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Large-scale recent expansion of European patrilineages shown by population resequencing

Batini, Chiara, Hallast, Pille, Zadik, Daniel, Delser, Pierpaolo Maisano, Benazzo, Andrea, Ghirotto, Silvia, Arroyo-Pardo, Eduardo, Cavalleri, Gianpiero L., de Knijff, Peter, Dupuy, Berit Myhre, Eriksen, Heidi A., King, Turi E., de Munain, Adolfo López, López-Parra, Ana M., Loutradis, Aphrodite, Milasin, Jelena, Novelletto, Andrea, Pamjav, Horolma, Sajantila, Antti, Tolun, Aslıhan, Winney, Bruce, Jobling, Mark A.·2015·Nature Communications
DOI 10.1038/ncomms8152PMC PMC4441248
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Abstract

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.

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Figure 1 Phylogeny and geographical distribution of European MSY lineages. (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.
Figure 1 Phylogeny and geographical distribution of European MSY lineages. (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.CC BY · PubMed Central
Figure 2 Bayesian skyline plots. Thick black lines indicate the median for effective population size (Ne) and thinner grey lines show 95% higher posterior density intervals. Grey shading indicates the confidence intervals of the time estimate of the minimum effective population size before the expansion, based on the limits of the 95% CI of the mutation rate. 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.
Figure 2 Bayesian skyline plots. Thick black lines indicate the median for effective population size (Ne) and thinner grey lines show 95% higher posterior density intervals. Grey shading indicates the confidence intervals of the time estimate of the minimum effective population size before the expansion, based on the limits of the 95% CI of the mutation rate. 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.CC BY · PubMed Central
Figure 3 Timeline of MSY ancient DNA data. The graph shows stacked frequencies of MSY haplogroups in ancient European DNA samples, based on data from 98 individuals, and binned into 500-year intervals. ‘other’ includes C1, F*, H2, R*, R1, R1b(xR1b1a). Below the timeline are indicated BEAST point estimates and highest posterior density intervals for three relevant haplogroups.
Figure 3 Timeline of MSY ancient DNA data. The graph shows stacked frequencies of MSY haplogroups in ancient European DNA samples, based on data from 98 individuals, and binned into 500-year intervals. ‘other’ includes C1, F*, H2, R*, R1, R1b(xR1b1a). Below the timeline are indicated BEAST point estimates and highest posterior density intervals for three relevant haplogroups.CC BY · PubMed Central

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Research works printed but not linked: 45

  1. Ammerman, A. J. & Cavalli-Sforza, L. L. Neolithic transition and the genetics of populations in Europe Princeton University Press (1984). · DOI
  2. Richards, M. et al. Paleolithic and neolithic lineages in the European mitochondrial gene pool. Am. J. Hum. Genet. 59, 185–203 (1996).
  3. Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747–751 (2014). · DOI · Paper page
  4. Richards, M. et al. Tracing European founder lineages in the near eastern mtDNA pool. Am. J. Hum. Genet. 67, 1251–1276 (2000). · DOI
  5. Rosser, Z. H. et al. Y-chromosomal diversity within Europe is clinal and influenced primarily by geography, rather than by language. Am. J. Hum. Genet. 67, 1526–1543 (2000). · DOI · Paper page
  6. Rootsi, S. et al. Phylogeography of Y-chromosome haplogroup I reveals distinct domains of prehistoric gene flow in Europe. Am. J. Hum. Genet. 75, 128–137 (2004). · DOI
  7. Semino, O. et al. Origin, diffusion, and differentiation of Y-chromosome haplogroups E and J: inferences on the neolithization of Europe and later migratory events in the Mediterranean area. Am. J. Hum. Genet. 74, 1023–1034 (2004). · DOI
  8. Semino, O. et al. The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. Science 290, 1155–1159 (2000). · DOI
  9. Balaresque, P. et al. A predominantly Neolithic origin for European paternal lineages. PLoS Biol. 8, e1000285 (2010). · DOI · Paper page
  10. Busby, G. B. et al. The peopling of Europe and the cautionary tale of Y chromosome lineage R-M269. Proc. Biol. Sci. 279, 884–892 (2012). · DOI
  11. Hallast, P. et al. The Y-chromosome tree bursts into leaf: 13,000 high-confidence SNPs covering the majority of known clades. Mol. Biol. Evol. 32, 661–673 (2015). · DOI
  12. Veeramah, K. R. & Hammer, M. F. The impact of whole-genome sequencing on the reconstruction of human population history. Nat. Rev. Genet. 15, 149–162 (2014). · DOI
  13. Francalacci, P. et al. Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y-chromosome phylogeny. Science 341, 565–569 (2013). · DOI
  14. Lippold, S. et al. Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences. Investig. Genet. 5, 13 (2014). · DOI · Paper page
  15. Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007). · DOI
  16. Brandt, G. et al. Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342, 257–261 (2013). · DOI · Paper page
  17. Karafet, T. M. et al. New binary polymorphisms reshape and increase resolution of the human Y-chromosomal haplogroup tree. Genome Res. 18, 830–838 (2008). · DOI · Paper page
  18. Ho, S. Y. & Shapiro, B. Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol. Ecol. Resour. 11, 423–434 (2011). · DOI
  19. Beaumont, M. A., Zhang, W. & Balding, D. J. Approximate Bayesian computation in population genetics. Genetics 162, 2025–2035 (2002). · DOI · Paper page
  20. Bertorelle, G., Benazzo, A. & Mona, S. ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol. Ecol. 19, 2609–2625 (2010). · DOI
  21. Helgason, A. et al. The Y-chromosome point mutation rate in humans. Nat. Genet. doi:10.1038/ng.3171 (2015). · DOI
  22. Xue, Y. et al. Human Y chromosome base-substitution mutation rate measured by direct sequencing in a deep-rooting pedigree. Curr. Biol. 19, 1453–1457 (2009). · DOI
  23. Mendez, F. L. et al. An African American paternal lineage adds an extremely ancient root to the human Y chromosome phylogenetic tree. Am. J. Hum. Genet. 92, 454–459 (2013). · DOI
  24. Scozzari, R. et al. An unbiased resource of novel SNP markers provides a new chronology for the human Y chromosome and reveals a deep phylogenetic structure in Africa. Genome Res. 24, 535–544 (2014). · DOI
  25. Elhaik, E., Tatarinova, T. V., Klyosov, A. A. & Graur, D. The 'extremely ancient' chromosome that isn't: a forensic bioinformatic investigation of Albert Perry's X-degenerate portion of the Y chromosome. Eur. J. Hum. Genet. 22, 1111–1116 (2014). · DOI
  26. Kuroki, Y. et al. Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nat. Genet. 38, 158–167 (2006). · DOI
  27. Skaletsky, H. et al. The male-specific region of the human Y chromosome: a mosaic of discrete sequence classes. Nature 423, 825–837 (2003). · DOI
  28. Poznik, G. D. et al. Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341, 562–565 (2013). · DOI · Paper page
  29. Cunliffe, B. Europe Between the Oceans: 9000 BC-AD 1000 Yale University Press (2011).
  30. Winney, B. et al. People of the British Isles: preliminary analysis of genotypes and surnames in a UK-control population. Eur. J. Hum. Genet. 20, 203–210 (2012). · DOI
  31. Kao, W. C., Stevens, K. & Song, Y. S. BayesCall: a model-based base-calling algorithm for high-throughput short-read sequencing. Genome Res. 19, 1884–1895 (2009). · DOI
  32. Lunter, G. & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936–939 (2011). · DOI · Paper page
  33. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011). · DOI
  34. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011). · DOI
  35. 1000 Genomes Project Consortium. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56–65 (2012). · DOI · Paper page
  36. Van Geystelen, A., Decorte, R. & Larmuseau, M. H. AMY-tree: an algorithm to use whole genome SNP calling for Y chromosomal phylogenetic applications. BMC Genomics 14, 101 (2013). · DOI
  37. Van Geystelen, A., Decorte, R. & Larmuseau, M. H. Updating the Y-chromosomal phylogenetic tree for forensic applications based on whole genome SNPs. Forensic Sci. Int. Genet. 7, 573–580 (2013). · DOI
  38. Drummond, A. J., Rambaut, A., Shapiro, B. & Pybus, O. G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192 (2005). · DOI
  39. Forster, P., Harding, R., Torroni, A. & Bandelt, H.-J. Origin and evolution of Native American mtDNA variation: a reappraisal. Am. J. Hum. Genet. 59, 935–945 (1996).
  40. Saillard, J., Forster, P., Lynnerup, N., Bandelt, H.-J. & Nørby, S. mtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. Am. J. Hum. Genet. 67, 718–726 (2000). · DOI · Paper page
  41. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989). · DOI
  42. Fu, Y. X. & Li, W. H. Statistical tests of neutrality of mutations. Genetics 133, 693–709 (1993). · DOI
  43. Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010). · DOI
  44. Excoffier, L., Dupanloup, I., Huerta-Sanchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013). · DOI
  45. Hamilton, G., Stoneking, M. & Excoffier, L. Molecular analysis reveals tighter social regulation of immigration in patrilocal populations than in matrilocal populations. Proc. Natl Acad. Sci. USA 102, 7476–7480 (2005). · DOI · Paper page

Cited by

Metadata

Authors
Batini, C., Hallast, P., Zadik, D., Delser, P. M., Benazzo, A., Ghirotto, S., Arroyo-Pardo, E., Cavalleri, G. L., de Knijff, P., Dupuy, B. M., Eriksen, H. A., King, T. E., de Munain, A. L., López-Parra, A. M., Loutradis, A., Milasin, J., Novelletto, A., Pamjav, H., Sajantila, A., Tolun, A., Winney, B., & Jobling, M. A.
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2015-05-19
Volume
6
Issue
1
ISSN
2041-1723
DOI
10.1038/ncomms8152
PMC
PMC4441248
Cited by
91
References
11
Language
en
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