Republication from nature.com
(a) Maximum-parsimony tree of European MSY lineages defined here by resequencing. Branch lengths are proportional to molecular divergence among haplotypes. Key mutation names are given next to some branches, and haplogroup names20 in the coloured bar below. Three sporadic haplogroups are coloured in black. The grey box within hg R1b-M269 shows the star phylogeny referred to in the text. (b) Map with pie-charts showing frequencies of Y-chromosome haplogroups (defined and coloured as in part a) in 17 populations from Europe and the Near East. Population abbreviations are as follows: bas: Basque; bav: Bavaria; CEU: Utah residents with Northern and Western European ancestry from the CEPH collection (France); den: Denmark; eng: England; fri: Frisia; gre: Greece; hun: Hungary; ire: Ireland; nor: Norway; ork: Orkney; pal: Palestinians; saa: Saami; ser: Serbia; spa: Spain; TSI: Toscani in Italia (Italy); tur: Turkey.
The proportion of Europeans descending from Neolithic farmers ∼10 thousand years ago (KYA) or Palaeolithic hunter-gatherers has been much debated. The male-specific region of the Y chromosome (MSY) has been widely applied to this question, but unbiased estimates of diversity and time depth have been lacking. Here we show that European patrilineages underwent a recent continent-wide expansion. Resequencing of 3.7 Mb of MSY DNA in 334 males, comprising 17 European and Middle Eastern populations, defines a phylogeny containing 5,996 single-nucleotide polymorphisms. Dating indicates that three major lineages (I1, R1a and R1b), accounting for 64% of our sample, have very recent coalescent times, ranging between 3.5 and 7.3 KYA. A continuous swathe of 13/17 populations share similar histories featuring a demographic expansion starting ∼2.1–4.2 KYA. Our results are compatible with ancient MSY DNA data, and contrast with data on mitochondrial DNA, indicating a widespread male-specific phenomenon that focuses interest on the social structure of Bronze Age Europe.
Controversy has surrounded the origins and antiquity of the people of Europe, focused on the proportions descending from Neolithic farmers originating ∼10 thousand years ago (KYA), or from earlier Palaeolithic hunter-gatherers. Early studies observed a European SE–NW cline in classical gene frequency data which was ascribed to demic diffusion of farmers1, or, in an alternative view, to the first Palaeolithic colonization2. More recent autosomal genome-wide SNP data sets reflect current population structure3,4 and admixture during the last 3,000 years5, but have provided little insight into older population processes.
Most debate on European prehistory has been stimulated by analyses of uniparentally-inherited markers. Spatial patterns in maternally-inherited mitochondrial DNA (mtDNA) are non-clinal, with age estimates of haplogroups (hg) taken to suggest a major Palaeolithic contribution6. Analyses of diversity in the male-specific region of the Y chromosome (MSY) show significant frequency clines in major lineages7, and geographical distributions and dates based on short-tandem repeats (STRs) have led to interpretations of both Palaeolithic8 and Neolithic9 major components. The most frequent western European lineage, hg R1b-M269, was originally believed to have originated in the Palaeolithic10, but in more recent analysis was assigned a Neolithic origin11, a claim challenged in turn12 on the basis of STR choice and sample ascertainment. In general, dates based on STRs are problematic because of uncertainty about appropriate mutation rates, and possible long-term mutation saturation due to their stepwise mutation processes13. Palaeolithic dates for the major lineages are challenged by scanty ancient MSY DNA data, which suggest a marked discontinuity between 5–7 KYA and the present14.
A major cause of the controversy about MSY evidence is that unbiased estimates of diversity and time depth have until recently been impossible to obtain in large samples. Next-generation sequencing (NGS) generally offers unbiased ascertainment of MSY SNPs, providing phylogenies in which topologies inform about past demography, and branch lengths are in principle proportional to time, avoiding dating problems associated with STRs. Some insights have emerged from recent work15,16, but no systematic population-based NGS study across Europe has yet been undertaken.