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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

Yıl 2023, Cilt: 47 Sayı: 3 - Yıl: 2023 Cilt: 47 Sayı:3, 271 - 282, 09.10.2023
https://doi.org/10.16970/entoted.1273612

Öz

The Caucasian honeybee, Apis mellifera caucasica Pollmann, 1889 (Hymenoptera: Apidae), is one of the most productive bee subspecies. This subspecies, which has special importance for Türkiye, has been taken under protection in two isolated regions (Artvin and Ardahan) since 2000. To date, no study has been conducted on whether genetic diversity has decreased in these protected Caucasian honeybee colonies. Therefore in 2022, worker bees were collected from 100 different colonies in 15 different locations in these two regions and their genetic variations were examined using 30 microsatellite loci. The average number of alleles per locus was 13.57, and the loci had a high level of information content according to the PIC (0.7) value. FIS (0.96) and FST (0.01) values showed low genetic diversity and high inbreeding in populations. Genetic variations were calculated as 0.77% among populations, 99.23% among individuals in populations, and 0% among all individuals. Also, populations deviated from the Hardy-Weinberg equilibrium (p<0.001). Significant bottleneck evidence was found for Artvin in the analysis results using the two-phase mutation model. These results provide important information that can be used as a guide for Caucasian bee breeding strategies and conservation programs.

Destekleyen Kurum

Türkiye Cumhuriyeti Tarım ve Orman Bakanlığı

Proje Numarası

2021A03-168656

Teşekkür

We thank The Republic of Turkey Ministry of Agriculture. The project was supported by HAYGEM with project number 2021A03-168656.

Kaynakça

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  • Arslan, S., M. M. Cengiz, A. Gül & S. Sayed, 2021. Evaluation of the standards compliance of the queen bees reared in the Mediterranean region in Turkey. Saudi Journal of Biological Sciences, 28 (5): 2686-2691.
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  • 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.
  • Botstein, D., R. L. White, M. Skolnick & R. W. Davis, 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American journal of human genetics, 32 (3): 314-331.
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  • Castric, V., L. Bernatchez, K. Belkhir & F. Bonhomme, 2002. Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity, 89 (1): 27-35.
  • Cornuet, J. M. & G. Luikart, 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144 (4): 2001-2014.
  • 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.
  • Dirienzo, A., A. C. Peterson, J. C. Garza, A. M. Valdes, M. Slatkin & N. B. Freimer, 1994. Mutational processes of simple-sequence repeat loci in human-populations. Proceedings of National Academy of Sciences, 91 (8): 3166-3170.
  • 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.
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İzole bölgelerde korunan Kafkas arısı, Apis mellifera caucasica Pollmann, 1889 (Hymenoptera: Apidae) popülasyonunda genetik varyasyonun azalıp azalmadığına dair bir çalışma

Yıl 2023, Cilt: 47 Sayı: 3 - Yıl: 2023 Cilt: 47 Sayı:3, 271 - 282, 09.10.2023
https://doi.org/10.16970/entoted.1273612

Öz

Kafkas arısı, Apis mellifera caucasica Pollmann, 1889 (Hymenoptera: Apidae), en verimli arı alt türlerinden biridir. Türkiye için özel bir öneme sahip olan bu alt tür, 2000 yılından itibaren iki izole bölgede (Artvin ve Ardahan) koruma altına alınmıştır. Bugüne kadar korunan Kafkas bal arısı kolonilerinde genetik çeşitliliğin azalıp azalmadığına dair bir çalışmaya rastlanmamıştır. Bu nedenle 2022 yılında, bu iki izole bölgede 15 farklı lokasyonda bulunan 100 farklı koloniden işçi arılar toplanmış ve 30 mikrosatelit lokusu kullanılarak genetik varyasyonlar incelenmiştir. Lokus başına ortalama allel sayısı 13.57 bulunmuştur ve PIC (0.7) değerine göre lokuslar yüksek düzeyde bilgi içeriğine sahiptir. FIS (0.96) ve FST (0.01) değerleri popülasyonlarda düşük genetik çeşitlilik ve yüksek akrabalı yetiştirme olduğunu göstermiştir. Genetik varyasyonlar, popülasyonlar arasında %0.77, popülasyonlardaki bireyler arasında %99.23 ve tüm bireyler arasında %0 olarak hesaplanmıştır. Ayrıca, popülasyonlar Hardy-Weinberg dengesinden sapmıştır (P<0.001). İki fazlı mutasyon modeli kullanılarak yapılan analiz sonuçlarında Artvin için önemli bir darboğaz kanıtı bulunmuştur. Bu sonuçlar, Kafkas arısı ıslah stratejileri ve koruma programları için kılavuz olarak kullanılabilecek önemli bilgiler sağlamaktadır.

Proje Numarası

2021A03-168656

Kaynakça

  • Al-Atiyat, R. M., 2008. Extinction probabilities of Jordan indigenous cattle using population viability analysis. Livestock Science, 123 (2-3): 121-128.
  • Arias, M. C., T. E. Rinderer & W. S. Sheppard, 2006. Further characterization of honey bees from the Iberian Peninsula by allozyme, morphometric and mtDNA haplotype analyses. Journal of Apicultural Research, 45 (4): 188-196.
  • Arslan, S., M. M. Cengiz, A. Gül & S. Sayed, 2021. Evaluation of the standards compliance of the queen bees reared in the Mediterranean region in Turkey. Saudi Journal of Biological Sciences, 28 (5): 2686-2691.
  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996-2004. GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Genome, Populations, Interactions, CNRS UMR 5000, Universite ́ de Montpellier II, Montpellier (France).
  • Bodur, C., 2005. Genetic Structure Analysis of Honeybee Populations based on Microsatellites. Middle East Technical University, (Unpublished) Ph.D. Thesis, Ankara, 116 pp.
  • 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.
  • Botstein, D., R. L. White, M. Skolnick & R. W. Davis, 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., C. Alaux, M. Bienkowska, R. Büchler, N. L. Carreck, E. Cauia, R. Chlebo, B. Dahle, R. Dall'Olio, P. De la Rúa, A. Gregorc, E. Ivanova, A. Kence, M. Kence, N. Kezic, H. Kiprijanovska, P. Kozmus, P. Kryger, Y. Le Conte, M. Lodesani, A. M. Murilhas, A. Siceanu, G. Soland, A. Uzunov & J. Wilde, 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50 (1): 51-84.
  • Castric, V., L. Bernatchez, K. Belkhir & F. Bonhomme, 2002. Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity, 89 (1): 27-35.
  • Cornuet, J. M. & G. Luikart, 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144 (4): 2001-2014.
  • 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.
  • Dirienzo, A., A. C. Peterson, J. C. Garza, A. M. Valdes, M. Slatkin & N. B. Freimer, 1994. Mutational processes of simple-sequence repeat loci in human-populations. Proceedings of National Academy of Sciences, 91 (8): 3166-3170.
  • 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.
  • Fatima, S., 2006. Study of Genetic Variability Among Gohilwadi, Surti and Zalawadi Goats Using Microsatellite Analysis. Anand Agriculture University, (Unpublished) Master Thesis, Anand, 120 pp.
  • Fıratlı, Ç. & E. Budak, 1994. Türkiye’de Çeşitli Kurumlarda Yetiştirilen Ana Arılar ile Oluşturulan Bal Arısı Apis mellifera L. Kolonilerinin Fizyolojik Morfolojik ve Davranış Özellikleri. Ankara Üniversitesi Ziraat Fakültesi, (Unpublished) Ph.D. Thesis, Ankara, 117 pp (in Turkish).
  • Franck P., L. Garnery, G. Celebrano, M. Solignac & J. M. Cornuet, 2000. 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.
  • Furlan, E., J. Stoklosa, J. Griffiths, N. Gust, R. Ellis, R. M. Huggins & A. R. Weeks, 2012. Small population size and extremely low levels of genetic diversity in island populations of the platypus, Ornithorhynchus anatinus. Ecology and evolution, 2 (4): 844-857.
  • Ganapathi, P., R. Rajendran & P. Kathiravan, 2012. Detection of occurrence of a recent genetic bottleneck event in Indian hill cattle breed Bargur using microsatellite markers. Tropical Animal Health and Production, 44 (8): 2007-2013.
  • 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.
  • Gül, A. & R. Nergiz, 2022. Kafkas Bal Arısı (Apis mellifera caucasia) gen merkezinin bozulmasına neden olan etmenler ve çözüm önerileri. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 25 (2): 545-554 (in Turkish with abstract in English).
  • 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.
  • Ivanova, E. N., T. A. Staykova & M. Bouga, 2007. Allozyme variability in honey bee populations from some mountainous regions in the southwest of Bulgaria. Journal of Apicultural Research, 46 (1): 3-7.
  • 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.
  • Jamieson, I. G., 2011. Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conservation Biology, 25 (1): 115-123.
  • 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.
  • 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, 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.
  • Karabağ, K., R. I. Tunca, E. Tüten & T. Doğaroğlu, 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., 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.
  • Kırpık, M. A., O. Bututaki & D. Tanrikulu, 2010. Determining the relative abundance of honey bee (Apis mellifera L.) races in Kars plateau and evaluating some of their characteristics. Kafkas Universitesi Veteriner Fakultesi Dergisi, 16 (1): 27-282.
  • Kuo, C. H. & F. J. Janzen, 2004. Genetic effects of a persistent bottleneck on a natural population of ornate box turtles (Terrapene ornata). Conservation Genetics, 5 (4): 425-437.
  • 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.
  • Luenser, K., J. Fickel, A. Lehnen, S. Speck & A. Ludwig, 2005. Low level of genetic variability in European bisons (Bison bonasus) from the Bialowieza National Park in Poland. European Journal of Wildlife Research, 51 (2): 84-87.
  • 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.
  • 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.
  • Mukherjee, S., A. Mukherjee, S. Kumar, H. Verma, S. Bhardwaj, O. Togla, S. N. Joardar, I. Longkumer, M. Mech, K. Khate, K. Vupru, M. H. Khan, S. Kumar & C. Rajkhowa, 2022. Genetic characterization of endangered Indian mithun (Bos frontalis), Indian bison/wild gaur (Bos gaurus) and tho-tho cattle (Bos indicus) populations using SSR markers reveals their diversity and unique phylogenetic status. Diversity, 14 (7): 548.
  • Nawrocka, A., I. 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.
  • 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., D. Oskay, R. Işık, S. Yatkın, A. Aydın & A. Güler, 2022. Morphometric and genetic characterization of honey bees (L.) from thrace region of Turkey. Journal of Apicultural Science, 66 (1): 67-83.
  • 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.
  • Park, S. D. E., 2001. The Excel Microsatellite-Toolkit. Animal Genomics Lab, University of College Dublin, Ireland.
  • Piry, S., G. Luikart & J. M. Cornuet, 1999. BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90 (4): 502-503.
  • Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics, 155 (2): 945-959.
  • Rahimi, A., A. Mirmoayedi, D. Kahrizi, L. Zarei & S. Jamali, 2016. Genetic diversity of Iranian honey bee (Apis mellifera Skorikow, 1829) populations based on ISSR markers. Cellular Molecular Biology, 62 (4): 53-58.
  • Rinderer, T. E., J. W. Harris, G. J. Hunt & L. I. de Guzman, 2010. Breeding for resistance to Varroa destructor in north America. Apidologie, 41 (3): 409-424.
  • Robertson, A. & W. G. Hill, 1984. Deviations from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficients. Genetics, 107 (4): 703-718.
  • Ruttner, F., 1988. Biogeography and Taxonomy of Honey Bees. Springer-Verlag, Berlin, Germany, 284 pp.
  • Simon, D. L. & D. Buchenauer, 1993. Genetic Diversity of European Livestock Breeds. European Association for Animal Production Publication, Wageningen, Netherlands, 581 pp.
  • 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., A. 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.
  • Wang, H., S. Gao, Y. Liu, P. Wang, Z. Zhang & D. Chen, 2022. A pipeline for effectively developing highly polymorphic simple sequence repeats markers based on multi-sample genomic data. Ecology and Evolution, 12 (3): e8705.
  • Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38 (6): 1358-1370.
  • Wu, Q., F. Zang, Y. Ma, Y. Zheng & D. Zang, 2020. Analysis of genetic diversity and population structure in endangered Populus wulianensis based on 18 newly developed EST-SSR markers. Global Ecology and Conservation, 24 (7): e01329.
  • 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.
  • Zhang, Y. P., X. X. Wang, O. A. Ryder, H. P. Li, H. M. Zhang, Y. Yong & P. Y. Wang, 2002. Genetic diversity and conservation of endangered animal species. Pure and Applied Chemistry, 74 (4): 575-584.
  • Zimmerman, S. J., C. L. Aldridge & S. J. Oyler-McCance, 2020. An empirical comparison of population genetic analyses using microsatellite and SNP data for a species of conservation concern. BMC Genomics, 21 (1): 1-16.
Toplam 62 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Entomoloji
Bölüm Makaleler
Yazarlar

Berkant İsmail Yıldız 0000-0001-8965-6361

Emel Tüten 0000-0002-3105-6416

Sinan Aydın 0000-0002-7234-5804

Yaprak Karaduman Aslan 0000-0002-8778-7699

Ramazan Çetin 0000-0002-3640-8185

Erdem Sur 0000-0002-9383-7146

Kemal Karabağ 0000-0002-4516-6480

Proje Numarası 2021A03-168656
Erken Görünüm Tarihi 7 Ekim 2023
Yayımlanma Tarihi 9 Ekim 2023
Gönderilme Tarihi 30 Mart 2023
Kabul Tarihi 25 Eylül 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 47 Sayı: 3 - Yıl: 2023 Cilt: 47 Sayı:3

Kaynak Göster

APA Yıldız, B. İ., Tüten, E., Aydın, S., Karaduman Aslan, Y., vd. (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. https://doi.org/10.16970/entoted.1273612
AMA Yıldız Bİ, Tüten E, Aydın S, Karaduman Aslan Y, Çetin R, Sur E, Karabağ K. 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. TED. Ekim 2023;47(3):271-282. doi:10.16970/entoted.1273612
Chicago Yıldız, Berkant İsmail, Emel Tüten, Sinan Aydın, Yaprak Karaduman Aslan, Ramazan Çetin, Erdem Sur, ve Kemal Karabağ. “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, sy. 3 (Ekim 2023): 271-82. https://doi.org/10.16970/entoted.1273612.
EndNote Yıldız Bİ, Tüten E, Aydın S, Karaduman Aslan Y, Çetin R, Sur E, Karabağ K (01 Ekim 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.
IEEE B. İ. Yıldız, E. Tüten, S. Aydın, Y. Karaduman Aslan, R. Çetin, E. Sur, ve K. Karabağ, “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”, TED, c. 47, sy. 3, ss. 271–282, 2023, doi: 10.16970/entoted.1273612.
ISNAD Yıldız, Berkant İsmail vd. “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 (Ekim 2023), 271-282. https://doi.org/10.16970/entoted.1273612.
JAMA Yıldız Bİ, Tüten E, Aydın S, Karaduman Aslan Y, Çetin R, Sur E, Karabağ K. 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. TED. 2023;47:271–282.
MLA Yıldız, Berkant İsmail vd. “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, c. 47, sy. 3, 2023, ss. 271-82, doi:10.16970/entoted.1273612.
Vancouver Yıldız Bİ, Tüten E, Aydın S, Karaduman Aslan Y, Çetin R, Sur E, Karabağ K. 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. TED. 2023;47(3):271-82.