UDK 902(4)''63i/634":577-2
Documenta PraehistoricaXXXIII (2006)
Y-chromosome haplogroup I
prehistoric gene flow in Europe
Siiri Rootsi
Estonian Biocentre and Tartu University, Estonia
sroots@ebc.ee
ABSTRACT - To investigate which aspects of contemporary human Y-chromosome variation in Europe
are characteristic of primary colonization, late-glacial expansions from refuge areas, Neolithic dis-
persals or more recent events in gene flow haplogroup I was analyzed. The analysis of Hg IY chro-
mosomes revealed several sub-clades with distinct geographic distributions. Sub-clade I1a accounts
for most of Hg I in Scandinavia, with a rapidly decreasing frequency towards the East European Plain
and the Atlantic fringe; but microsatellite diversity reveals that the Iberian Peninsula/Southern
France refugial area could be the source region of the early spread of both I1a and the less common
I1c. I1b* extends from the eastern Adriatic to Eastern Europe, and declines noticeably towards the
southern Balkans, and abruptly towards North Italy. This cladeprobably diffused after the Last Gla-
cial Maximum from a homeland in the Balkans or Eastern Europe. In contrast, I1b2 most probably
arose in southern France/Iberia, underwent a post-glacial expansion, and marked the human coloni-
zation of Sardinia about 9000 years ago.
IZVLEČEK - Da bi raziskali, kateri aspekti sodobne človeške variacije kromosoma Y v Evropi so zna-
čilni za primarno kolonizacijo, pozno glacialno širitev iz refugijev, neolitske širitve in bolj recentne
dogodke v genskem zapisu, smo analizirali haploskupine I. Analize kromosoma Y haploskupine I, so
pokazale sub-klade z jasnimi geografskimi porazdelitvami. Sub-klad I1a označuje Hg I v Skandina-
viji, s hitrim pojemanjem v smeri proti Vzhodnoevropski ravnici in obrobju Atlantika. Mikrosatelit-
ska raznolikost je pokazala, da je bil Iberijski polotok/južna Francija verjetni refugij in izvorno po-
dročje, iz katerega sta se razširila oba sub-klada I1a in manj pogosti I1c. I1b* se razteza od vzhod-
nega Jadrana do vzhodne Evrope in opazno pojema v smeri proti južnemu Balkanu ter strmo upa-
de v smeri proti severni Italiji. Ta klad se je verjetno razširil po zadnjem glacialnem maksimumu iz
domovine na Balkanu ali v vzhodni Evropi. I1b2 najverjetneje izhaja iz južne Francije/Iberije in
kaže post-glacialno širitev in človekovo kolonizacijo Sardinije pred okoli 9000 leti.
KEY WORDS - phylogeny of Y-chromosomal markers; haplogroup I sub-clades; late-glacial expansions;
Neolithic dispersals
Introduction
Although there is sound evidence that the majority
of present-day European genes descend from indige-
nous Palaeolithic ancestors, it is to be expected that
the pre-LGM landscape of the spread of genetic varia-
tion was profoundly re-shaped during and after the
LGM - Late Glacial Maximum (Richards et al. 2000;
Semino et al. 2000). The aim of this investigation
was to apply the phylogeographic approach to Y-chro-
mosomal haplogroup I, the only known Y-chromoso-
mal haplogroup that probably arose in Europe in Pa-
laeolithic times, and which is still common and wide-
spread there, whilst being virtually absent elsewhere.
The distribution of haplogroup I was intriguing, with
its two high frequency peaks in distant parts of Eu-
rope (the Balkan region and Scandinavia); and the
further large-scale I haplogroup study by Rootsi et
al. (2004) concentrated on achieving a better phylo-
genetic and phylogeographic resolution of this hap-
logroup, informative for the reconstruction of long-
distance gene flows in space and time.
Results and Discussion
It has been shown earlier that the high frequency of
hg I is characteristic of two distant and distinct re-
gions - around the Dinaric Alps (Semino et al. 2000;
Barać et al. 2003) and in Nordic populations of Scan-
dinavia (Semino et al. 2000; Passarino et al. 2002;
Tambets et al. 2004).
In a study by Rootsi et al. (2004), concentrating on
haplogroup I phylogeography and phylogeny, more
than seven thousand individuals from Europe and
the surrounding regions were assessed for the mar-
ker M170, which defines hg I.
1104 Y chromosomes from 48 European and 12 po-
pulations from surrounding regions which showed
the derived M170 C- allele were further genotyped
with a set of markers (M253, P37, M26 and M223)
that define distinct sub-clades of I, respectively I1a,
I1b, I1b2 and I1c.
Thanks to the new informative markers used, the
improved resolution of phylogeny of hg I enabled to
reveal distinct phylogeographical patterns of sub-
clades I1a, I1b and I1c, which jointly cover about
95% of hg I individuals. Sub-clade I1a is widely dis-
tributed in northern Europe, with its highest fre-
quencies in Scandinavia: in Norwegians, Swedes and
Saami, accounting for 88-100% of hg I individuals
in these populations and showing rapidly decreasing
frequency towards both the East European Plain and
the northwestern coastal areas of Europe. Combined
analysis of STR diversity and a relative portion of I1a
sub-clade among all I lineages suggests that France
or possibly more precisely - the Franco-cantabrian
refugial area - could have been the source region of
the spread of I1a during the post-LGM re-colonization
of Europe. The same may apply to the spread of the
less common sub-clade I1c. This scenario is also sup-
ported by a high positive correlation (0.75) between
the geographic distributions of I1a and I1c. I1c co-
vers a wide range in Europe, with the highest fre-
quencies in north-west coastal Europe, and a lower
frequency elsewhere (Fig. 1).
A totally different distribution pattern can be seen
for I1b*, which is the most frequent haplogroup I
clade in Eastern Europe and the Balkans. It reaches
its highest frequencies in Croatian and Bosnian po-
pulations, encompassing almost 80-90% of hg I
there. When comparing frequencies in different re-
gions of Croatia (Barać et al. 2003), clear and signi-
ficant differences between the three southern islands
with higher frequency and the mainland and the
northerly island of Krk with lower frequency, be-
came apparent. More than half of Croatian hg I sam-
pled individuals - 126 out of 221 (57%) - share an
identical STR haplotype, which was named the Di-
naric Modal Haplotype. This haplotype was not pre-
sent in 102 hg 2 chromosomes (according to Job-
ling's nomenclature) as reported by Helgason et al.
(2000); the most frequent among them was labeled
as the Nordic Haplotype (Barać et al. 2003).
The phylogenetic network of hg I STR haplotypes
points to characteristic haplotype patterns in diffe-
rent sub-clades, which allows us to identify possible
founder haplotypes for the different sub-clades, and
calculate their possible expansion times according to
the method described in Zhivotovsky et al. (2004).
The estimates for possible expansion times suggest
that the expansion phase of I1a and I1b occurred
around the early Holocene and only the less frequent
sub-clade I1c shows an earlier age for its STR varia-
tion, suggesting that the corresponding mutation
arose earlier.
High frequency combined with the high diversity of
sub-clade I1b in the Croatian population (both main-
land and island populations) suggests that during
the LGM there might have been a refugium nearby.
According to our knowledge, placing of the western
Balkans on the list of human refugia during the LGM
has not been confirmed so far unambigously by ar-
chaeologists. However, the northern part of the Ad-
riatic Sea, including the Dalmatian Islands, was at
that time a part of dry land, being covered by water
only much later, at the boundary of Holocene (refe-
rences within Barać et al. 2003). Therefore, one may
speculate that the wealth of the traces of human
occupancy of the area lies submerged. Nevertheless,
it is justified to suggest that the present-day western
Adriatic was the reservoir of M170 (I1b) lineages, as
well as a starting point for the spread of these linea-
ges during the post-glacial re-colonization of Europe.
Meanwhile, the star-like pattern of both, I1a and I1b*
STR haplotypes, might be explained by simultaneous
re-colonization of Europe from different refugia.
I1b* sub-clade dissipates very rapidly west of the
Balkans, being virtually absent among Italian, French
and Swiss populations, but extending eastwards at
Fig. 1. A - Median-joining net-
work of combined haplotypes
of six STR loci (DYS19, 388,
390,391,392,393) in 25 popu-
lations/584 individuals (Nor-
wegians, Estonians, Saami,
Swedes, Hungarians, Czechs
and Slovaks, Poles, Ukraini-
ans, Croats, Bosnians, Mace-
donians, Albanians, Greeks,
Moldavians, Gagauz, Turks,
Italians, Sardinians, French,
Dutch, Andalusians, Bearnais,
Basques and Swiss). Only ha-
plotypes with frequency >1
were used. Nodes indicate ha-
plotypes with sizes proportio-
nal to their frequency (smal-
lest node corresponds to 1 in-
dividual - only in case of over-
lap between subclades, other-
wise haplotypes with frequency >1 are presented). Haplotypes of different sub-clades are indicated with
different patterns.
The most frequent haplotype of I1a sub-clade (14-14-23-10-11-13) corresponds to the earlier named Nor-
dic Haplotype and the dominant in I1b* haplotype is the so-called Dinaric Modal Haplotype (16-13-24-11-
11-13) according to Barac et al. (2003). The possible founder lineage for the third sub-clade, I1c (15-13-
23-10-12-14), was revealed in Rootsi et al. (2004).
B - Median joining network of I1b(xI1b2) and I1b2 lineges based on seven STRs (DYS 19, 388, 390, 391,
392,393 and YCAIIa,b). I1b* (YCAIIa,b mostly 21,21 alleles) andI1b2 (YCAIIa,b; 21,10 alleles) lineages
are clearly separated from each other by the difference inYCAIIa,b haplotypes. They differ by 10 repeats
in YCAIIb allele length that is probably a result of one single mutational event rather than step-by step de-
letions - in particular because no intermediate repeat variants have been detected.
notable frequencies, mostly in the north Balkans and
among Slavic-speaking populations, including more
eastern Ukrainians. This finding suggests that I1b*
may have expanded from a glacial refuge area, which
may have been located in the Balkans. As indicated
above, there is only limited archaeological evidence
for such a refugium in this region at present. Never-
theless, data on the re-occupation of northern Eu-
rope from the Balkan region by mammals such as
the brown bear Ursus arctos (Taberlet and Bouvet
1994) and European hedgehog Erinaceus europeus
(Hewitt 2000), birds such as the European great tit
Parus major (Kvist et al. 1999; Kvist 2000) and in-
sects such as the meadow grasshopper Chortippus
parallelus (Hewitt 2000), supports its existence in-
directly.
It seems somewhat less likely though not impossible
that I1b* was preserved during the LGM in an area
of much better documented Periglacial refugium in
the present-day Ukraine. It appears less likely be-
cause (a) not only its frequency, but also diversity is
higher in the Adriatic region; (b) a branch of I1b* -
I1b2-M26 - has a clearly western pattern of distri-
bution, being totally absent in Ukrainians.
On the other hand, a clearly visible difference that
can be observed in the distribution patterns of I1b*
and an outshoot of it - I1b2 - suggests that their se-
paration may have occurred even before the LGM,
whereas isolation, genetic drift during the LGM, re-
colonization and an unknown number of putative
more recent demographic events created the pattern
that one observes among extant populations.
Meanwhile, the extremely high incidence of I1b2
among Sardinians (about 40%) can be explained by
the presence of carriers of I1b2 lineage among the
first inhabitants of the island early in Holocene and
by the influence of genetic drift thereafter.
Certain extent of similarity in distribution patterns
of some mtDNA haplogroups, in particular V (Tor-
roni et al. 1998; Torroni et al. 2001), with Y-chro-
mosomal hg I sub-branches has been suggested by
Rootsi et al. (2004). These findings show that distri-
bution patterns characteristic to Y-chromosomal ha-
plogroup I sub-clades are supported by parallel evi-
dence from other genetic markers and probably indi-
cate more general patterns in human past demogra-
phic movements.
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