SHORT COMMUNICATION

doi: 10.1111/j.1529-8817.2005.00190.x

The Peopling of Modern Bosnia-Herzegovina: Y-chromosome Haplogroups in the Three Main Ethnic Groups
D. Marjanovic1,∗ , S. Fornarino2 , S. Montagna2 , D. Primorac3,4 , R. Hadziselimovic1 , S. Vidovic5 , N. Pojskic1 , V. Battaglia2 , A. Achilli2 , K. Drobnic6 , S. Andjelinovic3 , A. Torroni2 , A. S. Santachiara-Benerecetti2 and O. Semino2,† 1 Institute for Genetic Engineering and Biotechnology, University of Sarajevo, Sarajevo, Bosnia and Herzegovina 2 Dipartimento di Genetica e Microbiologia “A. Buzzati-Traverso”, Universit` di Pavia, Pavia, Italy a 3 Medical School at Split University, Split, Croatia 4 Medical School at Osijek University, Osijek, Croatia 5 Faculty of Medicine, University of Banjaluka, Banjaluka, Bosnia and Herzegovina 6 Forensic Laboratory and Research Center, Ministry of the Interior, Ljubljana, Slovenia

Summary
The variation at 28 Y-chromosome biallelic markers was analysed in 256 males (90 Croats, 81 Serbs and 85 Bosniacs) from Bosnia-Herzegovina. An important shared feature between the three ethnic groups is the high frequency of the “Palaeolithic” European-specific haplogroup (Hg) I, a likely signature of a Balkan population re-expansion after the Last Glacial Maximum. This haplogroup is almost completely represented by the sub-haplogroup I-P37 whose frequency is, however, higher in the Croats (∼ 71%) than in Bosniacs (∼ 44%) and Serbs (∼ 31%). Other rather frequent haplogroups are E (∼ 15%) and J (∼ 7%), which are considered to have arrived from the Middle East in Neolithic and post-Neolithic times, and R-M17 (∼ 14%), which probably marked several arrivals, at different times, from eastern Eurasia. Hg E, almost exclusively represented by its subclade E-M78, is more common in the Serbs (∼ 20%) than in Bosniacs (∼ 13%) and Croats (∼ 9%), and Hg J, observed in only one Croat, encompasses ∼ 9% of the Serbs and ∼ 12% of the Bosniacs, where it shows its highest diversification. By contrast, Hg R-M17 displays similar frequencies in all three groups. On the whole, the three main groups of Bosnia-Herzegovina, in spite of some quantitative differences, share a large fraction of the same ancient gene pool distinctive for the Balkan area.
Keywords: Y-Chromosome haplogroups, Polymorphisms, Bosnia-Herzegovina, Balkans.

Introduction
Archaeological findings in central Bosnia (∼ 100,000 years old) and in the north of the country (∼ 50,000
∗ Address for correspondence: Dr. Damir Marjanovic, Institute for Genetic Engineering and Biotechnology, University of Sarajevo, Kemalbegova 10, 71.000 Sarajevo, Bosnia and Herzegovina. Tel. +387 33 220 926; Fax +387 33 442 891, E-mail: damirm.marjanovic@ingeb.ba † Dr. Ornella Semino, Dipartimento di Genetica e Microbiologia, Universit` di Pavia, Via Ferrata, 1, 27100 Pavia, a Italy. Tel +39 0382 985543; Fax +39 0382 528496, E-mail: semino@ipvgen.unipv.it
C

years old) indicate that the territory of modern BosniaHerzegovina was continuously settled since the Palaeolithic (Imamovi´ , 1998). At the beginning of the c second millennium BC this part of the Balkans was inhabited by different Illyrian tribes, which established the oldest central-western Balkan civilization (Wilkes, 1992). These local inhabitants probably completely assimilated most of the first immigrants (Avars and Slavs) who entered the region soon after the splitting of the Roman Empire. The process of the peopling of Bosnia and Herzegovina was extensively shaped with the arrival of two new tribes, the Croats and the Serbs, whose
Annals of Human Genetics (2005) 69,757–763

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and Croat collecting points. Boxed S. The recent detection of a large number of informative biallelic markers in the non-recombining region of the Y chromosome (NRY) has already significantly contributed to the understanding of European pre-history and history (Semino et al. M47. M89. 1996. Modern Bosnia-Herzegovina is a multinational and multi-religious country with a very stormy recent history. could be direct descendants of Bosnia’s non-Slavic aboriginal inhabitants (Malcolm. M74. 2002). Serbs – . M170. M26. and about the ancient and recent events of gene flow which have influenced this area located in the heart of Europe. M12. C University College London 2005 . M267 and M269) (The Y Chromosome Consortium. M9 was chosen as the initial marker and surveyed in all samples. Rootsi et al. 2000. Figure 1 The location of Bosnia-Herzegovina (left) and the locations in Bosnia-Herzegovina from which the population samples were collected (right). During the 20th century. 1994). 81 Serbs and 85 Bosniacs – the last previously identified as “Muslim”) unrelated males born in Bosnia-Herzegovina. A detailed analysis of the list of blood donors and their family records showed that the sample is representative of all of Bosnia-Herzegovina. Underhill et al. Cruciani et al. M102. M201. Blood collection was carried out at 6 collection points. M227. with the aim of providing new clues about their origin. Bosniac. Twenty-eight NRY biallelic markers (12f2. Places of sample origin: Croats – . The present BosniaHerzegovina territory is located between the areas inhabited by Croats (westward) and Serbs (eastward). M81. origins are still under discussion. M78. M123. M223. followed by ethanol precipitation. M253. The second important historical period for this country is represented by the expansion of the Ottoman Empire in the fifteen century that was responsible for the Islamicization of a large part of the population (Malcolm.757–763 Material and Methods The Sample The sample consists of 256 (90 Croats. political justifications for the conflicts in the area were sought through different interpretations of the origins of the three main ethnic groups (Croats. 2001). 758 Annals of Human Genetics (2005) 69. M67. according to the most diffused theory. M17. 2002. Y-chromosome DNA Analysis DNA was extracted from whole blood according to the standard phenol/chlorophorm procedure. 2002. M172. and pointed to this area as crossroads for different cultures and populations. The attribution of the subjects to the three ethnic groups was carried out according to the origin of their paternal grandfather.Marjanovic et al. M207. YAP. since the subjects are from more than 50 different locations (Figure 1). P37. Serbs and Bosniacs) from this region. 2004) were examined in hierarchical order in agreement with the Y-chromosome phylogeny (YCC. M35. from volunteers appropriately informed about the research. Here we have investigated the Y-chromosome variation in 256 individuals from the three major ethnic groups of Bosnia-Herzegovina. M92. Bosniacs – •. M68. B and C refer to Serb. M9. M173. The populations from the isolated mountain villages. 1994).

Croats vs Bosniacs P = 2 × 10− 4 < E Croats vs Serbs P < 0. Indeed.9% in Bosniacs) and Hg J (1. the Croats show the highest I-P37 frequency (71. F∗ .Y-chromosome haplogroups in Bosnia-Herzegovina Figure 2 Phylogeny of Y-chromosome haplogroups and their frequencies in Croats. respectively. G. as well between Croats and Serbs (P < 10− 5 ). The YCC (2002) nomenclature was used for haplogroup labelling.757–763 University College London 2005 759 . while I-M26 was not observed. Statistical Analysis Haplogroup diversity was computed using Nei’s standard method (Nei & Kumar. I. the Croats are the most homogeneous group (H = 0. Principal Component (PC) analysis was performed on haplogroup frequencies by using Excel implemented by the XL-stat program. (2001) (P37) and Cruciani et al. Their distributions. Serbs and Bosniacs) and in the pooled sample are illustrated in Figure 2 with the P values reported for significantly different frequencies.1% vs 30.47). Croats vs Bosniacs P Fisher = 0. differ in the three groups. the haplogroup distribution. (1983). (2000).9% in Bosniacs). All the other mutations were detected by PCR/DHPLC. Annals of Human Genetics (2005) 69.1%). their frequencies in the three studied sub-groups (Croats. M9 and M269 were typed through PCR/RFLP assays according to Karafet et al. The phylogenetic relationships of these haplogroups. 2000 (Schneider et al. and it is almost exclusively represented by its sub-haplogroup I-P37. Results The analysis of 28 Y-chromosome biallelic markers has allowed the classification of the 256 Bosnian samples C into haplogroups E.83). Haplogroup I is the most commonly represented haplogroup. 1984. 2000). 1992) were performed using the Arlequin package. significantly differs between Croats and Bosniacs (P < 10− 5 ). The 12f2 and YAP polymorphisms were analyzed according to Rosser et al.7%) and J (7. K∗ and R. Population differentiation tests (Raymond & Rousset. which accounts for 5.3% in Serbs and 12.020. Serbs and Bosniacs of modern Bosnia-Herzegovina. however. Significant differences: I-P37 Croats vs Serbs P< <10− 4 . accounting for more than 50% of the Y chromosomes.9% in Serbs and 43. R-M17 (13. On the whole.5% in Bosniacs) and the lowest frequencies for both Hg E (8.1% vs 8. In particular. 2000).003 a Intrapopulation haplogroup diversity. as reported by Underhill et al.8% of the variation among populations.5%).9% vs 22.02 J Croats vs Serbs P Fisher = 0. (2000) and Hammer & Horai (1995). J. mutations P37. followed by the Bosniacs (H = 0. ver. (2002) (M9 and M269). Excoffier et al.76) and the Serbs (H = 0. Additional haplogroups with overall frequencies higher than 5% are haplogroups E (14. Other subsets of Hg I such as I-M253 and I-M223 were scarce. Genetic distance tests were performed using the approach of Reynolds et al.7% in Serbs and 11. The particular haplogroup distribution in the Croats is mirrored in their intrapopulation diversity value (Figure 2). 1995) and AMOVA (Weir & Cockerham.

However. Slo = Slovenians. Mac (Gr) = Macedonian Greeks. Geo = Georgians. I-M26. Hu = Hungarians. G. J1. 2000).0082). and unpublished data. 2004). Ukrainian and Franco-Cantabrian refuges.Marjanovic et al. I∗ . Pl = Poles. I-M223. I-P37∗ . Croats and Serbs. Tk = Turks. J2. but not between Serbs and Bosniacs. Sm = Saami. 41% of the total variance is represented: 22% by the first PC and 19% by the second PC. N-It = North Italians. R-M17 and R-M269 in the three Bosnian groups (present paper). Semino et al.0550) and Serbs vs Bosniacs (D = 0. Gr = Greeks. The relationships among the three groups in the overall European scenario are summarized by the plot of the first and second principal components illustrated in Figure 3. and haplogroups considered to 760 Annals of Human Genetics (2005) 69. Iq = Iraqis. C University College London 2005 . The frequency of sub-haplogroup I-P37 observed in the Croats is particularly high (71.9%) show that the three population groups share a major subset of their gene pool. Figure 3 PC analysis performed using the frequencies of the Y-chromosome haplogroups E-M35. S-Bas = Spanish Basques. Cz & Sl = Czechoslovaks. Indeed the people of Bosnia-Herzegovina display Europeanspecific haplogroups that most likely arose in different glacial refuge areas of Europe (I-M170. Taking into account that a Palaeolithic origin of the P37 mutation in this Balkan district has been previously suggested (Rootsi et al. Cr = Croats of Croatia. are the most divergent from each other (D = 0. but the high frequencies observed also in the Bosniacs (43.1%) and could be partially attributed to genetic drift. Sar = Sardinians. followed by Croats vs Bosniacs (D = 0.757–763 have originated in Africa (E-SRY 4064 ) and the Middle East (J-12f2) and to have arrived in Europe through the prolonged gene flow from the Middle East (Cruciani et al. Uk = Ukrainians) are from Semino et al. The data from the additional European populations (Alb = Albanians. 2004. I-M253. Du = Dutch. Rootsi et al. Bosnian Serbs and Bosniacs harbour haplogroups which they share with many other Europeans (Semino et al. a specific sub-haplogroup of I. On the whole. it is possible that the post-LGM expansion of a population with a high frequency of I-P37 from one of the refuges present in the Balkans played a major role in the peopling of Bosnia-Herzegovina and surrounding areas. Discussion The analysis of Y-chromosome variation in the three main ethnic groups of modern Bosnia-Herzegovina reveals that Bosnian Croats. (2004). 2004). F-Bas = French Basques. respectively).5%) and Serbs (30. and in other European populations. the Y chromosomes in Bosnia-Herzegovina differ from those of most other European regions because more than 50% belong to I-P37. according to the calculated genetic distances. And = Andalusians.(2000). and that this ancestral gene pool was affected by a major demographic event. R-M17 and RM269 from Balkan.1234). Fr = French. Cat = Catalans.

2001). however.757–763 University College London 2005 761 . where the highest European frequencies of E-M78 are observed. and closely related to other populations of the Balkans. However.3% in the Bosniacs. Semino et al.2% in the Serbs.Y-chromosome haplogroups in Bosnia-Herzegovina The second most frequent haplogroup in BosniaHerzegovina is Hg E (14. In BosniaHerzegovina Y chromosomes belonging to J are found mainly in the Bosniacs who. were probably the group in which genetic drift and founder events played the most important role. Despite their relatively low frequency. 2004. the migratory processes from Central Asia and Eastern Europe – marked by haplogroup R-M17 – seem to have similarly Annals of Human Genetics (2005) 69. in whom a single undifferentiated J-M172 Y chromosome was encountered. J-M67. respectively. which has been associated with the Arab expansions. whose presence in Europe has been attributed to multiple migrations from the Middle East and North Africa during and after the Neolithic (Cruciani et al. in Neolithic and post-Neolithic times. g Cruciani et al. 2004. Hg E is almost exclusively represented by the sub-clade E-M78. The last.05) but it is similar to that in other southern Balkan populations (20% in Greeks and 25% in Albanians) (Semino et al. On the contrary. ranging from 12. 2000. the ancestral Balkan populations. Its frequency is very similar in the three groups. It is worth remembering that the clinal distribution in Europe of E-M78 and its internal microsatellite variance have been attributed to dispersals. as c c well as to the arrival of the Slav clans during the 6th and 7th centuries. interestingly. 2004). but also from the Croats of Croatia. Passarino et al. J-M92. However. appears to be more represented in the Serbs (6. Semino et al. 2004). Of interest is the presence of the R-M269 Y chromosomes in modern Bosnia-Herzegovina. they indicate that the gene pool of the ancestral population(s) of the FrancoCantabrian refuge area also contributed to some extent to this region of the Balkans. overall a higher extent of gene flow could have occurred in the Bosniacs.000 years ago (Jovanovi´ 1979. could also be due to infiltrations of IndoEuropean speaking peoples from southern Russia about 2. harbour almost all the known J sub-clades (Semino et al. These are: J-M267. Haplogroup J is another haplogroup that arrived in Europe from the Middle East and its sub-clades probably marked complex migration processes during and after Neolithic time (Cinnioˇ lu et al. initially attributed to expansion(s) from a Ukrainian glacial refuge (Semino et al. Thus. In contrast. 2004. This gradient. the first PC shows that the three populations are genetically extremely close to each other. to evaluate this latter scenario.7% of the pooled samples. 2000). Semino et al. Di g Giacomo et al. most likely. as already suggested by the extremely high frequency of I-P37. In the PC analysis (Figure 3). 2004. but is less common in Croats (8. 2004). which suggests genetic links between Anatolia and southern Italy. as additionally attested by the finding in the same region of the mtDNA haplogroup H1 (Achilli et al.8%). C R-M17 is the prevalent sub-haplogroup of R as previously observed in other eastern European populations (Semino et al.9%) and Bosniacs (12. 2003).9%) than in Serbs (19. 2004). 2004. from the Balkans to all directions. but provided some “Southern Balkan” (Hg E-M78) and “Anatolian” (different clades of Hg J) contributions to gene pools of the Serbs and Bosniacs. 2001. as far as Iberia to the west and. 2004).2% in the Croats to 15. and perfectly fits the expected distribution of R-M17 which is found almost exclusively in eastern Europe with a decreasing gradient from northeast to south-west. This accounts for 13. which is frequent in the Caucasus. which shows frequency peaks in the southern Balkans and central-southern Italy. 2004). In conclusion our data suggest that a post-glacial expansion – possibly from a LGM refuge area in the Balkans – probably gave rise to the frequency peak of haplogroup I-P37 in the region. and finally J-M102. ranging from 2. Neolithic and post-Neolithic gene flow appears to have played an overall less important role in all three populations.5%). while the Croats. The frequency observed in the Serbs is significantly different from that in Croats (P < 0.2%). to different extents. also to Turkey in the southeast (Cinnioˇ lu et al. the second PC tends to separate the Croat group not only from both Serbs and Bosniacs. In this frame.2% in the Croats to 6. Bara´ et al. with decreasing consequences for the Croats. our data suggest that the expansion(s) of E-M78 would have affected. larger samples of R-M17 Y chromosomes from the area and detailed analyses of their STR diversity are required. to the Bosniacs and then to the Serbs. However. Wells et al. It only marginally influenced the Bosnian Croats.

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