Ancient Biomolecules from Deep Ice Cores Reveal a Forested Southern Greenland
- From: Jack Linthicum <jacklinthicum@xxxxxxxxxxxxx>
- Date: Fri, 25 Jul 2008 14:13:36 -0700 (PDT)
Greenland DNA from 3400 years ago matches modern Siberians
"The discovery showed that Greenland was once covered in lush forest—
and helps refine climate models of global warming. He has also just
announced another find from the frozen north: a human hair sample from
Greenland that yielded a complete human genome more than 3,400 years
old. The DNA matches modern Siberians but not the Inuit who live in
Greenland today, suggesting that the wrinkled prehistory of the
Americas has yet to be fully ironed out."
Tables at the cite
http://www.sciencemag.org/cgi/content/full/317/5834/111
How Did People Reach the Americas?
Ancient DNA sheds light on the prehistoric humans who colonized a
hemisphere
By Andrew Curry
Posted July 24, 2008
After years of spirited debate over how and when people first reached
the Americas, scientists finally seem poised to reach agreement. The
emerging consensus: In contrast to what was long held as conventional
wisdom, it now seems likely that the first Americans did not wait for
ice sheets covering Canada to melt some 13,000 years ago, which would
have allowed them to traipse south over solid ground. Instead, early
nomads might well have traveled by boat or at least along the coast
from Siberia to North America, perhaps navigating arctic waters near
today's Bering Strait. The telltale evidence: ancient DNA from those
early people that's been coaxed, by powerful analytical technology,
into revealing its secret.
Video Channel: Science
Rewriting the prehistory of the Americas is perhaps the most
remarkable discovery—but hardly the only one—so far achieved through
the analysis of ancient DNA. Other new insights about the past are
being drawn from the same emerging scientific discipline. In the past
five years, the double helix has shed light, for example, on the
vanished woolly mammoth, the flightless dodo, and even humanity's long-
lost kin, the Neanderthals. Extracting and testing old DNA, once
considered practically impossible because too little of the stuff
survives the eons intact, are now at the cutting edge of archaeology,
paleontology, and other fields, thanks to new techniques and more
powerful technology.
"Archaeologists are used to stone tools and bones," says Ted Goebel of
Texas A&M. "So for us to be presented with this kind of evidence is
pretty intriguing." DNA, which contains the blueprints for organisms,
degrades over time, breaking down into tiny pieces or disintegrating
entirely. For years, the dearth of intact DNA in ancient samples—a
chunk of mammoth bone, for instance, or a human hair—stymied
researchers who were trying to analyze the material. But now, using a
technique called polymerase chain reaction, or PCR, researchers can
"unzip" minute fragments of surviving DNA and duplicate them millions
of times over, until they have a sample large enough to test. Then, by
comparing differences between the ancient material and modern samples
of known provenance, they can analyze a long-extinct animal's genome.
The resulting data, in some cases, can resolve a long-standing
scientific deadlock. For almost a century, most archaeologists
believed that people arrived in the Americas between 13,000 and 13,500
years ago. The date was based on flint tools first found in Clovis,
N.M., and later all over North America. From that evidence,
archaeologists sketched out a scenario in which fur-clad "Clovis"
hunters chased mammoths and other prey from Siberia to North America
across a land bridge exposed by low sea levels. Then, the theory goes,
they hunted along a path from Alaska down through Central America and
all the way to Chile in just a few centuries.
Before Clovis. But the notion that Clovis came first has collapsed in
the face of recent evidence, including DNA that pushes the arrival of
the first humans in the Americas back at least 1,000 years, centuries
before the ice that covered northern Canada at the time had melted
enough to allow migration. Instead, some argue, the first Americans
must have arrived by boat, skirting the coast from Siberia and sailing
south along the American coast.
University of Oregon archaeologist Dennis Jenkins discovered the
critical new evidence buried more than 4 feet below the floor of a
dusty cave near Paisley, Ore. The "artifacts" were 14,300-year-old
fossilized pieces of excrement, or coprolites. Jenkins, who has been
digging in Oregon's high desert for decades, handed off bits of
coprolite to geneticist Eske Willerslev of the University of
Copenhagen. In Willerslev's laboratory, PCR pulled enough DNA from the
ancient poop to prove it was human and even genetically link it to
modern American Indians.
Announced in April in the journal Science, the find backs up evidence
previously found at the other end of the Americas, at a site in Chile
called Monte Verde. There, a full-fledged campsite was radiocarbon
dated to 14,500 years ago, putting people in South America more than a
millennium before those Clovis hunters supposedly crossed the Bering
Strait. But carbon dating is inexact, and the Monte Verde find had not
convinced some skeptics. With DNA analysis, says Jenkins, "we can
directly date the item and verify it's human." The Oregon find has
largely silenced the last few Clovis adherents. "It's pretty
compelling stuff," says Goebel, a longtime Clovis supporter.
The success of ancient DNA analysis is likely to open up valuable new
sources of archaeological information in the United States. Coprolites—
stored in the thousands in museums all over the country—may yield
answers from the distant past without infringing on American Indian
beliefs about the sanctity of burial remains.
The technique has promise—and a quickly growing track record—in other
arenas, as well. In 2002, Penn State researcher Beth Shapiro, then at
the University of Oxford, successfully sequenced the DNA of the dodo
bird, extinct for more than three centuries—and discovered it was a
close relative of the pigeon. In 2006, Hendrik Poinar, a geneticist at
McMaster University in Canada, sequenced most of a woolly mammoth's
genome from fragments of bone, proving—at least in theory—that cloning
one might be possible. And a lab in Germany has been researching the
genetics of Neanderthals to see how closely they were related to
modern humans—and if the two species interbred.
Willerslev, meanwhile, is probing other genetic remains for further
discoveries. Last summer, he announced the recovery of the oldest
intact DNA ever found. It came from a soup of plants and animals, now
buried under a mile of Greenland glacier, that made up a forest at
least 450,000 years ago. The discovery showed that Greenland was once
covered in lush forest—and helps refine climate models of global
warming. He has also just announced another find from the frozen
north: a human hair sample from Greenland that yielded a complete
human genome more than 3,400 years old. The DNA matches modern
Siberians but not the Inuit who live in Greenland today, suggesting
that the wrinkled prehistory of the Americas has yet to be fully
ironed out. Now, Willerslev is planning a trip back to Greenland to
hunt for more ancient DNA. With traditional archaeology in one hand
and cutting-edge genetic techniques in the other, he may soon have
more to tell us about the Americas' earliest immigrants.
http://www.usnews.com/articles/science/2008/07/24/how-did-people-reach-the-americas.html?PageNr=2
Paper
Science 6 July 2007:
Vol. 317. no. 5834, pp. 111 - 114
DOI: 10.1126/science.1141758
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Reports
Ancient Biomolecules from Deep Ice Cores Reveal a Forested Southern
Greenland
Eske Willerslev,1* Enrico Cappellini,2 Wouter Boomsma,3 Rasmus Nielsen,
4 Martin B. Hebsgaard,1 Tina B. Brand,1 Michael Hofreiter,5 Michael
Bunce,6,7 Hendrik N. Poinar,7 Dorthe Dahl-Jensen,8 Sigfus Johnsen,8
Jørgen Peder Steffensen,8 Ole Bennike,9 Jean-Luc Schwenninger,10 Roger
Nathan,10 Simon Armitage,11 Cees-Jan de Hoog,12 Vasily Alfimov,13
Marcus Christl,13 Juerg Beer,14 Raimund Muscheler,15 Joel Barker,16
Martin Sharp,16 Kirsty E. H. Penkman,2 James Haile,17 Pierre Taberlet,
18 M. Thomas P. Gilbert,1 Antonella Casoli,19 Elisa Campani,19 Matthew
J. Collins2
It is difficult to obtain fossil data from the 10% of Earth's
terrestrial surface that is covered by thick glaciers and ice sheets,
and hence, knowledge of the paleoenvironments of these regions has
remained limited. We show that DNA and amino acids from buried
organisms can be recovered from the basal sections of deep ice cores,
enabling reconstructions of past flora and fauna. We show that high-
altitude southern Greenland, currently lying below more than 2
kilometers of ice, was inhabited by a diverse array of conifer trees
and insects within the past million years. The results provide direct
evidence in support of a forested southern Greenland and suggest that
many deep ice cores may contain genetic records of paleoenvironments
in their basal sections.
1 Centre for Ancient Genetics, University of Copenhagen, Denmark.
2 BioArch, Departments of Biology and Archaeology, University of York,
UK.
3 Bioinformatics Centre, University of Copenhagen, Denmark.
4 Centre for Comparative Genomics, University of Copenhagen, Denmark.
5 Max Planck Institute for Evolutionary Anthropology, Germany.
6 Murdoch University Ancient DNA Research Laboratory, Murdoch
University, Australia.
7 McMaster Ancient DNA Center, McMaster University, Canada.
8 Ice and Climate, University of Copenhagen, Denmark.
9 Geological Survey of Denmark and Greenland, Denmark.
10 Research Laboratory for Archaeology and the History of Art,
University of Oxford, UK.
11 Department of Geography, Royal Holloway, University of London, UK.
12 Department of Earth Sciences, University of Oxford, UK.
13 Paul Scherrer Institut (PSI)/Eidgenössische Technische Hochschule
(ETH) Laboratory for Ion Beam Physics, Institute for Particle Physics,
ETH Zurich, Switzerland.
14 Swiss Federal Institute of Aquatic Science and Technology (EAWAG),
Switzerland.
15 GeoBiosphere Science Center, Lund University, Sweden.
16 Department of Earth and Atmospheric Sciences, University of
Alberta, Canada.
17 Ancient Biomolecules Centre, Oxford University, UK.
18 Laboratoire d'Ecologie Alpine, CNRS Unité Mixte de Recherche 5553,
Université Joseph Fourier, Boîte Postale 53, 38041 Grenoble Cedex 9,
France.
19 Dipartimento di Chimica Generale e Inorganica, Università di Parma,
Italy.
* To whom correspondence should be addressed. E-mail:
ewillerslev@xxxxxxxx
The environmental histories of high-latitude regions such as Greenland
and Antarctica are poorly understood because much of the fossil
evidence is hidden below kilometer-thick ice sheets (1–3). We test the
idea that the basal sections of deep ice cores can act as archives for
ancient biomolecules.
The samples studied come from the basal impurity-rich (silty) ice
sections of the 2-km-long Dye 3 core from south-central Greenland (4),
the 3-km-long Greenland Ice Core Project (GRIP) core from the summit
of the Greenland ice sheet (5), and the Late Holocene John Evans
Glacier on Ellesmere Island, Nunavut, northern Canada (Fig. 1). The
last-mentioned sample was included as a control to test for potential
exotic DNA because the glacier has recently overridden a land surface
with a known vegetation cover (6). As an additional test for long-
distance atmospheric dispersal of DNA, we included five control
samples of debris-free Holocene and Pleistocene ice taken just above
the basal silty samples from the Dye 3 and GRIP ice cores (Fig. 1B).
Finally, our analyses included sediment samples from the Kap København
Formation from the northernmost part of Greenland, dated to 2.4
million years before the present (Ma yr B.P.) (1, 2).
Figure 1 Fig. 1. Sample location and core schematics. (A) Map showing
the locations of the Dye 3 (65°11'N, 45°50'W) and GRIP (72°34'N,
37°37'W) drilling sites and the Kap København Formation (82°22'N,
W21°14'W) in Greenland as well as the John Evans Glacier (JEG)
(79°49'N, 74°30'W) on Ellesmere Island (Canada). The inset shows the
ratio of D– to L–aspartic acid, a measure of the extent of protein
degradation; more highly degraded samples (above the line) failed to
yield amplifiable DNA. (B) Schematic drawing of ice core/icecap cross
section, with depth [recorded in meters below the surface (m.b.s.)]
indicating the depth of the cores and the positions of the Dye 3,
GRIP, and JEG samples analyzed for DNA, DNA/amino acid racemization/
luminescence (underlined), and 10Be/36Cl (italic). The control GRIP
samples are not shown. The lengths (in meters) of the silty sections
are also shown. [View Larger Version of this Image (66K GIF file)]
The silty ice yielded only a few pollen grains and no macrofossils
(7). However, the Dye 3 and John Evans Glacier silty ice samples
showed low levels of amino acid racemization (Fig. 1A, inset),
indicating good organic matter preservation (8). Therefore, after
previous success with permafrost and cave sediments (9–11), we
attempted to amplify ancient DNA from the ice. This was done following
strict criteria to secure authenticity (12–14), including covering the
surface of the frozen cores with plasmid DNA to control for potential
contamination that may have entered the interior of the samples
through cracks or during the sampling procedure (7). Polymerase chain
reaction (PCR) products of the plasmid DNA were obtained only from
extracts of the outer ice scrapings but not from the interior,
confirming that sample contamination had not penetrated the cores.
Using PCR, we could reproducibly amplify short amplicons [59 to 120
base pairs (bp)] of the chloroplast DNA (cpDNA) rbcLgeneand trnL
intron from ~50 g of the interior ice melts from the Dye 3 and the
John Evans Glacier silty samples. From Dye 3, we also obtained 97-bp
amplicons of invertebrate cytochrome oxidase subunit I (COI)
mitochondrial DNA (mtDNA). Attempts to reproducibly amplify DNA from
the GRIP silty ice and from the Kap København Formation sediments were
not successful. These results are consistent with the amino acid
racemization data demonstrating superior preservation of biomolecules
in the Dye 3 and John Evans Glacier silty samples, which is likely
because these samples are colder (Dye 3) or younger (John Evans
Glacier) than the GRIP sample (Fig. 1A, inset). We also failed to
amplify DNA from the five control samples of Holocene and Pleistocene
ice taken just above the silty samples from the Dye 3 and GRIP ice
cores (volumes: 100 g to 4 kg; Fig. 1B) (7). None of the samples
studied yielded putative sequences of vertebrate mtDNA.
A previous study has shown that simple comparisons of short DNA
sequences to GenBank sequences by means of the Basic Local Alignment
Search Tool (BLAST) make misidentification likely (15). Therefore, we
assigned the obtained sequences to the taxonomic levels of order,
family, or genus using a new rigorous statistical approach (7). In
brief, this Bayesian method calculates the probability that each
sequence belongs to a particular clade by considering its position in
a phylogenetic tree based on similar GenBank sequences. In the
calculation of these probabilities, uncertainties regarding phylogeny,
models of evolution, and missing data are taken into account.
Sequences with >90% posterior probability of membership to a taxonomic
group were assigned to that group. Additionally, a given plant taxon
was only considered genuine if sequences assigned to that taxon were
found to be reproducibly obtained in separate analyses (by independent
laboratories for the Dye 3 sample and within the laboratory for the
John Evans Glacier control sample). This strict criterion of
authenticity obviously dismisses many putative taxa that are present
at low abundance or have heterogeneous distributions, as is typical of
environmental samples (16), but efficiently minimizes the influence of
possible low-level contamination and misidentifications due to DNA
damage (17).
Approximately 31% of the sequences from the John Evans Glacier silty
sample were assigned to plant taxa that passed the authentication and
identification criteria. These belong to the order Rosales, the family
Salicaceae, and the genus Saxifraga (Table 1). This result is
consistent with the John Evans Glacier forming no more than a few
thousand years ago in a high Arctic environment (18), characterized by
low plant diversity and sparse vegetation cover similar to that
currently surrounding the glacier, which consists mainly of Arctic
willow (Salicaceae), purple saxifrage (Saxifraga), Dryas (Rosales),
and Arctic poppy (Papaver) (19). Thus, by confirming the expected
result, the John Evans Glacier study can be regarded as a positive
control, showing that DNA data from silty ice reliably record the
local ecology.
View this table:
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Table 1. Plant and insect taxa obtained from the JEG and Dye 3
silty ice samples. For each taxon (assigned to order, family, or genus
level), the genetic markers (rbcL, trnL, or COI), the number of clone
sequences supporting the identification, and the probability support
(in percentage) are shown. Sequences have been deposited in GenBank
under accession numbers EF588917 to EF588969, except for seven
sequences less than 50 bp in size that are shown below. Their taxon
identifications are indicated by symbols.
In contrast to the John Evans Glacier silty sample, the 45% of the Dye
3 DNA sequences that could be assigned to taxa reveal a community very
different from that of Greenland today. The taxa identified include
trees such as alder (Alnus), spruce (Picea), pine (Pinus), and members
of the yew family (Taxaceae) (Table 1). Their presence indicates a
northern boreal forest ecosystem rather than today's Arctic
environment. The other groups identified, including Asteraceae,
Fabaceae, and Poaceae, are mainly herbaceous plants and are
represented by many species found in northern regions at present
(Table 1). The presence of these herb-dominated families suggests an
open forest where heliophytes thrived. Additionally, we recorded taxa
that are common in present-day Arctic and/or boreal regions but lacked
identity between independent laboratories. These are yarrow
(Achillea), birch (Betula), chickweed (Cerastium), fescue (Festuca),
rush (Luzula), plantain (Plantago), bluegrass (Poa), saxifrage
(Saxifraga), snowberry (Symphoricarpos), and aspen (Populus). Although
not independently authenticated at the sequence level, the presence of
these taxa adds further support to the former existence of a northern
boreal forest ecosystem at Dye 3.
To date, the youngest well-dated fossil evidence of native forest in
Greenland is from macrofossils in the deposits of the Kap København
Formation from the northernmost part of Greenland and dates back to
around 2.4 Ma (1, 2). Other less well dated traces of forests in
Greenland include wood at two other late Cenozoic sites in northern
Greenland (20), pollen spectra of unknown age in marl concretions
found in a late glacial moraine, and wood and spruce seeds in eastern
Greenland (21). The core from Dye 3, located almost exactly 2000 km to
the southwest of the Kap København Formation (Fig. 1A), therefore,
provides direct evidence of a forested southern-central Greenland.
The invertebrate sequences obtained from the Dye 3 silty ice are
related to beetles (Coleoptera), flies (Diptera), spiders (Arachnida),
brush-foots (Nymphalidae), and other butterflies and moths
(Lepidoptera) (taxonomic identification probability support between 50
and 99%). However, only sequences of the Lepidoptera are supported by
more than 90% significance (Table 1). Thus, although detailed
identifications of the COI sequences are in general not strongly
supported, the results show that DNA from a variety of invertebrates
can be obtained from sediments even in the absence of macrofossils, as
was previously shown for plants, mammals, and birds (9–11).
Several observations suggest that the DNA sequences we obtained from
the Dye 3 ice are of local origin and not the result of long-distance
dispersal. The reproducible retrieval of diverse DNA from the silty
basal ice but not from similar or larger volumes of the overlying
"clean" ice largely precludes long-distance atmospheric dispersal of
microfossils as a source of the DNA.
Although pollen grains are found in the Greenland ice sheet, including
the Dye 3 silty ice (7), the concentrations are in general too low
[~15 grains per liter (22, 23)] for them to be present in the sample
volumes studied. Furthermore, long-term survival of DNA in pollen has
proved fairly poor (24), and the vast majority of angiosperm pollen
does not contain cpDNA (25). These factors effectively exclude pollen
as the general source of plant DNA from the silty ice. Moreover, the
Dye 3 silty ice appears to have originated as solid precipitation
without going through stages of superimposed ice and most likely
formed by mixing in the absence of free water (i.e., ice that has
never melted) (26), effectively excluding subsurface transportation.
As explained in (27), the ice is believed to be predominantly of local
origin, having been shielded from participating in the large-scale
glacier flow by a bedrock trough, in agreement with the solid ice–
mixing hypothesis (26). Thus, being of local origin, the DNA sequences
from the Dye 3 silty ice must be derived from the plants and animals
that inhabited this region the last time that it was ice-free, because
possible older DNA records from previous ice-free periods will vanish
with the establishment of a new ecosystem, or at least be out-competed
during PCR by DNA from the most recent record. The plant taxa suggest
that this period had average July temperatures that exceeded 10°C and
winter temperatures not colder than –17°C, which are the limits for
northern boreal forest and Taxus, respectively (1). Allowing for full
recovery of the isostatic depression that is produced by 2 km of ice,
Dye 3 would have been ~1 km above sea level. In combination, these
factors suggest that a high-altitude boreal forest at Dye 3 may date
back to a period considerably warmer than present.
There are no established methods for dating basal ice, and it remains
uncertain whether the overlying clean ice of Dye 3 is temporally
contiguous with the lower silty section. Therefore, to obtain a
tentative age estimate for the Dye 3 silty ice and its forest
community, we applied a series of dating techniques: 10Be/36Cl isotope
ratios, single-grain luminescence measurements, amino acid
racemization coupled with modeling of the basal ice temperature
histories of GRIP and Dye 3, and maximum likelihood estimates for the
branch length of the invertebrate COI sequences (7). All four dating
methods suggest that the Dye 3 silty ice and its forest community
predate the Last Interglacial (LIG) [~130 to 116 thousand years ago
(ka)] (Fig. 2), which contrasts with the results of recent models
suggesting that Dye 3 was ice-free during this period (28, 29).
Indeed, all four dating methods give overlapping dates for the silty
ice between 450 and 800 ka (Fig. 2), exceeding the current record of
long-term DNA survival from Siberian permafrost of 300 to 400 ka (9).
However, because of the many assumptions and uncertainties connected
with the interpretation of the age estimates (7), we cannot rule out
the possibility of a LIG age for the Dye 3 basal ice.
Figure 2 Fig. 2. Summary of dating results for the silty ice from Dye
3. From top to bottom, the bars indicate: maximum likelihood estimates
for the branch length of the invertebrate COI sequences (COI); amino
acid racemization results with the use of alternative activation
energies, models of racemization behavior, and basal temperature
histories (AAR); age estimate from 10Be/36Cl measurements in silty
ice; and minimum ages based on single-grain luminescence results
(optically stimulated luminescence or OSL). The time span covered by
all dating methods (450 to 800 ka) is marked in gray. Stippled lines
represent the results of less likely models. The maximum age estimate
for the invertebrate COI sequences is based on an unlikely slow
substitution rate [for details, see text and (6)]. [View Larger
Version of this Image (23K GIF file)]
Our results reveal that ancient biomolecules from basal ice offer a
means for environmental reconstruction from ice-covered areas and can
yield insights into the climate and the ecology of communities from
the distant past. Because many deep ice cores exist from both
hemispheres and further drillings are planned, this approach may be
used on a larger scale. Basal ice at even lower temperatures than Dye
3 might contain an archive of genetic data of even greater antiquity.
References and Notes
* 1. O. Bennike, Medd. Groenl. Geosci. 23, 85 (1990).
* 2. S. Funder et al., Bull. Geol. Soc. Den. 48, 117 (2001).
* 3. J. E. Francis, R. S. Hill, Palaios 11, 389 (1996).[Abstract/
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* 4. W. Dansgaard et al., Science 218, 1273 (1982).[Abstract/Free
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* 5. W. Dansgaard et al., Nature 364, 218 (1993). [CrossRef]
* 6. L. Copland, M. Sharp, J. Glaciol. 47, 232 (2001). [ISI]
* 7. Materials and methods are available as supporting material on
Science Online.
* 8. M. J. Collins, M. Riley, in Perspectives in Amino Acid and
Protein Geochemistry, G. A. Goodfriend et al., Eds. (Oxford Univ.
Press, New York, 2000), p. 142.
* 9. E. Willerslev et al., Science 300, 791 (2003).[Abstract/Free
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* 10. M. Hofreiter et al., Curr. Biol. 13, R693 (2003). [CrossRef]
[ISI] [Medline]
* 11. J. Haile et al., Mol. Biol. Evol. 24, 982 (2007).[Abstract/
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* 12. E. Willerslev et al., Trends Ecol. Evol. 19, 141 (2004).
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* 13. M. B. Hebsgaard et al., Trends Microbiol. 13, 212 (2005).
[CrossRef] [ISI] [Medline]
* 14. E. Willerslev, A. Cooper, Proc. R. Soc. London Ser. B 272, 3
(2005). [Medline]
* 15. M. Hofreiter et al., Mol. Ecol. 9, 1975 (2000). [CrossRef]
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* 18. W. Blake Jr., Radiocarbon 31, 570 (1989).
* 19. B. A. Bergsma et al., Arctic 37, 49 (1984). [ISI]
* 20. O. Bennike, Geol. Greenland Surv. Bull. 186, 29 (2000).
* 21. O. Bennike et al., Palaeogeogr. Palaeoclimatol. Palaeoecol.
186, 1 (2002). [CrossRef]
* 22. J. C. Bourgeois et al., J. Geophys. Res. 106, 5255 (2001).
[CrossRef]
* 23. J. C. Bourgeois, J. Glaciol. 36, 340 (1990). [ISI]
* 24. L. Parducci et al., Mol. Ecol. 14, 2873 (2005). [CrossRef]
[Medline]
* 25. H. Shi-yi, Acta Bot. Sin. 39, 363 (1997).
* 26. R. A. Souchez et al., Geophys. Res. Lett. 25, 1943 (1998).
[CrossRef] [ISI]
* 27. G. H. Gudmundsson, J. Glaciol. 43, 80 (1997). [ISI]
* 28. J. T. Overpeck et al., Science 311, 1747 (2006).[Abstract/
Free Full Text]
* 29. B. L. Otto-Bliesner et al., Science 311, 1751 (2006).
[Abstract/Free Full Text]
* 30. We thank S. Funder, P. Hartvig, J. C. Bourgeois, O. Seberg,
J. J. Böcher, K. Høegh, J.W. Leverenz, and S.Y.W. Hofor helpful
discussions and R. Bailey, N. Belshaw, N. Charnley, C. Doherty, and D.
Peat for technical assistance and advice. E.W., T.B.B., and M.B.H.
were supported by the Carlsberg Foundation, Denmark, and NSF. E.W. and
K.E.H.P. were both supported by Wellcome Trust Bioarchaeology
Fellowships. The Natural Environment Research Council supported
K.E.H.P. and M.J.C. E.C. received a Marie Curie Intra European
Fellowship (grant number 501340). E.W. and M.C. acknowledge support
from the European Union (MEST-CT-2004-007909). M.B. and H.N.P. were
supported by the Natural Sciences and Engineering Research Council of
Canada (NSERC) (grant number 299103-2004) and McMaster University.
M.S. and J.B. were supported by NSERC and the Polar Continental Shelf
Project. M.H. was supported by the Max Planck Society. J.B. was
supported by the Swiss National Science Foundation.
Supporting Online Material
www.sciencemag.org/cgi/content/full/317/5834/111/DC1
Materials and Methods
Figs. S1 to S8
Tables S1 to S8
References
Received for publication 26 February 2007. Accepted for publication 11
May 2007.
http://www.sciencemag.org/cgi/content/full/317/5834/111
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