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Age estimates for hominin fossils and the onset of the Upper Palaeolithic at Denisova Cave

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Bayesian modelling of chronometric, stratigraphic and genetic data from Denisova Cave provides a chronological framework for understanding Neanderthal and Denisovan presence at the site, as well as interactions between these groups.
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LETTER https://doi.org/10.1038/s41586-018-0870-z
Age estimates for hominin fossils and the onset of
the Upper Palaeolithic at Denisova Cave
Katerina Douka1,2*, Viviane Slon3, Zenobia Jacobs4,5, Christopher Bronk Ramsey2, Michael V. Shunkov6,7,
Anatoly P. Derevianko6,8, Fabrizio Mafessoni3, Maxim B. Kozlikin6, Bo Li4,5, Rainer Grün9, Daniel Comeskey2, Thibaut Devièse2,
Samantha Brown1, Bence Viola10, Leslie Kinsley11, Michael Buckley12, Matthias Meyer3, Richard G. Roberts4,5, Svante Pääbo3,
Janet Kelso3 & Tom Higham2*
Denisova Cave in the Siberian Altai (Russia) is a key site for
understanding the complex relationships between hominin
groups that inhabited Eurasia in the Middle and Late Pleistocene
epoch. DNA sequenced from human remains found at this
site has revealed the presence of a hitherto unknown hominin
group, the Denisovans1,2, and high-coverage genomes from
both Neanderthal and Denisovan fossils provide evidence for
admixture between these two populations
3
. Determining the age
of these fossils is important if we are to understand the nature of
hominin interaction, and aspects of their cultural and subsistence
adaptations. Here we present 50 radiocarbon determinations
from the late Middle and Upper Palaeolithic layers of the site.
We also report three direct dates for hominin fragments and
obtain a mitochondrial DNA sequence for one of them. We apply
a Bayesian age modelling approach that combines chronometric
(radiocarbon, uranium series and optical ages), stratigraphic and
genetic data to calculate probabilistically the age of the human
fossils at the site. Our modelled estimate for the age of theoldest
Denisovan fossil suggests that this group was present at the site as
early as 195,000years ago (at 95.4% probability). All Neanderthal
fossils—as well as Denisova11, the daughter of a Neanderthal
and a Denisovan4—date to between 80,000 and 140,000years ago.
The youngest Denisovan dates to 52,000–76,000years ago. Direct
radiocarbon dating of Upper Palaeolithic tooth pendants and bone
points yielded the earliest evidence for the production of these
artefacts in northern Eurasia, between43,000and49,000calibrated
years before present (taken as 1950). On the basis of current
archaeological evidence, it may be assumed that these artefacts
are associated with the Denisovan population. It is not currently
possible to determine whether anatomically modern humans
were involved in their production, as modern-human fossil and
genetic evidence of such antiquity has not yet been identified in
the Altai region.
Denisova Cave preserves the longest and most notable Palaeolithic
sequence in northern Asia. It consists of three chambers: Main
Chamber, East Chamber and South Chamber (Supplementary
Information, section1). Excavations at the site have so far yielded the
remains of 12 hominins (Extended Data Fig.1 and Supplementary
Information, section3); most of these remains are small and highly
fragmentary. Despite this, the preservation of DNA in some of these
remains is very good and has enabled genome-wide data to be obtained
from both Neanderthal and Denisovan human remains, as well as from
cave sediments, enabling comparisons to be madebetween the two
hominingroups1–8.
The chronology of the site and the age of the recovered human
remains are key unresolved issues. Previous attempts at building a
chronology at Denisova Cave have used radiocarbon dating in the
uppermost sections, and thermoluminescence dating in the older
layers9. More recently, radiocarbon dating from the uppermost
Pleistocene layers in East Chamber revealed some age variations, which
were ascribed to taphonomic mixing and carnivore bioturbation2.
A set of optical ages
10
has been obtained from Pleistocene sedimentary
layers in all three chambers.
Here we report 50 radiocarbon determinations from 40 samples,
collected from the upper parts of the Pleistocene sequence (layers
9–12) in Main Chamber and East Chamber (Fig.1 and Extended Data
Table1). A further 23 samples were processed but did not yield suffi-
cient carbon for dating (Supplementary Information, section2). We
selected samples of charcoal, and humanly modified bone and arte-
facts (Extended Data Fig.2 and Supplementary Information, section2)
from locations that were deemed during excavation to be undisturbed.
Where possible, the samples were prepared using robust decontamina-
tion protocols, including collagen ultrafiltration and single amino acid
extraction of hydroxyproline from bones and teeth, and acid-base-wet
oxidation stepped-combustion (ABOx-SC) or acid-wet oxidation
stepped-combustion (AOx-SC) for charcoal (Supplementary
Information, section2).
All samples from layers 11.3, 11.4 and 12 in East Chamber, as well
as the directly dated Denisova11 bone11, pre-date the radiocarbon
age limit. In layer 11.2, we found two age clusters: three samples
have infinite ages, and three samples have finite calibrated ages
(Extended Data Table1). A horse tooth from layer 9.2 gave a result of
45,720–50,000calibrated years before present (cal. years ) (Oxford
radiocarbon laboratory code OxA-29859). This date is statistically
indistinguishable from the group of finite dates (treated with ultrafil-
tration and ABOx) from layer 11.2.
In Main Chamber, our radiocarbon ages reveal a depositional hiatus
between layers 12 and 11.4. Samples from layer 12 (at the end of the
Middle Palaeolithic) all gave infinite radiocarbon ages compared to
samples from layer 11.4, which date to between approximately 35,000
and 40,000cal. years  (Fig.1).
Four pendants made from red deer (Cervus elaphus) and elk (Alces
alces) teeth—which are often associated with Upper Palaeolithic
technocomplexes—provided results of ~32,000, ~40,000 and ~45,000cal.
years  (Fig.1 and Extended Data Fig.2). The oldest of these dates
(OxA-30963) is corroborated by a charcoal date (OxA-31506)
from the same stratigraphic location and year of excavation, and is
the earliest direct date for an artefact of this type in northern Eurasia.
1Department of Archaeology, Max Planck Institute for the Science of Human History, Jena, Germany. 2Oxford Radiocarbon Accelerator Unit, Research Laboratory for Archaeology and the History
of Art, University of Oxford, Oxford, UK. 3Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany. 4Centre for Archaeological Science, School
of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, New South Wales, Australia. 5Australian Research Council (ARC) Centre of Excellence for Australian Biodiversity
and Heritage, University of Wollongong, Wollongong, New South Wales, Australia. 6Institute of Archaeology and Ethnography, Russian Academy of Sciences Siberian Branch, Novosibirsk, Russia.
7Novosibirsk State University, Novosibirsk, Russia. 8Altai State University, Barnaul, Russia. 9Australian Research Centre for Human Evolution, Griffith University, Brisbane, Queensland, Australia.
10Department of Anthropology, University of Toronto, Toronto, Ontario, Canada. 11Research School of Earth Sciences, The Australian National University, Canberra, Australian Capital Territory,
Australia. 12Manchester Institute of Biotechnology, University of Manchester, Manchester, UK. *e-mail: douka@shh.mpg.de; thomas.higham@rlaha.ox.ac.uk
640 | NATURE | VOL 565 | 31 JANUARY 2019
© 2019 Springer Nature Limited. All rights reserved.
... -Denisova 15 is a bone splinter identified as Neanderthal by collagen peptide mass fingerprinting (Douka et al., 2019). ...
... More recently, a radiocarbon dating campaign of Denisova has yielded three dates for the Central chamber: one for layer 11.1, at 37.5 ± 1 ka BP (OxA-29861) and two for layer 11.4, 42.9 ± 2 ka BP (OxA-29872) and 41.2 ± 1.4 ka BP (OxA-30271; manufactured bone point) (Douka et al., 2015). This dating campaign was completed in 2016 and 2017 with the addition of 63 dating samples in both the Central chamber and the Eastern gallery (Douka et al., 2019). ...
... Layer 9, which material is clearly Upper Palaeolithic, yielded a surprisingly old date at 43-47 ka BP or 45-49 ka cal BP (Douka et al., 2015). This date has been recently confirmed by the radiocarbon dating of a second bone 5 at 46,300 ± 2,600 BP (OxA-36011; Douka et al., 2019). ...
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... Besides microbial degradation, the protein concentrations decrease with weathering and fossilization (Rapp Py-Daniel 2014). Therefore, the oldest bones suitable for stable isotope ratios of collagen are often found in cool environments where there was a relatively rapid burial, such as in the Denisova Cave in the Siberian Altai, where the oldest hominin collagen containing bone has been estimated to date to 195,000 years ago (Douka et al. 2019). For bones, collagen yields (more than 1%) and quality indices such as atomic carbon to nitrogen ratios (2.9-3.5) and percentage nitrogen content (more than 0.5%) are the most important preservation criteria (Ambrose 1990, Brock et al. 2012). ...
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... Denisovans are a group of archaic Homo, most closely related to Neanderthals but known only from a few scattered fossils and a range of genetic data collected from the fossils, cave sediments and modern day human populations (Reich et al., 2010(Reich et al., , 2011Slon et al., 2017aSlon et al., ,b, 2018Douka et al., 2019). Denisovans may have been widespread across Asia, potentially forming distinct populations with little inter-group contact (Pääbo, 2014(Pääbo, , 2015Kuhlwilm et al., 2016). ...
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... Sequencing results for such fossils allow us to analyze them at the genome level. The Neandertals were recognized as a distinct group of hominids with numerous fossils as well as stone tool assemblages (Krings et al., 1997;Heyes et al., 2016;Douka et al., 2019). Nevertheless, few fossils of the Denisovans, another distinct member of the Homo genus, have been found. ...
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The population history of Aboriginal Australians remains largely uncharacterized. Here we generate high-coverage genomes for 83 Aboriginal Australians (speakers of Pama-Nyungan languages) and 25 Papuans from the New Guinea Highlands. We find that Papuan and Aboriginal Australian ancestors diversified 25-40 thousand years ago (kya), suggesting pre-Holocene population structure in the ancient continent of Sahul (Australia, New Guinea and Tasmania). However, all of the studied Aboriginal Australians descend from a single founding population that differentiated ∼10-32 kya. We infer a population expansion in northeast Australia during the Holocene epoch (past 10,000 years) associated with limited gene flow from this region to the rest of Australia, consistent with the spread of the Pama-Nyungan languages. We estimate that Aboriginal Australians and Papuans diverged from Eurasians 51-72 kya, following a single out-of-Africa dispersal, and subsequently admixed with archaic populations. Finally, we report evidence of selection in Aboriginal Australians potentially associated with living in the desert. © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved
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If radiocarbon measurements are to be used at all for chronological purposes, we have to use statistical methods for calibration. The most widely used method of calibration can be seen as a simple application of Bayesian statistics, which uses both the information from the new measurement and information from the 14 C calibration curve. In most dating applications, however, we have larger numbers of 14 C measurements and we wish to relate those to events in the past. Bayesian statistics provides a coherent framework in which such analysis can be performed and is becoming a core element in many 14 C dating projects. This article gives an overview of the main model components used in chronological analysis, their mathematical formulation, and examples of how such analyses can be performed using the latest version of the OxCal software (v4). Many such models can be put together, in a modular fashion, from simple elements, with defined constraints and groupings. In other cases, the commonly used “uniform phase” models might not be appropriate, and ramped, exponential, or normal distributions of events might be more useful. When considering analyses of these kinds, it is useful to be able run simulations on synthetic data. Methods for performing such tests are discussed here along with other methods of diagnosing possible problems with statistical models of this kind.