UDK 902(4/5)''633/634":577-2
Documenta PraehistoricaXXXIII (2006)
The role of Southeastern Europe in origins
and diffusion of major paternal lineages
Marijana Peričić, Lovorka Barać Lauc, Irena Martinović Klarić, Petra Rajić Šikanjić,
Branka Janićijević, Pavao Rudan
Institute for Anthropological Research, Zagreb, Croatia
mpericic@inantro.hr, lovorka@inantro.hr, irena@inantro.hr, petra@inantro.hr
branka@inantro.hr, pavao.rudan@inantro.hr
ABSTRACT - The aim of this study is to explore the existing data based on high-resolution phylogene-
tic studies of Y chromosome variation in populations from Southeastern Europe and elsewhere in
Eurasia in order to evaluate the role of the region in the process of the prehistoric colonization of
the European continent and the structuring of the modern paternal genetic pool. Even though the di-
stribution and estimated range expansions of major paternal lineages in Southeastern Europe are
consistent with the typical European Y chromosome gene pool, the specific role of this region in the
process of structuring the European paternal genetic landscape is evident in prehistoric episodes of
significant gene flow that diffused from or into the region.
IZVLEČEK - Cilj te študije je preučiti obstoječe podatke, ki so osnovani na visoko resolucijskih filoge-
netskih študijah variacije kromosoma Y v populacijah jugovzhodne Evrope in v drugih delih Evrazi-
je, z namenom, da ocenimo vlogo regije v procesu prazgodovinske kolonizacije evropskega kontinen-
ta ter pri strukturiranju modernega moškega genskega sklada. Čeprav sta distribucija in predviden
obseg širitve glavnih moških dednih linij v jugovzhodni Evropi skladna s tipičnim Evropskim gen-
skim skladom kromosoma Y, se posebna vloga te regije kaže v procesu strukturiranja evropskega
moškega dednega genetskega zemljevida, povezanega z dogodki v prazgodovini in genskim pretokom
v regijo in iz regije.
KEY WORDS - Human Y chromosome; phylogenetic analysis; Southeastern Europe
Introduction
The human Y chromosome defines male sex through
the action of the sex determining region (SRY). It is
an atypical segment of the human genome, since it is
haploid in most of its length, escapes recombination
with the X chromosome, and undergoes uniparental
transmission. These properties make the Y chromo-
some sequence a valuable tool for the purposes of
human history reconstruction and studies focused on
the dispersal of anatomically modern humans. The
non-recombining region of the Y (NRY) is inherited
as a single locus that changes exclusively via muta-
tions accumulating over time, thus allowing the pre-
servation of a relatively simple record of genetic hi-
story in comparison to nuclear DNA (autosomes).
There has been an interest in studying paternal ge-
netic history since the mid-80s (e.g. Casanova et al.
1985; Hammer 1994; Underbill et al. 2000). A con-
stantly growing number of evolutionary informative
polymorphisms provide a deeper resolution of hu-
man paternal history and evolution. Currently, there
are more than 300 known SNPs (single nucleotide
polymorphisms) and small indels (YCC 2002; Jobling
and Tyler-Smith 2003). In evolutionary genetics ter-
minology, the set of alleles at different biallelic loci
along the chromosome is called a haplogroup.
Assuming a 1:1 sex ratio, the effective population
size of the Y chromosome in a population would be
about one-quarter of that of any au-
tosome. Consequently, a genetic dif-
ference depicted by Y chromosomes,
in comparison to autosomes, is more
susceptible to the effects of random
genetic drift that accelerates geogra-
phic clustering and differentiation
between different (especially small)
populations. The general structure
of paternal genealogies is compati-
ble and indicative of the common
origin of all non-African contempo-
rary populations from a small subset
of Africans. Despite disagreement
about the time to the most recent
common ancestor (TMRCA) of the Y
chromosome, its phylogeny roots in
Africa around 100 KYA (e.g. Hammer et al. 1998;
Underbill et al. 2001; Underbill 2003).
The first extensive studies of European Y chromo-
some dispersal by Semino et al. (2000) and Rosser
et al. (2000) showed clinal patterns for the most fre-
quent European haplogroups. Moreover, Semino et
al. (2000) grouped more than 95% of European Y
chromosomes into 10 phylogenetically distinct hap-
logroups, of which 70-80% of the Y chromosome
gene pool was represented by R1a, R1b, I and N3,
and the remaining 20% by J2, E3b, and G.
Palaeolithic haplogroups
Haplogroup I is the only autochthonous European
haplogroup assumed to have arisen in an Epi-Gravet-
tian group among the descendants of people who ar-
rived in Europe from the Near East around 25 KYA
Fig. 2. R1a frequency distribution in Europe, Northern Africa and
Asia Minor (panel a) as well as in Southeastern Europe (panel b).
Frequency distributions surfaces are taken from Peričić et al.
(2005). R1a frequency data for different Eurasian populations
were generated from literature, as listed in Table 1 in Peričić et
al. (2005).
Fig. 1. IIb* frequency distribution in Europe, Northern Africa and
Asia Minor (panel a) as well as in Southeastern Europe (panel b).
Frequency distributions surfaces are taken from Peričić et al.
(2005). I1b* frequency data for different Eurasian populations
were generated from literature, as listed in Table 1 in Peričić et al.
(2005).
(Semino et al. 2000). This haplogroup is almost en-
tirely restricted to the European continent, where it
shows frequency peaks in two areas - Scandinavia
and Southeastern Europe (Semino et al. 2000). Fur-
ther phylogenetic subdivision revealed subclades
I1a, I1b*, I1b2, and I1c (Rootsi et al. 2004). The geo-
graphical distribution of I1a (the highest frequencies
in Northern Europe among Norwegians, Swedes and
Saami) is considered to be a result of the recoloni-
zation of Europe after the LGM from the Francocan-
tabrain refugial area (Rootsi et al. 2004). The origin
of the less frequent I1c, that covers a wide range of
Europe and peaks in northwest coastal Europe, is in
concordance with I1a (Rootsi et al. 2004). A com-
pletely different distribution pattern is observed in
IIb* Y chromosomes, the most frequent haplogroup
I clade in Eastern Europe and on the Balkan Penin-
sula. I1b* reaches maximum frequencies in South-
eastern Europe in Bosnia and Herzegovina (Fig. 1).
Our results indicate that the homo-
genous distribution of elevated I1b*
frequency among different popula-
tions in Southeastern Europe could
support the hypothesis of their hav-
ing a common paternal history shared
over a long period of time (Peričić
et al. 2005). Rootsi et al. (2004) es-
timated that IIb* diverged from I*
at 10.7+4.8 KYA, possibly in relation
to the post Younger Dryas (YD) cli-
mate amelioration in Europe, and
that I1b* expansion occurred around
the early Holocene at 7.6+2.7 KYA.
Our coalescent estimate of I1b* (Pe-
ričić et al. 2005) is substantially ol-
der (11.1+4.8 KYA). This finding sug-
gests that the I1b* lineages might
the current level of resolution it is
not possible to determine which of
three potential episodes of gene flow
might have influenced the estimated
age in Southeastern Europe: early
post-LGM recolonizations from the
direction of the Ukrainian refugium,
migrations from the northern Pontic
steppe in the period between 3000
to 1000 BC, or Slavic migrations be-
tween the 5th and 7th centuries AD.
Fig. 3. R1b frequency distribution in Europe, Northern Africa and
Asia Minor (panel a) as well as in Southeastern Europe (panel b).
Frequency distributions surfaces are taken from Pericic et al.
(2005). R1b frequency data for different Eurasian populations
were generated from literature, as listed in Table 1 in Pericic et al.
(2005).
have expanded from Southeastern to Central, Eastern
and Southern Europe in a period not earlier than
the YD to Holocene transition and not later than the
early Neolithic (Peričić et al. 2005). Although not
yet supported by archaeological evidence, the I1b*
spread in Europe suggests that Southeastern Europe
could have served as an LGM refugium, as previous-
ly suggested by Semino et al. (2000) and Barac et al.
(2003). This scenario could be indirectly supported
by the recolonization of Northern Europe from the
direction of Southeastern Europe by at least two spe-
cies - the brown bear Ursus arctos (Taberlet and
Bouvent 1994) and the European hedgehog Erina-
ceus europeus (Hewitt 2000).
Another widespread haplogroup in Europe, R1a, is
characteristic of Eastern European populations (Fig.
2a). The age of this haplogroup has been approxima-
ted 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. Present
R1a distribution in Europe shows an
increasing west-east frequency gra-
dient, with the highest frequencies
among Finno-Ugric and Slavic spea-
kers (Fig. 2a). R1a frequency shows
a decrease in the north-south direc-
tion in Southeastern Europe (Fig.
2b), where its age is estimated at
15.8 ± 2.1 KYA (Peričić et al. 2005).
This estimate is consistent with the
R1a deep Palaeolithic time depth
previously suggested by Semino et
al. (2000) and Wells et al. (2001). At
Its sister clade, haplogroup R1b, was
introduced by or arose in an Auri-
gnacian group who entered Europe
and diffused from east to west about
40 to 35 KYA (Semino et al. 2000).
R1b shows a frequency peak in West-
ern Europe and a decrease in Eastern and Southern
Europe (Fig. 3a). Even though R1b frequency decline
continues from Western to Southeastern and South-
ern Europe, two intermediate local peaks are evident
in Southeastern Europe (Fig. 3b). According to our
data, in Southeastern Europe the coalescent estimate
of R1b (11.6 ± 1.4 KYA) closely matches the estimate
for the I1b* lineages, pointing to the Younger Dryas
to Holocene transition as a possible expansion period
of these two major Y chromosome lineages (Peričić
et al. 2005).
Neolithic haplogroups
Approximately 20% of European Y chromosomes be-
long to haplogroups E3b, J2 and G that, due to their
decreasing frequency gradients from the Near East
to Europe, have been traditionally considered to re-
Fig. 4. E3b1 frequency distribution in Europe, Northern Africa and
Asia Minor (panel a) as well as in Southeastern Europe (panel b).
Frequency distributions surfaces are taken from Pericic et al.
(2005). E3b1 frequency data for different Eurasian populations
were generated from literature, as listed in Table 1 in Pericic et al.
(2005).
present the male contribution of a
demic diffusion of farmers (e.g. Se-
mino et al. 2000; Semino et al.
2004; Cruciani et al. 2004). E3b1
shows a frequency peak in Southern
and Southeastern Europe (Fig. 4a).
In fact, E3b1 shows a rather continu-
ous frequency decline in Southeast-
ern Europe (Fig. 4a). Populations of
the Adriatic-Dinaric complex are di-
stinguished from neighboring popu-
lations of the Vardar-Morava-Danube
river system by a lower frequency of
E3b1 (Fig. 4b), possibly due to its dif-
ferent dispersal modes in two proxi-
mate geographic regions. Moreover,
the Vardar-Morava-Danube river sy-
stem could have been one of major
routes for E3b1 expansion from South and South-
eastern to continental Europe, as evidenced in the
archeological record (e.g. Tringham 2000). The es-
timated age of this haplogroup of 7.3 ± 2.8 KYA in
Southeastern Europe accords with the time of ex-
pansion of the Neolithic in Europe (Cruciani et al.
2004; Semino et al. 2004).
Haplogroup J is subdivided into two major clades,
J1-M267 and J2-M172 (Cinnioglu et al. 2004). J2-
M172 is more frequent in Europe (Semino et al.
2004). In Southeastern Europe the most frequent is
haplogroup J2e, which comprises 5% of all chromo-
somes (Peričić et al. 2005), while haplogroup J2,
the main J2 cluster among Greeks and Italians (Di
Giacomo et al. 2004), is present at a frequency of
less than 1%. The estimated age of the haplogroup
J2e in Southeastern Europe (2.8+1.6 KYA), together
with its spatial distribution (two frequency peaks po-
sitioned in the Balkans and central Italy, Figs. 5a
and 5b), may be explained by the maritime spread
of J2e lineages from the southern Balkans towards
the Apennines later than is traditionally suggested
by the demic expansion model (Peričić et al. 2005).
Fig. 5. J2e frequency distribution in Europe, Northern Africa and
Asia Minor (panel a) as well as in Southeastern Europe (panel b).
Frequency distributions surfaces are taken from Peričić et al.
(2005). J2e frequency data for different Eurasian populations
were generated from literature, as listed in Table 1 in Peričić et al.
(2005).
Balkans, with subsequent R1a and I1b* gene flows
between Eastern and Southeastern Europe, and the
weaker extent of E3b1 dispersal out of Southern and
Southeastern Europe towards Eastern Europe than
towards Western (especially Mediterranean) Europe.
-ACKNOWLEDGEMENTS-
This research was supported by the Ministry of Sci-
ence, Education and Sports of the Republic of Croa-
tia grant for project 0196005 to P.R.
Concluding remarks
Even though the distribution and estimated range
expansions of major paternal lineages in Southeast-
ern Europe are consistent with the typical European
Y chromosome gene pool, the specific role of this re-
gion in the process of structuring the European pa-
ternal genetic landscape is evident in the following
prehistoric episodes of significant gene flow: the
post-LGM R1a expansion from Eastern to Western
Europe, the YD-Holocene I1b* diffusion out of the
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