Sami Lapps PDF

Am. J. Hum. Genet.
74:661–682, 2004
The Western and Eastern Roots of the Saami—the Story of Genetic

“Outliers” Told by Mitochondrial DNA and Y Chromosomes
Kristiina Tambets,1 Siiri Rootsi,1 Toomas Kivisild,1 Hela Help,1 Piia Serk,1 Eva-Liis Loogväli,1
Helle-Viivi Tolk,1 Maere Reidla,1 Ene Metspalu,1 Liana Pliss,1,2 Oleg Balanovsky,1,4
Andrey Pshenichnov,1,4 Elena Balanovska,4 Marina Gubina,1,5 Sergey Zhadanov,1,5
Ludmila Osipova,5 Larisa Damba,1,5 Mikhail Voevoda,5 Ildus Kutuev,1,6 Marina Bermisheva,1,6
Elza Khusnutdinova,6 Vladislava Gusar,1,7 Elena Grechanina,7 Jüri Parik,1 Erwan Pennarun,1
Christelle Richard,8 Andre Chaventre,8 Jean-Paul Moisan,8 Lovorka Barać,1,9 Marijana Peričić,1,9
Pavao Rudan,9 Rifat Terzić,10 Ilia Mikerezi,11 Astrida Krumina,3 Viesturs Baumanis,2
Slawomir Koziel,12 Olga Rickards,13 Gian Franco De Stefano,13 Nicholas Anagnou,14,16
Kalliopi I. Pappa,14,16 Emmanuel Michalodimitrakis,15 Vladimir Ferák,17 Sandor Füredi,18
Radovan Komel,19 Lars Beckman,20 and Richard Villems1
1
Department of Evolutionary Biology, Institute of Molecular and Cell Biology, University of Tartu and Estonian Biocentre, Tartu, Estonia;
2
Biomedical Research and Study Centre and 3P. Stradins University, Riga, Latvia; 4Research Centre for Medical Genetics, Russian Academy of
Medical Sciences, Moscow; 5Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk; 6Institute of
Biochemistry and Genetics, Ufa Research Center, Russian Academy of Sciences, Ufa; 7Kharkov Clinical Genetic and Prenatal Diagnostics
Center, Kharkov, Ukraine; 8Laboratoire d’Etude du Polymorphisme de l’ADN, Faculté de Médecine, Nantes, France; 9Institute for
Anthropological Research, Zagreb; 10Department of Biology and Genetics, Medical School Tuzla, Tuzla, Bosnia and Herzegovina;
11
Department of Biology, Faculty of Natural Sciences, Tirana University, Tirana; 12Institute of Anthropology, Wroclaw, Poland; 13Dipartimento
di Biologia, Università “Tor Vergata,” Rome; 14Institute of Molecular Biology and Biotechnology, Heraklion, and 15Department of Forensic
Sciences and Toxicology, University of Crete School of Medicine, Heraklion, Greece; 16Department of Basic Sciences, University of Athens
School of Medicine, Athens; 17Department of Molecular Genetics, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia;
18
Institute for Forensic Sciences, Budapest; 19Medical Center for Molecular Biology, University of Ljubljana, Ljubljana, Slovenia; and 20Gotland
University, Visby, Sweden
The Saami are regarded as extreme genetic outliers among European populations. In this study, a high-resolution
phylogenetic analysis of Saami genetic heritage was undertaken in a comprehensive context, through use of ma-
ternally inherited mitochondrial DNA (mtDNA) and paternally inherited Y-chromosomal variation. DNA variants
present in the Saami were compared with those found in Europe and Siberia, through use of both new and previously
published data from 445 Saami and 17,096 western Eurasian and Siberian mtDNA samples, as well as 127 Saami
and 2,840 western Eurasian and Siberian Y-chromosome samples. It was shown that the “Saami motif” variant of
mtDNA haplogroup U5b is present in a large area outside Scandinavia. A detailed phylogeographic analysis of
one of the predominant Saami mtDNA haplogroups, U5b1b, which also includes the lineages of the “Saami motif,”
was undertaken in 31 populations. The results indicate that the origin of U5b1b, as for the other predominant
Saami haplogroup, V, is most likely in western, rather than eastern, Europe. Furthermore, an additional haplogroup
(H1) spread among the Saami was virtually absent in 781 Samoyed and Ob-Ugric Siberians but was present in
western and central European populations. The Y-chromosomal variety in the Saami is also consistent with their
European ancestry. It suggests that the large genetic separation of the Saami from other Europeans is best explained
by assuming that the Saami are descendants of a narrow, distinctive subset of Europeans. In particular, no evidence
of a significant directional gene flow from extant aboriginal Siberian populations into the haploid gene pools of
the Saami was found.
Introduction distances between individual populations. Classic ge-

netic markers have revealed a few clearly pronounced
Although not homogeneous, the European genetic land- outliers, like the Sardinians, the Greeks, the Basques,
scape has been characterized by relatively short genetic the Finns and, in particular, the Saami (Cavalli-Sforza
Received November 24, 2003; accepted for publication January 16,
and Piazza 1993; Cavalli-Sforza et al. 1994). The Saami
2004; electronically published March 11, 2004. (Lapps) are aboriginal inhabitants of Fennoscandia. The
Address for correspondence and reprints: Dr. Kristiina Tambets, De- Saami language belongs to the Finno-Ugric branch of
partment of Evolutionary Biology, University of Tartu, Estonian Bio- the Uralic language family and can be divided into 10
centre, Riia 23, Tartu, 51010, Estonia. E-mail: ktambets@ebc.ee
䉷 2004 by The American Society of Human Genetics. All rights reserved.
dialects (Sammallahti 1998). The closest linguistic neigh-
0002-9297/2004/7404-0007$15.00 bors of the Saami are the Finns, the Karelians, and the
661
662 Am. J. Hum. Genet. 74:661–682, 2004
Estonians. At present, ∼60,000 Saami live in the north- and the variations in the mtDNA coding region of Eu-
ern regions of Norway, Sweden, and Finland, as well as ropean populations have been exploited to generate a
in the Russian Kola Peninsula (Haetta 1996). Soon after common phylogenetic nomenclature for mtDNA vari-
the beginning of the retreat of the ice sheets covering ants in Europe (Torroni et al. 1996; Macaulay et al.
the area, in the 8th–10th millennia before present (BP), 1999). Classification of the Saami mtDNA lineages re-
populations of hunters and fishermen, the producers of vealed that the absolute majority of these are clustered
the Mesolithic Komsa and Fosna-Hensbacka cultures, in a subset of the European mtDNA pool (Torroni et
inhabited the coastal region of Scandinavia, extending al. 1998; Villems et al. 1998), where two haplogroups—
well into Finland and to the Kola Peninsula (Kozlowski V and U—cover ∼80% of the variability of this subset
and Bandi 1984; Nygaard 1989; Sumkin 1990). The (Torroni et al. 1998; Tambets et al. 2000).
linguistic affiliation of these pioneer settlers of the north In contrast to the predominance of European mtDNA
is largely unknown, but it has been suggested that they haplogroups observed among the Saami, nearly half of
are the descendants of the Ahrensburgian population, their Y chromosomes share a TatC allele (haplogroup
which migrated toward the north from western Europe, N3, according to the nomenclature of the Y Chromosome
along the Atlantic coast of Norway. It has been proposed Consortium [YCC 2002]) with most Finno-Ugric and
that they might have been the ancestors of the present- Siberian populations. This variant is found at high fre-
day Saami (e.g., Sumkin 1990). Another presumably im- quencies among Siberian populations, such as the Yakuts
portant component in the postglacial recolonization of and the Buryats, but is virtually absent in western and
northern Fennoscandia came from the east, via Karelia Mediterranean Europe; even among the Norwegians and
and Finland. It has been associated with the movement the Swedes, populations that have historically lived in
of Mesolithic populations, carriers of post-Swiderian close proximity to the Saami, it is found at frequencies
cultures, to the north. Starting in the Neolithic period, of only 4%–8% (Zerjal et al. 2001; Passarino et al.
the northern population came into contact with tribes 2002). High frequencies of the TatC allele have also been
of territories lying to the south (e.g., Sumkin 1990). observed in Baltic (30%–40%) and Volga-Finnic–speak-
Thus, according to archeological data, the present-day ing populations (20%–50%) (Zerjal et al. 1997; Rootsi
Saami population might have been shaped in different et al. 2000; Rosser et al. 2000; Semino et al. 2000; Lai-
times both by the eastern and western influences.
tinen et al. 2002). These findings have been interpreted
Analyses of classic chromosomal marker variation
according to the classic view that a substantial element
have demonstrated that the genetic distances between
of the Saami (and other European Finno-Ugric–speaking
the Saami and other European populations are signifi-
populations) genetic lineages originated in a recent mi-
cantly larger than between any other pair of European
gration from Asia (Zerjal et al. 1997, 2001).
populations (Cavalli-Sforza et al. 1994). This distinctive
Another half of the Saami paternal lineages have pri-
pattern has suggested to some that the genetic com-
marily mutations M170, SRY-1532, or M173 (Semino
position of the Saami population arose from extensive
et al. 2000; Raitio et al. 2001; Wells et al. 2001). Ac-
admixture between Caucasoid and Mongoloid popu-
cordingly, they are identified as haplogroups I, R1a, and
lations. Estimates of the relative contribution of each
have varied from an equal input to ∼80% Caucasoid R1b (YCC 2002). Y chromosomes possessing those mu-
and 20% Mongoloid genes (Guglielmino et al. 1990; tations are widely spread in European populations (Ros-
Cavalli-Sforza et al. 1994, pp 272–273). However, not ser et al. 2000; Semino et al. 2000). Whereas SRY-1532
all classic genetic studies support an idea of an extensive and M173 are present at moderate frequencies in some
Caucasoid-Mongoloid admixture in the Saami genetic Siberian populations as well, M170 Y chromosomes are
background (e.g., Beckman et al. 1988, 1993). very rare there (Wells et al. 2001; Karafet et al. 2002).
Similarly, studies of mtDNA have identified large ge- Here, we first analyze mtDNA variation in the Swed-
netic distances between the Saami and other Europeans, ish Saami and improve the resolution level of their Y-
including the Finns (Sajantila and Pääbo 1995; Sajantila chromosomal haplotypes. Second, we examine the hy-
et al. 1995). Likewise, Lahermo et al. (1996) found no pothetical descent of the Saami gene pool from Siberian
overlap between Saami and the remaining European ancestors. We exploit extensive data on mtDNA and Y-
mtDNA patterns and concluded that the Saami and the chromosome variation in Eurasia, in particular among
Finns must have different genetic histories. One alter- Uralic-, Indo-European–, and Altaic-speaking popula-
native hypothesis to explain the presence of genetic dif- tions in eastern Europe and western Siberia. Finally, we
ferences and language similarities in the Finns and the refine the phylogenetic topology of a frequent Saami
Saami involves a language shift by the Finns from Indo- mtDNA haplogroup, U5b, to identify the founder hap-
European to Finno-Ugric (Sajantila and Pääbo 1995). lotypes. We draw conclusions about the possible origin
The combined sequence information from the first of mtDNA and NRY haplotypes present in the Saami
hypervariable segment (HVS-I) in the D-loop of mtDNA gene pool.
Tambets et al.: mtDNA and NRY Variation of the Saami 663
Subjects and Methods Karafet et al. 2002). The YAP and 12f2 polymorphisms
were identified following the procedures of Hammer and
Population Samples Horai (1995) and Casanova et al. (1985), respectively.
Furthermore, 35 Swedish Saami DNA samples that have
We analyzed mtDNA sequences from 17,541 Eurasian previously been analyzed for Y-chromosomal variation
individuals sampled from 65 different Eurasian popu- by Rosser et al. (2000) were also typed in the pres-
lations (table 1). These data consist of previously pub- ent study for the biallelic markers M89, M52, M130
lished sequences (n p 9,154) and new sequences an- (RSP4Y), M170, M173, M178, M201, and M269 (YCC
alyzed in this study (n p 8,387). Comparisons of dif- 2002).
ferent Saami subpopulations are presented separately in
table 2. Y-chromosomal markers were also analyzed Sequencing
from 32 different populations. Data from 1,598 of a
total of 2,967 individuals reported in table 3 were taken PCR-amplified products were purified using shrimp al-
from published sources, whereas the remaining 1,369 kaline phosphatase and exonuclease treatment follow-
DNA samples were extracted and analyzed in the present ing Kaessmann (1999). These were sequenced using the
study. Further details about the populations other than DYEnamic ET terminator cycle sequencing kit (Amer-
the Saami will be published elsewhere. Blood samples sham Pharmacia Biotech) on an ABI 377 DNA Sequencer.
were collected from healthy unrelated individuals after Sequences were aligned and analyzed using the Genetics
obtaining informed consent. DNA was extracted using Computer Group Wisconsin Package.
the phenol-chloroform method, as used by Sambrook
Data Analysis
(1989).
Principal-component (PC) analysis was undertaken
mtDNA Analysis using the POPSTR program, kindly provided by H. Har-
pending (see details described by Richards et al. [2002]).
HVS-I was sequenced between nucleotide positions Only those haplogroups that had a noticeable impact
(nps) 16024 and 16383 of the revised Cambridge Ref- on the scatterplot were used for the analysis (the sum
erence Sequence (Andrews et al. 1999) in 73 Swedish of the absolute values for both coordinates of each allele
Saami and 8,314 other mtDNA samples. RFLP analysis was 10.2 [M, V, U5, H, A, J, and U4 for mtDNA and
of diagnostic mtDNA positions was performed, and Q, N2, I, R1b, R1a, and N3 for the Y chromosome]).
mtDNA haplogroups were assigned to each sample by Bayesian 95% credible regions (CRs) for haplogroup
use of published criteria (Torroni et al. 1992, 1994, frequencies were calculated with the computer program
1996; Richards et al. 1998; Macaulay et al. 1999; Schurr SAMPLING, kindly provided by V. Macaulay. The di-
et al. 1999; Finnilä et al. 2000, 2001; Herrnstad et al. versity of mtDNA haplotypes was estimated as by Nei
2002; Kivisild et al. 2002). In addition, all U5b genomes (1987).
(n p 160) from 31 populations were typed by sequenc- Phylogenetic networks of mtDNA HVS-I haplotypes
ing for the np 5656 ArG mutation that differentiates were constructed using the program Network 3.1.1.1
between individuals belonging to haplogroups U5b* and (Fluxus Engineering Web site). Different weights were
U5b1. All identified U5b1 individuals (5656G) were fur- assigned to substitutions, as in the study by Richards et
ther sequenced to assess the variation at nps 7385 (A or al. (1998). Coalescence-age calculations and SDs were
G) and 10927 (T or C). A summary of these data is estimated following the formulae of Forster et al. (1996)
given in table 4. and Saillard et al. (2000).
Y-Chromosome Analysis Results

Sixteen Y-chromosomal biallelic markers were as-
sayed in 1,369 DNA samples. Nomenclature of haplo- Saami mtDNA Haplogroup Frequencies
groups is as defined by the YCC (2002). Markers were The mtDNA haplogroup frequencies were estimated in
analyzed as follows. The polymorphic SNPs underlying Swedish Saami (n p 73) and in 8,314 samples from dif-
markers M52, M130 (RSP4Y), M170, M173, M178, ferent European and Siberian populations, through use of
M201 (Underhill et al. 2001), M269 (Cruciani et al. HVS-I sequencing and RFLP analysis. The combined
2002), and M242 (Seielstad et al. 2003) were assayed D-loop and coding region information also enabled us
after PCR amplification and sequencing. Markers M9, to infer the haplogroup affiliations from previously pub-
Tat, SRY-1532, 92R7, M89, and P43 were assayed lished data for the Finnish, Swedish, and Norwegian
through restriction digest analysis by use of published Saami (Sajantila et al. 1995; Dupuy and Olaisen 1996;
protocols (Mathias et al. 1994; Whitfield et al. 1995; Delghandi et al. 1998) that has been scored for the pres-
Zerjal et al. 1997; Akey et al. 2001; Raitio et al. 2001; ence of the HVS-I polymorphisms (fig. 1; tables 1 and 2).
Table 1
Frequencies (%) of the Predominant mtDNA Haplogroups of the Saami among Other Eurasian Populations
FREQUENCY OFHAPLOGROUP
(%)
REGION AND LANGUAGE SAMPLE
POPULATIONa FAMILYb SIZE V U5b1b1c H1d D5e Z REFERENCE(S)
Scandinavia:
*Saami U-FU 445 41.6 47.6 2.5 3.1 1.3 Sajantila et al. 1995, corrected by Bandelt et al. 2001; Dupuy and Olaisen 1996;
Delghandi et al. 1998; present study
*Swedes IE-G 503 3.2 .8 3.4 0 .4 Sajantila et al. 1996; present study
*Norwegians IE-G 641 3.4 1.2 1.9 0 .6 Dupuy and Olaisen 1996; Opdal et al. 1998; Helgason et al. 2001; Passarino et
al. 2002
Northern Europe:
*Karelians U-FU 83 6.0 6.0 6.0 1.2 0 Sajantila et al. 1995
*Finns U-FU 581 6.4 6.7 3.6 .2 1.5 Pult et al. 1994; Sajantila et al. 1995; Lahermo et al. 1996; Kittles et al. 1999;
Meinilä et al. 2001
*Estonians U-FU 545 3.3 .7 4.8 .2 0 Sajantila et al. 1995, 1996; present study
664
Latvians IE-B 299 3.0 0 1.0 0 0 Present study

Lithuanians IE-B 45 2.2 2.2 2.2 0 0 Present study
North-Russians IE-S 134 0 3.0 2.2 5.2 0 Present study
Eastern Europe:
*Russians IE-S 761 3.8 1.2 1.2 0 .3 Orekhov et al. 1999; Malyarchuk et al. 2001, 2002; present study
Ukrainians IE-S 686 4.8 .6 1.5 0 .1 Malyarchuk et al. 2001; present study
*Poles IE-S 583 4.5g .7 1.0 0 0 Richards et al. 2000; Malyarchuk et al. 2002; present study
*Northwestern Europe IE-C/G 1,851 (1,547)f 2.8g 0 1.6 0 0 Piercy et al. 1993; Richards et al. 1996, 2000; Helgason et al. 2000, 2001
Volga-Ural region:
*Maris U-FU 147 10.2 .7 .7 0 2.7 Sajantila et al. 1995; Bermisheva et al. 2002; present study
*Mordvin U-FU 111 3.6 2.7 0 0 0 Sajantila et al. 1995; Bermisheva et al. 2002
Komis U-FU 340 .6 1.8 2.1 1.8 1.8 Bermisheva et al. 2002; present study
Udmurts U-FU 182 .5 0 8.2 0 7.1 Bermisheva et al. 2002; present study
Chuvashes A-T 89 5.6 1.1 2.2 0 0 Richards et al. 2000; Bermisheva et al. 2002
Tatars A-T 176 4.5 0 0 0 0 Bermisheva et al. 2002; present study
Bashkirs A-T 209 3.3 2.4 0 0 1.0 Bermisheva et al. 2002
Southern Europe:
*Italians IE-R 397 (240)f 1.7g 0 1.0 0 0 Francalacci et al. 1996; Richards et al. 2000; Mogentale-Profizi et al. 2001;
Tagliabracci et al. 2001; present study
Sardinians IE-R 115 (133)f 6.0g 0 .9 0 0 Richards et al. 2000; Cali et al. 2001
*Sicilians IE-R 732 (634)f 2.2g 0 .8 0 0 Di Rienzo and Wilson 1991; Richards et al. 2000; Cali et al. 2001; Forster et
al. 2002; present study
Cypriots IE 188 0 0 1.6 0 0 Present study
Greeks (mainland and Crete) IE 399 (414)f .7g 0 0 0 0 Richards et al. 2000; present study
Albanians IE 199 .5 0 0 0 0 Present study
Croats IE-S 440 2.7 .5 .5 0 0 Present study
Bosnians IE-S 395 3.3 .8 .8 0 .3 Malyarchuk et al. 2003; present study
Western Europe:
*French IE-R 577 3.1 .3 2.3 0 0 Rousselet and Mangin 1998; Danan et al. 1999; Richards et al. 2000; Cali et al.
2001; present study
*Spaniards IE-R 479 (293)f 2.0g 0 .4 0 0 Corte-Real et al. 1996; Salas et al. 1998; Crespillo et al. 2000
*Portugese IE-R 295 (54)f 3.7g 0 1.4 0 0 Corte-Real et al. 1996; Pereira et al. 2000
*Basques Isolate 106 (97)f 12.4g 0 0 0 0 Bertranpetit et al. 1995; Corte-Real et al. 1996
*Central Europe:
*Germans IE-G 582 4.3g 0 2.9 0 0 Richards et al. 1996; Hofmann et al. 1997; Baasner et al. 1998; Lutz et al.
1998; Pfeiffer et al. 1999
*Swiss IE-G 230 3.9 0 .9 0 0 Pult et al. 1994; Dimo-Simonin et al. 2000
Austrians IE-G 101 1.0 0 0 0 0 Parson et al. 1998
Hungarians U-FU 116 2.6 .9 1.7 0 0 Present study
Czechs IE-S 177 4.0 0 .6 0 0 Richards et al. 2000; present study
Slovaks IE-S 129 2.3 0 4.7 0 0 Present study
Slovenes IE-S 110 5.5 1.8 3.6 0 0 Present study
Caucasus IE, CA-N/S; A-M/T 1,383 .5 .4 .5 0 .7 Richards et al. 2000; present study
Siberia:
Khants U-FU 255 0 0 0 0 0 Present study
Mansis U-FU 138 .7 0 0 .7 0 Derbeneva et al. 2002b; present study
Nganasans U-SA 131 0 0 .8 0 2.3 Derbeneva et al. 2002a; present study
Nenets U-SA 137 0 0 0 0 0 Saillard et al. 2000; present study
Selkups U-SA 120 0 0 0 0 0 Present study
665
Kets Isolate 104 0 0 0 0 2.9 Derbeneva et al. 2002a; present study

Dolgans A-T 130 0 0 .8 0 1.5 Present study
*Yakuts A-T 395 0 .5 0 0 0 Fedorova et al. 2003; Pakendorf et al. 2003; Puzyrev et al. 2003
*Buryats A-M 126 0 0 0 0 1.6 Pakendorf et al. 2003
Evenks A-TN 105 0 0 0 0 1.0 Present study
Altaians A-T 339 0 0 0 .3 5.0 Present study
Total 17,541
a
Populations for which frequencies were deduced from published HVS-I sequences are indicated by an asterisk (*). Populations are divided into geographic regions; for northwestern
Europe (consists of Scots [n p 891], English and Welsh [n p 426], Irish [n p 101], and Icelanders [n p 433]) and for the Caucasus region (consists of Nogays [n p 183], Adygeis [n p
159], Abazins [n p 64], Kabardins [n p 66], Karachays [n p 106], Kumyks [n p 109], Kalmyks [n p 120], Georgians [n p 138], Southern Ossetians [n p 198], Armenians [n p 192],
and Azeris [n p 48]), only summary data are shown.
b
Language-family codes used for each population are as follows: U p Uralic (FU p Finno-Ugric; SA p Samoyedic); IE p Indo-European (B p Baltic; C p Celtic; G p Germanic; R
p Romance; S p Slavic); A p Altaic (M p Mongolic; T p Turkic, TN p Tungusic); CA p Caucasian (N p North; S p South).
c
Only haplotypes with HVS-I motif 16144-16189-16270 and its derivatives have been taken into account.
d
Only haplotypes with HVS-I motif 16162 and its derivatives have been taken into account.
e
Only haplotypes with HVS-I motif 16126-16136-16189-16223-16360-16362 and its derivatives have been taken into account.
f
In the estimation of haplogroup V proportions, data from Torroni et al. (2001) have been used, and the corresponding sample size is given in parentheses after the sample size analyzed
for calculating other haplogroup frequencies (in case of German population, the pooled data of different German subpopulations from Torroni et al. [2001] have been used).
g
Frequencies of haplogroup V are from Torroni et al. (2001).
666 Am. J. Hum. Genet. 74:661–682, 2004
Table 2
Frequencies (%) of mtDNA and Y-Chromosomal Haplogroups in Different Saami
Subpopulations
FREQUENCY (95% CR)a
(%)
Swedish Saamib Finnish Saamic Norwegian Saamid Kola Saamie
HAPLOGROUP (n p 98/35) (n p 69/69) (n p 278/ …) (n p … /23)
mtDNA:
H: 3.1 (1.1–8.6) 2.9 (.9–9.9) 4.7 (2.8–7.8) …
H1 .0 (.0–3.0) .0 (.0–4.2) 4.0 (2.2–6.9) …
W 1.0 (.2–5.5) .0 (.0–4.2) 1.4 (.6–3.6) …
T .0 (.0–3.0) .0 (.0–4.2) .4 (.1–2.0) …
U: 26.5 (18.8–36.1) 43.5 (32.4–55.3) 57.6 (51.7–63.2) …
U5a .0 (.0–3.0) 2.9 (.9–9.9) .7 (.2–2.6) …
U5b 26.5 (18.8–36.1) 40.6 (29.8–52.4) 56.8 (51.0–62.5) …
V 68.4 (58.6–76.7) 37.7 (27.2–49.5) 33.1 (27.8–38.8) …
M: 1.0 (.2–5.5) 15.9 (9.2–26.4) 2.9 (1.5–5.6) …
D5 .0 (.0–3.0) 8.7 (4.1–17.7) 2.9 (1.5–5.6) …
Z 1.0 (.2–5.5) 7.2 (3.2–15.9) .0 (.0–1.1) …
NRY:
E .0 (.0–8.0) .0 (.0–4.2) … 8.7 (2.7–27.0)
F* 5.7 (1.8–18.7) … .0 (.0–11.7)
I 31.4 (18.6–48.1) 40.6 (29.8–52.4)f … 17.4 (7.1–37.4)
J .0 (.0–.8) … 4.3 (1.0–21.1)
N3 37.1 (23.1–53.8) 55.1 (43.3–66.3) … 39.1 (22.1–59.4)
R1b 5.7 (1.8–18.7) 1.4 (.3–7.7) … 8.7 (2.7–27.0)
R1a 20.0 (10.1–36.0) 2.9 (.9–9.9) … 21.7 (9.8–42.2)
a
Sample size (n) is given separately for mtDNA/NRY data sets, respectively.
b
mtDNA data are from this study and inferred from Sajantila et al. (1995); NRY data from
Rosser et al. (2000) are further analyzed for markers M89, M52, M130 (RSP4Y), M170, M173,
M178, M201, and M269 (YCC 2002) in the present study.
c
mtDNA data are inferred from Sajantila et al. (1995); NRY data are inferred from Raitio et
al. (2001).
d
mtDNA data are inferred from Sajantila et al. (1995), Dupuy and Olaisen (1996), and Del-
ghandi et al. (1998).
e
NRY data are from Wells et al. (2001).
f
Frequency is that of haplogroups F, I, and J combined.
The phylogenetic network in figure 1 relates all the The frequencies of the most widely spread haplo-
HVS-I sequence haplotypes in the three geographic sub- groups among the Saami in other analyzed populations
populations of the Saami. It also indicates a limited num- are shown in table 1. Both haplogroups V and U5b are
ber of highly frequent haplotypes, which are, in most spread at moderate frequencies across Europe, from Ibe-
cases, shared by all analyzed geographic subpopulations ria to the Ural Mountains. In contrast, among 393 Ob-
(see table 2). Thus, 98% of the Saami mtDNA pool is Ugric speakers (including 98 Mansi, published elsewhere
encompassed within haplogroups V, U5b, H, Z, and D5. by Derbeneva et al. [2002b]) and 388 Samoyeds (in-
The two largest subsets, V and U5b, account for a lion’s cluding 58 Nenets, published elsewhere by Saillard et al.
share (89%) of the Saami mtDNA pool. The represen- [2000]), only one haplogroup V–carrying individual was
tative proportion of individual haplogroups varies sub- found in the Mansi sample, whereas not a single Saami
stantially among different Saami subpopulations (table variant of U5b (U5b1b1) was identified there (table 1).
2). Haplogroup V is by far the most frequent haplo- These two variants of maternal lineages are virtually
group in the Swedish Saami and is present at significantly absent in the other 1,199 native Siberians analyzed in
lower frequencies (P ! .0001) in Norwegian and Finnish this study.
subpopulations. We note that, in all three Saami sub- The third-most-frequent haplogroup among the Saami
populations, U5b was virtually the only subclade of the is H, which is present at a frequency of 4%, ∼10-fold
otherwise frequent and divergent western Eurasian hap- lower than that of other North European populations
logroup U5 (Tambets et al. 2003). It is the most frequent (Richards et al. 2000). The majority of the Saami hap-
haplogroup among Norwegian and Finnish subpopu- logroup H lineages (61%) contain transitions at nps 73
lations (table 2). and 16162. According to information obtained from
Table 3
Frequencies (%) of Selected Y-Chromosomal Haplogroups in the Saami and in Other Eurasian Populations
FREQUENCY OFHAPLOGROUP
(%)
REGION AND LANGUAGE SAMPLE
POPULATIONa FAMILYb SIZE Ic R1bd R1a N3 N2 Q C REFERENCE(S)
Scandinavia:
*Saamie U-FU 127 (58)f 25.9f 3.9 11.0 47.2 0 0 0 Raitio et al. 2001; Wells et al. 2001; present study
Swedes IE-G 141 48.2 22.0 18.4 2.8 0 0 0 Present study
Norwegians IE-G 72 40.3 27.8 23.6 6.9 0 0 0 Passarino et al. 2002
Danes IE-G 194 38.7 36.1 16.5 .5 0 0 0 Sanchez et al. 2003
Northern Europe:
*Finns U-FU 38 28.9 0 7.9 63.2 0 0 0 Zerjal et al. 2001
Estonians U-FU 209 18.2 9.1 33.5 30.6 0 0 0 Present study
Latvians IE-B 86 7.0 9.3 38.4 41.9 0 0 0 Present study
North Russians IE-S 77 20.8 0 40.3 28.6 0 0 0 Wells et al. 2001
Eastern Europe:
Russians IE-S 61 13.1 21.3 42.6 8.2 8.2 0 0 Karafet et al. 2002 (supplementary data obtained by request from the author)
Ukrainians IE-S 50 18.0 2.0 54.0 6.0 0 0 0 Semino et al. 2000
Polese IE-S 93 16.1 13.4 55.9 3.2 0 0 0 Present study
Volga-Ural region:
Maris U-FU 111 8.1 2.7 47.7 31.5 9.9 0 0 Semino et al. 2000; present study
Mordvin U-FU 83 19.3 13.3 26.5 16.9 2.4 0 0 Present study
Komis U-FU 94 5.3 16.0 33.0 22.3 12.8 0 0 Present study
Udmurts U-FU 87 1.1 2.3 10.3 56.3 28.7 0 0 Present study
Chuvashes A-T 79 11.4 3.8 31.6 17.7 10.1 0 1.3 Present study
Tatars A-T 126 4.0 8.7 34.1 18.3 4.8 .8 1.6 Present study
Southern Europe:
Croats IE-S 109 37.6 15.6 33.9 0 0 0 0 Barac et al. 2003
Western Europe:
French IE-R 61 16.4 59.0 0 0 0 0 0 Semino et al. 2000; present study
Central Europe:
Germans IE-G 16 37.5 0 0 0 0 0 0 Semino et al. 2000
Hungarians U-FU 113 28.3 20.4 20.4 .9 0 2.6 .9 Present study
Siberia:
Khants U-FU 47 0 19.1 4.3 38.3 38.3 0 0 Karafet et al. 2002 (supplementary data obtained by request from the author)
Nganasans U-SA 38 0 0 0 0 92.1 0 5.3 Karafet et al. 2002 (supplementary data obtained by request from the author)
Nenets U-SA 148 0 0 0 40.5 56.8 1.4 0 Karafet et al. 2002 (supplementary data obtained by request from the author)
Selkups U-SA 131 0 6.1 19.1 0 6.9 66.4 1.5 Karafet et al. 2002 (supplementary data obtained by request from the author)
Kets Isolate 48 0 0 0 0 0 93.7 6.2 Karafet et al. 2002 (supplementary data obtained by request from the author)
Dolgans A-T 67 1.5 1.5 16.4 22.4 11.9 0 37.3 Karafet et al. 2002 (supplementary data obtained by request from the author)
Yakuts A-T 155 1.3 1.9 1.9 88.4 0 0 3.2 Karafet et al. 2002 (supplementary data obtained by request from the author); present study
Buryats A-M 81 0 1.2 1.2 28.4 2.5 0 60.5 Karafet et al. 2002 (supplementary data obtained by request from the author)
Evenks A-TN 96 5.2 0 1.0 16.7 3.1 4.2 67.7 Karafet et al. 2002 (supplementary data obtained by request from the author)
Evens A-TN 31 3.2 0 6.5 12.9 0 0 74.2 Karafet et al. 2002 (supplementary data obtained by request from the author)
Altaians A-T 98 0 0 46.9 1.0 2.0 17.3 22.4 Karafet et al. 2002 (supplementary data obtained by request from the author)
Total 2,967
a
Populations for which data are deduced from published sources are indicated with an asterisk.
b
Language-family codes for each population are as follows: U p Uralic (FU p Finno-Ugric; SA p Samoyedic); IE p Indo-European (B p Baltic; G p Germanic; R p Romance; S p Slavic); A
p Altaic (M p Mongolic; T p Turkic, TN p Tungusic).
c
Haplogroup I is, in the case of data deduced from literature, defined by the characteristic STR pattern of haplogroup 2 Y chromosomes (Barac et al. 2003; present study).
d
Haplogroup R1b is, in the case of data deduced from literature, defined here by M173(xSRY-1532) as studied western Europeans (except three Danes, who belong to R1* [Sanchez et al. 2003])
from this clade have been shown to share the additional mutation M269 (Cruciani et al. 2002; present study).
e
35 Swedish Saami and 93 Poles from the study by Rosser et al. (2000) were further analyzed for markers M52, M89, M130, M170, M173, M178, M201, and M269.
f
In the estimation of haplogroup I proportions, only the data from the present study and from Wells et al. (2001) were used. The corresponding sample sizes are given in parentheses.
Table 4
Phylogeographic Distribution of Haplogroup U5b Subclades (Excluding U5b1b1)
NO. OF INDIVIDUALS IN POPULATIONc
a
WSE SC EE Other BASE AT NP
1
5 7 0
U5b 6 3 9
HVS-I SUB 5 8 2
SEQUENCEa HGb al bo br cr cz fr gr hu it si sk sl sw ba es ko la mo po ru ta ud uk mc ng go tu sh ku td nd 6 5 7
270 U5b* 1 2 3 A ND ND
051-168-189-270-362 U5b* 1 1 A ND ND
086-192-270-304 U5b* 1 1 A ND ND
093-172-189-270-362 U5b* 1 1 A ND ND
093-234-270-325 U5b* 1 1 A ND ND
668
093-258-270-292-362 U5b* 1 1 A ND ND
145-189-270 U5b* 1 1 A ND ND
169-172-189-270 U5b* 1 1 A ND ND
169CA-192-235-270-304 U5b* 1 1 A ND ND
189-192-201-270-398 U5b* 1 1 A ND ND
189-192-217-234-270-398 U5b* 2 2 A ND ND
189-192-234-256-270-311-362-398 U5b* 1 1 A ND ND
189-192-266-270-398 U5b* 1 1 A ND ND
189-192-270 U5b* 1 1 1 1 1 5 A ND ND
189-192-270-398 U5b* 1 1 1 3 A ND ND
189-239CA-270 U5b* 1 1 A ND ND
189-261-270 U5b* 1 1 A ND ND
189-270 U5b* 1 3 2 6 A ND ND
189-270-288-292 U5b* 1 1 A ND ND
189-270-311 U5b* 1 1 1 3 A ND ND
189-292-311 U5b* 1 1 A ND ND
192-212-270 U5b* 1 1 A ND ND
192-224-261 U5b* 1 1 A ND ND
192-235-270-304 U5b* 1 1 A ND ND
192-257-270-304 U5b* 1 1 A ND ND
192-270 U5b* 1 1 1 3 A ND ND
192-270-278-304 U5b* 1 1 A ND ND
192-270-304 U5b* 1 1 2 A ND ND
192-311 U5b* 1 1 1 4 2 9 A ND ND
222-224-270-311 U5b* 1 1 A ND ND
224-270-311 U5b* 1 1 2 A ND ND
234-270 U5b* 1 1 A ND ND
258-270-292-362 U5b* 1 1 A ND ND
261-270 U5b* 1 1 1 3 A ND ND
261-270-390 U5b* 1 1 A ND ND
051-189-270 U5b1* 2 2 G A T
086-189-192-270-311-336 U5b1* 3 3 G A T
092-189-270-294 U5b1* 1 1 G A T
093-182-189-192-270 U5b1* 1 1 G A T
093-189-270 U5b1* 1 1 2 G A T
093-189-270-362 U5b1* 2 2 G A T
129-189-223-270 U5b1* 1 1 G A T
129-189-270 U5b1* 1 1 G A T
129-192-270 U5b1* 1 1 G A T
147-189-270 U5b1* 1 3 1 5 G A T
174-189-223-270 U5b1* 1 1 G A T
174-189-270-311 U5b1* 1 1 2 G A T
182-189-192-270 U5b1* 1 1 G A T
186-189-270-293 U5b1* 1 1 G A T
189-192-218-270-320 U5b1* 1 1 G A T
189-192-270 U5b1* 6 3 1 10 G A T
189-192-270-292 U5b1* 1 1 G A T
189-192-270-311 U5b1* 1 1 G A T
189-221-223-270 U5b1* 1 1 G A T
189-221-270 U5b1* 1 1 2 G A T
189-223-270 U5b1* 1 1 G A T
189-270 U5b1* 8 1 1 1 5 2 1 5 2 26 G A T
189-270-311-336 U5b1* 1 1 G A T
192-224-261-270 U5b1* 1 1 G A T
192-270 U5b1* 1 1 1 1 1 5 G A T
192-270-296 U5b1* 1 1 G A T
192-270-319 U5b1* 1 1 G A T
074-172-189-270 U5b1b 1 1 G G C
074-189-270 U5b1b 1 1 G G C
093-129-189-270 U5b1b 1 2 1 4 G G C
093-189-270 U5b1b 1 1 2 G G C
669
093-189-270-301 U5b1b 1 1 G G C
093-189-270-301-311 U5b1b 1 1 G G C
173-189-270-235 U5b1b 1 1 G G C
189-192-270 U5b1b 1 1 2 G G C
189-270 U5b1b 1 1 1 1 1 5 G G C
189-270-325 U5b1b 1 1 G G C
Total 3 5 1 20 4 13 3 2 1 9 1 1 9 4 14 11 6 5 1 16 5 1 13 3 1 2 2 1 1 2 160
NOTE.—mtDNAs belonging to subclade U5b1b1 were screened selectively for the presence of the mutations in nps 5656, 7385, and 10927. All of those (18 Saami, 5 individuals from eastern Europe, and 5 individuals from
western and southern Europe) possessed aforementioned transitions.
a
Mutations in sequences are relative to the revised Cambridge Reference Sequence (Andrews et al. 1999). HVS-I sequences are given minus 16,000; only tranversions are further indicated. ND p not determined.
b
SubHG p subhaplogroup.
c
Geographic subdivision codes are as follows: WSE p western and southern Europe; SC p Scandinavian Europe; EE p eastern Europe. Population codes are as follows: al p Albanians; bo p Bosnians; br p Bretons; cr p
Croats; cz p Czechs; fr p French; gr p Greeks; hu p Hungarians; it p Italians; si p Sicilians; sk p Slovaks; sl p Slovenians; sw p Swedes; ba p Bashkirs; es p Estonians; ko p Komis; la p Latvians; mo p Mordvin; po
p Poles; ru p Russians; ta p Tatarians; ud p Udmurts; uk p Ukrainians; mc p Moroccans; ng p Nogays; go p Georgians; tu p Turks; sh p Shors; ku p Kumyks; td p Tadjik. In addition to population data from table 1,
data of Bretons, Moroccans, Shors, Tadjiks, and Turks are shown (authors’ unpublished data).
d
Number of subjects analyzed in haplotype.
Figure 1 Phylogenetic network of 445 Saami mtDNA HVS-I sequences. Only those coding-region markers that have been analyzed in this
study are shown (for finer resolution of haplogroup U subbranches, see fig. 3). Observed mutations are numbered according to the revised Cambridge
Reference Sequence (Anderson et al. 1981; Andrews et al. 1999). The tree is rooted in haplogroup L3. Variable nps are shown on the links; nucleotide
change is specified by suffixes only for transversions. Nodes indicate different haplotypes and have sizes that are proportional to their frequencies.
HVS-I sequences are from Sajantila et al. (1995), using the corrections given by Bandelt et al. (2001) (n p 114 ); from Dupuy and Olaisen (1996)
(n p 197); from Delghandi et al. (1998) (n p 61 ); and from the present study (n p 73 , underlined samples). The analysis of coding region variation
has been performed for only the 73 samples analyzed in the present study; haplogroup affiliations for data published elsewhere are inferred from
HVS-I sequences. sf p Saami from Finland, sn p Saami from Norway, ss p Saami from Sweden. Note that the presence of three transversions
reported in a single haplotype (sf) from haplogroup V (Sajantila et al. 1995) has not been reconfirmed by an independent study.
complete sequences, these lineages belong to subhaplo- I, the classification of the samples was more problematic.
group H1, defined by the coding region transition at np However, the STR pattern of those haplogroups in com-
3010 (Finnilä et al. 2001). We notice here that HVS-I bination with the typed biallelic markers is, in most cases,
haplotypes with a transition at np 16162 in the Volga- haplogroup-specific enough to make the misclassification
Ural area people (Bermisheva et al. 2002) and other of the samples highly unlikely. The probability of mis-
European populations studied by us belong exclusively classification is higher in the data set from Raitio et al.
to this branch of subhaplogroup H1 (authors’ unpub- (2001), in which only some informative biallelic markers
lished data). This variant of mtDNA can be found both and no STRs were scored. Therefore, these samples are
in western and eastern Europe, being as frequent in Ger- left at a lower resolution level in table 2. Detailed criteria
manic-speaking Scandinavians and the Germans as used in the process of deduction are given in the footnotes
among the Norwegian Saami but absent in the Finnish of table 3.
and Swedish Saami (table 2). Though present in several Three major haplogroups—N3, I, and R1a—comprise
Volga-Finnic populations, H1 haplotypes with mutation 180% of the Saami Y-chromosomal gene pool (table 2)
16162 are extremely rare or absent in almost 2,000 Si- and appear, likewise, as the major haplogroups in north-
berian Ugric-, Samoyedic-, and Altaic-speaking people eastern Europe (table 3). The nearly equal distribution
(table 1) as well as in central Asians (Comas et al. 1998; of the Y-chromosomal variants among different Saami
Metspalu et al. 1999)—that is to say that this clade has populations strongly supports their common paternal
an overwhelmingly European phylogeographic pattern. history. The comparison of the Y-chromosomal hap-
Its presence only in the Norwegian Saami sample may logroup frequencies in different subpopulations shows
have been generated by admixture with the Norwegian that, similar to mitochondrial haplogroup frequencies,
population. This inference is supported by the presence some Y-chromosomal haplogroups (J and R1a) exhibit
of one H1 haplotype, with HVS-I motif 16162–16189, notable variation between geographic subpopulations of
found among the Saami, in the Norwegian sample (Hel- the Saami (table 2).
gason et al. 2001). This haplotype has not been found Haplogroup N3, the most frequent haplogroup in the
in any other population analyzed in the present study. Saami population, is distributed in eastern European and
Only a minor portion of the Saami maternal lineages northern Asian populations but it is rare or absent in
(average ∼5%) that exhibit restricted diversity belong western Europe (table 3). All analyzed Swedish Saami
to haplogroups that are characteristic of Asian pop- N3 lineages fall into subcluster N3a, defined by M178
ulations—that is, D5 and Z (table 1). These eastern (YCC 2002). Although N3a is widespread in Siberia,
Eurasian haplogroups are significantly more frequent other haplogroups, characteristic of Samoyedic-speaking
(P ! .05) among the Finnish Saami compared with Nor- and other Siberian populations (such as C and Q), are
wegian and Swedish Saami samples (table 2). Such fluc- either almost absent in Baltic-Finnic populations, in-
tuations in haplogroup frequencies could be due to ge- cluding the Saami, or are only sporadic, as for haplo-
netic drift or just due to stochastic variation in relatively group N2, which is found only among Volga region
small samples. At the same time, the similar pattern of Finnic speakers (table 3).
mtDNA haplogroup distribution found in different sub- The second largest haplogroup, I, corresponds to
populations of the Saami provides evidence of their com- roughly one-third of the Saami Y-chromosomal lineages.
mon genetic background. It is widespread in Europe but virtually absent in Asian
populations (table 3). The defining mutation of haplo-
Saami Y-Chromosomal Haplogroup Pattern group I, M170, most likely arose in Europe (Semino et
and Frequencies al. 2000). It is well dispersed over the continent, as well
as among Volga River basin Finnic and Turkic speakers
The Y-chromosomal variation of 35 Swedish Saami, (table 3). At the current level of resolution, the phylo-
published by Rosser et al. (2000), was further analyzed genetic reconstructions do not identify the geographic
to improve the resolution of paternal lineage clusters ac- origin of haplogroup I in Europe. Nevertheless, its vir-
cording to the YCC (2002). For comparison, data from tual absence among Samoyeds as well as among Ugric-
different European and Siberian populations were used speaking Mansis and Khants suggests that these popu-
(table 3). To include the data published before the high- lations have not shared a recent ancestry with the Saami.
resolution nomenclature of biallelic markers (YCC 2002) Indeed, the high frequencies of haplogroup I in the Nor-
was available, a combination of the results of the analysis wegians, Swedes, Finns, and the Saami (table 3) suggest
of biallelic markers and polymorphisms of STRs was used, that haplogroup I represents the heritage from the very
when possible (Zerjal et al. 2001), to infer the haplogroup first settlers of Fennoscandia. Analyses of microsatellite
frequencies presented in table 3. In some cases (haplo- variation of the Saami haplogroup I Y chromosomes
groups N3 and R1a), the updating of the data was simple reveals that 9 of 10 Saami M170 chromosomes share
and unambiguous. In the case of haplogroups R1b and the same modal microsatellite haplotype (6/9) or its de-
672 Am. J. Hum. Genet. 74:661–682, 2004
rivatives with other Nordic haplogroup I chromosomes Figure 2B shows a similar analysis undertaken on the
(authors’ unpublished data). The latter corresponds to Y-chromosomal haplogroup frequencies. Here, the first
haplogroup 2 chromosomes with alleles 14-23-10-11- PC is determined, on the one hand, by the western Eu-
13, defined by DYS19-390-391-392-393, respectively, in rasian–specific haplogroups I, R1a, and R1b and, on the
the studies by Helgason et al. (2000), Zerjal et al. (2001), other hand, by Asian-specific haplogroup C and by the
Weale et al. (2002), and Capelli et al. (2003). These largely Siberian-specific N2, which both separate all
haplotypes form a subclade of haplogroup I that is dif- Samoyeds and Ob-Ugric-speaking populations (except
ferent from the variety of equally abundant M170 chro- Selkups) from the Saami. In contrast to that of other
mosomes found in the Adriatic coastal region, where the Samoyedic-speaking populations, the Selkup Y-chromo-
Dinaric Modal Haplotype (16-24-11-11-13) is common somal pool is dominated by eastern Eurasian haplogroup
(Barac et al. 2003). Q, which explains their solitary location on the second
Haplogroup R1a, encompassing 11% of the Saami Y- dimension of the PC graph. Two Saami subpopulations
chromosomal gene pool, is a frequent Y-chromosomal map close together and are placed in the immediate vi-
variety in eastern Europe, but it is also found in Siberia, cinity of the Finns, Volga-Finnic, and Volga-Turkic pop-
the Altai Mountains (table 3), and India (Kivisild et al. ulations, as well as the Russians. The latter two are
2003). Like haplogroup I, it is absent among Nenets, characterized by haplogroup N3 at moderate frequencies
the largest Samoyed population, living partly in north- (table 3). Furthermore, at this resolution, Germanic-
east Europe. Haplogroup R1a is present in the Swedish speaking populations (including Scandinavian Norwe-
and Kola Saami at frequencies that are comparable to gians and Swedes) and the French form an additional
those observed among other Scandinavian and north- cluster that is close to other European populations in-
eastern European populations, but it is relatively rare in cluded in the analysis.
Finland, both in the Saami and non-Saami populations
(table 3). Phylogeography of Haplogroup U5b1b
Haplogroup R1b is present in the Saami population and the “Saami-Specific” Motif (U5b1b1)
at a level of 4%. It is the most frequent haplogroup in
western Europe, especially among the French, and it is Haplogroup U5b is found at low frequencies all over
relatively frequent in Scandinavian Germanic-speaking Europe (Richards et al. 1998). A distinct phylogenetic
populations, but it has not been found among the Finns. subbranch of U5b carries the “Saami-specific” HVS-I
In the Volga-Ural region populations, R1b is present at motif defined by 16144-16189-16270 in the study by
frequencies similar to those of the Saami (table 3). Sajantila et al. (1995) and has been named “U5b1” by
Haplogroups J and E, found solely among Kola Saami Richards et al. (1998). All U5b sequences share two
(table 2), may have arisen as a recent contribution from diagnostic synonymous substitutions at nps 7768 and
the neighboring northern Russian population, since these 14182 (see fig. 3A). The major U5b subset found among
Y-chromosomal variants are present there (Wells et al. the Finns contains a derived G allele at noncoding np
2001). 5656 and a synonymous substitution at np 12618 (Fin-
nilä et al. 2001). Through use of complete mitochondrial
PC Analysis sequence data, it has previously been demonstrated that
the Finnish sequences containing the “Saami-specific”
The results of the PC analysis based on mtDNA hap- HVS-I motif share an additional synonymous mutation
logroup frequencies (fig. 2A) illustrate why the Saami at np 10927, which is often associated with another
are identified as mitochondrial genetic “outliers” in Eu- transition at np 7385 (Finnilä et al. 2001).
rope. Here, it is the relative haplogroup proportions and To study the phylogeography of the “Saami-specific”
not the phylogeographic affiliations that are distinctive. branch of U5b, an analysis of np 5656 variation among
The first PC (fig. 2A) reflects predominantly the differ- the relevant genomes was performed. The results reveal
ences between frequencies of haplogroups characteristic (see table 4) that 95 of 160 samples carried the derived
of the eastern and western parts of Eurasia (H, J, V, and 5656G allele and belong, thus, to a subhaplogroup re-
U5 vs. A and M). All Saami subpopulations cluster to- ferred to as “U5b1.” We note that this subhaplogroup
gether as a distinct group, but the distance between the is different from the U5b1 branch defined by Richards
Saami and native Siberians is much greater than between et al. (1998) using HVS-I data alone. Here, “U5b1”
the Saami and other Europeans. Different distributions refers to a deeper phylogenetic node of U5b (see fig. 3A).
of the populations along the axis of the second PC arise The transition at np 7385 was always found to be as-
primarily from the different proportions of haplogroups sociated with a transition at np 10927 and is referred
H, U5, and V in the populations. In addition, the lack to as “U5b1b.” This cluster also includes the “Saami-
of haplogroups J, U4, and A among the Saami plays a specific” subclade, which we name here as “U5b1b1”
relatively important role here. (fig. 3). Notice that the sequence motif 16189-16192-
Figure 2 PC analysis based on mtDNA (A) and Y-chromosomal (B) haplogroup frequencies in some European and Siberian populations.
Only the seven haplogroups (squares) having the main impact on the scatter plot have been used (see the “Subjects and Methods” section).
Numbers in parenthesis indicate the proportion of the total genetic information retained by a given PC. The Saami population is subdivided
according to the present location of the subpopulations. Population data (triangles) are the same as in tables 1 and 3 and are listed here in
alphabetical order as follows: at p Altaians, ch p Chuvashes, ev p Evenks, fi p Finns, fr p French, ge p Germans, kh p Khants, km p
Khants and Mansis, ko p Komis, ne p Nenets, nn p Nganasans, no p Norwegians, sf p Saami from Finland, sk p Saami from Kola
Peninsula, Russia, sn p Saami from Norway, ss p Saami from Sweden, se p Selkups, sw p Swedes, vt p Volga-Uralic Turkic-speakers
(Bashkirs and Chuvashes). Inclusion of all populations listed in tables 1 and 3 did not change the overall outcome (data not shown).
16270 in U5b1 appears to be associated with at least three the exploration of the phylogeography of haplogroup
independent subhaplogroups of U5b: U5b* (5656A), U5b1b ambiguous, and these sequences were not in-
U5b1*/U5b1a (5656G, 7385A, and 10927T), and U5b1b cluded in the analysis.
(5656G, 7385G, and 10927C) (fig. 3; table 4). Therefore, The 5656G allele, including all major subsets of U5b1,
reliance on published HVS-I sequences alone, without is broadly distributed both in western and eastern Eu-
regard to the relevant coding region information, makes rope (fig. 3A; table 4). The U5b1b subclade is found all
Figure 3 A, Phylogenetic network of U5b1b lineages based on HVS-I sequences and its position in the phylogeny of haplogroup U.
Sequence information from Herrnstadt et al. (2002) and Finnilä et al. (2001) has been used for the coding region and HVS-II (see also table
4). The nucleotide positions relative to the revised Cambridge Reference Sequence (Anderson et al. 1981; Andrews et al. 1999), at which two
nodes differ, are listed along links. Nucleotide changes are specified by suffixes only for transversions; “⫹” indicates an insertion. Note that
we have redefined subclade U5a of Finnilä et al. (2001) and Herrnstadt et al. (2002) as “U5b2,” on the basis of its position in the phylogenetic
tree. U5b1b1 haplotypes are shown as the square labeled as “Saami motif” and are further refined in panel B. B, Phylogenetic network of 330
U5b1b1 lineages based on HVS-I sequences. The star indicates the basal node (transitions in nps 16144, 16189, and 16270). Population sizes
and U5b1b1 frequencies are shown in table 1. Ar p Armenians, Ba p Bashkirs, Bo p Bosnians, Ch p Chuvashes, Cr p Croats, Cz p Czechs,
Es p Estonians, Fi p Finns, Fr p French, Hu p Hungarians, Ka p Karelians, Kb p Kabardians, Ko p Komis, La p Latvians, Li p
Lithuanians, Ma p Maris, Mc p Moroccans, Mo p Mordvin, Ng p Nogays, No p Norwegians, Po p Poles, Sa p Saami, Sl p Slovaks,
Ru p Russians, Si p Sicilians, Sw p Swedes, Ta p Tatars, Uk p Ukrainians. For further information, see the legend to figure 1.
Table 5
Coalescence Ages for Different Subsets of Subhaplogroup U5b1b1
Tc DT d
Set of Sequences Considereda n rb (years) (years)
U5b1b1 (without Sa) 118 25/118 p .212 4,300 1,400
U5b1b1 in Scandinavia (without Sa) 55 6/55 p .109 2,200 2,200
U5b1b1 in Scandinavia (with Sa,
without subfounder 16148) 187 11/187 p .059 1,200 700
U5b1b1 in eastern Europe (Es/Li/
Ma/Mo/Ko/Ru/Uk/Po/Ba/Ch) 47 13/47 p .277 5,600 1,700
U5b1b1 in southern and western
Europe (Bo/Cr/Sl/Hu/Fr) 11 3/11 p .273 5,500 3,200
a
Population codes are the same as those used in figure 3.
b
Average mutational distance to the founder haplotype of the cluster.
c
Coalescence time, calculated by means of r with a mutation rate of 1 transition
per 20,180 years in the HVS-I segment between nps 16090 and 16365 (Forster et
al. 1996).
d
SD for r, calculated as in the study by Saillard et al. (2000).
over Europe, but it occurs in western and central Europe all non-Saami U5b1b1 lineages in Europe (see fig. 3B) is
with notable sequence variation. The haplotype diversity 4,300 Ⳳ 1,400 years BP (table 5). This is approximately
(excluding subclade U5b1b1) is 0.96. We note that the same as that for the eastern or western-southern
U5b1b was also identified in a northwestern African European subsets but is older than that observed for
population, among the Moroccans (fig. 3A). In contrast, Scandinavians.
its diversity in eastern Europe is much lower. There, the
haplotype diversity (excluding subclade U5b1b1) is 0.79, Discussion
whereas most of the U5b1b sequences in eastern Europe
belong to the U5b1b1 branch (fig. 3A and 3B). In the
Samoyed/Siberian Heritage of the Saami Population?
Eurasian cohort, U5b1b (other than U5b1b1) is absent
from native Siberians and is notably absent from the Uralic-speaking Samoyeds, Khants, Mansis, and Altaic-
Ob-Ugric populations and the Samoyeds. speaking Siberians virtually lack the European mtDNA
Most importantly, the data indicate that U5b1b1, the haplogroups V and U5b1b1 that predominate in the
only subcluster of U5b in the Saami population, is present Saami mtDNA pool (fig. 1; table 1). Eastern Eurasian
outside the Scandinavian-Baltic and the Volga-Uralic mtDNA variants in the Saami are represented by a re-
regions—namely, in the French, Croatian, Bosnian, Slov- stricted set of lineages that belong to superhaplogroup M.
enian, Czech, Russian, Ukrainian, Polish, and Hungarian In this respect, the Saami do not differ markedly from
mtDNA pools—and, further, is present even in the Cau- Finnic-speaking Karelians, Maris, Komis, Udmurts, or
casus, among the Nogay, Kabardinian, and Armenian northern Russians, all of whom possess haplogroups of
mtDNAs (fig. 3B). Thus, this subhaplogroup is much eastern Eurasian origin at similar frequencies (table 1).
more widely distributed than was believed previously (Sa- This minor part of the Saami mtDNA pool consists of
jantila et al. 1995). Two principal haplotypes, differing two branches of the eastern Eurasian mtDNA tree—D5
by one mutational step, define the Saami U5b1b1 (fig. and Z1. According to published data, the frequency of
3B). One, with transitions at nps 16144, 16189, and haplogroup D5 is relatively high in China (Yao et al.
16270, can be identified as the founder haplotype because 2002). D5 is also present among Mongols and Siberians
of its presence in many other populations. The second, (Kolman et al. 1996; Derbeneva et al. 2002b). However,
containing an additional transition at np 16148, is so far the Saami haplogroup D5 lineages, with the HVS-I mo-
exclusive to the Saami population. This subfounder com- tif 16126-16136-16360 and its derivatives (defined as
prises 38% of their U5b1b1 mtDNAs and is present in “D5b” by Derenko et al. 2003), have been identified only
all studied subpopulations of the Saami. Furthermore, no in some northern and eastern European populations
other derivatives of the U5b1b1 founder node present in (among Karelians, Finns, Estonians, North-Russians, and
the Saami sample was identified in other Scandinavians, Komis) and in some Siberian populations but not in Sam-
including the Finns, irrespective of the previous obser- oyeds (table 1). This suggests, again, the lack of gene flow
vation that the northern-central Finnish population is rel- from Samoyeds to eastern Europe.
atively rich in U5b1b1 (Meinilä et al. 2001). Thus, the Haplogroup Z, a subcluster of the M8 clade within
“leakage” of the Saami U5b1b1 to neighboring popula- the haplogroup M family of mtDNA (Kivisild et al.
tions seems to be rather limited. The coalescence time of 2002), is found at highest frequencies in the northeastern
676 Am. J. Hum. Genet. 74:661–682, 2004
Asians: the Itelmens and Koryaks (Schurr et al. 1999). than Siberia, is a possible origin of the earliest expansion
It is also present in several Siberian populations, includ- of this haplogroup in northern Eurasia. Third, the lack
ing the Altaic people (table 1). Though not identified in of Y-chromosomal haplogroup C in Saami contrasts
a large data set of the Yakuts (Fedorova et al. 2003; with its high frequency among Tungusic-speaking native
Pakendorf et al. 2003), haplogroup Z has been observed Siberians (such as the Evenks and the Evens) as well as
among several Finnic- and Turkic-speaking populations among Mongolic-speaking Mongols, the Buryats, the
of the Volga-Ural region (Bermisheva et al. 2002). It is Kalmyks, and the Turkic-speaking Kazakhs and Uzbeks
curious that it is more frequent there in Finnic- than (Wells et al. 2001; Karafet et al. 2002; authors’ unpub-
in Turkic-speaking populations. The absence of haplo- lished data). Therefore, without introducing specific ad-
group Z from most of the Siberian Uralic-speaking pop- ditional ad hoc scenarios, these observations make it
ulations (Samoyedic-speaking Nenets and Selkups, as unlikely that there was recent Y-chromosomal flow from
well as Siberian Ob-Ugric-speaking Khants and Mansis) these Siberian populations into the gene pool of the
(table 1) is therefore striking. We note that all haplo- Saami.
group Z lineages that are found in eastern Europe belong
to a subhaplogroup Z1, characterized by transitions at Origins of the Saami mtDNA and Y Chromosomes
nps 151, 10325, and 16129 within the Z phylogeny
(Kong et al. 2003a, 2003b). A matching HVS-I founder Scenarios involving extremes of genetic drift, such as
haplotype has been observed in the Koryak and the Itel- that due to repeated bottlenecks, could explain how the
men populations (Schurr et al. 1999). The limited di- Saami mtDNA pool evolved as a narrow subset of that
versity of haplogroup Z in Europe suggests its relatively found in other European populations. Indeed, there are
recent spread west of the Urals. good reasons to believe that even a much larger Finnish
The sister clade of Z—haplogroup C—is far more di- population went through several “bottlenecks” in its
verse and frequent than haplogroup Z in eastern Eu- demographic history (Nevanlinna 1972; de la Chapelle
rasians (Derenko et al. 2003), as well as in the popu- and Wright 1998; Kittles et al. 1999; Peltonen et al.
lations of the Volga-Ural region (Bermisheva et al. 2002), 2000). Likewise, it is possible that, when the proto-
but it is absent among the Saami. Here, again, the lack Saami gene pool was in statu nascendi, it was restricted
of haplogroup C in the Saami is specifically indicative to only a few basic mtDNA haplotypes that were carried
of the absence of possible genetic links between the by the founding settlers—a plausible scenario during the
Saami and the Samoyeds. Indeed, the only Samoyedic- “Paleolithic isolation.”
speaking population that also inhabits northeastern Eu- Torroni et al. (1998, 2001) have suggested that the
rope and is thus geographically close to the Saami, the spread of haplogroup V in Scandinavia and in eastern
Nenets, has haplogroup C as the most frequent (∼30% Europe is due to its late Pleistocene/early Holocene
frequency) variant of mtDNA. expansion from a Franco-Cantabrian glacial refugium.
The predominant Saami Y-chromosomal haplogroup Haplogroup V shows high diversity and the presence of
N3 has a nearly uniform circumarctic distribution in pre-V lineages in Iberia and the islands of Croatia (Tolk
Eurasia (table 3). The closely related N2 lineages are et al. 2000; Torroni et al. 2001). However, the new data
frequent in Siberian and Volga-Uralic populations. Thus, on Volga River basin and Slavic-speaking populations
it is likely that haplogroup N variation represents a pre- (Bermisheva et al. 2002; Malyarchuk et al. 2002; present
historic link between the Siberian and eastern European/ study) show that haplogroup V is also well present in
proto-Finnic populations via their paternal heritage. The eastern Europeans. Furthermore, haplogroup V lineages
improved resolution of the Y-chromosomal phylogenetic with HVS-I transitions 16153 and 16298 (fig. 1) that
tree (Jobling and Tyler-Smith 2003) reveals an ancestral are frequent in the Saami population are much more
node shared by haplogroups N and O, with the latter widespread in eastern than in western Europe (Torroni
restricted largely to eastern Asia. This connection is in- et al. 2001; Bermisheva et al. 2002; authors’ unpublished
triguing, but it is still unclear when and where this com- data). This indicates that haplogroup V might have
mon ancestor first appeared. Nevertheless, one does not reached Fennoscandia via central/eastern Europe (see fig.
need to postulate a recent Siberian flow of Y chromo- 4A). Such a scenario is indirectly supported by the ab-
somes into the Saami gene pool to explain their high N3 sence, among the Saami, of the pre-V mtDNAs that are
frequency. First, such a flow from Samoyedic-speaking characteristic of southwestern Europeans and north-
aboriginal Siberians to the Saami Y-chromosomal pool western Africans and that are also present in Germans
would predict the presence there of haplogroup N2 and/ (Torroni et al. 2001).
or haplogroup Q, widely spread in Samoyeds (Karafet The phylogeography and the ancestry of the other
et al. 2002). Second, the much higher diversity of N3 components of the Saami mitochondrial profile have so
in eastern Europe than in Siberia (Villems et al. 1998; far not been well understood. Here, we showed that
Rootsi et al. 2000) suggests that eastern Europe, rather mtDNA haplogroup U5b1b1—the set of lineages with
other western European populations. That makes it less

likely that U5b1b1 entered the Saami mtDNA pool (or
that the proto-Saami tribes carried it) directly from the
west. The wide geographic distribution of both U5b1b1
and U5b1b in western Eurasian populations and the ap-
parent absence of U5b1b “twigs” (except of U5b1b1)
in Finno-Ugric speakers suggests that the latter may have
originated before the differentiation of the European
Finnic-speaking people.
Haplogroup H1 lineages most probably spread to Fen-
noscandia via a western route (fig. 4A). The diversity of
H1 is relatively higher in Norwegian (0.76), Swedish
(0.78), German (0.78), and Polish (0.80) populations
than in Finnish (0.09), Estonian (0.35), Latvian (0.50),
Karelian (0.0), and Volga-Uralic populations (highest
among Komis: 0.40). Furthermore, as was mentioned
above, the Saami may have obtained their H1 lineages
from recent admixture with the Norwegians.
The two eastern Eurasian mtDNA variants, haplogroup
Z1 and the particular subbranch of D5, have probably
reached northeastern Europe not via the Arctic but via a
more southern route across the southern Urals and, pass-
ing the Volga River basin (fig. 4A), left their “traces”
among the gene pools of the Volga-Ural peoples, although
not, as we have already stressed above, among Ob-Ugric
and Nenets populations (table 1). Here, history and ar-
cheology provide several possible scenarios: not only
events of historic times, like migrations of Huns, Avars,
and Mongols, but also a likely influx of Asian tribes to
eastern Europe during the early Holocene and contrib-
uting to the Kama culture of the upper Volga and Petchora
basins (Kozlowski and Bandi 1984), could have been be-
Figure 4 Schematic reconstruction of possible entry routes of
hind movements that brought a few selected and specific
the predominant Saami maternal (A) and paternal (B) lineages to Fen-
noscandia. Broken lines indicate that the exact place of origin/route eastern Asian mtDNA variants to Fennoscandia. Note
of spread of the haplogroup is unsolved/not indicated. that northern Fennoscandia became accessible to humans
at the very end of the Pleistocene/early Holocene, both
from the west and the east (Donner 1995).
the so-called “Saami-specific” motif—is spread, besides The Y-chromosomal haplogroups N3 and R1a, which
among the Saami, mostly in eastern Europe (fig. 3B). make up ∼60% of the Saami Y-chromosomal variants,
This might suggest that haplogroup U5b1b1 may have have likely reached Fennoscandia from eastern Europe
spread/arisen from eastern Europe. On the other hand, (fig. 4B), where these haplogroups can be found in high
the considerable diversity of the U5b1b cluster in west- frequencies, as among the Saami. Haplogroups I and
ern and southern Europe suggests that these regions, R1b, which together make up a third of Saami Y chro-
rather than eastern Europe, were the likely place of or- mosomes, seem to have arisen in western Europe (fig.
igin of U5b1b. Thus, the distribution of U5b1b is similar 4B). For R1b, this scenario is most plausible because it
to that suggested above for haplogroup V. Notice that is a characteristically frequent Y-chromosomal variant
this cluster, like haplogroup V, is also found in north- in western Europe (table 3). In the case of haplogroup
western Africa (table 4). Hence, we envision an initial I, a specific pattern of STR variation in the Saami is close
diversification of U5b1b in western Europe, followed by to that observed among other Scandinavians and west-
the spread of a particular subhaplogroup in eastern Eu- ern Europeans and is dissimilar to that observed in
rope, finally reaching Fennoscandia (but not the Sam- southern Europe.
oyeds or any other aboriginal Siberians) via an eastern We conclude that the phylogeography of mtDNA and
route (fig. 4A). Indeed, U5b1b1 is absent from a large Y-chromosome variants that correspond to the maternal
sample set of Germans from Lower Saxony (Pfeiffer et and paternal gene pools of the Saami does not provide
al. 2001), and it is detected only in trace frequencies in any evidence for the Saami population arising among
678 Am. J. Hum. Genet. 74:661–682, 2004
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torate General Research grant ICA1CT20070006. The re- Capelli C, Redhead N, Abernethy JK, Gratrix F, Wilson JF,
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Am. J. Hum. Genet.

The Western and Eastern Roots of the Saami—the Story of Genetic

Introduction distances between individual populations. Classic ge-

Y-Chromosome Analysis Results

Latvians IE-B 299 3.0 0 1.0 0 0 Present study

Kets Isolate 104 0 0 0 0 2.9 Derbeneva et al. 2002a; present study

other western European populations. That makes it less

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