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Introduction
Southeastern Europe (SEE) has traditionally been
viewed as a bridge (Childe 1958) between the Near East
and temperate Europe or as a key area in the process of transition from hunter-gathering to agropastoral, farming societies in Europe (e.g., Ammerman and Cavalli-Sforza 1984;
Renfrew 1987; Zvelebil and Lillie 2000). Recent phylogeographic analyses of Y chromosome E and J haplogroups
indicate that southern Europe and the Balkans indeed could
have been both the receptors and sources of gene flow during and after the Neolithic (Cruciani et al. 2004; Semino
et al. 2004). The STR haplotype diversity of these two haplogroups is considerably younger than that of other Y chromosome haplogroups spread in Europe. Among the latter,
haplogroup I, perhaps, most clearly represents the paternal
genetic component of the pre-Neolithic Europeans. In contrast to E and J, haplogroup I is virtually absent in Middle East
and West Asia (Semino et al. 2000), and two of its major subclades have frequency peaks in northern Balkans and Scandinavia (Rootsi et al. 2004). Semino et al. (2000) and Barac
et al. (2003) hypothesized that, besides southwest Europe, the
northern Balkans could have been another possible Last Glacial Maximum (LGM) refugium and a reservoir of M170.
In this study we first examined the extent and nature of
SEE paternal genetic contribution to the European genetic
landscape based on a high-resolution Y chromosome typing
involving 681 unrelated males from four modern states,
1
Key words: phylogenetic analysis, Y chromosomal binary haplogroups, southeastern Europe (SEE).
E-mail: mpericic@luka.inantro.hr
Mol. Biol. Evol. 22(10):19641975. 2005
doi:10.1093/molbev/msi185
Advance Access publication June 8, 2005
The Author 2005. Published by Oxford University Press on behalf of
the Society for Molecular Biology and Evolution. All rights reserved.
For permissions, please e-mail: journals.permissions@oupjournals.org
The extent and nature of southeastern Europe (SEE) paternal genetic contribution to the European genetic landscape were
explored based on a high-resolution Y chromosome analysis involving 681 males from seven populations in the region.
Paternal lineages present in SEE were compared with previously published data from 81 western Eurasian populations and
5,017 Y chromosome samples. The finding that five major haplogroups (E3b1, I1b* (xM26), J2, R1a, and R1b) comprise
more than 70% of SEE total genetic variation is consistent with the typical European Y chromosome gene pool. However,
distribution of major Y chromosomal lineages and estimated expansion signals clarify the specific role of this region in
structuring of European, and particularly Slavic, paternal genetic heritage. Contemporary Slavic paternal gene pool, mostly
characterized by the predominance of R1a and I1b* (xM26) and scarcity of E3b1 lineages, is a result of two major prehistoric
gene flows with opposite directions: the post-Last Glacial Maximum R1a expansion from east to west, the Younger DryasHolocene I1b* (xM26) diffusion out of SEE in addition to subsequent R1a and I1b* (xM26) putative gene flows between
eastern Europe and SEE, and a rather weak extent of E3b1 diffusion toward regions nowadays occupied by Slavic-speaking
populations.
FIG. 1.Map of the studied region and sample locations (1 5 Zabok, 2 5 Zagreb, 3 5 Donji Miholjac, 4 5 Delnice, 5 5 Pazin, 6 5 Dubrovnik,
7 5 Zenica, 8 5 Mostar, 9 5 Siroki Brijeg, 10 5 Belgrade, 11 5 Pristhina, 12 5 Skopje).
FIG. 2.Y chromosomal SNP tree and haplogroup frequencies (percent) in seven SEE populations. *Croatian mainland from Barac et al. (2003) was
additionally genotyped for deeper resolution of I in Rootsi et al. (2004) and for E and J in the present study. E3b1a chromosomes were defined by
A7.1 nine-repeat allele.
Table 1
Summarized Percent Frequencies of R1b, R1a, I1b* (xM26), E3b1 and J2e
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Greek)
IE (Indo-Iranian)
IE (Albanian)
IE (Albanian)
IE (Greek)
IE (Greek)
IE (Balto-Slavic)
IE (Italic)
Uralic (Finno-Ugric)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Balto-Slavic)
IE (Germanic)
IE (Germanic)
IE (Germanic)
Uralic (Finno-Ugric)
Uralic (Finno-Ugric)
IE (Germanic)
IE (Germanic)
IE (Balto-Slavic)
IE (Balto-Slavic)
Uralic (Finno-Ugric)
IE (Italic)
Uralic (Finno-Ugric)
Uralic (Finno-Ugric)
Altaic (Turkic)
Caucasian (S. Caucasian)
IE (Indo-Iranian)
IE (Armenian)
IE (Germanic)
IE (Germanic)
IE (Celtic)
IE (Celtic)
IE (Celtic)
N R1b-M173a
70
108
69
141
113
79
20
57
114
51
118
45
24
45
45
45
55
41
122
50
181
110
48
127
57
112
12
38
34
207
63
47
49
32
215
88
71
61
21.0b
15.7d
1.4d
3.6d
10.6d
5.1d
10.0f
1.8d
21.1d
17.6f
22.8f,i
9.0b
17.0b
18.0b
13.3f
35.6f
16.4f
10.0b
7.0b
2.0f
41.4i
20.0i
23.0b
3.9k
2.0b
25.9i
41.7i
5.0b
15.0b
9.0b
14.3f
43.0b
25.0b
68.8i
61.9l
89.0m
66.0m
77.1i
95% CR
(13.532.4)
(10.123.8)
(0.37.7)
(1.68.0)
(6.217.7)
(0.2112.3)
(3.030.4)
(0.49.2)
(14.629.4)
(9.630.3)
(16.231.3)
(3.620.8)
(6.836.1)
(9.431.4)
(6.326.3)
(23.250.2)
(8.928.3)
(4.022.6)
(14.244.6)
(0.510.4)
(34.548.7)
(13.628.5)
(13.336.6)
(1.78.9)
(0.49.2)
(18.734.7)
(19.268.4)
(1.617.3)
(6.630.3)
(6.013.9)
(7.825.0)
(29.556.8)
(14.638.2)
(51.382.0)
(55.268.1)
(80.393.7)
(54.676.1)
(65.085.8)
N R1a-M17
70
108
69
141
113
79
20
57
114
51
118
45
34
45
113
45
55
41
122
50
181
110
48
127
57
112
12
38
34
74
46
46
63
47
89
32
215
88
71
61
37.0b
34.3d
24.6d
12.1d
15.9d
15.2d
35.0f
1.8d
4.4d
9.8f
8.3f,i
2.0b
14.7j
20.0b
20.4k
26.7f
56.4f
39.0b
47.0b
54.0f
23.8i
17.3i
19.0b
11.0k
10.0b
17.9i
16.7i
34.0b
41.0b
36.5j
39.1j
21.7j
7.9f
2.0b
6.0b
9.4i
3.3l
1.0m
19.7m
6.6i
95% CR
(26.848.9)
(26.043.6)
(16.036.0)
(7.718.5)
(10.323.8)
(8.924.7)
(18.157.0)
(0.49.2)
(1.99.9)
(4.421.0)
(4.714.9)
(0.511.5)
(6.630.3)
(10.933.9)
(14.028.7)
(16.041.1)
(43.268.7)
(25.654.4)
(38.155.6)
(40.367.1)
(18.130.5)
(11.425.4)
(10.232.0)
(6.717.7)
(2.916.7)
(11.926.0)
(5.045.4)
(21.250.2)
(26.357.9)
(26.447.9)
(26.453.6)
(12.335.7)
(3.517.3)
(1.314.3)
(3.213.9)
(3.424.3)
(1.66.6)
(0.36.1)
(12.230.5)
(2.715.7)
N I1b* (xM26)-P37
55
108
69
141
113
79
50
57
114
106
261
361
162
198
191
147
78
50
144
97
53
127
120
585
225
35
72
86
210
60
79
20.0c
32.4ce
52.2d
63.8d
29.2d
29.1d
18.0c
3.5d
2.7d
17.0c
8.4c
17.7c
11.1c
7.1c
9.9c
15.0c
16.7c
2.0c
12.5c
15.5c
9.4c
3.9c
9.1c
16.1c
0c
0c
0c
1.2c
2.9c
21.7c
24.1c
95% CR
(11.632.4)
(24.341.7)
(40.663.6)
(55.671.3)
(21.638.2)
(20.340.0)
(9.830.9)
(1.111.9)
(1.07.4)
(11.025.3)
(5.612.4)
(14.122.0)
(7.216.9)
(4.311.5)
(6.515.0)
(10.121.6)
(10.026.5)
(0.510.4)
(8.118.9)
(9.624.0)
(4.220.3)
(1.78.9)
(5.215.7)
(13.319.3)
(0.01.3)
(0.08.0)
(0.04.0)
(0.36.2)
(1.36.1)
(13.233.7)
(16.034.6)
N E3b1-M78
108
69
141
113
79
59
57
114
63
84
116
14
53
137
93
35
74
5.6d
10.1d
8.5d
20.4d
24.1d
18.6g
29.8d
45.6d
27.0g,h
21.4g
20.7h
21.4h
7.5g
3.6g,h
7.5g
2.9h
4.1h
0h
95% CR
(2.611.6)
(5.119.5)
(5.014.3)
(14.028.7)
(16.034.6)
(10.830.4)
(19.542.7)
(36.854.8)
(17.639.1)
(14.031.4)
(14.329.0)
(7.848.1)
(3.117.9)
(1.68.3)
(3.714.7)
(0.714.5)
(1.511.2)
(0.031.2)
N J2e-M102
108
69
141
113
79
57
114
56
92
49
97
82
1.0d
0d
0.7d
5.3d
6.3d
1.8d
16.7d
14.3g
6.5g
0g
1.0g
2.4g
95% CR
(0.25.0)
(0.04.2)
(0.23.9)
(2.511.1)
(2.814.0)
(0.49.2)
(11.024.6)
(7.525.8)
(3.113.5)
(0.05.8)
(0.25.6)
(0.88.4)
Slovenian
Croatian (mainland)
Bosnian
Herzegovinian
Serbian
Macedonian
Macedonian (Greek)
Macedonian Romani
Albanian (Kosovar)
Albanian
Greek
Cypriot
Bulgarian
Romanian
Hungarian
Czech and Slovak
Polish
Byelorussian
Russian
Russian (Adygea)
Russian (Bashkortostan)
Russian (Belgorod region)
Russian (Cossacks)
Russian (Kostroma region)
Russian (North, Pinega)
Russian (Smolensk region)
Ukrainian
Icelander
Swedish
Swedish (Northern)
Saami
Finnish
Norwegian
Danish
Lithuanian
Latvian
Estonian
Moldavian
Moldovan (Erzya)
Moldovan (Moksi)
Moldovan (Gagauz)
Georgian
Ossetian
Armenian
British
English (Central)
Welsh
Orcandin
Scottish
Language Family
Population
Population
Irish
Frisian
German
Dutch
Belgian
French
Bearnais
Swiss
Italian
Italian (Calabria)
Italian (Apulia)
Italian (Sardinia)
Italian (North-central)
Italian (South)
Italian (Siciliy)
Spanish
Catalan
Andalusian
Basque (French, Spanish)
Portuguese
Portuguese (South)
Portuguese (North)
Turkish
Anatolian (Central)
Turkish (Istanbul)
Turkish (Konya)
Turkish (Cypriot)
Turkish (Southeastern)
Turkish (Erzurum)
Algerian
Tunisian
Moroccan
Language Family
IE (Celtic)
IE (Germanic)
IE (Germanic)
IE (Germanic)
IE (Germanic)
IE (Italic)
IE (Italic)
IE (German/Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
IE (Italic)
Basque (Basque)
IE (Italic)
IE (Italic)
IE (Italic)
Altaic (Turkic)
Altaic (Turkic)
Altaic (Turkic)
Altaic (Turkic)
Altaic (Turkic)
Altaic (Turkic)
Altaic (Turkic)
Afro-Asiatic (Semitic)
Afro-Asiatic (Semitic)
Afro-Asiatic (Semitic)
R1b-M173a 95% CR
222
94
48
27
92
23
37
81.5
56.0m
47.9f,i
70.4f
63.0b
52.2f
32.4f
(75.986.1)
(46.366.0)
(34.461.7)
(51.384.1)
(52.872.2)
(32.870.9)
(19.648.7)
77
50
126
24
29
67
57
328
523
35
148
44
22.1f
62.0f
68.0b
79.2f
65.5f
88.1f
56.0b
62.0b
16.3n
0o
6.7o
6.8o
(14.332.6)
(47.973.5)
(60.576.5)
(59.390.6)
(47.280.1)
(78.193.8)
(43.268.3)
(56.567.0)
(13.319.7)
(0.08.0)
(3.712.0)
(2.518.3)
N
222
94
48
27
92
23
332
126
29
26
57
328
523
35
148
44
R1a-M17 95% CR
i
0.5
7.4m
8.1f,i
3.7f
4.0b
0f
2.7i
2.0b
0f
0b
2.0b
0b
6.9n
0o
0o
0o
(0.12.5)
(3.714.6)
(3.419.6)
(0.918.3)
(1.910.6)
(0.011.7)
(1.45.1)
(0.55.6)
(0.09.5)
(0.010.5)
(0.49.2)
(0.00.9)
(5.29.6)
(0.08.0)
(0.02.0)
(0.06.4)
16
30
179
26
144
148
78
142
390
32
103
100
303
741
35
148
44
0c
0c
0c
0c
0c
0.7c
1.3c
0c
0.5c
0c
0c
0c
0.7c
2.3c
0o
0o
0o
(0.016.2)
(0.09.2)
(0.01.7)
(0.010.5)
(0.02.0)
(0.23.7)
(0.36.9)
(0.02.1)
(0.21.8)
(0.08.7)
(0.02.8)
(0.02.9)
(0.22.4)
(1.43.6)
(0.08.0)
(0.02.0)
(0.06.4)
85
43
80
86
506
212
87
191
33
113
61
81
117
46
24
25
32
58
93
E3b1-M78 95% CR
4.7h
4.6g,h
16.3g
11.6g
3.4g,h
10.4g,h
11.5h
13.6g,h
3.0g
3.5g
6.6h
8.6g,h
12.8g
13.0h
4.2h
4.0h
6.3g
15.5g
27.9g
(1.911.5)
(0.918.3)
(9.825.9)
(6.520.1)
(2.15.3)
(7.015.2)
(6.419.9)
(9.519.2)
(0.715.3)
(1.48.7)
(2.715.7)
(4.316.8)
(8.020.1)
(6.225.7)
(1.020.4)
(0.919.6)
(1.920.2)
(8.427.0)
(19.937.8)
J2e-M102 95% CR
34
26
57
86
144
52
0g
3.8g
1.8g
3.5g
2.1g
9.6g
(0.08.2)
(0.919.0)
(0.49.2)
(1.39.7)
(0.85.9)
(4.320.7)
42
28
93
92
73
129
55
73
44
0g
0g
1.1g
0
0g
0.8g
0g,o
1.4g
0o
(0.06.7)
(0.09.8)
(0.35.8)
(0.03.2)
(0.04.0)
(0.24.2)
(0.05.2)
(0.37.3)
(0.06.4)
NOTE.IE 5 Indo-European.
a
R1b haplogroup is defined by M173 (xSRY-1532); data from Rosser et al. (2000), Helgason et al. (2000), Weale et al. (2002), and Wilson et al. (2001) are deducted based on the last typed marker 92R7 (xSRY-1532).
b
Rosser et al. (2000).
c
Rootsi et al. (2004).
d
This study.
e
Barac et al. (2003).
f
Semino et al. (2000).
g
Semino et al. (2004).
h
Cruciani et al. (2004).
i
Helgason et al. (2000).
j
Malaspina et al. (2003).
k
Tambets et al. (2004).
l
Weale et al. (2002).
m
Wilson et al. (2001).
n
Cinnioglu et al. (2004)
o
Arredi et al. (2004).
Table 1
Continued
FIG. 3.I1b* (xM26) frequency and variance surfaces in SEE (panels A and B) were generated from the data in this study. I1b* (xM26) frequency
surfaces in Europe, northern Africa, and Asia Minor (panel C) were generated from the data reported in table 1, and variance surfaces (panel D) were
generated from STR data in this study and Rootsi et al. (2004).
as one of major routes for E3b1, in fact E3b1a, expansion from south and southeastern to continental Europe.
In fact, dispersals of farmers throughout the VardarMorava-Danube catchments basin are also evidenced in
the archaeological record (Tringham 2000).
R1a haplogroup occurs at 16% frequency in SEE
(fig. 2). The age of M17 has been approximated to
15 KYA (Semino et al. 2000; Wells et al. 2001). Kivisild
et al. (2003) suggested that southern and western Asia
might be the source of R1 and R1a differentiation. Current
R1a-M17/SRY-1532 distribution in Europe shows an increasing west-east frequency and variance gradients with
peaks among Finno-Ugric and Slavic speakers (fig. 5C
and D). Similar to I1b* (xM26), R1a frequency gradient
decreases slowly to the south (to 10% in Albanians, 8%
in Greeks, and 7% in Turks) and abruptly in the west
(3% in Italians) (table 1). R1a frequency and STR variance
decrease in the north-south direction in SEE, from 34%
25% in mainland Croatians and Bosnians to 12%16%
in Herzegovinians, Macedonians, and Serbians (fig. 5A
and B). Moreover, R1a frequency is significantly correlated
with latitude (table 2) when all studied SEE populations are
considered (r 5 0.865, P 5 0.01) and also when Kosovar
FIG. 4.E3b1 frequency and variance surfaces in SEE (panels A and B) were generated from the data in this study. E3b1 frequency surfaces in
Europe, northern Africa, and Asia Minor (panel C) were generated from the data reported in table 1, and variance surfaces (panel D) were calculated from
STR data in this study and Semino et al. (2004).
FIG. 5.R1a frequency and variance surfaces in SEE (panels A and B) were generated from the data in this study. R1a frequency surfaces in Europe,
northern Africa, and Asia Minor (panel C) were generated from the data reported in table 1, and variance surfaces (panel D) were calculated from STR data
in this study, Rootsi et al. unpublished data, Cinnioglu et al. (2004), Behar et al. (2003), Weale et al. (2002), Wilson et al. (2001), Helgason et al. (2000),
and Hurles et al. (1999). Shaded areas in panel D correspond to regions for which combined SNP and STR Y chromosomal data are not available.
FIG. 6.R1b frequency and variance surfaces in SEE (panels A and B) were generated from the data in this study. R1b frequency surfaces in Europe,
northern Africa, and Asia Minor (panel C) were generated from the data reported in table 1, and variance surfaces (panel D) were calculated from STR
data in this study, Rootsi et al. unpublished data, Cinnioglu et al. (2004), Behar et al. (2003), Weale et al. (2002), Wilson et al. (2001), Helgason et al.
(2000), and Hurles et al. (1999). Shaded areas in panel D correspond to regions for which combined SNP and STR Y chromosomal data are not
available.
Table 2
Correlations of Major Y Chromosome Haplogroup Frequencies and Variances with Geography
Spearmans r (Frequency)
Haplogroup
I1b* (xM26)
I1b* (xM26) (without KA and MR)a
I1a
I1a (without KA and MR)
R1a
R1a (without KA and MR)
R1b
R1b (without KA and MR)
E3b1
E3b1 (without KA and MR)
J2e1
J2e1 (without KA and MR)
a
*
**
Spearmans r (Variance)
Latitude
Longitude
Latitude
Longitude
207
202
28
21
104
98
63
38
131
62
26
6
0.077
0.464
0.491
0.584
0.865*
0.743*
0.175
0.364
0.651**
0.597**
0.148
0.042
0.084
0.327
0.249
0.299
0.480
0.159
0.238
0.373
0.501
0.360
0.304
0.806
0.385
0.455
0.374
0.457
0.385
0.491
0.118
0.103
0.706**
0.676**
0.949**
0.949**
0.280
0.345
0.244
0.203
0.238
0.191
0.209
0.079
0.572
0.511
0.949**
0.949**
FIG. 7.J2e frequency and variance surfaces in SEE (panels A and B) were generated from the data in this study. J2e frequency surfaces in Europe,
northern Africa, and Asia Minor (panel C) were generated from the data reported in table 1, and variance surfaces (panel D) were generated from STR data
in this study and Semino et al. (2004).
in a substantial admixture of them with the substratum populations, inhabiting East Europe, among whom this
largely northern Eurasian haplogroup was and still is
widely spread.
Acknowledgments
We are grateful to all the donors for their kind participation in this study. Special thanks go to Toomas Kivisild
for friendly guidance and helpful comments for this manuscript. We wish to express our gratitude to two anonymous
reviewers for their helpful suggestions. This research was
supported by the Ministry of Science, Education and Sports
of the Republic of Croatia grant for project 0196005
(to P.R.), Estonian basic research grant 514 (to R.V.),
European Commission Directorate General Research
grant ICA1CT20070006 (to R.V.), and Estonian Science
Foundation grant number 6040 to Kristiina Tambets.
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