae)] from five provinces (Artvin, Düzce, Hatay, Kırklareli and Muğla) selected based on their importance in apicultural activities were studied using 30 microsatellite loci in 2018. The genetic distances of populations ranged from 0.30 to 0.70. Genetic variation was 8.96% among the populations, 44.9% among the individuals within the populations and 46.1% for all individuals. Further genetic researches on the honey bee populations will be of advantage for anticipating potential future problems.

Destekleyen Kurum

Agriculture Ministry of Turkey

Proje Numarası

TAGEM-15/ARGE/19

Teşekkür

We thank to Agriculture Ministry of Turkey. The project was supported by TAGEM-15/ARGE/19.

Kaynakça

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  • Akyol, E., A. Unalan, H. Yeninar, D. Ozkok & C. Ozturk, 2014. Comparison of colony performances of Anatolian, Caucasian and Carniolan honeybee (Apis mellifera L.) genotypes in temperate climate conditions. Italian Journal of Animal Science, 13 (3): 637-640.
  • Alburaki, M., B. Bertrand, H. Legout, S. Moulin, A. Alburaki, W. S. Sheppard & L. Garnery, 2013. A fifth major genetic group among honeybees revealed in Syria. BMC Genetics, 14 (1): 117-127.
  • Amakpe, F., L. De Smet, M. Brunain, F. J. Jacobs, B. Sinsin & D. C. de Graaf, 2018. Characterization of Native Honey Bee Subspecies in Republic of Benin Using Morphometric and Genetic Tools. Journal of Apicultural Science, 62 (1): 47-60.
  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996-2004. GENETIX 4.05, logiciel sous Windows pour la ge´ne´tique des populations. Laboratoire Ge ́nome, Populations, Interactions,CNRS UMR 5000, Universite ́de Montpellier II, Montpellier (France).
  • Bodur, C., M. Kence & A. Kence, 2007. Genetic structure of honey bee, Apis mellifera L. (Hymenoptera: Apidae) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research, 46 (1): 50-56.
  • Bouga, M., C. Alaux, M. Bienkowska, R. Büchler, N. L. Carreck, E. Cauia & A. Gregorc, 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50 (1): 51-84.
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  • Chahbar, N., I. Munoz, R. Dall’Olio, P. De la Rúa, J. Serrano & S. Doumandji, 2013. Population structure of North African honey bees is influenced by both biological and anthropogenic factors. Journal of Insect Conservation, 17 (2): 385-392.
  • Dall’Olio, R., A. Marino, M. Lodesani & R. F. A. Moritz, 2007. Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie, 38 (2): 207-217.
  • De la Rúa, P., J. Galián, J. Serrano & R. F. Moritz, 2003. Genetic structure of Balearic honeybee populations based on microsatellite polymorphism. Genetics Selection Evolution, 35 (3): 339-350.
  • Doyle, J. J., 1990. Isolation of plant DNA from fresh tissue. Focus, 12: 13-15.
  • Earl, D. A. & B. M. vonHoldt, 2012. Structure harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4: 359-361.
  • Ellis, J. S., G. Soland-Reckeweg, V. G. Buswell, J. V. Huml, A. Brown & M. E. Knight, 2018. Introgression in native populations of Apis mellifera mellifera L: implications for conservation. Journal of Insect Conservation, 22 (4): 377-390.
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  • Franck P., L. Garnery, G. Celebrano, M. Solignac & J. M. Cornuet, 2000a. Hybrid origins of honeybees from Italy (Apis mellifera ligustica) and Sicily (A. m. sicula). Molecular Ecology, 9 (7): 907-921.
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  • Güder, A., R. Işık & F. Özdil, 2017. Analysis of mtDNA 16S rDNA and ND5 Genes in Thracen Honey Bees of Turkey (Apis mellifera L.). Journal of Animal Production, 58 (2): 7-14.
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Anadolu'da bulunan bal arılarının otuz polimorfik mikrosatellit belirteçleri açısından güncel genetik durumları

Yıl 2020, Cilt: 44 Sayı: 3, 333 - 346, 01.09.2020
https://doi.org/10.16970/entoted.678808

Öz

            Üç fitocoğrafik floristik bölgeye sahip olan Türkiye, üç kıta arasında doğal bir köprüdür. Bugüne kadar Türkiye sınırları içerisinde birçok bal arısı alt türü ve ekotipi bildirilmiştir. Ancak, kayıt dışı yetiştiricilik ve kontrolsüz göçer arıcılık uygulamalarına bağlı melezleşmenin yerel bal arısı popülasyonlarının genetik çeşitliliğini etkilediği düşünülmektedir ve bu, uzun evrimsel süreçlerden kaynaklanan allel kombinasyonlarının kaybıyla sonuçlanabilir. Bal arısı alttürleri üzerinde genetik değişkenliğin kaybını önlemek amacıyla birçok ülkede tanımlama ve koruma çalışmaları yapılmıştır. Bu temelde, 2018’de arıcılık faaliyetlerindeki öneminden dolayı seçilen beş ilden (Artvin, Düzce, Hatay, Kırklareli ve Muğla) dört yaygın bal arısı ırkının [Apis mellifera anatoliaca Maa, 1953, Apis mellifera carnica Pollmann,1879, Apis mellifera caucasica Pollmann, 1889, Apis mellifera syriaca Skorikov, 1829 (Hymenoptera: Apidae)] genetik açıdan durumları ve filogenetik ilişkileri otuz mikrosatellit lokusu kullanılarak güncellenmeye çalışılmıştır. Popülasyonlar arası genetik mesafe 0.30 ile 0.70 arasında değişmiştir. Genetik varyasyonlar, popülasyonlar arasında %8.96, popülasyonlardaki bireyler arasında %44.9 ve tüm bireyler arasında %46.1 olarak hesaplanmıştır. Bal arısı ile ilgili daha fazla genetik araştırma, gelecekteki potansiyel sorunlardan kaçınmak için avantajlı olacaktır.

Proje Numarası

TAGEM-15/ARGE/19

Kaynakça

  • Agra, M. N., C. A. Conte, P. M. Corva, J. L. Cladera, S. B. Lanzavecchia & M. A. Palacio, 2018. Molecular characterization of Apis mellifera colonies from Argentina: genotypic admixture associated with ecoclimatic regions and apicultural activities. Entomologia Experimentalis et Applicata, 166 (9): 724-738.
  • Akyol, E., A. Unalan, H. Yeninar, D. Ozkok & C. Ozturk, 2014. Comparison of colony performances of Anatolian, Caucasian and Carniolan honeybee (Apis mellifera L.) genotypes in temperate climate conditions. Italian Journal of Animal Science, 13 (3): 637-640.
  • Alburaki, M., B. Bertrand, H. Legout, S. Moulin, A. Alburaki, W. S. Sheppard & L. Garnery, 2013. A fifth major genetic group among honeybees revealed in Syria. BMC Genetics, 14 (1): 117-127.
  • Amakpe, F., L. De Smet, M. Brunain, F. J. Jacobs, B. Sinsin & D. C. de Graaf, 2018. Characterization of Native Honey Bee Subspecies in Republic of Benin Using Morphometric and Genetic Tools. Journal of Apicultural Science, 62 (1): 47-60.
  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996-2004. GENETIX 4.05, logiciel sous Windows pour la ge´ne´tique des populations. Laboratoire Ge ́nome, Populations, Interactions,CNRS UMR 5000, Universite ́de Montpellier II, Montpellier (France).
  • Bodur, C., M. Kence & A. Kence, 2007. Genetic structure of honey bee, Apis mellifera L. (Hymenoptera: Apidae) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research, 46 (1): 50-56.
  • Bouga, M., C. Alaux, M. Bienkowska, R. Büchler, N. L. Carreck, E. Cauia & A. Gregorc, 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50 (1): 51-84.
  • Cánovas, F., P. De la Rua, J. Serrano & J. Galián, 2011. Microsatellite variability reveals beekeeping influences on Iberian honeybee populations. Apidologie, 42 (3): 235-251.
  • Chahbar, N., I. Munoz, R. Dall’Olio, P. De la Rúa, J. Serrano & S. Doumandji, 2013. Population structure of North African honey bees is influenced by both biological and anthropogenic factors. Journal of Insect Conservation, 17 (2): 385-392.
  • Dall’Olio, R., A. Marino, M. Lodesani & R. F. A. Moritz, 2007. Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie, 38 (2): 207-217.
  • De la Rúa, P., J. Galián, J. Serrano & R. F. Moritz, 2003. Genetic structure of Balearic honeybee populations based on microsatellite polymorphism. Genetics Selection Evolution, 35 (3): 339-350.
  • Doyle, J. J., 1990. Isolation of plant DNA from fresh tissue. Focus, 12: 13-15.
  • Earl, D. A. & B. M. vonHoldt, 2012. Structure harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4: 359-361.
  • Ellis, J. S., G. Soland-Reckeweg, V. G. Buswell, J. V. Huml, A. Brown & M. E. Knight, 2018. Introgression in native populations of Apis mellifera mellifera L: implications for conservation. Journal of Insect Conservation, 22 (4): 377-390.
  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of cluster of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14 (8): 2611-2620.
  • Excoffier, L., G. Laval & S. Schneider, 2007. ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 23 (1): 47-50.
  • Excoffier, L., P. E. Smousse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131 (2): 479-491.
  • Fontana, P., C. Costa, G. Di Prisco, E. Ruzzier, D. Annoscia, A. Battisti & R. Dall’Olio, 2018. Appeal for biodiversity protection of native honey bee subspecies of Apis mellifera in Italy (San Michele all'Adige declaration). Bulletin of Insectology, 71 (2): 257-271.
  • Franck P., L. Garnery, G. Celebrano, M. Solignac & J. M. Cornuet, 2000a. Hybrid origins of honeybees from Italy (Apis mellifera ligustica) and Sicily (A. m. sicula). Molecular Ecology, 9 (7): 907-921.
  • Franck, P., L. Garnery & A. Loiseau, 2001. Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity, 86 (4): 420-430.
  • Franck, P., L. Garnery, M. Solignac & J. M. Cornuet, 1998. The origin of west European subspecies of honeybees (Apis mellifera): New insights from microsatellite and mitochondrial data. Evolution, 52 (4): 1119-1134.
  • Franck, P., L. Garnery, M. Solignac & J. M. Cornuet, 2000b. Molecular confirmation of a fourth lineage in honeybees from the Near East. Apidologie, 31 (2): 167-180.
  • Garnery, L., P. Franck, E. Baudry, D. Vautrin, J. M. Cornuet, & M. Solignac, 1998. Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica) II. Microsatellite loci. Genetics Selection Evolution, 30 (1): 1-26.
  • Garza, J. C. & E. G. Williamson, 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology, 10 (2): 305-318.
  • Ghassemi-Khademi, T., H. Rajabi-Maham & S. Pashaei-Rad, 2018. Genetic diversity evaluation of Persian honeybees (Apis mellifera meda) in North West of Iran, using microsatellite markers. Journal of Wildlife and Biodiversity, 2 (2): 37-46.
  • Güder, A., R. Işık & F. Özdil, 2017. Analysis of mtDNA 16S rDNA and ND5 Genes in Thracen Honey Bees of Turkey (Apis mellifera L.). Journal of Animal Production, 58 (2): 7-14.
  • Haddad, N. J., N. Adjlane, D. Saini, A. Menon, V. Krishnamurthy, D. Jonklaas, J. P. Tomkins, W. L. Ayad & L. Horth, 2018. Whole genome sequencing of north African honey bee Apis mellifera intermissa to assess its beneficial traits. Entomological Research, 48 (3): 174-186.
  • Hassett, J., K. A. Browne, G. P. McCormack, E. Moore, N. I. H. B. Society, G. Soland & M. Geary, 2018. A significant pure population of the dark European honey bee (Apis mellifera mellifera) remains in Ireland. Journal of Apicultural Research, 57 (3): 337-350.
  • Ilyasov, R. A., A. V. Poskryakov, A. V. Petukhov & A. G. Nikolenko, 2016. Molecular genetic analysis of five extant reserves of black honeybee Apis melifera melifera in the Urals and the Volga region. Russian Journal of Genetics, 52 (8): 828-839.
  • Ivgin Tunca, R., 2009. Determination and Comparison of Genetic Variation in Honey Bee (Apis mellifera L.) Populations of Turkey by Random Amplified Polymorphic DNA and Microsatellite Analyses. Middle East Technical University, (Unpublished) Ph.D. Thesis, Ankara, 152 pp.
  • Ivgin Tunca, R. & M. Kence, 2011. Genetic diversity of honey bee (Apis mellifera L.: Hymenoptera: Apidae) populations in Turkey revealed by RAPD markers. African Journal of Agricultural Research, 6 (29): 6217-6225.
  • Ivgin Tunca, R., M. Kence, A. Galindo, T. Giray & A. Kence, 2012. “SNP (Single Nucleotide Polymorphism) analysis on the honeybees of Turkey, 138”. 5th European Conference of Apidology, (03-07.09.2012, Halle an der Saale, Germany), Martin-Luther-University, 296 pp.
  • Kalinowski, S. T. & M. L. Taper, 2006. Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conservation Genetics, 7 (6): 991-995.
  • Kambur, M. & M. Kekeçoğlu, 2018. The loss of genetic diversity on native Turkish honey bee (Apis mellifera L.) subspecies. Anadolu Journal of Agricultural Sciences, 33 (1): 73-84.
  • Kandemir, I. & A. Kence, 1995. Allozyme variability in a central Anatolian honey bee (Apis mellifera L.) population. Apidologie, 26 (6): 503-510.
  • Kandemir, I., M. Kence & A. Kence, 2000. Genetic and morphometric variation in honeybee (Apis mellifera L.) populations of Turkey. Apidologie, 31 (3): 343-356.
  • Kandemir, İ., M. Kence & A. Kence, 2005. Morphometric and electrophoretic variation in different honeybee (Apis mellifera L.) populations. Turkish Journal of Veterinary and Animal Sciences, 29 (3): 885-890.
  • Kandemir, I., M. Kence, W. S. Sheppard & A. Kence, 2006. Mitochondrial DNA variation in honey bee (Apis mellifera L.) populations from Turkey. Journal of Apicultural Research, 45 (1): 33-38.
  • Kekeçoğlu, M., M. Bouga, P. Harizanis & M. I. Soysal, 2009. Genetic divergence and phylogenetic relationships of honey bee populations from Turkey using PCR-RFLP’s analysis of two mtDNA segments. Bulgarian Journal of Agricultural Science, 15 (6): 589-597.
  • Kekeçoğlu, M. & M. I. Soysal, 2010. Genetic diversity of bee ecotypes in Turkey and evidence for geographical differences. Romanian Biotechnological Letters, 15 (5): 5646-5653.
  • Kence, M., H. J. Farhoud & R. I. Tunca, 2009. Morphometric and genetic variability of honey bee (Apis mellifera L.) populations from northern Iran. Journal of Apicultural Research, 48 (4): 247-255.
  • Kence, A., R. Ivgin Tunca, M. Kence & T. Giray, 2012. “Studies on the characterization and conservation of Kırklareli Honey Bees, 28.” 1st International Symposium on the Carniolan honey bee, (16 March 2012, Celje, Slovenia).
  • Liu, F., T. Shi, S. Huang, L. Yu & S. Bi, 2016. Genetic structure of Mount Huang honey bee (Apis cerana) populations: evidence from microsatellite polymorphism. Hereditas, 153 (8): 1-6.
  • Luikart, G., F. W. Allendorf, J. M. Cornuet & W. B. Sherwin, 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity, 89 (3): 238-247.
  • McMenamin, A. J., K. F. Daughenbaugh, F. Parekh, M. C. Pizzorno & M. L. Flenniken, 2018. Honey bee and bumble bee antiviral defense. Viruses, 10 (8): 395.
  • Meixner, M. D., M. A. Pinto, M. Bouga, P. Kryger, E. Ivanova & S. Fuchs, 2013. Standard methods for characterizing subspecies and ecotypes of Apis mellifera. Journal of Apicultural Research, 52 (4): 1-28.
  • Mielnik-Sikorska, M., P. Daca, B. Malyarchuk, M. Derenko, K. Skonieczna, M. Perkova, T. Dobosz & T. Grzybowski, 2013. The history of Slavs inferred from complete mitochondrial genome sequences. Plos One, 8 (1): e54360.
  • Nawrocka, A., İ. Kandemir, S. Fuchs & A. Tofilski, 2018. Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie, 49 (2): 172-184.
  • Nei, M., 1972. Genetic distance between populations. The American Naturalist, 106 (949): 283-292.
  • Nikolova, S. R., M. Bienkowska, D. Gerula & E. N. Ivanova, 2015. Microsatellite DNA polymorphism in selectively controlled Apis mellifera carnica and Apis mellifera caucasica populations from Poland. Archives of Biological Sciences, 67 (3): 889-894.
  • Oleksa, A. & A. Tofilski, 2015. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of honey bee subspecies. Apidologie, 46 (1): 49-60.
  • Özdil, F., M. A. Yildiz & H. G. Hall, 2009. Molecular characterization of Turkish honey bee populations (Apis mellifera L.) inferred from mitochondrial DNA RFLP and sequence results. Apidologie, 40 (5): 570-576.
  • Palmer, M. R., D. R. Smith & O. Kaftanoglu, 2000. Turkish honey bees: Genetic variation and evidence for a fourth lineage of Apis mellifera mtDNA. Journal of Heredity, 91 (1): 42-46.
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  • Park, S. D. E., 2001. The Excel Microsatellite-Toolkit. Animal Genomics Lab, University of College Dublin, Ireland.
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  • Smith, D. R., A. Slaymaker, M. Palmer & O. Kaftanoglu, 1997. Turkish honey bees belong to the east Mediterranean mitochondrial lineage. Apidologie, 28 (5): 269-274.
  • Solignac, M., D., Vautrin, A. Loiseau, F. Mougel, E. Baudry, A. Estoup, L. Garnery, M. Haberl & J. M. Cornuet, 2003. Five hundred and fifty microsatellite markers for the study of the honey bee (Apis mellifera L.) genome. Molecular Ecology Notes, 3 (2): 307-311.
  • Tantillo, G., M. Bottaro, A. Di Pinto, V. Martella, P. Di Pinto & V. Terio, 2015. Virus infections of honeybees Apis Mellifera. Italian Journal of Food Safety, 4 (3): 157-168.
  • Ünal, G. & F. Özdil, 2018. Genetic characterization of Thrace honey bee populations of Turkey: restriction and sequencing of inter cytochrome C oxidase I-II (CoxI-CoxII) genes. Journal of Apicultural Research, 57 (2): 213-218.
  • Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38 (6): 1358-1370.
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  • Yeh, F. C., R. C. Yang, T. B. J. Boyle, Z. H. Ye & J. X. Mao, 1997. POPGENE, The User-Friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada.
  • Yu, Y., S. Zhou, X. Zhu, X. Xu, W. Wang, L. Zha, P. Wang, J. Wang, K. Lai, S. Wang, L. Hao & B. Zhou, 2019. Genetic differentiation of Eastern honey bee (Apis cerana) populations across Qinghai-Tibet Plateau-Valley Landforms. Frontiers in Genetics, 10 (483): 1-11.
Toplam 70 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm Makaleler
Yazarlar

Kemal Karabağ 0000-0002-4516-6480

Rahşan İvgin Tunca 0000-0003-0745-6732

Emel Tüten 0000-0002-3105-6416

Taylan Doğaroğlu 0000-0002-4671-1372

Proje Numarası TAGEM-15/ARGE/19
Yayımlanma Tarihi 1 Eylül 2020
Gönderilme Tarihi 22 Ocak 2020
Kabul Tarihi 11 Mayıs 2020
Yayımlandığı Sayı Yıl 2020 Cilt: 44 Sayı: 3

Kaynak Göster

APA Karabağ, K., İvgin Tunca, R., 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. https://doi.org/10.16970/entoted.678808
AMA Karabağ K, İvgin Tunca R, Tüten E, Doğaroğlu T. Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers. TED. Eylül 2020;44(3):333-346. doi:10.16970/entoted.678808
Chicago Karabağ, Kemal, Rahşan İvgin Tunca, Emel Tüten, ve Taylan Doğaroğlu. “Current Genetic Status of Honey Bees in Anatolia in Terms of Thirty Polymorphic Microsatellite Markers”. Turkish Journal of Entomology 44, sy. 3 (Eylül 2020): 333-46. https://doi.org/10.16970/entoted.678808.
EndNote Karabağ K, İvgin Tunca R, Tüten E, Doğaroğlu T (01 Eylül 2020) Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers. Turkish Journal of Entomology 44 3 333–346.
IEEE K. Karabağ, R. İvgin Tunca, E. Tüten, ve T. Doğaroğlu, “Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers”, TED, c. 44, sy. 3, ss. 333–346, 2020, doi: 10.16970/entoted.678808.
ISNAD Karabağ, Kemal vd. “Current Genetic Status of Honey Bees in Anatolia in Terms of Thirty Polymorphic Microsatellite Markers”. Turkish Journal of Entomology 44/3 (Eylül 2020), 333-346. https://doi.org/10.16970/entoted.678808.
JAMA Karabağ K, İvgin Tunca R, Tüten E, Doğaroğlu T. Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers. TED. 2020;44:333–346.
MLA Karabağ, Kemal vd. “Current Genetic Status of Honey Bees in Anatolia in Terms of Thirty Polymorphic Microsatellite Markers”. Turkish Journal of Entomology, c. 44, sy. 3, 2020, ss. 333-46, doi:10.16970/entoted.678808.
Vancouver Karabağ K, İvgin Tunca R, Tüten E, Doğaroğlu T. Current genetic status of honey bees in Anatolia in terms of thirty polymorphic microsatellite markers. TED. 2020;44(3):333-46.