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Distribution of Y-chromosome haplogroups in Serbian population groups originating from historically and geographically significant distinct parts of the Balkan Peninsula

      Highlights

      • 1200 Serbian males from Balkan Peninsula were analyzed using combination of 23 Y-STRs and 17 Y-SNPs typing.
      • Three dominant haplogroups were determined (I-P37.2, E-P170 and R-M198) with haplogroup I-P37.2 being the most frequent one.
      • Highest number of unique haplotypes and discrimination capacity was detected in the present(S) dataset.
      • Highest genetic distance values were obeserved between OH(S) and KM(S) datasets.

      Abstract

      Our study enrolled 1200 Serbian males originating from three geographical regions in the Balkan Peninsula inhabited by Serbs: present-day Serbia, regions of Old Herzegovina and Kosovo and Metohija. These samples were genotyped using the combination of 23 Y-chromosomal short tandem repeats (Y-STRs) loci and 17 Ychromosomal single nucleotide polymorphisms (Y-SNPs) loci for the haplotype and haplogroup analysis in order to characterize in detail Y chromosome flow in the recent history. Serbia’s borders have changed through history, forcing Serbs constantly to migrate to different regions of Balkan Peninsula. The most significant migration waves in the recent history towards present-day Serbia occurred from the regions of Old- Herzegovina and Kosovo and Metohija that lie in the south-west/south. High haplotype diversity and discrimination capacity were observed in all three datasets, with the highest number of unique haplotypes (381) and discrimination capacity (0.97) detected in the samples originating from the present-day Serbia. Haplogroup composition didn’t differ significantly among datasets, with three dominant haplogroups (I-M170, E-P170 and R-M198), and haplogroup I-M170 being the most frequent in all three datasets. Haplogroup E-P170 was the second most dominant in the dataset originating from geographical region of Kosovo and Metohija, whereas haplogroup R-M198 was the second most prevalent in the dataset from historical region of Old Herzegovina. Based on the phylogenetic three for haplogroup I constructed within this study, haplogroup I2a1-P37.2 was the most dominant within all three datasets, especially in the dataset from historical region of Old Herzegovina, where 182 out of 400 samples were derived for SNP P37.2. Genetic distances between three groups of samples, evaluated by the Fst and Rst statistical values, and further visualized through multidimensional scaling plot, showed great genetic similarity between datasets from Old Herzegovina and present-day Serbia. Genetic difference in the haplogroup distribution and frequency between datasets from historical region of Old Herzegovina and from geographical region of Kosovo and Metohija was confirmed with highest Fst and Rst vaules. In this study we have distinguished genetic structure, diversity and haplogroup frequencies within 1200 Serbian males from three datasets, relationships among them as well as with other Balkan and European populations, which is useful for studying recent demographic history.

      Keywords

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      References

        • Kayser M.
        Forensic use of Y-chromosome DNA: a general overview.
        Hum. Genet. 2017; 136: 621-635
        • Jobling M.A.
        Y-chromosomal SNP haplotype diversity in forensic analysis.
        Forensic Sci. Int. 2001; 118: 158-162
        • Roewer L.
        • Croucher P.J.
        • Willuweit S.
        • Lu T.T.
        • Kayser M.
        • Lessig R.
        • de Knijff P.
        • Jobling M.A.
        • Tyler-Smith C.
        • Krawczak M.
        Signature of recent historical events in the European Y-chromosomal STR haplotype distribution.
        Hum. Genet. 2005; 116: 279-291
        • Lahr M.M.
        • Foley R.
        • Pinhasi R.
        Expected regional patterns of Mesolithic-Neolithic human population admixture in Europe based on archaeological evidence.
        in: Renfrew C. Boyle K. Archaeogenetics: DNA and the Population Prehistory of Europe. MacDonald Institute for Archaeological Research, Cambridge, UK2001: 81-88
        • Pinhasi R.
        • Foley R.
        • Lahr M.M.
        Spatial and temporal patterns in the Mesolithic-Neolithic archaeological record of Europe.
        in: Renfrew C. Boyle K. Archaeogenetics: DNA and the Population Prehistory of Europe. MacDonald Institute for Archaeological Research, Cambridge, UK2001: 45-56
        • Malyarchuk B.A.
        • Grzybowski T.
        • Derenko M.V.
        • Czarny J.
        • Drobnic K.
        • Miścicka-Sliwka D.
        Mitochondrial DNA variability in Bosnians and Slovenians.
        Ann. Hum. Genet. 2003; 67: 412-425
        • Coles J.M.
        • Harding A.F.
        The Bronze Age in Europe: An Introduction to the Prehistory of Europe c. 2000-700.
        Methuen, London, UK1979
        • Piggott S.
        Ancient Europe from the Beginnings of Agriculture to Classical Antiquity.
        The University Press, Edinburgh, UK1965
        • Wilkes J.J.
        The Illyrians (The Peoples of Europe).
        Blackwell, Cambridge, UK1992
        • Rębała K.
        • Mikulich A.I.
        • Tsybovsky I.S.
        • Siváková D.
        • Džupinková Z.
        • Szczerkowska-Dobosz A.
        • Szczerkowska Z.
        Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin.
        J. Hum. Genet. 2007; 52: 406-414
        • Živković T.
        Južni Sloveni Pod Vizantijskom Vlašću 600–1025.
        Čigoja štampa, Belgrade, Serbia2007: 59-60
        • Mirabal S.
        • Varljen T.
        • Gayden T.
        • Regueiro M.
        • Vujovic S.
        • Popovic D.
        • Djuric M.
        • Stojkovic O.
        • Herrera R.J.
        Human Y-chromosome short tandem repeats: a tale of acculturation and migrations as mechanisms for the diffusion of agriculture in the Balkan Peninsula.
        Am. J. Phys. Anthropol. 2010; 142: 380-390
        • Terzić S.
        Stara Srbija - Nastanak Imena I Znanja O Njoj do 1912.
        Istorijski institut, Belgrade, Serbia1997: 91-110
        • Samardžić R.
        Migrations in Serbian history.
        in: Ninić I. Migrations in Balkan History. Serbian Academy of Sciences and Arts, Belgrade, Serbia1989: 83-91
        • Battaglia V.
        • Fornarino S.
        • Al-Zahery N.
        • Olivieri A.
        • Pala M.
        • Myres N.M.
        • King R.J.
        • Rootsi S.
        • Marjanovic D.
        • Primorac D.
        • Hadziselimovic R.
        • Vidovic S.
        • Drobnic K.
        • Durmishi,A. Torroni N.
        • Santachiara-Benerecetti A.S.
        • Underhill P.A.
        • Semino O.
        Y-chromosomal evidence of the cultural diffusion of agriculture in Southeast Europe.
        Eur. J. Hum. 2009; 17: 820-830
        • Regueiro M.
        • Rivera L.
        • Damnjanovic T.
        • Lukovic L.
        • Milasin J.
        • Herrera R.J.
        High levels of paleolithic Y-chromosome lineages characterize Serbia.
        Gene. 2012; 498: 59-67
        • Scorrano G.
        • Finocchio A.
        • Angelis F.D.
        • Martínez-Labarga C.
        • Šarac J.
        • Contin I.
        • Scano G.
        • Novokmet N.
        • Frezza D.
        • Rickards O.
        The genetic landscape of Serbian populations through mitochondrial DNA sequencing and non-recombining region of the Y chromosome microsatellites.
        Coll. 2017; 41: 275-296
        • Marjanovic D.
        • Fornarino S.
        • Montagna S.
        • Primorac D.
        • Hadziselimovic R.
        • Vidovic S.
        • Pojskic N.
        • Battaglia V.
        • Achilli A.
        • Drobnic K.
        • Andjelinovic S.
        • Torroni A.
        • Santachiara-Benerecetti A.S.
        • Semino O.
        The peopling of modern Bosnia-Herzegovina: Y-chromosome haplogroups in the three main ethnic group.
        Ann. Hum. Genet. 2005; 69: 757-763
        • Roewer L.
        • Andersen M.
        • Ballantyne J.
        • Butler J.M.
        • Caliebe A.
        • Corach D.
        • D'Amato M.E.
        • Gusmão L.
        • Hou Y.
        • de Knijff P.
        • Parson W.
        • Prinz M.
        • Schneider P.M.
        • Taylor D.
        • Vennemann M.
        • Willuweit S.
        DNA commission of the international society of forensic genetics (ISFG): Recommendations on the interpretation of Y-STR results in forensic analysis.
        Forensic Sci. Int. Genet. 2020; 48
        • Geppert M.
        • Roewer L.
        SNaPshot® minisequencing analysis of multiple ancestry-informative Y-SNPs using capillary electrophoresis.
        Methods Mol. Biol. 2012; 830: 127-140
        • Excoffier L.
        • Laval G.
        • Schneider S.
        Arlequin (version 3.0): an integrated software package for population genetics data analysis.
        Evol. Bioinform. 2007; : 47-50
        • Nei M.
        • Tajima F.
        DNA polymorphism detectable by restriction endonucleases.
        Genetics. 1981; 97: 145-163
        • Willuweit S.
        • Roewer L.
        The new Y chromosome haplotype reference database.
        Forensic Sci. Int. Genet. 2015; 15: 43-48
      1. M. Cetkovic Gentula, A. Nevski Y-DNA Haplogroup Predictor-NevGen, (2015). Available at: 〈www.nevgen.org/〉 (Accessed February 1, 2022).

        • Gusmão L.
        • Butler J.M.
        • Linacre A.
        • Parson W.
        • Roewer L.
        • Schneider P.M.
        • Carracedo A.
        Revised guidelines for the publication of genetic population data.
        Forensic Sci. Int. Genet. 2017; 30: 160-163
        • Willuweit S.
        • Roewer L.
        International forensic Y chromosome user group, Y chromosome haplotype reference database (YHRD): update.
        Forensic Sci. Int. Genet. 2007; 1: 83-87
        • Zgonjanin D.
        • Alghafri R.
        • Antov M.
        • Stojiljković G.
        • Petković S.
        • Vuković R.
        • Drašković D.
        Genetic characterization of 27 Y-STR loci with the Yfiler® Plus kit in the population of Serbia.
        Forensic Sci. Int. Genet. 2017; 31: 48-49
        • Veselinovic I.S.
        • Zgonjanin D.M.
        • Maletin M.P.
        • Stojkovic O.
        • Djurendic-Brenesel M.
        • Vukovic R.M.
        • Tasic M.M.
        Allele frequencies and population data for 17 Y-chromosome STR loci in a Serbian population sample from Vojvodina province.
        Forensic Sci. Int. 2008; 176: 23-28
        • Pericić M.
        • Lauc L.B.
        • Klarić I.M.
        • Janićijević B.
        • Behluli I.
        • Rudan P.
        Y chromosome haplotypes in Albanian population from Kosovo.
        Forensic Sci. Int. 2004; 146: 61-64
        • Mršić G.
        • Gršković B.
        • Vrdoljak A.
        • Popović M.
        • Valpotić I.
        • Anđelinović Š.
        • Stenzl V.
        • Ehler E.
        • Urban L.
        • Lacković G.
        • Underhill P.A.
        • Primorac D.
        Croatian national reference Y-STR haplotype database.
        Mol. Biol. Rep. 2012; 39: 7727-7741
        • Kovačević L.
        • Fatur-Cerić V.
        • Hadzic N.
        • Čakar J.
        • Primorac D.
        • Marjanović D.
        Haplotype data for 23 Y-chromosome markers in a reference sample from Bosnia and Herzegovina.
        Croat. Med. J. 2013; 54: 286-290
        • Karafet T.M.
        • Mendez F.L.
        • Meilerman M.B.
        • Underhill P.A.
        • Zegura S.L.
        • Hammer M.F.
        New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree.
        Genome Res. 2008; 18: 830-838
        • Rootsi S.
        • Magri C.
        • Kivisild T.
        • Benuzzi G.
        • Help H.
        • Bermisheva M.
        • Kutuev I.
        • Barać L.
        • Pericić M.
        • Balanovsky O.
        • Pshenichnov A.
        • Dion D.
        • Grobei M.
        • Zhivotovsky L.A.
        • Battaglia V.
        • Achilli A.
        • Al-Zahery J.N.
        • ParikKing R.
        • Cinnioğlu C.
        • Semino O.
        Phylogeography of Y-chromosome haplogroup I reveals distinct domains of prehistoric gene flow in Europe.
        Am. J. Hum. Genet. 2004; 75
        • Marjanovic D.
        • Fornarino S.
        • Montagna S.
        • Primorac D.
        • Hadziselimovic R.
        • Vidovic S.
        • Pojskic N.
        • Battaglia V.
        • Achilli A.
        • Drobnic K.
        • Andjelinovic S.
        • Torroni A.
        • Santachiara-Benerecetti A.S.
        • Semino O.
        The peopling of modern Bosnia-Herzegovina: Y-chromosome haplogroups in the three main ethnic groups.
        Ann. Hum. Genet. 2005; 69: 757-763
        • Zupan A.
        • Vrabec K.
        • Glavač D.
        The paternal perspective of the Slovenian population and its relationship with other populations.
        Ann. Hum. Biol. 2013; 40: 515-526
      2. O.M. Utevska Генофонд українців за різними системами генетичних маркерів: походження і місце на європейському генетичному просторі (The gene pool of Ukrainians revealed by different systems of genetic markers: the origin and statement in Europe) (PhD) (in Ukrainian). National Research Center for Radiation Medicine of National Academy of Sciences of Ukraine, (2017) pp. 219–226, 302.

        • Sedov V.
        Sloveni u Dalekoj Prošlosti.
        Akademska knjiga, Novi Sad, Serbia2012: 34
        • Neparáczki E.
        • Maróti Z.
        • Kalmár T.
        • Maár K.
        • Nagy I.
        • Latinovics D.
        • Kustár Á.
        • Pálfi G.
        • Molnár E.
        • Marcsik A.
        • Balogh C.
        • LőrinczyGál G.
        • Tomka P.
        • Kovacsóczy B.
        • Kovács L.
        • Raskó I.
        • Török T.
        Y-chromosome haplogroups from Hun, Avar and conquering Hungarian period nomadic people of the Carpathian Basin.
        Sci. Rep. 2019; 9: 16569
        • Fóthi E.
        • Gonzalez A.
        • Fehér T.
        • Gugora A.
        • Fóthi Á.
        • Biró O.
        • Keyser C.
        Genetic analysis of male Hungarian Conquerors: European and Asian paternal lineages of the conquering Hungarian tribes.
        Archaeol. Anthr. Sci. 2020; 12
        • Semino O.
        • Magri C.
        • Benuzzi G.
        • Lin A.A.
        • Al-Zahery N.
        • Battaglia V.
        • Maccioni L.
        • Triantaphyllidis C.
        • Shen P.
        • Oefner P.J.
        • Zhivotovsky L.A.
        • King R.
        • Torroni A.
        • Cavalli-Sforza L.L.
        • Underhill P.A.
        • Santachiara-Benerecetti A.S.
        Origin, diffusion, and differentiation of Y-chromosome haplogroups E and J: inferences on the neolithization of Europe and later migratory events in the Mediterranean area.
        Am. J. Hum. Genet. 2004; 74: 1023-1034
        • Šehović E.
        • Zieger M.
        • Spahić L.
        • Marjanovic D.
        • Dogan S.
        A glance of genetic relations in the Balkan populations utilizing network analysis based on in silico assigned Y-DNA haplogroups.
        Anthropol. Rev. 2018; 81: 252-268
        • Cruciani F.
        • La Fratta R.
        • Trombetta B.
        • Santolamazza P.
        • Sellitto D.
        • Colomb E.B.
        • Dugoujon J.
        • Crivellaro F.
        • Benincasa T.
        • Pascone R.
        • Moral P.
        • Watson E.
        • Melegh B.
        • Barbujani G.
        • Fuselli S.
        • Vona G.
        • Zagradisnik B.
        • AssumBrdicka G.R.
        • Kozlov A.I.
        • Scozzari … R.
        Tracing past human male movements in northern/eastern Africa and western Eurasia: new clues from Y-chromosomal haplogroups E-M78 and J-M12.
        Mol. Biol. Evol. 2007; 24: 1300-1311
        • Karachanak S.
        • Grugni V.
        • Fornarino S.
        • Nesheva D.
        • Al-Zahery N.
        • Battaglia V.
        • Carossa V.
        • Yordanov Y.
        • Torroni A.
        • GalabovToncheva A.S.D.
        • Semino O.
        Y-chromosome diversity in modern Bulgarians: new clues about their ancestry.
        PloS One. 2013; 8e56779
        • Wells R.S.
        • Yuldasheva N.
        • Ruzibakiev R.
        • Underhill P.A.
        • Evseeva I.
        • Blue-Smith J.
        • Jin L.
        • Su B.
        • Pitchappan R.
        • Shanmugalakshmi S.
        • Balakrishnan K.
        • Read M.
        • Pearson N.M.
        • Zerjal T.
        • Webster M.T.
        • Zholoshvili I.
        • Jamarjashvili E.
        • Gambarov S.
        • Nikbin B.
        • Dostiev A.
        • Bodmer W.F.
        The Eurasian heartland: a continental perspective on Y-chromosome diversity.
        PNAS USA. 2001; 98: 10244-10249
        • Maisano Delser P.
        • Ravnik-Glavač M.
        • Gasparini P.
        • Glavač D.
        • Mezzavilla M.
        Genetic landscape of slovenians: past admixture and natural selection pattern.
        Fron. Genet. 2018; 9: 551
        • Semino O.
        • Passarino G.
        • Oefner P.J.
        • Lin A.A.
        • Arbuzova S.
        • Beckman L.E.
        • De Benedictis G.
        • Francalacci P.
        • Kouvatsi A.
        • Limborska S.
        • Marcikiae M.
        • Mika A.
        • Mika B.
        • Primorac D.
        • Santachiara-Benerecetti A.S.
        • Cavalli-Sforza L.L.
        • Underhill P.A.
        The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective.
        Science. 2000; 290: 1155-1159
        • Sengupta S.
        • Zhivotovsky L.A.
        • King R.
        • Mehdi S.Q.
        • Edmonds C.A.
        • Chow C.E.
        • Lin A.A.
        • Mitra M.
        • Sil S.K.
        • Ramesh A.
        • Usha M.V.
        • Rani C.M.
        • Thakur L.
        • Cavalli-Sforza L.
        • Majumder P.P.
        • Underhill P.A.
        Polarity and temporality of high-resolution Y-chromosome distributions in India identify both indigenous and exogenous expansions and reveal minor genetic influence of Central Asian pastoralists.
        Am. J. Hum. Genet. 2006; 78: 202-221
        • Thanseem I.
        • Thangaraj K.
        • Chaubey G.
        • Singh V.K.
        • Bhaskar L.V.
        • Reddy B.M.
        • Reddy A.G.
        • Singh L.
        Genetic affinities among the lower castes and tribal groups of India: inference from Y chromosome and mitochondrial DNA.
        BMC Genet. 2006; 7: 42
        • Rootsi S.
        • Zhivotovsky L.A.
        • Baldovic M.
        • Kayser M.
        • Kutuev I.A.
        • Khusainova R.
        • Bermisheva M.A.
        • Gubina M.
        • Fedorova S.A.
        • Ilumäe A.M.
        • Khusnutdinova E.K.
        • Voevoda M.I.
        • Osipova L.P.
        • Stoneking M.
        • Lin A.A.
        • Ferak V.
        • Parik J.
        • Kivisild T.
        • Underhill P.A.
        • Villems R.
        A counter-clockwise northern route of the Y-hromosome haplogroup N from Southeast Asia towards Europe.
        Eur. J. Hum. 2007; 15: 204-211
        • Zegura S.L.
        • Karafet T.M.
        • Zhivotovsky L.A.
        • Hammer M.F.
        High-resolution SNPs and microsatellite haplotypes point to a single, recent entry of Native American Y chromosomes into the Americas.
        Mol. Biol. Evol. 2004; 21: 164-175
        • Mendez F.L.
        • Karafet T.M.
        • Krahn T.
        • Ostrer H.
        • Soodyall H.
        • Hammer M.F.
        Increased resolution of Y chromosome haplogroup T defines relationships among populations of the Near East, Europe, and Africa.
        Hum. Biol. 2011; 83: 39-53