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Human Y-Chromosome Short Tandem Repeats a Tale of Acculturation and Migrations as Mechanisms for the Diffusion of Agriculture in the Balkan Peninsula

Human Y-Chromosome Short Tandem Repeats a Tale of Acculturation and Migrations as Mechanisms for the Diffusion of Agriculture in the Balkan Peninsula

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Human Y-Chromosome Short Tandem Repeats: A Taleof Acculturation and Migrations as Mechanisms for theDiffusion of Agriculture in the Balkan Peninsula
Sheyla Mirabal,
Tatjana Varljen,
Tenzin Gayden,
Maria Regueiro,
Slavica Vujovic,
Danica Popovic,
Marija Djuric,
Oliver Stojkovic,
and Rene J. Herrera
 Department of Molecular and Human Genetics, College of Medicine, Florida International University, Miami, FL
 Department of Biological Sciences, Florida International University, Miami, FL
 Institute of Forensic Medicine, School of Medicine, University of Belgrade, Belgrade, Serbia
Clinical Center of Montenegro, Podgorica, Montenegro
Security Information Agency, Belgrade, Serbia KEY WORDS
YSTR; human evolution; Balkan States
Southeastern Europe and, particularly,the Balkan Peninsula are especially useful when study-ing the mechanisms responsible for generating the cur-rent distribution of Paleolithic and Neolithic geneticsignals observed throughout Europe. In this study, 404individuals from Montenegro and 179 individuals fromSerbia were typed for 17 Y-STR loci and comparedacross 9 Y-STR loci to geographically targeted previ-ously published collections to ascertain the phylogeneticrelationships of populations within the Balkan Penin-sula and beyond. We aim to provide information onwhether groups in the region represent an amalgama-tion of Paleolithic and Neolithic genetic substrata, orwhether acculturation has played a critical role in thespread of agriculture. We have found genetic markersof Middle Eastern, south Asian and European descentin the area, however, admixture analyses indicate thatover 80% of the Balkan gene pool is of Europeandescent. Altogether, our data support the view that thediffusion of agriculture into the Balkan region wasmostly a cultural phenomenon although some geneticinfiltration from Africa, the Levant, the Caucasus, andthe Near East has occurred. Am J Phys Anthropol142:380–390, 2010.
2010 Wiley-Liss, Inc.
Modern humans are believed to have colonized Europeas early as 40,000 years before present (YBP) (Boyd andSilk, 1997; Mellars, 2006; Anikovich et al., 2007). How-ever, the Last Glacial Maximum (LGM), which ended
10,000 YBP, forced a contraction that forever changedthe landscape of the region; most of Europe was thenrepopulated from a number of refugia in the IberianPeninsula, present-day Ukraine, and the northern Bal-kans (Otte, 1990). Along with the Paleolithic inhabi-tants, the recession of the ice caps allowed Neolithic pas-toral agriculturalists (Zvelebil, 1986; Pinhasi et al.,2000) to traverse into Europe from present-day Anatolia,carrying not only the newly developed farming lifestylebut Middle and Near Eastern Y-chromosomal hap-logroups as well (Rosser et al., 2000; Chikhi et al., 2002;Zei et al., 2003; Di Giacomo et al., 2004; Semino et al.,2004; Cruciani et al., 2006; Cadenas et al., 2008). East-to-west gradients of these Neolithic patrimonial geneticsignals have been detected throughout the continent(Cavalli-Sforza and Piazza, 1993; Comas et al., 1997;Semino et al., 2000; Gusma˜o et al., 2003; Dupanloup etal., 2004; Currat and Excoffier, 2005), and several stud-ies have revealed that Europeans represent an amalga-mation of both Paleolithic and Neolithic influences.Together, these findings suggest that the assimilation of people, and not just culture, has occurred (Richardset al., 2000; Dupanloup et al., 2004; Roewer et al., 2005).Southeastern Europe and specifically the Balkan statesare of particular interest when studying the events thatled to the current genetic admixture profiles characteris-tic of European populations, since they are strategicallylocated and likely served as a corridor for the passage of Neolithic agriculturalists into Europe and possibly forthe movement of European migrants into the Levant Anatolia and the Middle East.The Balkans consist of Slovenia, Croatia, Bosnia andHerzegovina, Serbia, Romania, and Moldova to thenorth; Greece to the south; and Montenegro, Albania,Macedonia, and Bulgaria, which lay in between. Archaeological studies suggest that repopulation of theBalkan Peninsula occurred early during the Mesolithicand Neolithic periods although the populace duringMesolithic times was scarce (Lahr et al., 2000; Pinhasiet al., 2000; Malyarchuk et al., 2003). During the late-Bronze age, migrants belonging to the Urnfield culture
 Additional Supporting Information may be found in the onlineversion of this article.Grant sponsor: Ministry of Sciences, Serbia; Grant number:145,007. Authors Sheyla Mirabal and Tatjana Varljen contributed equallyto this work.*Correspondence to: Rene J. Herrera, Department of Molecularand Human Genetics, College of Medicine, Florida InternationalUniversity, University Park, OE 304, Miami, FL 33199.E-mail: herrerar@fiu.eduReceived 1 August 2009; accepted 16 October 2009DOI 10.1002/ajpa.21235Published online 20 January 2010 in Wiley InterScience(www.interscience.wiley.com).
from central Europe (Coles and Harding, 1979) colonizedthe entire region from the Baltic to the Adriatic Sea(Pigott, 1965) while around 3,000 YBP, the Illyrians(Wilkes, 1992) and Thracians (Best and DeVries, 1989),both proto-Indo European tribes, are believed to haveattained dominion of the West and Southeast of the pen-insula, respectively. Slavic tribes from central and south-ern Europe are thought to have traversed into the areaaround the Middle Ages (Alekseeva, 1973; Rebala et al.2007), assimilating both the Illyrian and Thracian peo-ples and gradually transforming into modern-day Balkangroups (Malyarchuk et al., 2003).Mitochondrial DNA (mtDNA) studies suggest that themajority of haplogroups present in the Balkans are com-monly found in Western Eurasia (Calafell et al., 1996;Richards et al., 1996; Tolk et al., 2000; Malyarchuk etal., 2003), but there also exist minor contributions from Asia and Africa (Tolk et al., 2000; Malyarchuk et al.,2003); however, these signals are present in other south-eastern European populations which lay beyond the con-fines of the Balkan peninsula (Malyarchuk et al., 2006,2008). Moreover, Malyarchuk et al. (2003) have notedthat the differentiation between the two Balkan popula-tions of Bosnia and Slovenia indicates two separatewaves of migration from the Slavic domain into theBalkans during the Middle Ages. Y-chromosomal studies indicate that the Balkansplayed a pivotal role in the repopulation of Europe fol-lowing the LGM. Rootsi et al. (2004) and Pericic et al.(2005) have reported that the current distribution of haplogroup I2a1 throughout Europe follows I2a1’s diffu-sion out of the Balkans and into southeastern and east-ern Europe. The authors also report that the region mayhave served as a corridor for the propagation of hap-logroup E1b1b1a, which accounts for 98% of haplogroupE chromosomes in Europe (Cruciani et al., 2004; Seminoet al., 2004). Frequency gradients of markers withinhaplogroup J also suggest that the region has served asa migratory bridge between the Levant and Europe(Semino et al., 2004), and yet other data sets indicatethat acculturation has played a major role in the currentgenetic patterns observed throughout the peninsula(Battaglia et al., 2008).Given the important geographical and historical posi-tion of the Balkan states, the current project aims to elu-cidate the genetic relationships between the region andthe surrounding European and Near Eastern popula-tions to better understand the mechanisms that haveshaped the current genetic composition of the peninsula.Four hundred and four unrelated male individuals fromMontenegro and 179 from Serbia were typed across 17 Y-STR loci and compared across 9 Y-STR loci (DYS19,DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393,and DYS385a/b) to geographically targeted collections fromEurope, the Middle East, Anatolia, and the Caucasus. Forthe first time, we report on the phylogenetic relationshipsamong Balkan populations as well as between neighboringregions (i.e., Europe and the Middle East) based on allelicfrequencies of individual Y-STR loci.
MATERIALS AND METHODSSample collection and DNA purification
Samples were collected from total of 404 unrelatedMontenegrin and 179 Serbian males with informed con-sent and typed for 17 Y-STR loci. Genealogical informa-tion was recorded dating back to a minimum of twogenerations to establish regional ancestry and a lack of familial ties among the individuals sampled. One hun-dred and forty-one blood samples on FTA cards wereprocessed according to the manufacturer’s specifications(Whatman, Middlesex, UK) and an additional 263 buccalswabs were extracted using the conventional phenolchloroform method (Novick et al., 1995; Antunez deMayolo et al., 2002) for Montenegro. The 179 buccalswabs from Serbian individuals were phenol-chloroformextracted. Sample collection and processing were con-ducted abiding to the guidelines stipulated by the ethicalreview boards at all the research institutions involved inthe project.
Previously published data
 A total of 19 geographically targeted reference popula-tions were included for comparison across 9 Y-STR loci(DYS19, DYS389I, DYS389II, DYS390, DYS391,DYS392, DYS393, and DYS385a/b), since the rest of theloci typed in this study were not reported for several of the reference collections. The geographical locations,population designations, number of individuals, andreferences are included in Table 1 and Figure 1.
DNA amplification and STR genotyping
PCR amplification of the 17 Y-STR loci (DYS19,DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393,DYS385a/b, DYS437, DYS438, DYS439, DYS448, DYS456,DYS458, DYS635, and GATA H4) was conducted usingthe AmpFl/STR Yfiler PCR Amplifcation Kit (AppliedBiosystems, Foster City, CA) following the manufacturer’srecommendations (Applied Biosystems, 2005). Productswere sized on an ABI Prism 310 Genetic Analyzer(Mansfield et al., 1998) using the GeneScan v. 3.7 software(Applied Biosystems). Alleles were named according tonomenclature guidelines established by the InternationalSociety for Forensic Genetics (Gusma˜o et al., 2006) usingthe Yfiler kit’s allelic ladder.
Data analyses
The direct gene-counting method was used to estimate Y-STR allelic frequencies (Li, 1976). Basic diversity sta-tistics were computed using the software package Arle-quin v. 3.11 (Schneider et al., 2005), whereas observedgene and haplotype diversities were calculated accordingto Nei (1987). A correspondence analysis (CA) and a Neighbor-Join-ing (NJ) phylogram, both based on Y-STR allelic fre-quency distributions for loci DYS19, DYS389I,DYS389II, DYS390, DYS391, DYS392, DYS393, andDYS385a/b, were generated with the aid of the NTSYSpc2.02i (Rohlf, 2002) and PHYLIP 3.52c (Felsenstein, 2002)programs, respectively. The bootstrap values for the NJtree were calculated performing 1,000 replications andusing Nei’s genetic distance (Saiton and Nei, 1987). Admixture estimates based on Y-STR allelic frequencydistributions were performed using the SPSS 14.0 statis-tical software package (Long et al., 1991; Perez-Mirandaet al., 2006). The first set of analyses consisted of popula-tions grouped based on geographical and phylogeneticrelationships (Table 1) as parents while using theBalkan states as hybrids or offspring. The selection of populations to include in each group was based onthe co-segregation of collections in the CA and NJ
 American Journal of Physical Anthropology
dendrograms, defining biogeographical regions withgenetic affinities. A second set of analyses consisted of using individual Balkan collections as parental popula-tions to each Balkan data set in order to ascertain gene-flow throughout the region. Y-chromosomal haplogroup predictions were generatedusing Whit Athey’s haplogroup predictor (Athey, 2006)on the web (http://www.hprg.com/hapest5/). A networkprojection was produced with the aid of the programNETWORK 4.2.00 (Rohl, 1997); bifurcations wereassigned based on predicted haplogroup distributions(Supporting Information Fig. 1). Gradient maps based onthe frequencies of haplogroups I2a, R1b, R1a, and E1b1bwere generated with the aid of the Surfer 9 packagefrom Golden Software (www.goldensoftware.com). Pre-cise latitudes and longitudes for all populations includedin these projections can be found in Supporting Informa-tion Table 1.
RESULTS Y-STR intrapopulation diversity 
 A total of 318 and 171 different haplotypes weredetected in the Montenegro and Serbian populations,respectively; haplotypes, and their frequencies arepresented in Supporting Information Tables 2 and 3 forMontenegro and Serbia respectively. Y-STR allelic fre-quencies for Montenegro can be found in Table 2 on alocus-by-locus basis, whereas Table 3 presents similardata for Serbia. The most common haplotype observed isfound at a frequency of 2.72% for Montenegro. In theSerbian collection, the most notable haplotype isobserved at a frequency of 1.12%. A total of 270 uniquehaplotypes are represented in Montenegro, whereas 163are found in Serbia.The most abundant Y-chromosomal haplogroup basedon Athey’s haplogroup predictor for the Montenegro
Fig. 1.
Populations analyzed using Y-STR allelic frequency data. Population denominations are provided in Table 1.
TABLE 1. Populations analyzed using Y-STR data
Population Abbreviation
ReferencesBalkans Albanians (Kosovo) ALBK 117 Pericic´et al., 2004Bosnia and Herzegovina BOH 181 Klaric´et al., 2005Croatia CRO 166 Ljubkovic´et al., 2008Greece GRE 39 Bosch et al., 2006Macedonia MAC 150 Spiroski et al., 2005Montenegro MON 400 PresentSerbia SER 179 PresentSerbia (Vojvodina) SERV 185 Veselinovic´et al., 2008Slovenia SLO 121 Sterlinko et al., 2001West Croatia WCR 101 Lovrecic et al., 2005EuropeGermany (Hamburg) HAM 49 Rodig et al., 2007Italy ITA 155 Turrina et al., 2006Lithuania LIT 127 Pepinski et al., 2004Russia (Lipezkaja) LIP 47 Roewer et al., 2008Russia (Penzenskaya) PEN 81 Roewer et al., 2008Romania (Poiesti) ROM 37 Bosch et al., 2006Caucasus Armenia ARM 100 Nasidze et al., 2003 Azerbaijan AZE 72 Nasidze et al., 2003Georgia GEO 77 Nasidze et al., 2003Middle East/AnatoliaIran IRA 80 Nasidze et al., 2003Turkey TUR 39 Nasidze et al., 2003
 American Journal of Physical Anthropology

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