The Archaeogenetics of European Ancestry

Abstract

The archaeogenetics of Europe remains deeply controversial. Advances in ancient deoxyribonucleic acid (DNA) analysis have suggested gene flow between Neanderthals and modern humans, who arrived in Europe <50 000 years ago, but have so far failed to support evolution of Neanderthals from a population of Homo heidelbergensis represented by remains in northern Spain. The extent to which European Mesolithic forager populations versus Neolithic pioneers from the Near East contributed to the extant gene pool of Europeans also continues to be contested. Whilst analyses of extant mitochondrial lineages have emphasised late Palaeolithic and Mesolithic expansions, ancient DNA (aDNA) results suggest significant Neolithic dispersals from the southern ‘refugial’ zone into the northern ‘bio‐tidal’ zone. However, whether these had a primarily Near Eastern or North Mediterranean source remains a matter for debate. Meanwhile, aDNA has also begun to highlight an important role for later dispersals, especially during the late Neolithic, in shaping the European gene pool.

Key Concepts:

  • The archaeogenetics of Europe has been intensively studied but remains in flux and deeply controversial, with no universally accepted methodological approach.

  • Hominins, including Homo antecessor, Homo heidelbergensis, Neanderthals and modern humans, have been present in Europe for more than 1 million years (My).

  • Neanderthals and modern humans are thought to have a common ancestor, Homo heidelbergensis, approximately half a million years ago, and to have interbred at low levels as modern humans dispersed into Eurasia from Africa approximately 60 000 years ago.

  • However, the status of hominin remains from northern Spain as representing a step from this ancestor towards the Neanderthals has recently been questioned by mtDNA evidence.

  • The importance of the phylogeographic approach can be seen in the elucidation of the relationships between the north European, Finnic‐speaking Saami people, who traditionally lacked agriculture, and farming‐based Europeans.

  • Analyses of contemporary mtDNAs suggest that most arose within the pre‐Neolithic foraging communities of Europe >10 000 years ago, rather than being introduced with farming from the Near East approximately 9000 years ago, but ancient DNA evidence from central and northern Europe has questioned this view.

  • The solution may lie in the distinction between ‘bio‐tidal’ sink and ‘refugium’ source areas, north and south of the continental divide respectively – there may have been significant dispersals from the latter into the former regions in the Neolithic as well as in the Late Glacial and immediate postglacial periods.

  • With increasing success in the recovery of ancient DNA, archaeogenetics is finally also beginning to shed light on post‐Neolithic dispersals – as illustrated by the recent demonstration that most Ashkenazi maternal lineages have a European, rather than Levantine, source.

  • An integrated combination of both ancient and contemporary DNA studies and an eclectic variety of approaches to data analysis may be the best way forward for archaeogenetics.

Keywords: archaeogenetics; phylogeography; founder analysis; STRUCTURE‐like analyses; principal components analysis; genealogy; whole‐mtDNA genomes; Y‐chromosome variation; genome‐wide autosomal variation; ancient DNA

Figure 1.

Phylogenetic tree of whole‐mtDNA genome sequences from two modern humans (within haplogroups L0 and R0: the latter is the revised Cambridge Reference sequence), nine Neanderthals, three ‘Denisovans’ and a H. heidelbergensis from Atapuerca, estimated by hand and rooted with chimpanzee and bonobo sequences. Ambiguous nucleotides are emboldened when the missing base is inferred for the tree reconstruction. Approximate ages of the remains in ka are given below the GenBank accession codes. Age estimates of the major nodes calculated using BEAST software and a phylogenetic tree containing 5 Pan troglodytes, 5 Pan paniscus, 139 human mtDNA genomes (representing all the oldest nodes in the human mtDNA tree) and the 11 archaic Homo sequences and 4 Pleistocene human sequences (FN600416, KC521459, KC521458 and KC417443), using a relaxed molecular‐clock (uncorrelated lognormal with γ‐distributed rates) and incorporating estimates of the ages of the samples.

Figure 2.

Principal components analysis (PCA) of genome‐wide autosomal single‐nucleotide polymorphism (SNP) data of individuals from Europe including several ‘outliers’, the Caucasus and the Near East. Analysis carried out using the smartpca program (with default settings) of the EIGENSOFT package, and data thinned by removing one SNP from all pairs in strong linkage disequilibrium (LD). The fraction of variance explained by each component is given in parentheses: note the extremely low values for these high‐resolution data. All data from Illumina 610 K to 650 K chip with 544 193 SNPs; after LD pruning the total number of SNPs was 234 699.

Figure 3.

Genome‐wide SNP ADMIXTURE analysis of populations from Europe, the Near East, the Caucasus and North and Eastern Africa. Analysis conducted on global populations with random seed number generator on the LD pruned data set at K=2–16. K=14, which had the lowest cross‐validation scores, is shown. Data source as above.

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References

Abi‐Rached L, Jobin MJ, Kulkarni S et al. (2011) The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334: 89–94.

Achilli A, Rengo C, Battaglia V et al. (2005) Saami and Berbers – an unexpected mitochondrial DNA link. American Journal of Human Genetics 76: 883–886.

Bandelt H‐J, Macaulay VA and Richards MB (2002) What molecules can't tell us about the spread of languages and the Neolithic. In: Renfrew C and Bellwood P (eds) Examining the Language‐Farming Dispersal Hypothesis, pp. 99–107. Cambridge: McDonald Institute for Archaeological Research.

Bocquet‐Appel JP (2011) When the world's population took off: the springboard of the Neolithic Demographic Transition. Science 333: 560–561.

Bollongino R, Nehlich O, Richards M et al. (2013) 2000 years of parallel societies in Stone Age Central Europe. Science 342: 479–481.

Bramanti B, Thomas MG, Haak W et al. (2009) Genetic discontinuity between local hunter–gatherers and Central Europe's first farmers. Science 326: 137–140.

Brandt G, Haak W, Adler CJ et al. (2013) Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342: 257–261.

Brotherton P, Haak W, Templeton J et al. (2013) Neolithic mitochondrial haplogroup H genomes and the genetic origins of Europeans. Nature Communications 4: 1764.

Buck LT and Stringer CB (2014) Homo heidelbergensis. Current Biology 24: R214–R215.

Busby GB, Brisighelli F, Sánchez‐Diz P et al. (2011) The peopling of Europe and the cautionary tale of Y chromosome lineage R‐M269. Proceedings of the Royal Society of London, Series B: Biological Sciences 279: 884–892.

Carbonell E, Bermúdez de Castro JM, Parés JM et al. (2008) The first hominin of Europe. Nature 452: 465–469.

Costa MD, Pereira JB, Pala M et al. (2013) A substantial prehistoric European ancestry amongst Ashkenazi maternal lineages. Nature Communications 4: 2543.

Dalén L, Orlando L, Shapiro B et al. (2012) Partial genetic turnover in neandertals: continuity in the East and population replacement in the West. Molecular Biology and Evolution 29: 1893–1897.

Davies W and Gollop P (2003) The human presence in Europe during the Last Glacial Period II: climate tolerance and climate preferences of Mid‐and Late Glacial hominids. In: van Andel T and Davies W (eds) Neanderthals and Modern Humans in the European Landscape During the Last Glaciation, pp. 131–146. Cambridge: McDonald Institute Monographs.

Eriksson A and Manica A (2012) Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Proceedings of the National Academy of Sciences of the USA 109: 13956–13960.

Fernandes V, Alshamali F, Alves M et al. (2012) The Arabian cradle: mitochondrial relicts of the first steps along the southern route out of Africa. American Journal of Human Genetics 90: 347–355.

Fu Q, Mittnik A, Johnson PLF et al. (2013) A revised timescale for human evolution based on ancient mitochondrial genomes. Current Biology 23: 553–559.

Gamble CS (2009) Human display and dispersal: a case study from biotidal Britain in the Middle and Upper Pleistocene. Evolutionary Anthropology 18: 144–156.

Haak W, Balanovsky O, Sanchez JJ et al. (2010) Ancient DNA from European early Neolithic farmers reveals their Near Eastern affinities. PLoS Biology 8: e1000536.

Haak W, Forster P, Bramanti B et al. (2005) Ancient DNA from the first European farmers in 7500‐year‐old Neolithic sites. Science 310: 1016–1018.

Hoffecker JF (2009) The spread of modern humans in Europe. Proceedings of the National Academy of Sciences of the USA 106: 16040–16045.

Huyghe JR, Fransen E, Hannula S et al. (2011) A genome‐wide analysis of population structure in the Finnish Saami with implications for genetic association studies. European Journal of Human Genetics 19: 347–352.

Krause J, Briggs AW, Kircher M et al. (2010) A complete mtDNA genome of an early modern human from Kostenki, Russia. Current Biology 20: 231–236.

Lacan M, Keyser C, Crubézy E and Ludes B (2013) Ancestry of modern Europeans: contributions of ancient DNA. Cellular and Molecular Life Sciences 70: 2473–2487.

Lacan M, Keyser C, Ricaut FX et al. (2011a) Ancient DNA reveals male diffusion through the Neolithic Mediterranean route. Proceedings of the National Academy of Sciences of the USA 108: 9788–9791.

Lacan M, Keyser C, Ricaut FX et al. (2011b) Ancient DNA suggests the leading role played by men in the Neolithic dissemination. Proceedings of the National Academy of Sciences of the USA 108: 18255–18259.

Lowery RK, Uribe G, Jimenez EB et al. (2013) Neanderthal and Denisova genetic affinities with contemporary humans: introgression versus common ancestral polymorphisms. Gene 530: 83–94.

Macaulay V, Hill C, Achilli A et al. (2005) Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308: 1034–1036.

Malmstrom H, Gilbert MTP, Thomas MG et al. (2009) Ancient DNA reveals lack of continuity between Neolithic hunter–gatherers and contemporary Scandinavians. Current Biology 19: 1758–1762.

Malyarchuk B, Derenko M, Denisova G et al. (2010a) Mitogenomic diversity in Tatars from the Volga‐Ural region of Russia. Molecular Biology and Evolution 27: 2220–2226.

Malyarchuk B, Derenko M, Grzybowski T et al. (2010b) The peopling of Europe from the mitochondrial haplogroup U5 perspective. PLoS One 21: e10285.

Malyarchuk B, Grzybowski T, Derenko M et al. (2008) Mitochondrial DNA phylogeny in Eastern and Western Slavs. Molecular Biology and Evolution 25: 1651–1658.

McBrearty A and Brooks AS (2000) The revolution that wasn't: a new interpretation of the origin of modern human behaviour. Journal of Human Evolution 39: 453–563.

Mellars P (2011) The earliest modern humans in Europe. Nature 479: 483–485.

Mellars P, Gori KC, Carr M, Soares PA and Richards MB (2013) Genetic and archaeological perspectives on the initial modern human colonization of southern Asia. Proceedings of the National Academy of Sciences of the USA 110: 10699–10704.

Meyer M, Fu Q, Aximu‐Petri A et al. (2014) A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505: 403–406.

Meyer M, Kircher M, Gansauge M et al. (2012) A high‐coverage genome sequence from an archaic Denisovan individual. Science 338: 222–226.

Morelli L, Contu D, Santoni F et al. (2009) A comparison of Y‐chromosome variation in Sardinia and Anatolia is more consistent with cultural rather than demic diffusion of agriculture. PLoS One 5: e10419.

Müller UC, Pross J, Tzedakis CP et al. (2011) The role of climate in the spread of modern humans into Europe. Quaternary Science Reviews 30: 273–279.

Myres NM, Rootsi S, Lin AA et al. (2011) A major Y‐chromosome haplogroup R1b Holocene era founder effect in Central and Western Europe. European Journal of Human Genetics 19: 95–101.

Novembre J, Johnson T, Bryc K et al. (2008) Genes mirror geography within Europe. Nature 456: 98–101.

Olalde I, Allentoft ME, Sánchez‐Quinto F et al. (2014) Derived immune and ancestral pigmentation alleles in a 7000‐year‐old Mesolithic European. Nature 507: 225–228.

Olivieri A, Pala P, Gandini F et al. (2013) Mitogenomes from two uncommon haplogroups mark Late Glacial/postglacial expansions from the Near East and Neolithic dispersals within Europe. PLoS One 8: e70492.

Pala M, Achilli A, Olivieri A et al. (2009) Mitochondrial haplogroup U5b3: a distant echo of the Epipaleolithic in Italy and the legacy of the early Sardinians. American Journal of Human Genetics 84: 814–821.

Pala M, Olivieri A, Achilli A et al. (2012) Mitochondrial DNA signals of Late Glacial re‐colonization of Europe from Near Eastern refugia. American Journal of Human Genetics 90: 915–924.

Palanichamy Mg, Zhang CL, Mitra B et al. (2010) Mitochondrial haplogroup N1a phylogeography, with implication to the origin of European farmers. BMC Evolutionary Biology 10: 304.

Pinhasi R, Thomas MG, Hofreiter M, Currat M and Burger J (2012) The genetic history of Europeans. Trends in Genetics 28: 496–505.

Prüfer K, Racimo F, Patterson N et al. (2014) The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505: 43–49.

Renfrew C (2000) Archaeogenetics: towards a population prehistory of Europe. In: Renfrew C and Boyle K (eds) Archaeogenetics, pp. 3–11. Cambridge: McDonald Institute.

Ricaut F‐X, Cox MP, Lacan M et al. (2011) A time series of prehistoric mitochondrial DNA reveals western European genetic diversity was largely established by the Bronze Age. Advances in Anthropology 2: 14–23.

Richards M, Macaulay V, Hickey E et al. (2000) Tracing European founder lineages in the Near Eastern mtDNA pool. American Journal of Human Genetics 67: 1251–1276.

Rootsi S, Behar DM, Järve M et al. (2013) Phylogenetic applications of whole Y‐chromosome sequences and the Near Eastern origin of Ashkenazi Levites. Nature Communications 4: 2928.

Rowley‐Conwy P (2011) Westward ho! The spread of agriculture from central Europe to the Atlantic. Current Anthropology 52: S431–S451.

Sajantila A, Lahermo P, Anttinen T et al. (1995) Genes and languages in Europe – an analysis of mitochondrial lineages. Genome Research 5: 42–52.

Sajantila A and Pääbo S (1995) Language replacement in Scandinavia. Nature Genetics 11: 359–360.

Sánchez‐Quinto F, Schroeder H, Ramirez O et al. (2012) Genomic affinities of two 7000‐year‐old Iberian hunter–gatherers. Current Biology 22: 1494–1499.

Sankararaman S, Patterson N, Li H, Pääbo S and Reich D (2012) The date of interbreeding between Neandertals and modern humans. PLoS Genetics 8: e1002947.

Sankararaman S, Mallick S, Dannemann M et al. (2014) The genomic landscape of Neanderthal ancestry in present‐day humans. Nature 507: 354–357.

Semino O, Passarino G, Oefner PJ et al. (2000) The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. Science 290: 1155–1159.

Shennan S, Downey SS, Timpson A et al. (2013) Regional population collapse followed initial agriculture booms in mid‐Holocene Europe. Nature Communications 4: 2486.

Skoglund P and Jakobsson M (2011) Archaic human ancestry in East Asia. Proceedings of the National Academy of Sciences of the USA 108: 18301–18306.

Skoglund P, Malmström H, Raghavan M et al. (2012) Origins and genetic legacy of Neolithic farmers and hunter–gatherers in Europe. Science 336: 466–469.

Soares P, Alshamali F, Pereira JB et al. (2012) The expansion of mtDNA haplogroup L3 within and out of Africa. Molecular Biology and Evolution 29: 915–927.

Tambets K, Rootsi S, Kivisild T et al. (2004) The western and eastern roots of the Saami – the story of genetic “outliers” told by mitochondrial DNA and Y chromosomes. American Journal of Human Genetics 74: 661–682.

Torroni A, Bandelt H‐J, D'Urbano L et al. (1998) mtDNA analysis reveals a major late Paleolithic population expansion from southwestern to northeastern Europe. American Journal of Human Genetics 62: 1137–1152.

Torroni A, Bandelt H‐J, Macaulay V et al. (2001) A signal, from human mtDNA, of post‐glacial recolonization in Europe. American Journal of Human Genetics 69: 844–852.

Vernot B and Akey JM (2014) Resurrecting surviving Neandertal lineages from modern human genomes. Science 343: 1017–1021.

Wall JD, Yang MA, Jay F et al. (2013) Higher levels of neanderthal ancestry in East Asians than in Europeans. Genetics 194: 199–209.

Wood RE, Barroso‐Ruíz C, Caparrós M et al. (2013) Radiocarbon dating casts doubt on the late chronology of the Middle to Upper Palaeolithic transition in southern Iberia. Proceedings of the National Academy of Sciences of the USA 110: 2781–2786.

Yang MA, Malaspinas AS, Durand EY and Slatkin M (2012) Ancient structure in Africa unlikely to explain Neanderthal and non‐African genetic similarity. Molecular Biology and Evolution 29: 2987–2995.

Zvelebil M (2004) Who were we 6000 years ago? In search of prehistoric social identities. In: Jones M (ed.) Traces of Ancestry: Studies in Honour of Colin Renfrew, 41–60. Cambridge: McDonald Institute Monographs.

Further Reading

Ammerman AJ and Cavalli‐Sforza LL (1984) The Neolithic Transition and the Genetics of Populations in Europe. Princeton, NJ: Princeton University Press.

van Andel, TH and Davies W eds (2003) Neanderthals and Modern Humans in the European Landscape during the Last Glaciation: Archaeological Results of the Stage 3 Project. Cambridge: McDonald Institute for Archaeological Research.

Cavalli‐Sforza LL, Menozzi P and Piazza A (1994) The History and Geography of Human Genes. Princeton: Princeton University Press.

Deguilloux MF, Leahy R, Pemonge MH et al. (2012) European neolithization and ancient DNA: an assessment. Evolutionary Anthropology 21: 24–37.

Gamble C (2013) Settling the Earth: The Archaeology of Deep Human History. Cambridge: Cambridge University Press.

Richards M (2003) The Neolithic invasion of Europe. Annual Review of Anthropology 62: 135–162.

Soares P, Achilli A, Semino O et al. (2010) The archaeogenetics of Europe. Current Biology 20: R174–R183.

Soares P, Ermini L, Thomson N et al. (2009) Correcting for purifying selection: an improved human mitochondrial molecular clock. American Journal of Human Genetics 84: 740–759.

Thomas MG, Kivisild T, Chikhi L et al. (2013) Europe and western Asia: genetics and population history. In: Ness I and Bellwood P (eds) The Encycopedia of Global Human Migration, pp. 146–156. Malden, MA: Oxford: Wiley‐Blackwell.

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Pala, Maria, Chaubey, Gyaneshwer, Soares, Pedro, and Richards, Martin B(Jul 2014) The Archaeogenetics of European Ancestry. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024624]