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Y-Chromosome Diversity in Modern Bulgarians: New Clues About Their Ancestry

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Y-Chromosome Diversity in Modern Bulgarians: New Clues About Their Ancestry Y-Chromosome Diversity in Modern Bulgarians: New Clues about Their Ancestry Sena Karachanak1,2., Viola Grugni2., Simona Fornarino2, Desislava Nesheva1, Nadia Al-Zahery2, Vincenza Battaglia2, Valeria Carossa2, Yordan Yordanov3, Antonio Torroni2, Angel S. Galabov4, Draga Toncheva1*, Ornella Semino2* 1 Department of Medical Genetics, Medical University of Sofia, Sofia, Bulgaria, 2 Dipartimento di Biologia e Biotecnologie ‘‘L. Spallanzani’’, Universita` di Pavia, Pavia, Italy, 3 Institute of Experimental Morphology and Anthropology with Museum, Bulgarian Academy of Sciences, Sofia, Bulgaria, 4 The Stephan Angeloff Institute of Microbiology, Bulgarian Academy of Sciences, Sofia, Bulgaria Abstract To better define the structure and origin of the Bulgarian paternal gene pool, we have examined the Y-chromosome variation in 808 Bulgarian males. The analysis was performed by high-resolution genotyping of biallelic markers and by analyzing the STR variation within the most informative haplogroups. We found that the Y-chromosome gene pool in modern Bulgarians is primarily represented by Western Eurasian haplogroups with , 40% belonging to haplogroups E-V13 and I-M423, and 20% to R-M17. Haplogroups common in the Middle East (J and G) and in South Western Asia (R-L23*) occur at frequencies of 19% and 5%, respectively. Haplogroups C, N and Q, distinctive for Altaic and Central Asian Turkic-speaking populations, occur at the negligible frequency of only 1.5%. Principal Component analyses group Bulgarians with European populations, apart from Central Asian Turkic-speaking groups and South Western Asia populations. Within the country, the genetic variation is structured in Western, Central and Eastern Bulgaria indicating that the Balkan Mountains have been permeable to human movements. The lineage analysis provided the following interesting results: (i) R-L23* is present in Eastern Bulgaria since the post glacial period; (ii) haplogroup E-V13 has a Mesolithic age in Bulgaria from where it expanded after the arrival of farming; (iii) haplogroup J-M241 probably reflects the Neolithic westward expansion of farmers from the earliest sites along the Black Sea. On the whole, in light of the most recent historical studies, which indicate a substantial proto-Bulgarian input to the contemporary Bulgarian people, our data suggest that a common paternal ancestry between the proto-Bulgarians and the Altaic and Central Asian Turkic-speaking populations either did not exist or was negligible. Citation: Karachanak S, Grugni V, Fornarino S, Nesheva D, Al-Zahery N, et al. (2013) Y-Chromosome Diversity in Modern Bulgarians: New Clues about Their Ancestry. PLoS ONE 8(3): e56779. doi:10.1371/journal.pone.0056779 Editor: Luı´sa Maria Sousa Mesquita Pereira, IPATIMUP (Institute of Molecular Pathology and Immunology of the University of Porto), Portugal Received August 30, 2012; Accepted January 15, 2013; Published March 6, 2013 Copyright: ß 2013 Karachanak et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was supported by the National Science Fund of Bulgaria, project ‘‘Characterization of the anthropo-genetic identity of Bulgarians’’, contract number DOO 2-110/22.05.2009, and Fondazione Alma Mater Ticinensis (to OS and AT), the Italian Ministry of the University: Progetti Ricerca Interesse Nazionale 2009 (to OS and AT). NA-Z was supported by a fellowship from the Institute of International Education. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (DT); [email protected] (OS) . These authors contributed equally to this work. Introduction domestication of the horse, spread into the Balkans in three waves , 4 ky BC through Bulgarian territory [5]. Bulgaria is situated in the eastern part of the Balkan Peninsula, In terms of history, the earliest among well-documented on the shores of the Black Sea linking Southeastern Europe to the civilizations that inhabited present-day Bulgaria are the Thracians Eurasian steppe as well as Anatolia and the Aegean islands. It lies whose cultural legacy is still evident in the modern country, on the postulated pathway that introduced modern humans into especially in its southern part. Two other populations playing an Europe in the Upper Paleolithic as attested by the series of important role in the Bulgarian ethnogenesis were the Slavs and assemblages at Bacho Kiro and Temnata Dupka Caves, which are the proto-Bulgarians, who arrived almost simultaneously in the considered signs of the Aurignacian culture expansion , 40 kya Early Middle Ages. [1–3]. It appears to have remained habitable even during the Last Until recently, it was considered that proto-Bulgarians, who Glacial Maximum (LGM) [4] fuelling different expansion routes of founded the Danubian (Asparukh) Bulgaria (ancestor of the post-glacial re-colonization. The presence in Bulgaria of some of present-day Bulgaria) in the late 7th century AD, were a sparse the earliest farming sites, as well as some of the earliest evidence of Turkic population, which took the leadership and ruled over much copper metallurgy in Europe, indicates that this area also played a more numerous Slavic populations living in the same area. From significant role in the Neolithic spread. On the other hand, the this scenario arose the notion that proto-Bulgarians did not play a Kurgan expansion, triggered by the adoption of pastoral significant role in the formation of the gene pool of contemporary nomadism by peoples in the Pontic Steppes and by the Bulgarians. PLOS ONE | www.plosone.org 1 March 2013 | Volume 8 | Issue 3 | e56779 Y-Chromosome Diversity in Modern Bulgarians The initial homeland of the proto-Bulgarians, called Balhara by From a genetic point of view, recent analyses of mtDNA [24] Indians and Bactria by Greeks, was situated in the foothills of and autosomal [25], variation locate modern Bulgarians between Pamir and Hindu Kush Mountains. In antiquity and the early Eastern European and Mediterranean populations. In particular, Middle Ages, proto-Bulgarians founded three large and stable almost the entire Bulgarian mtDNA pool has West Eurasian origin states in Europe: the first one was called ‘‘Old Great Bulgaria’’ (G and includes signature lineages of all the European peopling events Palaia´ Meca´lg Boulcara) by the scholars of the Eastern from the Upper Paleolithic colonization of Europe to the more Roman Empire and was situated in the area delimited by the recent onset of the Neolithic in Europe [24]. Scarce information is Caucasus, the Caspian Sea and Dnieper River. Subsequently but however available for the patrilineal Bulgarian gene pool that, for almost simultaneously two other large states were establish- its holoandric transmission, could retain signs of male mediated ed:Volga-Kama Bulgaria and Asparukh (Danubian) Bulgaria [6– past migrations not necessarily detectable by mtDNA. To address 12]. this deficiency, we have conducted a high-resolution biallelic In their states, proto-Bulgarians built a number of towns- marker analysis of 808 Y chromosomes from contemporary fortresses (Bulkhar-Balkh in the East Caucasus, Bilar and Bolgar Bulgarians, followed by a survey of microsatellite variation within on the Volga, Bolgarfehervar north of the Danube, and Pliska, the the most informative haplogroups (Hgs). The observed diversity first capital of Danubian Bulgaria) as well as a defensive wall patterns were analyzed at both macro- and micro-geographic connecting the Danube and the Black Sea called ‘‘The Great levels. This allowed us to establish a link between Y-chromosome Wall’’ [6,8,9,11,12]. Proto-Bulgarians were not only founders and lineages in modern Bulgarians and known prehistoric and historic organizers of state and unique military power, but they were also events. carriers of a developed civilization embracing the economy and artistic culture [8,10,11]. On the other hand, it is well known that Materials and Methods at the time of the Danubian Bulgaria foundation Slavic tribes in the Balkans did not have any significant state and military Sample Collection organization [13]. We genotyped a total of 808 DNA samples from unrelated Novel analyses of proto-Bulgarians epigraphic monuments, Bulgarian males. All of them gave informed consent and provided especially, of the major historical inscription – ‘‘the List of the personal genealogical information prior to the sampling. Only Bulgarian Khans’’ - have revealed that the proto-Bulgarian individuals whose fathers were of Bulgarian origin and were born language did not belong to the Turkic linguistic family. Therefore, in the country were included in the study. The analyzed samples leading turkologists [14–16] do not consider proto-Bulgarians a are a subset of those previously investigated for mtDNA variation Turkic people, as also attested by the adoption of distinctive [24]. calendar systems by the two groups [17]. Differently, for In accordance with a comprehensive anthropological study of grammatical features the proto-Bulgarian language gravitates Bulgarians [26] we classified the samples according to the former towards the Pamir languages of the East Iranian group, which (before 1999) administrative subdivision of the
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