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Ancient DNA and the Rewriting of Human History: Be Sparing with Occam’S Razor Marc Haber1, Massimo Mezzavilla1,2, Yali Xue1 and Chris Tyler-Smith1*

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Ancient DNA and the Rewriting of Human History: Be Sparing with Occam’S Razor Marc Haber1, Massimo Mezzavilla1,2, Yali Xue1 and Chris Tyler-Smith1* Haber et al. Genome Biology (2016) 17:1 DOI 10.1186/s13059-015-0866-z REVIEW Open Access Ancient DNA and the rewriting of human history: be sparing with Occam’s razor Marc Haber1, Massimo Mezzavilla1,2, Yali Xue1 and Chris Tyler-Smith1* Origin and expansion of modern humans and Abstract admixture with archaic species Ancient DNA research is revealing a human history far For decades, the theories about the origin of modern more complex than that inferred from parsimonious humans were summarized in two main competing models: models based on modern DNA. Here, we review some multiregional evolution or recent replacement from Africa of the key events in the peopling of the world in the [1, 2]. Genetic studies beginning in the 1980s provided light of the findings of work on ancient DNA. explicit support for a recent origin of modern humans in Africa around 200,000 years ago (ya) [3], followed by an expansion out of Africa around 50,000–60,000 ya and Background subsequent colonization of the rest of the world [4]. The human past on many timescales is of broad intrinsic There are hundreds of research papers discussing the interest, and genetics contributes to our understanding out-of-Africa migration using archaeological data, present- of it, as do paleontology, archaeology, linguistics and day human genetic data or even genetic data from the other disciplines. Geneticists have long studied present- human microbiome. Most of this work refines the recent day populations to glean information about their past, replacement model, including suggesting a time-frame for using models to infer past population events such as mi- the expansion [5] as well as the number of waves and ’ grations or replacements, generally invoking Occam s routes taken by humans in their exit from Africa [4]. A razor to favor the simplest model consistent with the few early studies did propose admixture with archaic data. But this is not the most straightforward approach humans [6, 7], but alternative interpretations of their ex- to understanding such events: the obvious way to study amples were usually possible [8]. A major revision of the any aspect of human genetic history is to analyze popula- replacement model was introduced as the result of aDNA tion samples from before, during and after the period of research published in 2010, in which DNA was retrieved interest, and to simply catalogue the changes. Advances in from three Neanderthal bones from the Vindija Cave in ancient DNA (aDNA) technology are now beginning to Croatia [9] and from a finger bone found in Denisova make this more direct approach possible, facilitated by Cave in southern Siberia [10]. Analyses of DNA from new sequencing technologies that are now capable of gen- the archaic humans showed strong evidence of a small erating gigabases of data at moderate cost (Box 1). This amount of gene flow to modern humans, giving rise to abundance of data, combined with an understanding of a ‘leaky replacement’ model. The initial report was met the damage patterns indicative of authentic aDNA, greatly with some criticism, suggesting that ancient population simplify the recognition and avoidance of the bugbear of substructure could produce a genetic signal similar to the field: contamination. the one interpreted as introgression from Neanderthals Here, we review some of the key events in the peop- [11] (see Box 2 for more details on the D-statistics rele- ling of the world in the light of recent aDNA findings, vant to this discussion). However, several later studies discussing new evidence for how migration, admixture using different statistics showed that ancient structure and selection have shaped human populations. alone cannot explain the introgression signal [12, 13]. Neanderthal ancestry in all present-day non-Africans is estimated to be 1.5–2.1 % [14]. The broad geographical distribution, together with the size of the DNA segments * Correspondence: [email protected] 1The Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, contributed by Neanderthals, suggests that the gene flow Cambridgeshire CB10 1SA, UK most likely occurred at an early stage of the out-of-Africa Full list of author information is available at the end of the article © 2016 Haber et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Haber et al. Genome Biology (2016) 17:1 Page 2 of 8 Box 1 The evolution of genetic studies: from ‘markers’ to whole-genome sequences Over the past 100 years, the datasets and mathematical methodologies used in population genetics have changed enormously, providing an ever better understanding of human genetic diversity over time and space. In 1954, Arthur Mourant published his ground-breaking book “The distribution of the human blood groups” [47], probably the first full anthropological work to use a genetic perspective, showing that detectable genetic differences exist among different human populations. Blood groups and protein types constitute what are now known as ‘classical markers’ and were used to compare human populations for several decades, preceding the DNA-based datasets utilized today. The development of the polymerase chain reaction (PCR) in the 1980s introduced the use of molecular markers to population genetics and allowed, for the first time, the study of evolutionary distances between alleles at a locus. This methodological progress, along with theoretical advances such as identity by descent developed by Gustave Malécot in 1939 [48] and coalescent theory developed by John Kingman in 1982 [49], provided an unprecedented understanding of the genetic relationships among human populations, as well as their relatedness and divergence from other species. The first widely used molecular markers were variants of the mitochondrial DNA (mtDNA) and the non-recombining region of the Y-chromosome (NRY). mtDNA is inherited maternally and transmitted from a mother to her children, while the NRY is inherited paternally passing down from father to son. These uniparental markers are transmitted from one generation to the next intact (apart from new mutations) and have known mutation rates, allowing straightforward construction of phylogenies and inference of some aspects of population relationships. Uniparental loci are, however, sex-specific and experience strong drift, providing a limited view of the complex human history. For example, Neanderthal mtDNA analysis shows no evidence of admixture with modern humans [50], although admixture has occurred and is detectable when the whole genome is considered. The study of genome-wide markers was initiated using microsatellites (short tandem repeats, STRs) but was simplified by the development of single nucleotide polymorphism (SNP) arrays. The effective population size of autosomal variants is expected to be four times that of mtDNA and NRY, making autosomal variants less prone to drift and providing insight further back into human history. Nevertheless, inferences from SNP arrays are limited by ascertainment biases arising from their design, which generally incorporated SNPs that were discovered in a few populations and were inadequate to capture global genetic diversity. The development of next-generation sequencing (NGS) resolved many of the limitations of the previous methodologies by generating gigabases of sequence data from the whole genome, reducing ascertainment biases while increasing the power to detect evolutionary processes. NGS produces large numbers of short sequencing reads. This feature is particularly useful for ancient DNA analysis and has allowed the sequencing of genomes that are tens of thousands of years old, making the direct study of the evolutionary changes over time and space possible. NGS is thus currently revolutionizing the field of population genetics. expansion: around 47,000–65,000 ya [12], before the diver- previous range. Moreover, the Neanderthal-derived DNA in gence of Eurasian groups from each other. Sequences all non-Africans is more closely related to a Neanderthal from the genomes of ancient Eurasians show that they car- from the Caucasus than it is to either the Neanderthal from ried longer archaic segments that have been affected by Siberia or the Neanderthal from Croatia [14], providing less recombination than those in present-day humans, more evidence that archaic admixture occurred in West consistent with the ancient individuals being closer to the Asia early during modern humans’ exit from Africa. It re- time of the admixture event with Neanderthals. For ex- mains unclear how frequent mixture between Neanderthals ample, a genome sequence from Kostenki 14 who lived in and modern humans was, or how many Neanderthal indi- Russia 38,700–36,200 ya had a segment of Neanderthal viduals contributed; however, a higher level of Neanderthal ancestry of ~3 Mb on chromosome 6 [15], whereas ancestry in East Asians than in Europeans has been present-day humans carry, on average, introgressed haplo- proposed to result from a second pulse of Neanderthal types of ~57 kb in length [16]. The genome sequence of a gene flow into the ancestors of East Asians [18, 19]. 45,000-year-old modern human male named Ust’-Ishim DNA from a 37,000–42,000-year-old modern human (after the region in Siberia where he was discovered), from Romania (named Oase) had 6–9 % Neanderthal- shows genomic segments of Neanderthal ancestry that derived alleles, including three large segments of Neander- are ~1.8–4.2 times longer than those observed in present- thal ancestry of over 50 centimorgans in size, suggesting day individuals, suggesting that the Neanderthal gene flow that Oase had a Neanderthal ancestor as a fourth-, fifth- occurred 232–430 generations before Ust’-Ishim lived, or sixth-degree relative [20].
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