A rare deep-rooting D0 African Y-chromosomal haplogroup and its implications for the expansion of modern humans out of Africa

Genetics

Volumn 212, Issue 4, 2019, Pages 1421-1428

  Haber, Marc ^a   Jones, Abigail L ^b   Connell, Bruce A ^c   Asan, ^d   Arciero, Elena ^a   Yang, Huanming ^d,e   Thomas, Mark G ^f   Xue, Yali ^a   Tyler Smith, Chris ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b LIVERPOOL WOMEN S HOSPITAL   (United Kingdom)

^c YORK UNIVERSITY   (Canada)

^d BGI SHENZHEN   (China)

^e James D Watson Institute of Genome Science   (China)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Human Y chromosome; Out of Africa migration; Phylogeography; YAP+ Y chromosomes

Indexed keywords

ADULT; AFRICA; ARTICLE; CASE REPORT; CLINICAL ARTICLE; HUMAN; HUMAN EXPERIMENT; MALE; NIGERIAN; PHYLOGENY; PHYLOGEOGRAPHY; ROOTING; RUNNING; Y CHROMOSOME HAPLOGROUP; GENETIC POLYMORPHISM; GENETICS; HAPLOTYPE; MIGRATION; MOLECULAR EVOLUTION; NIGERIA; Y CHROMOSOME;

CHROMOSOMES, HUMAN, Y; EVOLUTION, MOLECULAR; HAPLOTYPES; HUMAN MIGRATION; HUMANS; MALE; NIGERIA; PHYLOGENY; POLYMORPHISM, GENETIC;

EID: 85071351886     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.119.302368     Document Type: Article

References (55)

1. Altheide, T. K., and M. F. Hammer, 1997 Evidence for a possible Asian origin of YAP+ Y chromosomes. Am. J. Hum. Genet. 61: 462-466. https://doi.org/10.1016/S0002-9297(07)64077-4
2. Bae, C. J., K. Douka, and M. D. Petraglia, 2017 On the origin of modern humans: Asian perspectives. Science 358: 1269. https://doi.org/10.1126/science.aai9067
3. Balanovsky, O., 2017 Toward a consensus on SNP and STR mutation rates on the human Y-chromosome. Hum. Genet. 136: 575-590. https://doi.org/10.1007/s00439-017-1805-8
4. Barbieri, C., A. Hübner, E. Macholdt, S. Ni, S. Lippold et al., 2016 Refining the Y chromosome phylogeny with southern African sequences. Hum. Genet. 135: 541-553. https://doi.org/10.1007/s00439-016-1651-0
5. Bravi, C. M., G. Bailliet, V. L. Martinez-Marignac, and N. O. Bianchi, 2000 Origin of YAP+ lineages of the human Y-chromosome. Am. J. Phys. Anthropol. 112: 149-158. https://doi.org/10.1002/(SICI)1096-8644(2000)112:2,149::AID-AJPA2.3.0.CO;2-M
6. Clarkson, C., Z. Jacobs, B. Marwick, R. Fullagar, L. Wallis et al., 2017 Human occupation of northern Australia by 65,000 years ago. Nature 547: 306-310. https://doi.org/10.1038/nature22968
7. D'Atanasio, E., B. Trombetta, M. Bonito, A. Finocchio, G. Di Vito et al., 2018 The peopling of the last Green Sahara revealed by high-coverage resequencing of trans-Saharan patrilineages. Genome Biol. 19: 20. https://doi.org/10.1186/s13059-018-1393-5
8. Demeter, F., L. L. Shackelford, A. M. Bacon, P. Duringer, K. Westaway et al., 2012 Anatomically modern human in Southeast Asia (Laos) by 46 ka. Proc. Natl. Acad. Sci. USA 109: 14375-14380. https://doi.org/10.1073/pnas.1208104109
9. Devièse, T., D. Massilani, S. Yi, D. Comeskey, S. Nagel et al., 2019 Compound-specific radiocarbon dating and mitochondrial DNA analysis of the Pleistocene hominin from Salkhit Mongolia. Nat. Commun. 10: 274. https://doi.org/10.1038/s41467-018-08018-8
10. Fernandes, V., F. Alshamali, M. Alves, M. D. Costa, J. B. Pereira et al., 2012 The Arabian cradle: mitochondrial relicts of the first steps along the southern route out of Africa. Am. J. Hum. Genet. 90: 347-355. https://doi.org/10.1016/j.ajhg.2011.12.010
11. Forster, P., R. Harding, A. Torroni, and H. J. Bandelt, 1996 Origin and evolution of Native American mtDNA variation: a reappraisal. Am. J. Hum. Genet. 59: 935-945.
12. Fu, Q., A. Mittnik, P. L. F. Johnson, K. Bos, M. Lari et al., 2013 A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23: 553-559. https://doi.org/10.1016/j.cub.2013.02.044
13. Fu, Q., H. Li, P. Moorjani, F. Jay, S. M. Slepchenko et al., 2014 Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514: 445-449. https://doi.org/10.1038/nature13810
14. Garrison, E., and G. Marth, 2012 Haplotype-based variant detection from short-read sequencing. arXiv:1207.3907.
15. Green, R. E., J. Krause, A. W. Briggs, T. Maricic, U. Stenzel et al., 2010 A draft sequence of the Neandertal genome. Science 328: 710-722. https://doi.org/10.1126/science.1188021
16. Gronau, I., M. J. Hubisz, B. Gulko, C. G. Danko, and A. Siepel, 2011 Bayesian inference of ancient human demography from individual genome sequences. Nat. Genet. 43: 1031-1034. https://doi.org/10.1038/ng.937
17. Haber, M., M. Mezzavilla, A. Bergstrom, J. Prado-Martinez, P. Hallast et al., 2016 Chad genetic diversity reveals an African history marked by multiple Holocene Eurasian migrations. Am. J. Hum. Genet. 99: 1316-1324. https://doi.org/10.1016/j.ajhg.2016.10.012
18. Hallast, P., C. Batini, D. Zadik, P. Maisano Delser, J. H. Wetton et al., 2015 The Y-chromosome tree bursts into leaf: 13,000 high-confidence SNPs covering the majority of known clades. Mol. Biol. Evol. 32: 661-673. https://doi.org/10.1093/molbev/msu327
19. Hammer,M. F., T. Karafet, A. Rasanayagam, E. T.Wood, T. K. Altheide et al., 1998 Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol. Biol. Evol. 15: 427-441. https://doi.org/10.1093/oxfordjournals.molbev.a025939
20. Helgason, A., A. W. Einarsson, V. B. Guethmundsdottir, A. Sigurethsson, E. D. Gunnarsdottir et al., 2015 The Y-chromosome point mutation rate in humans. Nat. Genet. 47: 453-457. https://doi.org/10.1038/ng.3171
21. Henn, B. M., T. E. Steele, and T. D. Weaver, 2018 Clarifying distinct models of modern human origins in Africa. Curr. Opin. Genet. Dev. 53: 148-156. https://doi.org/10.1016/j.gde.2018. 10.003
22. Higham, T., T. Compton, C. Stringer, R. Jacobi, B. Shapiro et al., 2011 The earliest evidence for anatomically modern humans in northwestern Europe. Nature 479: 521-524. https://doi.org/10.1038/nature10484
23. Ingman, M., H. Kaessmann, S. Paabo, and U. Gyllensten, 2000 Mitochondrial genome variation and the origin of modern humans. Nature 408: 708-713. https://doi.org/10.1038/35047064
24. Karmin, M., L. Saag, M. Vicente, M. A. Wilson Sayres, M. Jarve et al., 2015 A recent bottleneck of Y chromosome diversity coincides with a global change in culture. Genome Res. 25: 459-466. https://doi.org/10.1101/gr.186684.114
25. Lazaridis, I., D. Nadel, G. Rollefson, D. C. Merrett, N. Rohland et al., 2016 Genomic insights into the origin of farming in the ancient Near East. Nature 536: 419-424. https://doi.org/10.1038/nature19310
26. Letunic, I., and P. Bork, 2016 Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44: W242-W245. https://doi.org/10.1093/nar/gkw290
27. Liu,W., M. Martinon-Torres, Y. J. Cai, S. Xing, H.W. Tong et al., 2015 The earliest unequivocally modern humans in southern China. Nature 526: 696-699. https://doi.org/10.1038/nature15696
28. Mallick, S., H. Li, M. Lipson, I. Mathieson, M. Gymrek et al., 2016 The simons genome diversity project: 300 genomes from 142 diverse populations. Nature 538: 201-206. https://doi.org/10.1038/nature18964
29. Mendez, F. L., T. Krahn, B. Schrack, A. M. Krahn, K. R. Veeramah et al., 2013 An African American paternal lineage adds an extremely ancient root to the human Y chromosome phylogenetic tree. Am. J. Hum. Genet. 92: 454-459 (erratum: Am J. Hum. Genet. 92: 637). https://doi.org/10.1016/j.ajhg.2013. 02.002
30. Mondal, M., A. Bergström, Y. Xue, F. Calafell, H. Laayouni et al., 2017 Y-chromosomal sequences of diverse Indian populations and the ancestry of the Andamanese. Hum. Genet. 136: 499-510. https://doi.org/10.1007/s00439-017-1800-0
31. Pagani, L., D. J. Lawson, E. Jagoda, A. Morseburg, A. Eriksson et al., 2016 Genomic analyses inform on migration events during the peopling of Eurasia. Nature 538: 238-242. https://doi.org/10.1038/nature19792
32. Patin, E., M. Lopez, R. Grollemund, P. Verdu, C. Harmant et al., 2017 Dispersals and genetic adaptation of Bantu-speaking populations in Africa and North America. Science 356: 543-546. https://doi.org/10.1126/science.aal1988
33. Patterson, N., A. L. Price, and D. Reich, 2006 Population structure and eigenanalysis. PLoS Genet. 2: e190. https://doi.org/10.1371/journal.pgen.0020190
34. Patterson, N., P. Moorjani, Y. Luo, S. Mallick, N. Rohland et al., 2012 Ancient admixture in human history. Genetics 192: 1065-1093. https://doi.org/10.1534/genetics.112.145037
35. Poznik, G. D., 2016 Identifying Y-chromosome haplogroups in arbitrarily large samples of sequenced or genotyped men. bio-Rxiv: 088716.
36. Poznik, G. D., B. M. Henn, M. C. Yee, E. Sliwerska, G. M. Euskirchen et al., 2013 Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males vs. females. Science 341: 562-565. https://doi.org/10.1126/science.1237619
37. Poznik, G. D., Y. Xue, F. L. Mendez, T. F. Willems, A. Massaia et al., 2016 Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences. Nat. Genet. 48: 593-599. https://doi.org/10.1038/ng.3559
38. R Core Team, 2017 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
39. Rosa, A., C. Ornelas, M. A. Jobling, A. Brehm, and R. Villems, 2007 Y-chromosomal diversity in the population of Guinea-Bissau: a multiethnic perspective. BMC Evol. Biol. 7: 124. https://doi.org/10.1186/1471-2148-7-124
40. Scally, A., and R. Durbin, 2012 Revising the human mutation rate: implications for understanding human evolution. Nat. Rev. Genet. 13: 745-753 (erratum: Nat. Rev. Genet. 13: 824). https://doi.org/10.1038/nrg3295
41. Scerri, E. M. L., M. G. Thomas, A. Manica, P. Gunz, J. T. Stock et al., 2018 Did our species evolve in subdivided populations across Africa, and why does it matter? Trends Ecol. Evol. 33: 582-594. https://doi.org/10.1016/j.tree.2018.05.005
42. Schlebusch, C. M., P. Skoglund, P. Sjodin, L. M. Gattepaille, D. Hernandez et al., 2012 Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science 338: 374-379. https://doi.org/10.1126/science.1227721
43. Schlebusch, C. M., H. Malmstrom, T. Gunther, P. Sjodin, A. Coutinho et al., 2017 Southern African ancient genomes estimate modern human divergence to 350,000 to 260,000 years ago. Science 358: 652-655. https://doi.org/10.1126/science.aao6266
44. Scozzari, R., A. Massaia, B. Trombetta, G. Bellusci, N. M. Myres et al., 2014 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. https://doi.org/10.1101/gr.160788.113
45. Shi, H., H. Zhong, Y. Peng, Y. L. Dong, X. B. Qi et al., 2008 Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations. BMC Biol. 6: 45. https://doi.org/10.1186/1741-7007-6-45
46. Skoglund, P., J. C. Thompson, M. E. Prendergast, A. Mittnik, K. Sirak et al., 2017 Reconstructing prehistoric African population structure. Cell 171: 59-71. https://doi.org/10.1016/j.cell. 2017.08.049
47. Stamatakis, A., 2014 RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. https://doi.org/10.1093/bioinformatics/btu033
48. Underhill, P. A., and C. C. Roseman, 2001 The case for an African rather than an Asian origin of the human Y-chromosome YAP insertion, pp. 43-56 in Genetic, Linguistic and Archaeological Perspectives on Human Diversity in Southeast Asia: Recent Advances in Human Biology, edited by L. Jin, M. Seielstad, and C. Xiao. World Scientific Publishing, Singapore. https://doi.org/10.1142/9789812810847-0004
49. Underhill, P. A., G. Passarino, A. A. Lin, P. Shen, M. Mirazon Lahr et al., 2001 The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann. Hum. Genet. 65: 43-62. https://doi.org/10.1046/j.1469-1809.2001.6510043.x
50. van Oven, M., and M. Kayser, 2009 Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat. 30: E386-E394. https://doi.org/10.1002/humu.20921
51. Veeramah, K. R., D. Wegmann, A. Woerner, F. L. Mendez, J. C. Watkins et al., 2012 An early divergence of KhoeSan ancestors from those of other modern humans is supported by an ABCbased analysis of autosomal resequencing data. Mol. Biol. Evol. 29: 617-630. https://doi.org/10.1093/molbev/msr212
52. Veth, P., I. Ward, T. Manne, S. Ulm, K. Ditchfield et al., 2017 Early human occupation of a maritime desert, Barrow Island, North-West Australia. Quat. Sci. Rev. 168: 19-29. https://doi.org/10.1016/j.quascirev.2017.05.002
53. Weale, M. E., T. Shah, A. L. Jones, J. Greenhalgh, J. F. Wilson et al., 2003 Rare deep-rooting Y chromosome lineages in humans: lessons for phylogeography. Genetics 165: 229-234.
54. Wei, W., Q. Ayub, Y. Chen, S. McCarthy, Y. Hou et al., 2013 A calibrated human Y-chromosomal phylogeny based on resequencing. Genome Res. 23: 388-395. https://doi.org/10.1101/gr.143198.112
55. Xue, Y., T. Zerjal, W. Bao, S. Zhu, Q. Shu et al., 2006 Male demography in East Asia: a north-south contrast in human population expansion times. Genetics 172: 2431-2439. https://doi.org/10.1534/genetics.105.054270