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Ancient DNA Reveals Lack of Continuity
between Neolithic Hunter-Gatherers
and Contemporary Scandinavians
Helena Malmström,1,2 M.Thomas P. Gilbert,2 Results and Discussion
Mark G. Thomas,3 Mikael Brandström,4 Jan Storå,5
Petra Molnar,5 Pernille K. Andersen,6 Christian Bendixen,6 By 6,700 years before present (BP) the Neolithization process
Gunilla Holmlund,7 Anders Götherström,1,8,* had influenced most of northern Europe [9]. However, Scandi-
and Eske Willerslev2,8,* navia (including Denmark) was still occupied by highly mobile
1Department of Evolutionary Biology, Uppsala University, hunter-gatherer groups. Although the hunter-gatherers of
SE-11863 Uppsala, Sweden Denmark and southern Sweden adopted pottery early on,
2Centre for GeoGenetics, University of Copenhagen, the Neolithization first took real shape with the appearance
DK-2100 Copenhagen, Denmark of the Funnel Beaker Cultural complex (FBC, also known as
3Research Department of Genetics, Evolution and the Trichterbecher Kultur [TRB]) some 6,000 years BP (the old-
Environment, and the AHRC Centre for the Evolution of est evidence possible dating back some 6,200 years BP [9]). At
Cultural Diversity, University College London, Gower Street, this time domestic cattle and sheep, cereal cultivation, and the
London WC1E 6BT, UK characteristic TRB pottery were introduced into most of
4Department of Forest Mycology and Pathology, Swedish Denmark and southern parts of Sweden [6]. Nevertheless,
University of Agricultural Sciences, SE-10691 Uppsala, the Neolithization process was slow in Scandinavia, and large
Sweden areas remained populated by hunter-gatherer groups until the
5Osteoarchaeological Research Laboratory, Stockholm end of the 5th millennium BP.
University, Stockholm, Sweden One of these last hunter-gatherer complexes was the Pitted
6Department of Genetics and Biotechnology, Faculty of Ware culture (PWC), which can be identified by its single-inhu-
Agricultural Sciences, University of Aarhus, PO Box 50, mation graves distributed over the coastal areas of Sweden
DK-8830 Tjele, Denmark and the Baltic Sea islands that lie closest to the Swedish coast.
7National Board of Forensic Medicine, Department of Forensic Intriguingly, the PWC first appears in the archaeological record
Genetics and Forensic Toxicology, SE-58758 Linköping, of Scandinavia after the arrival of the TRB (some 5,300 years
Sweden BP) and existed in parallel with farmers for more than a millen-
nium before vanishing about 4,000 years BP (Figure 1). This
prolonged coexistence of hunter-gatherers and farmers in
Summary Scandinavia has been a focal point of debate within archae-
ology since 1909, when PWC human remains were used to
The driving force behind the transition from a foraging to argue for an early eastern influence on Neolithic Scandinavia,
a farming lifestyle in prehistoric Europe (Neolithization) thus favoring relations to modern Saami people [10]. However,
has been debated for more than a century [1–3]. Of particular it has mainly been used as a key argument against both a rapid
interest is whether population replacement or cultural Neolithic transition and a large-scale population replacement
exchange was responsible [3–5]. Scandinavia holds a unique between the Mesolithic and the present [7, 8].
place in this debate, for it maintained one of the last major Three main hypotheses have been proposed to explain the
hunter-gatherer complexes in Neolithic Europe, the Pitted origin of the PWC: (1) it has an origin in the late Mesolithic
Ware culture [6]. Intriguingly, these late hunter-gatherers hunter-gatherer complexes of northern Europe [11] that, given
existed in parallel to early farmers for more than a millennium that Neolithic or post-Neolithic population replacement took
before they vanished some 4,000 years ago [7, 8]. The pro- place, would make them genetically distinct from modern
longed coexistence of the two cultures in Scandinavia has Scandinavians; (2) the PWC arose from a reversion to the
been cited as an argument against population replacement hunter-gathering subsistence strategy among TRB peoples
between the Mesolithic and the present [7, 8]. Through anal- [12], and, given that no population replacement took place in
ysis of DNA extracted from ancient Scandinavian human Scandinavia during the Neolithization process, PWC peoples
remains, we show that people of the Pitted Ware culture are the direct ancestors of modern Scandinavians; and (3)
were not the direct ancestors of modern Scandinavians the PWC originated in populations ancestral to modern Saami
(including the Saami people of northern Scandinavia) but people of present-day northern Scandinavia [10, 13].
are more closely related to contemporary populations of To investigate PWC ancestry components in modern Scan-
the eastern Baltic region. Our findings support hypotheses dinavians and peoples of the Baltic region, we recovered
arising from archaeological analyses that propose ancient mitochondrial (mtDNA) sequences (316 bp of the
a Neolithic or post-Neolithic population replacement in D-loop) from the skeletons of 22 individuals deriving from the
Scandinavia [7]. Furthermore, our data are consistent with two different cultures (see Table S1 available online). Three
the view that the eastern Baltic represents a genetic refugia of these were TRB (all from one passage tomb, Gökhem, dated
for some of the European hunter-gatherer populations. to 5,500–4,500 years BP, Figure 1), and 19 belong to the PWC
(recovered from three different sites on the Baltic island of Got-
land dated to 4,800–4,000 years BP, Figure 1).
Quantitative real-time PCR was used to assess the total
*Correspondence: anders.gotherstrom@ebc.uu.se (A.G.), ewillerslev@snm. human mtDNA content in all samples (Tables S2 and S3, Fig-
ku.dk (E.W.) ure S1) and to screen for appropriate molecular behavior (degra-
8These authors contributed equally to the work dation ratio [14], Table S4). Amplicons were sequenced with the
Please cite this article in press as: Malmström et al., Ancient DNA Reveals Lack of Continuity between Neolithic Hunter-Gatherers and
Contemporary Scandinavians, Current Biology (2009), doi:10.1016/j.cub.2009.09.017
Current Biology Vol 19 No 20
2
B 0.003 0 0 0 0 0 0
C 0.003 0 0 0 0 0 0
H1f 0.003 0 0 0 0 0 0
H2 0.003 0 0 0 0.009 0 0
I 0.024 0 0 0 0 0 0
U5 0 0 0 0 0.009 0.158 0
X 0.024 0 0.009 0 0 0 0
[26], and modern [4, 5] genetic data suggest that this is prob- and 3 TRB) met all requirements demanded for authenticity (Supplemental
ably the case. Thus, theories favoring a Neolithization process Data). A set of nonhuman samples, mainly harp seals (Phoca groenlandica,
n = 31), of the same age and from the same sites as the human remains were
that involved population continuity and was mediated by
used as controls and screened for human DNA (contamination) as well as for
culture exchange only appear increasingly unlikely. Interest- putative animal DNA (preservation). The material was extracted in dupli-
ingly, however, the data analyses are consistent with a view cates via a silica spin-column method including chemical decontamination
that the eastern Baltic area remained a genetic refugia for [14] (Supplemental Data).
some of the European hunter-gatherer populations. This is in Quantitative real-time PCR of an 80 bp and a 136 bp coding-region fragment
agreement with findings of Mesolithic to Neolithic continuity was used to assess the total human mtDNA content in all samples and to
screen for appropriate molecular behavior (degradation [14]) (Supplemental
among Latvian cemeteries [27]. Although the hunter-gatherer
Data, Table S1). We amplified the D-loop in seven overlapping fragments of
lifestyle was culturally replaced here, as in Scandinavia, the varying size and sequenced them on the Roche Genome Sequencer FLX
populations of the eastern Baltic area may have kept a certain System to retrieve synthetic clones. Tagged primers were used to provide
level of population continuity. for individual identification after sequencing [15] (Supplemental Data).
For analyses, we used 316 bp of the D-loop, spanning 16,051–16,383 (16
Experimental Procedures positions were removed, Supplemental Data). Analysis of molecular vari-
ance and Fst calculations was carried out with the Arlequin 3.1 software
Skeletal remains from 74 individuals of eight middle-Neolithic sites were [19]. Networks were constructed with the NETWORK software and the
initially selected. Of these, 41 yielded sequence data, but only 22 (19 PWC reduced median algorithm [16], with the threshold set for 1. Coalescent
Please cite this article in press as: Malmström et al., Ancient DNA Reveals Lack of Continuity between Neolithic Hunter-Gatherers and
Contemporary Scandinavians, Current Biology (2009), doi:10.1016/j.cub.2009.09.017
Current Biology Vol 19 No 20
4
A PWC v Norwegians (FST = 0.06148) B PWC v Swedes (FST = 0.05174) Figure 3. Probabilities of Obtaining the Observed
Genetic Differences, as Measured by FST,
4950
4950
between Ancient PWC and Modern Population
Ne at colonization of Europe 45,000 BP
3962
Population sample comparisons are (A) PWC
hunter-gatherers versus modern Norwegians, (B)
2974
2974
PWC hunter-gatherers versus modern Swedes,
and (C) PWC hunter-gatherers versus modern
1986
1986
Saami. Probabilities were calculated by compar-
ing observed FST values to those obtained by coa-
lescent simulation across a range of combinations
998
998
of ancestral effective female population sizes at
the start of farming in Scandinavia 6,200 years
10
10
ago (x axis) and the initial colonization of Europe
500 4450 8400 12350 16300 20250 500 4450 8400 12350 16300 20250 45,000 years ago (y axis). Observed FST values
are indicated, and black shaded areas indicate
Ne at onset of LBK 6,200 BP Ne at onset of LBK 6,200 BP
p values > 0.05.
0.05
3962
0.04
2974
0.01
10
0.00
500 4450 8400 12350 16300 20250