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      Successful reconstruction of whole mitochondrial genomes from ancient Central America and Mexico

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          Abstract

          The northern and southern peripheries of ancient Mesoamerica are poorly understood. There has been speculation over whether borderland cultures such as Greater Nicoya and Casas Grandes represent Mesoamerican outposts in the Isthmo-Colombian area and the Greater Southwest, respectively. Poor ancient DNA preservation in these regions challenged previous attempts to resolve these questions using conventional genetic techniques. We apply advanced in-solution mitogenome capture and high-throughput sequencing to fourteen dental samples obtained from the Greater Nicoya sites of Jícaro and La Cascabel in northwest Costa Rica (n = 9; A.D. 800–1250) and the Casas Grandes sites of Paquimé and Convento in northwest Mexico (n = 5; A.D. 1200–1450). Full mitogenome reconstruction was successful for three individuals from Jícaro and five individuals from Paquimé and Convento. The three Jícaro individuals belong to haplogroup B2d, a haplogroup found today only among Central American Chibchan-speakers. The five Paquimé and Convento individuals belong to haplogroups C1c1a, C1c5, B2f and B2a which, are found in contemporary populations in North America and Mesoamerica. We report the first successfully reconstructed ancient mitogenomes from Central America, and the first genetic evidence of ancestry affinity of the ancient inhabitants of Greater Nicoya and Casas Grandes with contemporary Isthmo-Columbian and Greater Southwest populations, respectively.

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          Most cited references 66

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          Mitochondrial genome variation and the origin of modern humans.

          The analysis of mitochondrial DNA (mtDNA) has been a potent tool in our understanding of human evolution, owing to characteristics such as high copy number, apparent lack of recombination, high substitution rate and maternal mode of inheritance. However, almost all studies of human evolution based on mtDNA sequencing have been confined to the control region, which constitutes less than 7% of the mitochondrial genome. These studies are complicated by the extreme variation in substitution rate between sites, and the consequence of parallel mutations causing difficulties in the estimation of genetic distance and making phylogenetic inferences questionable. Most comprehensive studies of the human mitochondrial molecule have been carried out through restriction-fragment length polymorphism analysis, providing data that are ill suited to estimations of mutation rate and therefore the timing of evolutionary events. Here, to improve the information obtained from the mitochondrial molecule for studies of human evolution, we describe the global mtDNA diversity in humans based on analyses of the complete mtDNA sequence of 53 humans of diverse origins. Our mtDNA data, in comparison with those of a parallel study of the Xq13.3 region in the same individuals, provide a concurrent view on human evolution with respect to the age of modern humans.
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            Beringian Standstill and Spread of Native American Founders

            Native Americans derive from a small number of Asian founders who likely arrived to the Americas via Beringia. However, additional details about the intial colonization of the Americas remain unclear. To investigate the pioneering phase in the Americas we analyzed a total of 623 complete mtDNAs from the Americas and Asia, including 20 new complete mtDNAs from the Americas and seven from Asia. This sequence data was used to direct high-resolution genotyping from 20 American and 26 Asian populations. Here we describe more genetic diversity within the founder population than was previously reported. The newly resolved phylogenetic structure suggests that ancestors of Native Americans paused when they reached Beringia, during which time New World founder lineages differentiated from their Asian sister-clades. This pause in movement was followed by a swift migration southward that distributed the founder types all the way to South America. The data also suggest more recent bi-directional gene flow between Siberia and the North American Arctic.
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              A "Copernican" reassessment of the human mitochondrial DNA tree from its root.

              Mutational events along the human mtDNA phylogeny are traditionally identified relative to the revised Cambridge Reference Sequence, a contemporary European sequence published in 1981. This historical choice is a continuous source of inconsistencies, misinterpretations, and errors in medical, forensic, and population genetic studies. Here, after having refined the human mtDNA phylogeny to an unprecedented level by adding information from 8,216 modern mitogenomes, we propose switching the reference to a Reconstructed Sapiens Reference Sequence, which was identified by considering all available mitogenomes from Homo neanderthalensis. This "Copernican" reassessment of the human mtDNA tree from its deepest root should resolve previous problems and will have a substantial practical and educational influence on the scientific and public perception of human evolution by clarifying the core principles of common ancestry for extant descendants. Copyright © 2012 The American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                aymorale@ucalgary.ca
                warinner@shh.mpg.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                22 December 2017
                22 December 2017
                2017
                : 7
                Affiliations
                [1 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Department of Anthropology and Archaeology, , University of Calgary, ; Calgary, Alberta T2N 1N4 Canada
                [2 ]ISNI 0000 0004 0447 0018, GRID grid.266900.b, Department of Anthropology, , University of Oklahoma, ; Norman, Oklahoma 73019 USA
                [3 ]ISNI 0000 0004 1936 8227, GRID grid.25073.33, McMaster Ancient DNA Centre, Department of Anthropology, , McMaster University, Hamilton, ; Ontario, L8S 4L8 Canada
                [4 ]ISNI 0000 0004 4914 1197, GRID grid.469873.7, Department of Archaeogenetics, , Max Planck Institute for the Science of Human History, ; Jena, 07743 Germany
                Article
                18356
                10.1038/s41598-017-18356-0
                5741722
                29273718
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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