Microsatellite-based genetic characterisation of honeybee populations from Bingöl

Abstract

The conservation of endemic genetic resources is crucial for maintaining genetic diversity in animal production, particularly in honeybees, where preserving local adaptations is challenging. Türkiye’s rich flora, supported by diverse climates, fosters various honeybee races and ecotypes. Bingöl province, situated at the intersection of three phytogeographic regions, is a biodiversity hotspot and a key beekeeping center. Genetic characterization of 141 worker bees from five Bingöl locations, using 30 microsatellite loci, revealed 6.77% genetic variation among locations, 65.69% among individuals, and 27.54% overall. The population exhibited signs of a genetic bottleneck and deviated from Hardy-Weinberg equilibrium. Phylogenetic analysis distinguished the Bingöl honeybee population from other Turkish populations, representing five different honeybee genotypes: Muğla (Apis mellifera anatolica), Hatay (Apis mellifera syriaca), Kırklareli (Apis mellifera carnica), Artvin (Apis mellifera caucasica), and Düzce (Apis mellifera anatolica, Yığılca ecotype), revealing 18 specific alleles that may indicate local genetic distinctiveness.

Keywords

• Honeybee
• Genetic characterization
• Microsatellite
• Population structure

References

1. Abdelkrim J, Robertson BC, Stanton JAL, Gemmell NJ (2009) Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. BioTechniques 46: 185-192.
2. Alburaki M, Bertrand B, Legout H, Moulin S, Alburaki A, Sheppard WS, Garnery L (2013) A fifth major genetic group among honeybees revealed in Syria. BMC Genetics 14: 1-11.
3. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) GENETIX 4.05, Windows TM software for population genetics. University of Montpellier II, Montpellier (in French).
4. Bodur Ç, Kence M, Kence A (2007) Genetic structure of honeybee, Apis mellifera L. (Hymenoptera: Apidae) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research 46: 50-56.
5. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics 32: 314-331.
6. Bourgeois L, Sylvester A, Danka R, Rinderer T (2008) Comparison of microsatellite DNA diversity among commercial queen breeder stocks of Italian honey bees in the United States and Italy. Journal of Apicultural Research 47: 93-98.
7. Castric V, Bernatchez L, Belkhir K, Bonhomme F (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity 89: 27-35.
8. Chen GH, Wu XS, Wang DQ, Qin J, Wu SL, Zhou QL, Olowofeso O (2004) Cluster analysis of 12 Chinese native chicken populations using microsatellite markers. Asian-Australasian Journal of Animal Sciences 17: 1047-1052.

9. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
10. De la Rua P, Galian J, Serrano J, Moritz RFA (2003) Genetic structure of Balearic honey bee populations based on microsatellite polymorphism. Genetics, Selection, and Evolution 35: 339-350.
11. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359-361.
12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611-2620.
13. Excoffier L, Laval G, Schneider S (2007) ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 23: 47-50.
14. Franck P, Garnery L, Solignac M, Cornuet JM (2000) Molecular confirmation of a fourth lineage in honeybees from the Near East. Apidologie 31: 167-180.
15. Gomes F, Costa R, Ribeiro MM, Figueiredo E, Canhoto JM (2013) Analysis of genetic relationship among Arbutus unedo L. genotypes using RAPD and SSR markers. Journal of Forestry Research 24: 227-236.
16. 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. PhD Thesis, Middle East Technical University, Ankara.
17. Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conservation Genetics 7: 991-995.
18. Kambur M, Kekeçoğlu M (2020) Is the natural honey bee biodiversity of Anatolia in the process of extinction? Yuzuncu Yıl University Journal of Agricultural Sciences 30: 593-600.
19. Kandemir I, Kence M, Kence A (2000) Genetic and morphometric variation in honeybee (Apis mellifera L.) populations of Turkey. Apidologie 31: 343-356.
20. Karabağ K, Tunca RI, 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: 333-346.
21. Kence M, Kence A, Kandemir I (1997) Türkiye’de bal (Apis mellifera L.) ırklarının karakterizasyonu ve koruması. Project Number: VHAG-1077, Ankara.
22. Kesik HK, Kutlu MA, Kılınç ŞG, Gül A, Şimşek S (2022) Bingöl Yöresi Bal Arılarında Varroasis'in Yaygınlığı. Türk Tarım ve Doğa Bilimleri Dergisi 9: 26-32.
23. Luenser K, Fickel J, Lehnen A, Speck S, Ludwig A (2005) Low level of genetic variability in European bisons (Bison bonasus) from the Bialowieza National Park in Poland. European Journal of Wildlife Research 51: 84-87.
24. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238-247.
25. Mielnik-Sikorska M, Daca P, Malyarchuk B, Derenko M, Skonieczna K, Perkova M, Grzybowski T (2013) The history of Slavs inferred from complete mitochondrial genome sequences. PloS One 8: e54360.
26. Mukherjee S, Mukherjee A, Kumar S, Verma H, Bhardwaj S, Togla O, Rajkhowa C (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: 548.
27. Nei M (1972) Genetic distance between populations. The American Naturalist 106: 283-292.
28. Özdil F, Aytekin I, Ilhan F, Boztepe S (2012) Genetic variation in Turkish honeybees Apis mellifera anatoliaca, A.m. caucasica, A.m. meda (Hymenoptera: Apidae) inferred from RFLP analysis of three mtDNA regions (16S rDNA-COI-ND5). European Journal of Entomology 109: 161.
29. Park SDE (2001) The Excel Microsatellite-Toolkit. University of College Dublin, Ireland.
30. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90: 502-503.
31. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
32. Rinderer TE, Harris JW, Hunt GJ, de Guzman LI (2010) Breeding for resistance to Varroa destructor in North America. Apidologie 41: 409-424.
33. Ruttner F (1988) Biogeography and Taxonomy of Honeybees. Springer-Verlag, Berlin, Heidelberg and New York.
34. Simon DL, Buchenauer D (1993) Genetic Diversity of European Livestock Breeds. European Association for Animal Production Publication, Wageningen.
35. Solignac M, Vautrin D, Loiseau A, Mougel F, Baudry E, Estoup A, Garnery L, Haberl M, Cornuet JM (2003) Five hundred and fifty microsatellite markers for the study of the honey bee (Apis mellifera L.) genome. Molecular Ecology Notes 3: 307-311.
36. Şahin İ, Esim N (2024) Bingöl koşullarında farklı bal arısı genotiplerinin bazı performans özelliklerinin karşılaştırılması. Türk Tarım ve Doğa Bilimleri Dergisi 11: 206-215.
37. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
38. Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1997) POPGENE, The User-Friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada.
39. Yıldız Bİ, Tüten E, Aydın S, Aslan YK, 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: 271-282.