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      Optimal Ancient DNA Yields from the Inner Ear Part of the Human Petrous Bone

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          Abstract

          The invention and development of next or second generation sequencing methods has resulted in a dramatic transformation of ancient DNA research and allowed shotgun sequencing of entire genomes from fossil specimens. However, although there are exceptions, most fossil specimens contain only low (~ 1% or less) percentages of endogenous DNA. The only skeletal element for which a systematically higher endogenous DNA content compared to other skeletal elements has been shown is the petrous part of the temporal bone. In this study we investigate whether (a) different parts of the petrous bone of archaeological human specimens give different percentages of endogenous DNA yields, (b) there are significant differences in average DNA read lengths, damage patterns and total DNA concentration, and (c) it is possible to obtain endogenous ancient DNA from petrous bones from hot environments. We carried out intra-petrous comparisons for ten petrous bones from specimens from Holocene archaeological contexts across Eurasia dated between 10,000-1,800 calibrated years before present (cal. BP). We obtained shotgun DNA sequences from three distinct areas within the petrous: a spongy part of trabecular bone (part A), the dense part of cortical bone encircling the osseous inner ear, or otic capsule (part B), and the dense part within the otic capsule (part C). Our results confirm that dense bone parts of the petrous bone can provide high endogenous aDNA yields and indicate that endogenous DNA fractions for part C can exceed those obtained for part B by up to 65-fold and those from part A by up to 177-fold, while total endogenous DNA concentrations are up to 126-fold and 109-fold higher for these comparisons. Our results also show that while endogenous yields from part C were lower than 1% for samples from hot (both arid and humid) parts, the DNA damage patterns indicate that at least some of the reads originate from ancient DNA molecules, potentially enabling ancient DNA analyses of samples from hot regions that are otherwise not amenable to ancient DNA analyses.

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          Patterns of damage in genomic DNA sequences from a Neandertal.

          High-throughput direct sequencing techniques have recently opened the possibility to sequence genomes from Pleistocene organisms. Here we analyze DNA sequences determined from a Neandertal, a mammoth, and a cave bear. We show that purines are overrepresented at positions adjacent to the breaks in the ancient DNA, suggesting that depurination has contributed to its degradation. We furthermore show that substitutions resulting from miscoding cytosine residues are vastly overrepresented in the DNA sequences and drastically clustered in the ends of the molecules, whereas other substitutions are rare. We present a model where the observed substitution patterns are used to estimate the rate of deamination of cytosine residues in single- and double-stranded portions of the DNA, the length of single-stranded ends, and the frequency of nicks. The results suggest that reliable genome sequences can be obtained from Pleistocene organisms.
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            Ancient human genome sequence of an extinct Palaeo-Eskimo.

            We report here the genome sequence of an ancient human. Obtained from approximately 4,000-year-old permafrost-preserved hair, the genome represents a male individual from the first known culture to settle in Greenland. Sequenced to an average depth of 20x, we recover 79% of the diploid genome, an amount close to the practical limit of current sequencing technologies. We identify 353,151 high-confidence single-nucleotide polymorphisms (SNPs), of which 6.8% have not been reported previously. We estimate raw read contamination to be no higher than 0.8%. We use functional SNP assessment to assign possible phenotypic characteristics of the individual that belonged to a culture whose location has yielded only trace human remains. We compare the high-confidence SNPs to those of contemporary populations to find the populations most closely related to the individual. This provides evidence for a migration from Siberia into the New World some 5,500 years ago, independent of that giving rise to the modern Native Americans and Inuit.
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              An Aboriginal Australian genome reveals separate human dispersals into Asia.

              We present an Aboriginal Australian genomic sequence obtained from a 100-year-old lock of hair donated by an Aboriginal man from southern Western Australia in the early 20th century. We detect no evidence of European admixture and estimate contamination levels to be below 0.5%. We show that Aboriginal Australians are descendants of an early human dispersal into eastern Asia, possibly 62,000 to 75,000 years ago. This dispersal is separate from the one that gave rise to modern Asians 25,000 to 38,000 years ago. We also find evidence of gene flow between populations of the two dispersal waves prior to the divergence of Native Americans from modern Asian ancestors. Our findings support the hypothesis that present-day Aboriginal Australians descend from the earliest humans to occupy Australia, likely representing one of the oldest continuous populations outside Africa.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 June 2015
                2015
                : 10
                : 6
                : e0129102
                Affiliations
                [1 ]School of Archaeology and Earth Institute, Belfield, University College Dublin, Dublin 4, Ireland
                [2 ]Department of Anthropology, Emory University, Atlanta, Georgia, United States of America
                [3 ]independent researcher, Santpoort-Noord, The Netherlands
                [4 ]Netherlands Institute in Turkey, Istiklal Caddesi, Nur-i Ziya Sokak 5, Beyoğlu, Istanbul, Turkey
                [5 ]Peter the Great Museum of Anthropology and Ethnography (Kunstkamera), Russian Academy of Sciences, Universitetskaya Nab. 3, St. Petersburg, Russia
                [6 ]Eötvös Loránd University University, Faculty of Humanities, Institute of Archaeological Sciences, Múzeum körút 4/b, Budapest, Hungary
                [7 ]Department of Anthropology, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America
                [8 ]Whitman College, Walla Walla, Washington, United States of America
                [9 ]Museum of Vojvodina, 21 000 Novi Sad, Ulica Dunavska 35, Serbia
                [10 ]Institute of Archaeology, Hoan Kiem District, Hanoi, Vietnam
                [11 ]Zinman Institute of Archaeology, University of Haifa, Mount Carmel, Israel
                [12 ]School of Archaeology and Anthropology, Australian National University, Canberra, Australia
                [13 ]School of Health Science, Sapporo Medical University, Sapporo, Japan
                [14 ]Institute for Biochemistry and Biology, Faculty for Mathematics and Natural Sciences, University of Potsdam, Karl-Liebknechtstr. 24–25, 14476 Potsdam Golm, Germany
                [15 ]Department of Biology, University of York, Wentworth Way, Heslington, York, United Kingdom
                University of Oxford, UNITED KINGDOM
                Author notes

                Competing Interests: SAR is a self employed freelance osteologist. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: RP DF KS MN SC GB MH. Performed the experiments: RP DF KS MN SC MH. Analyzed the data: RP DF KS MN SC MH. Contributed reagents/materials/analysis tools: SA-R FG VM AG PR AA MP GR MJ HT MO HM. Wrote the paper: RP DF KS MN SC SA-R FG VM AG PR AA MP GR MJ HT GB MO HM.

                Article
                PONE-D-15-10882
                10.1371/journal.pone.0129102
                4472748
                26086078
                99679e56-b4d5-40d3-b82c-164415f59c8a
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 15 March 2015
                : 6 May 2015
                Page count
                Figures: 3, Tables: 2, Pages: 13
                Funding
                This research was supported by Ron Pinhasi's European Research Council Starting grant (ERC- 2010-StG 263441);ERC Grant to RP (ADNABIOARC, 263441); MH was supported by ERC grant GeneFlow (310763). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Data are available from BioProject - PRJNA283950 and Sequence Read Archive - SRP058345.

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