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Ancestry of modern Europeans: contributions of ancient DNA

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Abstract

Understanding the peopling history of Europe is crucial to comprehend the origins of modern populations. Of course, the analysis of current genetic data offers several explanations about human migration patterns which occurred on this continent, but it fails to explain precisely the impact of each demographic event. In this context, direct access to the DNA of ancient specimens allows the overcoming of recent demographic phenomena, which probably highly modified the constitution of the current European gene pool. In recent years, several DNA studies have been successfully conducted from ancient human remains thanks to the improvement of molecular techniques. They have brought new fundamental information on the peopling of Europe and allowed us to refine our understanding of European prehistory. In this review, we will detail all the ancient DNA studies performed to date on ancient European DNA from the Middle Paleolithic to the beginning of the protohistoric period.

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Authors and Affiliations

  1. Laboratoire AMIS, CNRS UMR 5288, 37 Allées Jules Guesde, 31073, Toulouse cedex 3, France

    Marie Lacan, Christine Keyser, Eric Crubézy & Bertrand Ludes

  2. Laboratoire d’Anthropologie moléculaire, CNRS UMR 5288, Université de Strasbourg, Institut de Médecine Légale, 11 rue Humann, 67085, Strasbourg, France

    Marie Lacan, Christine Keyser & Bertrand Ludes

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  1. Marie Lacan
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Correspondence to Marie Lacan.

Box 1: Human ancient DNA research, a booming field

Box 1: Human ancient DNA research, a booming field

In 1984, an American team was able to extract for the first time mitochondrial DNA fragments from an extinct specimen of the genus Equus (the quagga) and revealed that DNA molecules could survive within ancient remains [84]. But it was really after 1987 and the development of the polymerase chain reaction (PCR), which allows a small amount of DNA to be amplified exponentially [85], that the discipline became a promising field, notably to reconstruct the evolution of species or populations. However, because of the low amount of available material in ancient samples and the degraded state of the DNA, limitations linked with the PCR principle have also been highlighted.

Indeed, after the death of an organism, several enzymatic or chemical reactions lead to irreversible modifications of the DNA molecules. The quantity and quality of authentic DNA will vary greatly from a sample to another according to the taphonomic history of the sample. When ancient DNA can be extracted, it is almost systematically highly fragmented and its bases are chemically altered [86]: fragments extracted are rarely longer than 150 bp, and they exhibit base modifications which will have important consequences during PCR. These miscoding lesions can thus provoke replication errors such as C/G to T/A transitions (due to hydrolytic deaminations) or C/G to A/T transversions (because of oxidative damages) [87]. Above all, these alterations make ancient DNA analyses particularly sensitive to contamination by exogenous DNA. Indeed, there is a higher chance that, during PCR, the polymerase preferentially amplifies contemporary and intact molecules rather than ancient and degraded ones. This contamination issue is particularly problematic when analyses are performed on ancient human specimens, since it is not always possible to distinguish if the sequences obtained correspond to endogenous fragments or to contaminating molecules brought by contemporary people involved in the study of the ancient samples. Handling precautions and drastic authenticity criteria have, of course, been implemented to avoid publication of erroneous data [88]. Analyses are thus always performed in specific clean room facilities (positive air pressure and UV decontamination), free of any modern or amplified DNA. But most ancient samples coming from museum collections have been manipulated by several people without precautions over several years. So, despite all precautions taken during analysis, the DNA study of ancient human skeletal remains is still a huge challenge, and, in addition, thoughtful analysis strategies must in particular be developed to prove the authenticity of the data produced [89].

In recent years, the improvement of sequencing technologies offers new perspectives. Indeed, the “Next Generation Sequencing” or NGS technologies use a different approach to investigate ancient genomes. They allow large-scale studies through the massive sequencing of a set of ancient DNA molecules without prior targeted amplification [90]. The high throughput sequencers are thus able to produce over one gigabase of data in a single run, and offer the possibility notably through particular strategies such as targeted capture approaches, to achieve a high coverage of a lot of genetic loci of interest [91, 92]. These techniques are particularly promising in the study of ancient human DNA since they offer many advantages regarding the detection of potential contamination. For example, the high coverage permits the obtaining of an important number of fragments that overlap particular DNA positions and provides internal replications necessary to confirm that the DNA studied really does originate from a single individual. In addition, these technologies provide an overview on the degraded state of DNA through the detection of nucleotide misincorporation patterns. The estimation of purine frequency at the ends of fragments, or the length of fragments themselves, can, for example, be used to distinguish the presence of modern contaminant DNA [93, 94]. However, the number of degradation patterns can vary from sample to sample according to the age of the specimen or the taphonomic conditions. Moreover, some contaminant molecules can also exhibit degradation patterns, notably if the contamination occurred several years prior to the analysis or if samples were cleaned with a depurinating agent [94, 95]. NGS are thus a promising approach for the future analysis of ancient human remains. However, such technologies are not always accessible for all ancient DNA laboratories and their cost remains high compared to traditional approaches by PCR. This is a reason why these technologies are not yet used routinely in all laboratories and are mainly employed to study exceptional specimens such as ancient hominins [11, 23, 27, 28, 31, 96, 97] or samples containing particularly well-preserved DNA [98, 99].

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Lacan, M., Keyser, C., Crubézy, E. et al. Ancestry of modern Europeans: contributions of ancient DNA. Cell. Mol. Life Sci. 70, 2473–2487 (2013). https://doi.org/10.1007/s00018-012-1180-5

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  • DOI: https://doi.org/10.1007/s00018-012-1180-5

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