Abstract
The genetic characterization of the Iranian honey bee was investigated by analyzing 10 polymorphic DNA microsatellite loci in 300 honey bee samples representative of twenty Iranian provinces. This study evaluated the heterozygosity (Ho and He), the Shannon index, the number of observed alleles, and F-statistics among tested populations as genetic parameters. Our finding demonstrated that the Iranian honey bee populations were described by low genetic diversity in terms of the number of observed alleles, Shannon index, and Heterozygosity values. Most populations had significant deviations from Hardy Weinberg equilibrium cause of heterozygote shortage. Low FST and FIS values proposed the absence or very low genetic diversity within and among A. m. meda populations in the present study. The cluster analysis has categorized the honey bee samples gathered from various regions of Iran into two main groups, including honey bees in the North-West (i.e., North, Northwest, and West) provinces and honey bees in the East-South (i.e., Eastern North, Central part, and Southern) provinces of Iran. Our results also revealed lower genetic differentiation and heterozygosity among tested honey bee populations. The results from this study are consistent with previous investigations in Iran, alarming the loss of genetic diversity in the Iranian honey bee populations, which leads to more homozygosity. This study presented new data and reports on genetic structure in investigated native Iranian honey bee populations, and it will benefit future studies on selection, native biodiversity preservation and other conservation breeding projects.
Similar content being viewed by others
References
Alburaki M, Moulin S, Legout H, Alburaki A, Garnery L (2011) Mitochondrial structure of Eastern honey bee populations from Syria, Lebanon and Iraq. Apidologie 42:628–641. https://doi.org/10.1007/s13592-011-0062-4
Alburaki M, Bertrand B, Legout H, Moulin S, Alburaki A (2013) A fifth major genetic group among honey bees revealed in Syria. BMC Genet 14:117. https://doi.org/10.1186/1471-2156-14-117
Aljianabi SM, Martinez I (1997) Universal and rapid salt extraction of high-quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693
Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35. https://doi.org/10.1016/j.ympev.2005.02.017
Asadi N, Rahimi A, Ghaheri M, Kahrizi D, Bagheri Dehbaghi M, Khederzadeh S, Esmaeilkhanian E, Veisi B, Geravandi M, Karim H, Vaziri B, Daneshgar F, Zargooshi J (2016) Genetic diversity of the Dwarf honeybee (Apis florea Fabricius, 1787) populations based on microsatellite markers. Cell Mol Biol 62:51–55. https://doi.org/10.14715/cmb/2016.62.12.9
Aziziaram Z, Bilal I, Zhong Y, Mahmod A, Roshandel MR (2021) Protective effects of curcumin against naproxen-induced mitochondrial dysfunction in rat kidney tissue. Cell Mol Biomed Rep 1(1):23–32. https://doi.org/10.55705/cmbr.2021.138879.1001
Barker JSF (1994) A global protocol for determining genetic distances among domestic livestock breeds. In Proceedings of the fifth World Congress on Genetics Applied to Livestock Production. University of Guelph, (pp. 508). Guelph.
Bassam BJ, Caetano-Anolles G (1993) Silver staining of DNA in polyacrylamide gels. Appl Biochem Biotech 42:181–188
Bilal I, Xie S, Elburki M, Aziziaram Z, Ahmed S, Jalal Balaky ST (2021) Cytotoxic effect of diferuloylmethane, a derivative of turmeric on different human glioblastoma cell lines. Cell Mol Biomed Rep 1(1):14–22. https://doi.org/10.55705/cmbr.2021.138815.1004
Cánovas F, De La Rúa P, Serrano J, Galián J (2011) Microsatellite variability reveals beekeeping influences on Iberian honeybee populations. Apidologie 42:235–251. https://doi.org/10.1007/s13592-011-0020-1
Carpenter MH, Harpur BA (2021) Genetic past, present, and future of the honey bee (Apis mellifera) in the United States of America. Apidologie 52:63–79. https://doi.org/10.1007/s13592-020-00836-4
Chahbar N, Muñoz I, Dall’Olio R, De la Rua P, Serrano J (2012) Population structure of North African honey bees is influenced by both biological and anthropogenic factors. J Insect Conserv 17:385–392
Chen C, Liu Z, Pan Q, Chen X, Wang H, Guo H, Liu S, Lu H, Tin S, Li R, Shi W (2016) Genomic analyses reveal demographic history and temperate adaptation of the newly discovered honey bee subspecies Apis mellifera sinisxinyuan n. ssp. Mol Biol Evol 33:1337–1348. https://doi.org/10.1093/molbev/msw017
Consortium (2006) Insights into social insects from the genome of the honey bee Apis mellifera. Nature 443:931–949. https://doi.org/10.1038/nature05260
Dadgostar S, Delkash-Roudsari S, Nozari J, Tahmasbi G (2019) Comparison between native’s honey bee (Apis mellifera meda) and Carniolan Hybrid Races (Apis mellifera carnica) in Hamedan Province. J Plant Prot Sci 50:187–195
Dadgostar S, Nozari J, Tahmasbi GH (2020) Wing characters for morphological study on the honey bee (Apis mellifera L.) populations among six provinces of Iran. Arthropods 9:129–138
Dall’Olio R, Marino A, Lodesani M, Moritz RFA (2007) Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie 38:207–217. https://doi.org/10.1051/apido:2006073
De La Rua P, Galian J, Serrano J, Moritz RFA (2003) Genetic structure of Balearic honey bee populations based on microsatellite polymorphism. Genet Sel Evol 35:339–350. https://doi.org/10.1051/gse:2003012
De la Rua P, Radloff S, Hepburn R, Serrano J (2007) Do molecular markers support morphometric and pheromone analyses. A preliminary case study in Apis mellifera populations of Morocco. Arch Zootec 56:33–42
Dollati L, Mollaei M, Tahmasebi GH (2014) Genetic diversity assessment of Iranian honey bee population in Northwest of Iran using microsatellite markers and morphological characteristics. Anim Sci J 104:3–16
Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera, Apidae, Apis). J Hymenopt Res 8:165–196. https://doi.org/10.1007/978-1-4614-4960-718
Ercisli M, Lechun G, Azeez S, Hamasalih R, Song S, Aziziaram Z (2021) Relevance of genetic polymorphisms of the human cytochrome P450 3A4 in rivaroxaban-treated patients. Cell Mol Biomed Rep 1(1):33–41
Estoup A, Solignac M, Harry M, Cornuet JM (1993) Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris. Nucleic Acids Res 21:1427–1431. https://doi.org/10.1093/nar/21.6.1427
Estoup A, Garnery L, Solignac M, Cornuet JM (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679–695
Fathi A, Barak M, Damandan M, Amani F, Moradpour R, Khalilova I, Valizadeh M (2021) Neonatal screening for glucose-6-phosphate dehydrogenase deficiency in Ardabil Province, Iran, 2018–2019. Cell Mol Biomed Rep 1(1):1–6
Fetayeh A, Meixner M, Fuchs S (1994) Morphometrical investigation in Syrian honey bee. Apidologie 25:396–440. https://doi.org/10.1051/apido:19940406
Franck P, Garnery L, Loiseau A, Oldroyd BP, Hepburn HR, Solignac M, Cornuet JM (2001) Genetic diversity of the honey bee in Africa: Microsatellite and mitochondrial data. Heredity 86:420–430. https://doi.org/10.1046/j.1365-2540.2001.00842.x
Garnery L, Mosshine EH, Oldroyd BP, Cornuet JM (1995) Mitochondrial DNA variation in Moroccan and Spanish honey bee populations. Mol Ecol 4:465–472. https://doi.org/10.1111/j.1365-294x.1995.tb00240.x
Garnery L, Franck P, Baudry E, Vautrin D, Cornuet JM (1998a) Genetic biodiversity of the West European honey bee (Apis mellifera mellifera and Apis mellifera iberica) I: Mitochondrial DNA. Genet Sel Evol 30:S31–S47
Garnery L, Franck P, Baudry E, Vautrin D, Cornuet JM (1998b) Genetic diversity of the west European honey bee (Apis mellifera mellifera and Apis mellifera iberica) II. Microsatellite Loci. Genet Sel Evol 30:S49–S74
Ghassemi-Khademi T, Rajabi-Maham M, Pashaei-Rad S (2018) Genetic diversity evaluation of Persian honeybees (Apis mellifera meda) in North West of Iran, using microsatellite markers. JWB 2:37–46. https://doi.org/10.22120/jwb.2018.86877.1026
Goldstein DB, Schlotterer C (1999) Microsatellites, evolution and applications, 1st edn. Oxford University Press, New York
Hammer O, David ATH, Paul DR (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol Electron 1–9.
Han F, Wallberg A, Webster MT (2012) From where did the Western honey bee (Apis mellifera) originate? Ecol Evol 2:1949–1957. https://doi.org/10.1002/ece3.312
Ilyasov RA, Park J, Takahashi J, Kwon HW (2018) Phylogenetic uniqueness of honeybee Apis cerana from the Korean peninsula inferred from the mitochondrial, nuclear and morphological data. J Apic Sci 62:189–214. https://doi.org/10.2478/JAS-2018-0018
Ilyasov R, Lee M, Takahashi J, Kwon HW, Nikolenko AG (2020) A revision of subspecies structure of western honey bee Apis mellifera. Saudi J Biol Sci 27:3615–3621. https://doi.org/10.1016/j.sjbs.2020.08.001
Kandemir I, Ozkan A, Mohammad GM (2004) A scientific note on allozyme in Persian honey bee (Apis mellifera meda) from the Elburz mountains in Iran. Apidologie 35:521–522. https://doi.org/10.1051/apido:2004039
Kence M, Jabbari Farhoud H, Tunca RI (2009) Morphometric and genetic variability of honey bee (Apis mellifera L.) populations from northern Iran. J Apic Res 48:247–255
Kazemi E, Zargooshi J, Kaboudi M, Heidari P, Kahrizi D, Mahaki B, Mohammadian Y, Khazaei H, Ahmed K (2021) A genome-wide association study to identify candidate genes for erectile dysfunction. Brief Bioinform 22(4). https://doi.org/10.1093/bib/bbaa338
Loucif-Ayad W, Achou M, Legout H, Alburaki M, Garnery L (2014) Genetic assessment of Algerian honeybee populations by microsatellite markers. Apidologie 46:392–402. https://doi.org/10.1007/s13592-014-0331-0
Meixner MD, Costa C, Kryger P, Hatjina F, Bouga M, Ivanova E, Büchler R (2010) Conserving diversity and vitality for honey bee breeding. J Apic Res 49(1):85–92. https://doi.org/10.3896/IBRA.1.49.1.12
Meixner MD, Leta MA, Koeniger N, Fuchs S (2011) The honey bees of Ethiopia represent a new subspecies of Apis mellifera - Apis mellifera simensis n. ssp. Apidologie 42:425–437. https://doi.org/10.1007/s13592-011-0007-y
Meixner MD, Pinto MA, Bouga M, Kryger P, Ivanova E, Fuchs S (2013) Standard methods for characterizing subspecies and ecotypes of Apis mellifera. J Apic Res 52(4):1–28. https://doi.org/10.3896/IBRA.1.52.4.05
Mosavi M (2011) Genetic diversity of honey bee populations in Gilan and Mazandaran provinces using microsatellite markers. MSc.Thesis. Zanjan university, Zanjan.
Munoz I, Dall’Olio R, Lodesani M, De La Rua P (2009) Population genetic structure of coastal Croatian honey bee s (Apis mellifera carnica). Apidologie 40:617–626. https://doi.org/10.1051/apido/2009041
Peakall R, Smouse E (2012) GenAlEx 6.5: Genetic Analysis in Excel. Population genetic software for teaching and research — an update. Bioinformatics 28:2537–2539
Potts SG, Roberts SPM, Dean R, Marris G, Brown M, Jones R, Settele J (2010) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49:15–22. https://doi.org/10.3896/IBRA.1.49.1.02
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard JK, Wen W (2004). Documentation for the STRUCTURE software Version 2. Chicago. http://www.pritch.bsd.uchicago. edu/software/structure2_1.html.
Radoslavov G, Hristov P, Shumkova R, Mitkov I, Sirakova D, Bough M (2017) A specific genetic marker for the discrimination of native Bulgarian honey bees (Apis mellifera rodopica): duplication of COI gene fragment. J Apic Res 56:196–202. https://doi.org/10.1080/00218839.2017.1307713
Rahimi A (2015) Study of the genetic diversity of Iranian honey bee (Apis mellifera meda Skorikow, 1929) populations using the mtDNA COI–COII intergenic region. Biologija 61:54–59
Rahimi A, Asadi M (2010) Morphological characteristics of Apis mellifera meda (Hymenoptera: Apidae) in Saghez (West of Iran). Nature Montenegro 10:101–107
Rahimi A, Mirmoayedi A (2013) Evaluation of morphological characteristics of honey bee Apis mellifera meda (Hymenoptera: Apidae) in Mazandaran (North of Iran). TJEA 3:1280–1284
Rahimi A, Asadi M, Mahdavi V, Abdulshahi R (2013) Morphological characteristics of Apis mellifera meda (Hym: Apidae) in Kerman (south of Iran). TJEA 3:614–624
Rahimi A, Asadi M, Abdolshahi R (2014a) Genetic diversity of honey bee (Apis mellifera meda) populations using microsatellite markers in Jiroft. J Sci Tact Honey Bee 6:26–33
Rahimi A, Miromayedi A, Kahrizi D, Abdolshahi R, Kazemi E, Yari KH (2014b) Microsatellite genetic diversity of Apis mellifera meda Skorikov. Mol Biol Rep 41:7755–7761. https://doi.org/10.1007/s11033-014-3667-7
Rahimi A, Mirmoayedi A, Kahriz D, Zarei L, Jamali S (2021) Genetic diversity of Iranian honey bee (Apis mellifera meda Skorikow, 1929) populations based on ISSR markers. Cell Mol Biol 62:53–58. https://doi.org/10.14715/cmb/2016.62.4.10
Rahimi A, Mirmoayedi A, Kahriz D, Zarei L, Jamali S (2017) Morphological diversity and phylogenetic relationships Study of Iranian subspecies honey bee (Apis mellifera meda) populations via morphological characteristics. Sociobiology 64:33–41. https://doi.org/10.13102/sociobiology.v64i1.1179
Rahimi A, Mirmoayedi A, Kahriz D, Zarei L, Jamali S (2018) Genetic Variation in Iranian Honeybees, Apis mellifera meda Skorikow, 1829, (Hymenoptera: Apidae) Inferred from RFLP Analysis of two mtDNA Regions (COI and 16S rDNA). Sociobiology 65:482–490. https://doi.org/10.13102/sociobiology.v65i3.2876
Rahimi A, Mirmoayedi A, Kahriz D, Zarei L, Jamali S (2019) Phylogenic relationships study of Iranian honeybee with other honeybee subspecies using morphological and molecular markers. Anim Sci J 123:323–334
Roelfs AP, Singh RP, Saari EE (1988) NTSYS-pc numerical Taxonomy and multivariate analysis system. Version 2.02. Exeter Publications Setauket, New York.
Rortais A, Arnold G, Alburaki M, Legout H, Garnery L (2011) Review of the DraI COI-COII test for the conservation of the black honey bee (Apis mellifera mellifera). Conserv Genet Resour 3:383–391. https://doi.org/10.1007/s12686-010-9351-x
Royan M, Rahim G, Esmaeilkhanian S, Mirhoseini S, Ansari Z (2007) A study on the genetic diversity of the Apis mellifera meda population in the south coast of the Caspian Sea using microsatellite markers. J Apic Res 46:236–241. https://doi.org/10.1080/00218839.2007.11101401
Ruttner F, Tassencourt L, Louveaux J (1978) Biometrical-statistical analysis of the geographic variability of Apis mellifera. Apidologie 9:363–381. https://doi.org/10.1051/apido:19780408
Ruttner F, Pourasghar D, Kauhausen D (1985) Die Honigbienen des Iran I. Apis florea Fabricius. Apidologie 16:119–125. https://doi.org/10.1051/apido:19850203
Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer-Verlag Berlin Heidelberg GmbH, 288. https://doi.org/10.1016/0169-5347(89)90176-6.
Smith DR (1991) Mitochondrial DNA and honeybee biogeography. In: Smith DR (ed) Diversity in the genus Apis. Westview Press, Boulder, pp 131–176
Tahmasebi GH, Abadi R, Esmaili M, Kambozia J (1998) Morphological study of honey bee (Aips mellifare L) in Iran. J Agri Scien Natu Res 2:89–100
Tahmasebi GH (1996) Morpological and biochemical survey of honey bee (Apis mellifera L) populations in Iran. Ph.D. Thesis, Tarbit Modares University, Tahran, Iran.
Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399
Themudo GE, Rey-Iglesia A, Tascón LR, Jensen AB, Fonseca R, Campos PF (2020) Declining genetic diversity of European honeybees along the twentieth century. Sci Rep 10:10520. https://doi.org/10.1038/s41598-020-67370-2
Tourang M, Fang L, Zhong Y, Suthar R (2021) Association between Human Endogenous Retrovirus K gene expression and breast cancer. Cell Mol Biomed Rep 1(1):7–13
Veisi H, Nazemi-Rafe N, Azizi A, Rajabi-Maham H (2020) Genetic characteristics of the Iranian honey bee, Apis mellifera meda, based on mitochondrial genes of ND4, ND4L and ND6 and their internal transcribed spacers. Insect Soc 67:439–448. https://doi.org/10.1007/s00040-020-00769-2
Ya Y, Zhou S, Zhu X, Xu X, Wang W, Zha L, Wang P, Wang J, Lai K, Wang S, Hao L, Zhou B (2019) Genetic Differentiation of Eastern Honey Bee (Apis cerana) Populations Across Qinghai-Tibet Plateau-Valley Landforms. Fron Genet 10:1–11
Yeh FC, Yang RC, Boyil TBJ, Mao JX (1997) POPGENE, the Uswe-friendly Shareware for Population Genetic Analysis. Molecular Biology and Biotechnology Centre. University of Alberta, Alberta
Acknowledgements
The authors thank Dr. Rasoul Bahreini, Dr. Esmaeil Amiri and Dr. Reza Amiri for the scientific editing of the article and are equally grateful to all the beekeepers who helped us with the sampling of their apiary.
Funding
The authors have not disclosed any funding.
Author information
Authors and Affiliations
Contributions
Conceptualization, Methodology, Software, Formal analysis, Validation, Investigation, Data curation, Writing—original draft, Project administration: AR, DK and LZ; Methodology, Validation, Supervision: AM and SJ; Writing— review and editing: AR, DK, AM and LZ.
Corresponding author
Ethics declarations
Conflict of interest
The authors state that there is no conflict of interest to report.
Ethical Approval
This article does not include any researches with human participants or animals conducted by any of the co-authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rahimi, A., Kahrizi, D., Mirmoayedi, A. et al. Genetic Characterizations of the Iranian Honey Bee (Apis mellifera meda Skorikov 1929) Populations Using the Microsatellite DNA Markers. Biochem Genet 61, 2293–2317 (2023). https://doi.org/10.1007/s10528-023-10368-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10528-023-10368-y