Publications by authors named "Christina Warinner"

53 Publications

The genomic origins of the Bronze Age Tarim Basin mummies.

Nature 2021 11 27;599(7884):256-261. Epub 2021 Oct 27.

Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Beijing, China.

The identity of the earliest inhabitants of Xinjiang, in the heart of Inner Asia, and the languages that they spoke have long been debated and remain contentious. Here we present genomic data from 5 individuals dating to around 3000-2800 BC from the Dzungarian Basin and 13 individuals dating to around 2100-1700 BC from the Tarim Basin, representing the earliest yet discovered human remains from North and South Xinjiang, respectively. We find that the Early Bronze Age Dzungarian individuals exhibit a predominantly Afanasievo ancestry with an additional local contribution, and the Early-Middle Bronze Age Tarim individuals contain only a local ancestry. The Tarim individuals from the site of Xiaohe further exhibit strong evidence of milk proteins in their dental calculus, indicating a reliance on dairy pastoralism at the site since its founding. Our results do not support previous hypotheses for the origin of the Tarim mummies, who were argued to be Proto-Tocharian-speaking pastoralists descended from the Afanasievo or to have originated among the Bactria-Margiana Archaeological Complex or Inner Asian Mountain Corridor cultures. Instead, although Tocharian may have been plausibly introduced to the Dzungarian Basin by Afanasievo migrants during the Early Bronze Age, we find that the earliest Tarim Basin cultures appear to have arisen from a genetically isolated local population that adopted neighbouring pastoralist and agriculturalist practices, which allowed them to settle and thrive along the shifting riverine oases of the Taklamakan Desert.
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http://dx.doi.org/10.1038/s41586-021-04052-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8580821PMC
November 2021

Ethics of DNA research on human remains: five globally applicable guidelines.

Nature 2021 11 20;599(7883):41-46. Epub 2021 Oct 20.

Department of Genetics, Harvard Medical School, Boston, MA, USA.

We are a group of archaeologists, anthropologists, curators and geneticists representing diverse global communities and 31 countries. All of us met in a virtual workshop dedicated to ethics in ancient DNA research held in November 2020. There was widespread agreement that globally applicable ethical guidelines are needed, but that recent recommendations grounded in discussion about research on human remains from North America are not always generalizable worldwide. Here we propose the following globally applicable guidelines, taking into consideration diverse contexts. These hold that: (1) researchers must ensure that all regulations were followed in the places where they work and from which the human remains derived; (2) researchers must prepare a detailed plan prior to beginning any study; (3) researchers must minimize damage to human remains; (4) researchers must ensure that data are made available following publication to allow critical re-examination of scientific findings; and (5) researchers must engage with other stakeholders from the beginning of a study and ensure respect and sensitivity to stakeholder perspectives. We commit to adhering to these guidelines and expect they will promote a high ethical standard in DNA research on human remains going forward.
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http://dx.doi.org/10.1038/s41586-021-04008-xDOI Listing
November 2021

Reply to Ben-Dor et al.: Oral bacteria of Neanderthals and modern humans exhibit evidence of starch adaptation.

Proc Natl Acad Sci U S A 2021 09;118(37)

Department of Archaeogenetics, Max Planck Institute of Evolutionary Anthropology, Leipzig 04103, Germany.

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http://dx.doi.org/10.1073/pnas.2112526118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8449415PMC
September 2021

PyDamage: automated ancient damage identification and estimation for contigs in ancient DNA assembly.

PeerJ 2021 27;9:e11845. Epub 2021 Jul 27.

Microbiome Sciences Group, Max Planck Institute for the Science of Human History, Department of Archaeogenetics, Jena, Germany.

DNA assembly can be used to reconstruct longer stretches of DNA (contigs), including genes and even genomes, from short DNA sequencing reads. Applying this technique to metagenomic data derived from archaeological remains, such as paleofeces and dental calculus, we can investigate past microbiome functional diversity that may be absent or underrepresented in the modern microbiome gene catalogue. However, compared to modern samples, ancient samples are often burdened with environmental contamination, resulting in metagenomic datasets that represent mixtures of ancient and modern DNA. The ability to rapidly and reliably establish the authenticity and integrity of ancient samples is essential for ancient DNA studies, and the ability to distinguish between ancient and modern sequences is particularly important for ancient microbiome studies. Characteristic patterns of ancient DNA damage, namely DNA fragmentation and cytosine deamination (observed as C-to-T transitions) are typically used to authenticate ancient samples and sequences, but existing tools for inspecting and filtering aDNA damage either compute it at the read level, which leads to high data loss and lower quality when used in combination with assembly, or require manual inspection, which is impractical for ancient assemblies that typically contain tens to hundreds of thousands of contigs. To address these challenges, we designed PyDamage, a robust, automated approach for aDNA damage estimation and authentication of assembled aDNA. PyDamage uses a likelihood ratio based approach to discriminate between truly ancient contigs and contigs originating from modern contamination. We test PyDamage on both on simulated aDNA data and archaeological paleofeces, and we demonstrate its ability to reliably and automatically identify contigs bearing DNA damage characteristic of aDNA. Coupled with aDNA assembly, Pydamage opens up new doors to explore functional diversity in ancient metagenomic datasets.
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http://dx.doi.org/10.7717/peerj.11845DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8323603PMC
July 2021

Shifts in gut and vaginal microbiomes are associated with cancer recurrence time in women with ovarian cancer.

PeerJ 2021 17;9:e11574. Epub 2021 Jun 17.

Department of Anthropology, University of Oklahoma, Norman, Oklahoma, United States.

Many studies investigating the human microbiome-cancer interface have focused on the gut microbiome and gastrointestinal cancers. Outside of human papillomavirus driving cervical cancer, little is known about the relationship between the vaginal microbiome and other gynecological cancers, such as ovarian cancer. In this retrospective study, we investigated the relationship between ovarian cancer, platinum-free interval (PFI) length, and vaginal and gut microbiomes. We observed that -dominated vaginal communities were less common in women with ovarian cancer, as compared to existing datasets of similarly aged women without cancer. Primary platinum-resistance (PPR) disease is strongly associated with survivability under one year, and we found over one-third of patients with PPR (PFI < 6 months, = 17) to have a vaginal microbiome dominated by (>20% relative abundance), while only one platinum super-sensitive (PFI > 24 months, = 23) patient had an -dominated microbiome. Additionally, was associated with little, or no, gross residual disease, while other species were dominant in women with >1 cm gross residual disease. In the gut microbiome, we found patients with PPR disease to have lower phylogenetic diversity than platinum-sensitive patients. The trends we observe in women with ovarian cancer and PPR disease, such as the absence of and presence of in the vaginal microbiome as well as low gut microbiome phylogenetic diversity have all been linked to other diseases and/or pro-inflammatory states, including bacterial vaginosis and autoimmune disorders. Future prospective studies are necessary to explore the translational potential and underlying mechanisms driving these associations.
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http://dx.doi.org/10.7717/peerj.11574DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8214851PMC
June 2021

Reconstruction of ancient microbial genomes from the human gut.

Nature 2021 06 12;594(7862):234-239. Epub 2021 May 12.

Section on Pathophysiology and Molecular Pharmacology, Joslin Diabetes Center, Boston, MA, USA.

Loss of gut microbial diversity in industrial populations is associated with chronic diseases, underscoring the importance of studying our ancestral gut microbiome. However, relatively little is known about the composition of pre-industrial gut microbiomes. Here we performed a large-scale de novo assembly of microbial genomes from palaeofaeces. From eight authenticated human palaeofaeces samples (1,000-2,000 years old) with well-preserved DNA from southwestern USA and Mexico, we reconstructed 498 medium- and high-quality microbial genomes. Among the 181 genomes with the strongest evidence of being ancient and of human gut origin, 39% represent previously undescribed species-level genome bins. Tip dating suggests an approximate diversification timeline for the key human symbiont Methanobrevibacter smithii. In comparison to 789 present-day human gut microbiome samples from eight countries, the palaeofaeces samples are more similar to non-industrialized than industrialized human gut microbiomes. Functional profiling of the palaeofaeces samples reveals a markedly lower abundance of antibiotic-resistance and mucin-degrading genes, as well as enrichment of mobile genetic elements relative to industrial gut microbiomes. This study facilitates the discovery and characterization of previously undescribed gut microorganisms from ancient microbiomes and the investigation of the evolutionary history of the human gut microbiota through genome reconstruction from palaeofaeces.
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http://dx.doi.org/10.1038/s41586-021-03532-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8189908PMC
June 2021

The evolution and changing ecology of the African hominid oral microbiome.

Proc Natl Acad Sci U S A 2021 05;118(20)

Department of Humanities, University of Ferrara, 44121 Ferrara, Italy.

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent -specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.
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http://dx.doi.org/10.1073/pnas.2021655118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8157933PMC
May 2021

Evidence for early dispersal of domestic sheep into Central Asia.

Nat Hum Behav 2021 09 8;5(9):1169-1179. Epub 2021 Apr 8.

ArchaeoZOOlogy in Siberia and Central Asia - ZooSCAn, CNRS - IAET SB RAS International Research Laboratory, IRL 2013, Institute of Archaeology SB RAS, Novosibirsk, Russia.

The development and dispersal of agropastoralism transformed the cultural and ecological landscapes of the Old World, but little is known about when or how this process first impacted Central Asia. Here, we present archaeological and biomolecular evidence from Obishir V in southern Kyrgyzstan, establishing the presence of domesticated sheep by ca. 6,000 BCE. Zooarchaeological and collagen peptide mass fingerprinting show exploitation of Ovis and Capra, while cementum analysis of intact teeth implicates possible pastoral slaughter during the fall season. Most significantly, ancient DNA reveals these directly dated specimens as the domestic O. aries, within the genetic diversity of domesticated sheep lineages. Together, these results provide the earliest evidence for the use of livestock in the mountains of the Ferghana Valley, predating previous evidence by 3,000 years and suggesting that domestic animal economies reached the mountains of interior Central Asia far earlier than previously recognized.
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http://dx.doi.org/10.1038/s41562-021-01083-yDOI Listing
September 2021

Components of a Neanderthal gut microbiome recovered from fecal sediments from El Salt.

Commun Biol 2021 02 5;4(1):169. Epub 2021 Feb 5.

Unit of Microbiome Science and Biotechnology, Department of Pharmacy and Biotechnology, University of Bologna, Via Belmeloro 6, Bologna, Italy.

A comprehensive view of our evolutionary history cannot ignore the ancestral features of our gut microbiota. To provide some glimpse into the past, we searched for human gut microbiome components in ancient DNA from 14 archeological sediments spanning four stratigraphic units of El Salt Middle Paleolithic site (Spain), including layers of unit X, which has yielded well-preserved Neanderthal occupation deposits dating around 50 kya. According to our findings, bacterial genera belonging to families known to be part of the modern human gut microbiome are abundantly represented only across unit X samples, showing that well-known beneficial gut commensals, such as Blautia, Dorea, Roseburia, Ruminococcus, Faecalibacterium and Bifidobacterium already populated the intestinal microbiome of Homo since as far back as the last common ancestor between humans and Neanderthals.
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http://dx.doi.org/10.1038/s42003-021-01689-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864912PMC
February 2021

Community-curated and standardised metadata of published ancient metagenomic samples with AncientMetagenomeDir.

Sci Data 2021 01 26;8(1):31. Epub 2021 Jan 26.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, 07745, Jena, Germany.

Ancient DNA and RNA are valuable data sources for a wide range of disciplines. Within the field of ancient metagenomics, the number of published genetic datasets has risen dramatically in recent years, and tracking this data for reuse is particularly important for large-scale ecological and evolutionary studies of individual taxa and communities of both microbes and eukaryotes. AncientMetagenomeDir (archived at https://doi.org/10.5281/zenodo.3980833 ) is a collection of annotated metagenomic sample lists derived from published studies that provide basic, standardised metadata and accession numbers to allow rapid data retrieval from online repositories. These tables are community-curated and span multiple sub-disciplines to ensure adequate breadth and consensus in metadata definitions, as well as longevity of the database. Internal guidelines and automated checks facilitate compatibility with established sequence-read archives and term-ontologies, and ensure consistency and interoperability for future meta-analyses. This collection will also assist in standardising metadata reporting for future ancient metagenomic studies.
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http://dx.doi.org/10.1038/s41597-021-00816-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838265PMC
January 2021

Exotic foods reveal contact between South Asia and the Near East during the second millennium BCE.

Proc Natl Acad Sci U S A 2021 01 21;118(2). Epub 2020 Dec 21.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07743 Jena, Germany;

Although the key role of long-distance trade in the transformation of cuisines worldwide has been well-documented since at least the Roman era, the prehistory of the Eurasian food trade is less visible. In order to shed light on the transformation of Eastern Mediterranean cuisines during the Bronze Age and Early Iron Age, we analyzed microremains and proteins preserved in the dental calculus of individuals who lived during the second millennium BCE in the Southern Levant. Our results provide clear evidence for the consumption of expected staple foods, such as cereals (Triticeae), sesame (), and dates (). We additionally report evidence for the consumption of soybean (), probable banana (), and turmeric (), which pushes back the earliest evidence of these foods in the Mediterranean by centuries (turmeric) or even millennia (soybean). We find that, from the early second millennium onwards, at least some people in the Eastern Mediterranean had access to food from distant locations, including South Asia, and such goods were likely consumed as oils, dried fruits, and spices. These insights force us to rethink the complexity and intensity of Indo-Mediterranean trade during the Bronze Age as well as the degree of globalization in early Eastern Mediterranean cuisine.
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http://dx.doi.org/10.1073/pnas.2014956117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7812755PMC
January 2021

Data integration for prediction of weight loss in randomized controlled dietary trials.

Sci Rep 2020 11 18;10(1):20103. Epub 2020 Nov 18.

Department of Health Technology, Technical University of Denmark, Kgs. Lyngby, 2800, Denmark.

Diet is an important component in weight management strategies, but heterogeneous responses to the same diet make it difficult to foresee individual weight-loss outcomes. Omics-based technologies now allow for analysis of multiple factors for weight loss prediction at the individual level. Here, we classify weight loss responders (N = 106) and non-responders (N = 97) of overweight non-diabetic middle-aged Danes to two earlier reported dietary trials over 8 weeks. Random forest models integrated gut microbiome, host genetics, urine metabolome, measures of physiology and anthropometrics measured prior to any dietary intervention to identify individual predisposing features of weight loss in combination with diet. The most predictive models for weight loss included features of diet, gut bacterial species and urine metabolites (ROC-AUC: 0.84-0.88) compared to a diet-only model (ROC-AUC: 0.62). A model ensemble integrating multi-omics identified 64% of the non-responders with 80% confidence. Such models will be useful to assist in selecting appropriate weight management strategies, as individual predisposition to diet response varies.
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http://dx.doi.org/10.1038/s41598-020-76097-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7674420PMC
November 2020

A Dynamic 6,000-Year Genetic History of Eurasia's Eastern Steppe.

Cell 2020 11 5;183(4):890-904.e29. Epub 2020 Nov 5.

Department of Archaeology, Max Planck Institute for the Science of Human History, Jena 07745, Germany.

The Eastern Eurasian Steppe was home to historic empires of nomadic pastoralists, including the Xiongnu and the Mongols. However, little is known about the region's population history. Here, we reveal its dynamic genetic history by analyzing new genome-wide data for 214 ancient individuals spanning 6,000 years. We identify a pastoralist expansion into Mongolia ca. 3000 BCE, and by the Late Bronze Age, Mongolian populations were biogeographically structured into three distinct groups, all practicing dairy pastoralism regardless of ancestry. The Xiongnu emerged from the mixing of these populations and those from surrounding regions. By comparison, the Mongols exhibit much higher eastern Eurasian ancestry, resembling present-day Mongolic-speaking populations. Our results illuminate the complex interplay between genetic, sociopolitical, and cultural changes on the Eastern Steppe.
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http://dx.doi.org/10.1016/j.cell.2020.10.015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7664836PMC
November 2020

Genomic History of Neolithic to Bronze Age Anatolia, Northern Levant, and Southern Caucasus.

Cell 2020 05;181(5):1158-1175.e28

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena 07745, Germany. Electronic address:

Here, we report genome-wide data analyses from 110 ancient Near Eastern individuals spanning the Late Neolithic to Late Bronze Age, a period characterized by intense interregional interactions for the Near East. We find that 6 millennium BCE populations of North/Central Anatolia and the Southern Caucasus shared mixed ancestry on a genetic cline that formed during the Neolithic between Western Anatolia and regions in today's Southern Caucasus/Zagros. During the Late Chalcolithic and/or the Early Bronze Age, more than half of the Northern Levantine gene pool was replaced, while in the rest of Anatolia and the Southern Caucasus, we document genetic continuity with only transient gene flow. Additionally, we reveal a genetically distinct individual within the Late Bronze Age Northern Levant. Overall, our study uncovers multiple scales of population dynamics through time, from extensive admixture during the Neolithic period to long-distance mobility within the globalized societies of the Late Bronze Age. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cell.2020.04.044DOI Listing
May 2020

CoproID predicts the source of coprolites and paleofeces using microbiome composition and host DNA content.

PeerJ 2020 17;8:e9001. Epub 2020 Apr 17.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, Germany.

Shotgun metagenomics applied to archaeological feces (paleofeces) can bring new insights into the composition and functions of human and animal gut microbiota from the past. However, paleofeces often undergo physical distortions in archaeological sediments, making their source species difficult to identify on the basis of fecal morphology or microscopic features alone. Here we present a reproducible and scalable pipeline using both host and microbial DNA to infer the host source of fecal material. We apply this pipeline to newly sequenced archaeological specimens and show that we are able to distinguish morphologically similar human and canine paleofeces, as well as non-fecal sediments, from a range of archaeological contexts.
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http://dx.doi.org/10.7717/peerj.9001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7169968PMC
April 2020

Dairy pastoralism sustained eastern Eurasian steppe populations for 5,000 years.

Nat Ecol Evol 2020 03 2;4(3):346-355. Epub 2020 Mar 2.

Department of Archaeology, Max Planck Institute for the Science of Human History, Jena, Germany.

Dairy pastoralism is integral to contemporary and past lifeways on the eastern Eurasian steppe, facilitating survival in agriculturally challenging environments. While previous research has indicated that ruminant dairy pastoralism was practiced in the region by circa 1300 BC, the origin, extent and diversity of this custom remain poorly understood. Here, we analyse ancient proteins from human dental calculus recovered from geographically diverse locations across Mongolia and spanning 5,000 years. We present the earliest evidence for dairy consumption on the eastern Eurasian steppe by circa 3000 BC and the later emergence of horse milking at circa 1200 BC, concurrent with the first evidence for horse riding. We argue that ruminant dairying contributed to the demographic success of Bronze Age Mongolian populations and that the origins of traditional horse dairy products in eastern Eurasia are closely tied to the regional emergence of mounted herding societies during the late second millennium BC.
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http://dx.doi.org/10.1038/s41559-020-1120-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7212056PMC
March 2020

Biogeographic study of human gut-associated crAssphage suggests impacts from industrialization and recent expansion.

PLoS One 2020 15;15(1):e0226930. Epub 2020 Jan 15.

Laboratories of Molecular Anthropology and Microbiome Research, University of Oklahoma, Norman, Oklahoma, United States of America.

CrAssphage (cross-assembly phage) is a bacteriophage that was first discovered in human gut metagenomic data. CrAssphage belongs to a diverse family of crAss-like bacteriophages thought to infect gut commensal bacteria belonging to Bacteroides species. However, not much is known about the biogeography of crAssphage and whether certain strains are associated with specific human populations. In this study, we screened publicly available human gut metagenomic data from 3,341 samples for the presence of crAssphage sensu stricto (NC_024711.1). We found that crAssphage prevalence is low in traditional, hunter-gatherer populations, such as the Hadza from Tanzania and Matses from Peru, as compared to industrialized, urban populations. Statistical comparisons showed no association of crAssphage prevalence with variables such as age, sex, body mass index, and health status of individuals. Phylogenetic analyses show that crAssphage strains reconstructed from the same individual over multiple time-points, cluster together. CrAssphage strains from individuals from the same study population do not always cluster together. Some evidence of clustering is seen at the level of broadly defined geographic regions, however, the relative positions of these clusters within the crAssphage phylogeny are not well-supported. We hypothesize that this lack of strong biogeographic structuring is suggestive of an expansion event within crAssphage. Using a Bayesian dating approach, we estimate that this expansion has occurred fairly recently. Overall, we determine that crAssphage presence is associated with an industrialized lifestyle and the absence of strong biogeographic structuring within global crAssphage strains is likely due to a recent population expansion within this bacteriophage.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0226930PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961876PMC
April 2020

HOPS: automated detection and authentication of pathogen DNA in archaeological remains.

Genome Biol 2019 12 16;20(1):280. Epub 2019 Dec 16.

Max Planck Institute for the Science of Human History, Jena, Germany.

High-throughput DNA sequencing enables large-scale metagenomic analyses of complex biological systems. Such analyses are not restricted to present-day samples and can also be applied to molecular data from archaeological remains. Investigations of ancient microbes can provide valuable information on past bacterial commensals and pathogens, but their molecular detection remains a challenge. Here, we present HOPS (Heuristic Operations for Pathogen Screening), an automated bacterial screening pipeline for ancient DNA sequences that provides detailed information on species identification and authenticity. HOPS is a versatile tool for high-throughput screening of DNA from archaeological material to identify candidates for genome-level analyses.
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http://dx.doi.org/10.1186/s13059-019-1903-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6913047PMC
December 2019

Comparison of extraction methods for recovering ancient microbial DNA from paleofeces.

Am J Phys Anthropol 2020 02 30;171(2):275-284. Epub 2019 Nov 30.

Max Planck Institute for the Science of Human History, Jena, Germany.

Objectives: Paleofeces are valuable to archeologists and evolutionary biologists for their potential to yield health, dietary, and host information. As a rich source of preserved biomolecules from host-associated microorganisms, they can also provide insights into the recent evolution and changing ecology of the gut microbiome. However, there is currently no standard method for DNA extraction from paleofeces, which combine the dual challenges of complex biological composition and degraded DNA. Due to the scarcity and relatively poor preservation of paleofeces when compared with other archeological remains, it is important to use efficient methods that maximize ancient DNA (aDNA) recovery while also minimizing downstream taxonomic biases.

Methods: In this study, we use shotgun metagenomics to systematically compare the performance of five DNA extraction methods on a set of well-preserved human and dog paleofeces from Mexico (~1,300 BP).

Results: Our results show that all tested DNA extraction methods yield a consistent microbial taxonomic profile, but that methods optimized for ancient samples recover significantly more DNA.

Conclusions: These results show promise for future studies that seek to explore the evolution of the human gut microbiome by comparing aDNA data with those generated in modern studies.
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http://dx.doi.org/10.1002/ajpa.23978DOI Listing
February 2020

Relief food subsistence revealed by microparticle and proteomic analyses of dental calculus from victims of the Great Irish Famine.

Proc Natl Acad Sci U S A 2019 09 9;116(39):19380-19385. Epub 2019 Sep 9.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany.

Food and diet were class markers in 19th-century Ireland, which became evident as nearly 1 million people, primarily the poor and destitute, died as a consequence of the notorious Great Famine of 1845 to 1852. Famine took hold after a blight destroyed virtually the only means of subsistence-the potato crop-for a significant proportion of the population. This study seeks to elucidate the variability of diet in mid-19th-century Ireland through microparticle and proteomic analysis of human dental calculus samples ( = 42) from victims of the famine. The samples derive from remains of people who died between August 1847 and March 1851 while receiving poor relief as inmates in the union workhouse in the city of Kilkenny (52°39' N, -7°15' W). The results corroborate the historical accounts of food provisions before and during the famine, with evidence of corn (maize), potato, and cereal starch granules from the microparticle analysis and milk protein from the proteomic analysis. Unexpectedly, there is also evidence of egg protein-a food source generally reserved only for export and the better-off social classes-which highlights the variability of the prefamine experience for those who died. Through historical contextualization, this study shows how the notoriously monotonous potato diet of the poor was opportunistically supplemented by other foodstuffs. While the Great Irish Famine was one of the worst subsistence crises in history, it was foremost a social disaster induced by the lack of access to food and not the lack of food availability.
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http://dx.doi.org/10.1073/pnas.1908839116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6765296PMC
September 2019

"The dead shall be raised": Multidisciplinary analysis of human skeletons reveals complexity in 19th century immigrant socioeconomic history and identity in New Haven, Connecticut.

PLoS One 2019 9;14(9):e0219279. Epub 2019 Sep 9.

Connecticut State Museum of Natural History, University of Connecticut, Storrs, Connecticut, United States of America.

In July 2011, renovations to Yale-New Haven Hospital inadvertently exposed the cemetery of Christ Church, New Haven, Connecticut's first Catholic cemetery. While this cemetery was active between 1833 and 1851, both the church and its cemetery disappeared from public records, making the discovery serendipitous. Four relatively well-preserved adult skeletons were recovered with few artifacts. All four individuals show indicators of manual labor, health and disease stressors, and dental health issues. Two show indicators of trauma, with the possibility of judicial hanging in one individual. Musculoskeletal markings are consistent with physical stress, and two individuals have arthritic indicators of repetitive movement/specialized activities. Radiographic analyses show osteopenia, healed trauma, and other pathologies in several individuals. Dental calculus analysis did not identify any tuberculosis indicators, despite osteological markers. Isotopic analyses of teeth indicate that all four were likely recent immigrants to the Northeastern United States. Nuclear and mitochondrial DNA were recovered from three individuals, and these analyses identified ancestry, hair/eye color, and relatedness. Genetic and isotopic results upended our initial ancestry assessment based on burial context alone. These individuals provide biocultural evidence of New Haven's Industrial Revolution and the plasticity of ethnic and religious identity in the immigrant experience. Their recovery and the multifaceted analyses described here illuminate a previously undescribed part of the city's rich history. The collective expertise of biological, geochemical, archaeological, and historical researchers interprets socioeconomic and cultural identity better than any one could alone. Our combined efforts changed our initial assumptions of a poor urban Catholic cemetery's membership, and provide a template for future discoveries and analyses.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0219279PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6733446PMC
March 2020

Genetic diversity of HLA system in two populations from Oaxaca, Mexico: Oaxaca city and rural Oaxaca.

Hum Immunol 2020 Sep 22;81(9):553-556. Epub 2019 Jul 22.

Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición "Salvador Zubirán" (INCMNSZ), Mexico City, Mexico.

We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 636 Mexicans from the state of Oaxaca living in the city of Oaxaca (N = 151) and rural communities (N = 485), to obtain information regarding allelic and haplotypic frequencies. We found that the 13 most frequent haplotypes in Oaxaca are all of putative Native American origin. Admixture estimates revealed that the main genetic components in the state of Oaxaca are Native American (73.12 ± 2.77% by ML; 61.52% of Native American haplotypes) and European (17.36 ± 2.07% by ML; 20.69% of European haplotypes), and a relatively high African genetic component (9.52 ± 0.88% by ML; 8.94% of African haplotypes).
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http://dx.doi.org/10.1016/j.humimm.2019.07.278DOI Listing
September 2020

Microbial differences between dental plaque and historic dental calculus are related to oral biofilm maturation stage.

Microbiome 2019 07 6;7(1):102. Epub 2019 Jul 6.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745, Jena, Germany.

Background: Dental calculus, calcified oral plaque biofilm, contains microbial and host biomolecules that can be used to study historic microbiome communities and host responses. Dental calculus does not typically accumulate as much today as historically, and clinical oral microbiome research studies focus primarily on living dental plaque biofilm. However, plaque and calculus reflect different conditions of the oral biofilm, and the differences in microbial characteristics between the sample types have not yet been systematically explored. Here, we compare the microbial profiles of modern dental plaque, modern dental calculus, and historic dental calculus to establish expected differences between these substrates.

Results: Metagenomic data was generated from modern and historic calculus samples, and dental plaque metagenomic data was downloaded from the Human Microbiome Project. Microbial composition and functional profile were assessed. Metaproteomic data was obtained from a subset of historic calculus samples. Comparisons between microbial, protein, and metabolomic profiles revealed distinct taxonomic and metabolic functional profiles between plaque, modern calculus, and historic calculus, but not between calculus collected from healthy teeth and periodontal disease-affected teeth. Species co-exclusion was related to biofilm environment. Proteomic profiling revealed that healthy tooth samples contain low levels of bacterial virulence proteins and a robust innate immune response. Correlations between proteomic and metabolomic profiles suggest co-preservation of bacterial lipid membranes and membrane-associated proteins.

Conclusions: Overall, we find that there are systematic microbial differences between plaque and calculus related to biofilm physiology, and recognizing these differences is important for accurate data interpretation in studies comparing dental plaque and calculus.
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http://dx.doi.org/10.1186/s40168-019-0717-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6612086PMC
July 2019

The efficacy of whole human genome capture on ancient dental calculus and dentin.

Am J Phys Anthropol 2019 03 26;168(3):496-509. Epub 2018 Dec 26.

Faculty of Archaeology, Leiden University, Leiden, The Netherlands.

Objectives: Dental calculus is among the richest known sources of ancient DNA in the archaeological record. Although most DNA within calculus is microbial, it has been shown to contain sufficient human DNA for the targeted retrieval of whole mitochondrial genomes. Here, we explore whether calculus is also a viable substrate for whole human genome recovery using targeted enrichment techniques.

Materials And Methods: Total DNA extracted from 24 paired archaeological human dentin and calculus samples was subjected to whole human genome enrichment using in-solution hybridization capture and high-throughput sequencing.

Results: Total DNA from calculus exceeded that of dentin in all cases, and although the proportion of human DNA was generally lower in calculus, the absolute human DNA content of calculus and dentin was not significantly different. Whole genome enrichment resulted in up to four-fold enrichment of the human endogenous DNA content for both dentin and dental calculus libraries, albeit with some loss in complexity. Recovering more on-target reads for the same sequencing effort generally improved the quality of downstream analyses, such as sex and ancestry estimation. For nonhuman DNA, comparison of phylum-level microbial community structure revealed few differences between precapture and postcapture libraries, indicating that off-target sequences in human genome-enriched calculus libraries may still be useful for oral microbiome reconstruction.

Discussion: While ancient human dental calculus does contain endogenous human DNA sequences, their relative proportion is low when compared with other skeletal tissues. Whole genome enrichment can help increase the proportion of recovered human reads, but in this instance enrichment efficiency was relatively low when compared with other forms of capture. We conclude that further optimization is necessary before the method can be routinely applied to archaeological samples.
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http://dx.doi.org/10.1002/ajpa.23763DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6519167PMC
March 2019

The genetic prehistory of the Andean highlands 7000 years BP though European contact.

Sci Adv 2018 11 8;4(11):eaau4921. Epub 2018 Nov 8.

Department of Human Genetics, University of Chicago, Chicago, IL 60637, USA.

The peopling of the Andean highlands above 2500 m in elevation was a complex process that included cultural, biological, and genetic adaptations. Here, we present a time series of ancient whole genomes from the Andes of Peru, dating back to 7000 calendar years before the present (BP), and compare them to 42 new genome-wide genetic variation datasets from both highland and lowland populations. We infer three significant features: a split between low- and high-elevation populations that occurred between 9200 and 8200 BP; a population collapse after European contact that is significantly more severe in South American lowlanders than in highland populations; and evidence for positive selection at genetic loci related to starch digestion and plausibly pathogen resistance after European contact. We do not find selective sweep signals related to known components of the human hypoxia response, which may suggest more complex modes of genetic adaptation to high altitude.
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http://dx.doi.org/10.1126/sciadv.aau4921DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6224175PMC
November 2018

Bronze Age population dynamics and the rise of dairy pastoralism on the eastern Eurasian steppe.

Proc Natl Acad Sci U S A 2018 11 5;115(48):E11248-E11255. Epub 2018 Nov 5.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany;

Recent paleogenomic studies have shown that migrations of Western steppe herders (WSH) beginning in the Eneolithic (ca. 3300-2700 BCE) profoundly transformed the genes and cultures of Europe and central Asia. Compared with Europe, however, the eastern extent of this WSH expansion is not well defined. Here we present genomic and proteomic data from 22 directly dated Late Bronze Age burials putatively associated with early pastoralism in northern Mongolia (ca. 1380-975 BCE). Genome-wide analysis reveals that they are largely descended from a population represented by Early Bronze Age hunter-gatherers in the Baikal region, with only a limited contribution (∼7%) of WSH ancestry. At the same time, however, mass spectrometry analysis of dental calculus provides direct protein evidence of bovine, sheep, and goat milk consumption in seven of nine individuals. No individuals showed molecular evidence of lactase persistence, and only one individual exhibited evidence of >10% WSH ancestry, despite the presence of WSH populations in the nearby Altai-Sayan region for more than a millennium. Unlike the spread of Neolithic farming in Europe and the expansion of Bronze Age pastoralism on the Western steppe, our results indicate that ruminant dairy pastoralism was adopted on the Eastern steppe by local hunter-gatherers through a process of cultural transmission and minimal genetic exchange with outside groups.
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http://dx.doi.org/10.1073/pnas.1813608115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6275519PMC
November 2018

Proteomic evidence of dietary sources in ancient dental calculus.

Proc Biol Sci 2018 07 18;285(1883). Epub 2018 Jul 18.

BioArCh, Department of Archaeology, University of York, York, UK

Archaeological dental calculus has emerged as a rich source of ancient biomolecules, including proteins. Previous analyses of proteins extracted from ancient dental calculus revealed the presence of the dietary milk protein β-lactoglobulin, providing direct evidence of dairy consumption in the archaeological record. However, the potential for calculus to preserve other food-related proteins has not yet been systematically explored. Here we analyse shotgun metaproteomic data from 100 archaeological dental calculus samples ranging from the Iron Age to the post-medieval period (eighth century BC to nineteenth century AD) in England, as well as 14 dental calculus samples from contemporary dental patients and recently deceased individuals, to characterize the range and extent of dietary proteins preserved in dental calculus. In addition to milk proteins, we detect proteomic evidence of foodstuffs such as cereals and plant products, as well as the digestive enzyme salivary amylase. We discuss the importance of optimized protein extraction methods, data analysis approaches and authentication strategies in the identification of dietary proteins from archaeological dental calculus. This study demonstrates that proteomic approaches can robustly identify foodstuffs in the archaeological record that are typically under-represented due to their poor macroscopic preservation.
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http://dx.doi.org/10.1098/rspb.2018.0977DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6083251PMC
July 2018

Selection of Appropriate Metagenome Taxonomic Classifiers for Ancient Microbiome Research.

mSystems 2018 Jul-Aug;3(4). Epub 2018 Jul 17.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, Germany.

Metagenomics enables the study of complex microbial communities from myriad sources, including the remains of oral and gut microbiota preserved in archaeological dental calculus and paleofeces, respectively. While accurate taxonomic assignment is essential to this process, DNA damage characteristic of ancient samples (e.g., reduction in fragment size and cytosine deamination) may reduce the accuracy of read taxonomic assignment. Using a set of -generated metagenomic data sets, we investigated how the addition of ancient DNA (aDNA) damage patterns influences microbial taxonomic assignment by five widely used profilers: QIIME/UCLUST, MetaPhlAn2, MIDAS, CLARK-S, and MALT. -generated data sets were designed to mimic dental plaque, consisting of 40, 100, and 200 microbial species/strains, both with and without simulated aDNA damage patterns. Following taxonomic assignment, the profiles were evaluated for species presence/absence, relative abundance, alpha diversity, beta diversity, and specific taxonomic assignment biases. Unifrac metrics indicated that both MIDAS and MetaPhlAn2 reconstructed the most accurate community structure. QIIME/UCLUST, CLARK-S, and MALT had the highest number of inaccurate taxonomic assignments; false-positive rates were highest by CLARK-S and QIIME/UCLUST. Filtering out species present at <0.1% abundance greatly increased the accuracy of CLARK-S and MALT. All programs except CLARK-S failed to detect some species from the input file that were in their databases. The addition of ancient DNA damage resulted in minimal differences in species detection and relative abundance between simulated ancient and modern data sets for most programs. Overall, taxonomic profiling biases are program specific rather than damage dependent, and the choice of taxonomic classification program should be tailored to specific research questions. Ancient biomolecules from oral and gut microbiome samples have been shown to be preserved in the archaeological record. Studying ancient microbiome communities using metagenomic techniques offers a unique opportunity to reconstruct the evolutionary trajectories of microbial communities through time. DNA accumulates specific damage over time, which could potentially affect taxonomic classification and our ability to accurately reconstruct community assemblages. It is therefore necessary to assess whether ancient DNA (aDNA) damage patterns affect metagenomic taxonomic profiling. Here, we assessed biases in community structure, diversity, species detection, and relative abundance estimates by five popular metagenomic taxonomic classification programs using -generated data sets with and without aDNA damage. Damage patterns had minimal impact on the taxonomic profiles produced by each program, while false-positive rates and biases were intrinsic to each program. Therefore, the most appropriate classification program is one that minimizes the biases related to the questions being addressed.
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http://dx.doi.org/10.1128/mSystems.00080-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6050634PMC
July 2018

Differential preservation of endogenous human and microbial DNA in dental calculus and dentin.

Sci Rep 2018 06 29;8(1):9822. Epub 2018 Jun 29.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, 07745, Germany.

Dental calculus (calcified dental plaque) is prevalent in archaeological skeletal collections and is a rich source of oral microbiome and host-derived ancient biomolecules. Recently, it has been proposed that dental calculus may provide a more robust environment for DNA preservation than other skeletal remains, but this has not been systematically tested. In this study, shotgun-sequenced data from paired dental calculus and dentin samples from 48 globally distributed individuals are compared using a metagenomic approach. Overall, we find DNA from dental calculus is consistently more abundant and less contaminated than DNA from dentin. The majority of DNA in dental calculus is microbial and originates from the oral microbiome; however, a small but consistent proportion of DNA (mean 0.08 ± 0.08%, range 0.007-0.47%) derives from the host genome. Host DNA content within dentin is variable (mean 13.70 ± 18.62%, range 0.003-70.14%), and for a subset of dentin samples (15.21%), oral bacteria contribute > 20% of total DNA. Human DNA in dental calculus is highly fragmented, and is consistently shorter than both microbial DNA in dental calculus and human DNA in paired dentin samples. Finally, we find that microbial DNA fragmentation patterns are associated with guanine-cytosine (GC) content, but not aspects of cellular structure.
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http://dx.doi.org/10.1038/s41598-018-28091-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6026117PMC
June 2018
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