The Y-chromosome tree bursts into leaf: 13,000 high-confidence SNPs covering the majority of known clades

Molecular Biology and Evolution

Volumn 32, Issue 3, 2014, Pages 661-673

  Hallast, Pille ^a   Batini, Chiara ^a   Zadik, Daniel ^a   Delser, Pierpaolo Maisano ^a   Wetton, Jon H ^a   Arroyo Pardo, Eduardo ^b   Cavalleri, Gianpiero L ^c   De Knijff, Peter ^d   Bisol, Giovanni Destro ^e,f   Dupuy, Berit Myhre ^g   Eriksen, Heidi A ^h,i   Jorde, Lynn B ^j   King, Turi E ^a   Larmuseau, Maarten H ^k,l   De Munain, Adolfo López ^m   López Parra, Ana M ^b   Loutradis, Aphrodite ⁿ   Milasin, Jelena ^o   Novelletto, Andrea ^p   Pamjav, Horolma ^q   Sajantila, Antti ^r,s   Schempp, Werner ^t   Sears, Matt ^a   Tolun, Aslihan ^u   Tyler Smith, Chris ^v   Van Geystelen, Anneleen ^k   Watkins, Scott ^j   Winney, Bruce ^w   Jobling, Mark A ^a   more..

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c Faculty of Medicine   (Ireland)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e Istituto Italiano di Antropologia   (Italy)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^h UNIVERSITY OF OULU   (Finland)

ⁱ Municipality of Utsjoki Health Centre   (Finland)

^j UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

^k UNIVERSITY OF LEUVEN   (Belgium)

^l DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^m UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

ⁿ Unit of Prenatal Diagnosis   (Greece)

^o UNIVERSITY OF BELGRADE   (Serbia)

^p UNIVERSITY OF ROME TOR VERGATA   (Italy)

^q Institute of Forensic Medicine   (Hungary)

^r UNIVERSITY OF HELSINKI   (Finland)

^s UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^t UNIVERSITY OF FREIBURG   (Germany)

^u BOGAZICI UNIVERSITY   (Turkey)

^v WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^w UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

Purifying selection; Single nucleotide polymorphisms; Targeted resequencing; Y chromosome phylogeny; Y STRs

Indexed keywords

ARTICLE; CLADISTICS; GENE MUTATION; HUMAN; MALE; MOLECULAR EVOLUTION; PHYLOGENETIC TREE; PHYLOGENY; PURIFYING SELECTION; SHORT TANDEM REPEAT; SINGLE NUCLEOTIDE POLYMORPHISM; Y CHROMOSOME; DNA SEQUENCE; GENETICS; HAPLOTYPE MAP;

CHROMOSOMES, HUMAN, Y; EVOLUTION, MOLECULAR; HAPMAP PROJECT; HUMANS; MALE; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA;

EID: 84927738893     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu327     Document Type: Article

References (57)

1. Genomes Project Consortium, Durbin RM, Abecasis GR, Altshuler DL, Auton A, Brooks LD, Gibbs RA, Hurles ME, McVean GA. 2010. A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073. 1000
2. Balaresque P, Bowden GR, Parkin EJ, Omran GA, Heyer E, Quintana-Murci L, Roewer L, Stoneking M, Nasidze I, Carvalho-Silva DR. 2008. Dynamic nature of the proximal AZFc region of the human Y chromosome: Multiple independent deletion and duplication events revealed by microsatellite analysis. Hum Mutat. 29: 1171-1180.
3. Balaresque P, King TE, Parkin EJ, Heyer E, Carvalho-Silva D, Kraaijenbrink T, de Knijff P, Tyler-Smith C, Jobling MA. 2014. Gene conversion violates the stepwise mutation model for microsatellites in Y-chromosomal palindromic repeats. Hum Mutat. 35: 609-617.
4. Balaresque P, Parkin EJ, Roewer L, Carvalho-Silva DR, Mitchell RJ, van Oorschot RAH, Henke J, Stoneking M, Nasidze I, Wetton J. 2008. Genomic complexity of the Y-STR DYS19: Inversions, deletions and founder lineages carrying duplications. Int J Legal Med. 123: 15-23.
5. Ballantyne KN, Goedbloed M, Fang R, Schaap O, Lao O, Wollstein A, Choi Y, van Duijn K, Vermeulen M, Brauer S. 2010. Mutability of Ychromosomal microsatellites: Rates, characteristics, molecular bases, and forensic implications. Am J Hum Genet. 87: 341-353.
6. Ballantyne KN, Keerl V, Wollstein A, Choi Y, Zuniga SB, Ralf A, Vermeulen M, de Knijff P, Kayser M. 2012. A new future of forensic Y-chromosome analysis: Rapidly mutating Y-STRs for differentiating male relatives and paternal lineages. Forensic Sci Int Genet. 6: 208-218.
7. Bandelt H-J, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16: 37-48.
8. Bellott DW, Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Cho TJ, Koutseva N, Zaghlul S, Graves T, Rock S. 2014. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508: 494-499.
9. Berniell-Lee G, Calafell F, Bosch E, Heyer E, Sica L, Mouguiama-Daouda P, van der Veen L, Hombert JM, Quintana-Murci L, Comas D. 2009. Genetic and demographic implications of the Bantu expansion: Insights from human paternal lineages. Mol Biol Evol. 26: 1581-1589.
10. Bosch E, Hurles ME, Navarro A, Jobling MA. 2004. Dynamics of a human interparalog gene conversion hotspot. Genome Res. 14: 835-844.
11. Busby GB, Brisighelli F, Sanchez-Diz P, Ramos-Luis E, Martinez-Cadenas C, Thomas MG, Bradley DG, Gusmao L,Winney B, BodmerW. 2012. The peopling of Europe and the cautionary tale of Y chromosome lineage R-M269. Proc Biol Sci. 279: 884-892.
12. Chang X, Wang K. 2012. wANNOVAR: Annotating genetic variants for personal genomes via the web. J Med Genet. 49: 433-436.
13. Charchar FJ, Bloomer LD, Barnes TA, Cowley MJ, Nelson CP, Wang Y, Denniff M, Debiec R, Christofidou P, Nankervis S. 2012. Inheritance of coronary artery disease in men: An analysis of the role of the Y chromosome. Lancet 379: 915-922.
14. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7: 214.
15. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 22: 1185-1192.
16. Elhaik E, Tatarinova TV, Klyosov AA, Graur D. 2014. 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.
17. Felsenstein J 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author (Department of Genome Sciences, University of Washington, Seattle, WA).
18. Forster P, Harding R, Torroni A, Bandelt H-J. 1996. Origin and evolution of Native American mtDNA variation: A reappraisal. Am J Hum Genet. 59: 935-945.
19. Francalacci P, Morelli L, Angius A, Berutti R, Reinier F, Atzeni R, Pilu R, Busonero F, Maschio A, Zara I. 2013. Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y-chromosome phylogeny. Science 341: 565-569.
20. Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW. 1995a. An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463-471.
21. Goldstein DB, Linares AR, Cavalli-Sforza LL, Feldman MW. 1995b. Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci U S A. 92: 6723-6727.
22. Hallast P, Balaresque P, Bowden GR, Ballereau SJ, Jobling MA. 2013. Recombination dynamics of a human Y-chromosomal palindrome: Rapid GC-biased gene conversion, multi-kilobase conversion tracts, and rare inversions. PLoS Genet. 9: E1003666.
23. Hammer MF. 1995. A recent common ancestry for human Y chromosomes. Nature 378: 376-378.
24. Hammer MF, Behar DM, Karafet TM, Mendez FL, Hallmark B, Erez T, Zhivotovsky LA, Rosset S, Skorecki K. 2009. Extended Y chromosome haplotypes resolvemultiple and unique lineages of the Jewish priesthood. Hum Genet. 126: 707-717.
25. Jobling MA, Lo IC, Turner DJ, Bowden GR, Lee AC, Xue Y, Carvalho-Silva D, Hurles ME, Adams SM, Chang YM. 2007. Structural variation on the short arm of the human Y chromosome: Recurrent multigene deletions encompassing Amelogenin Y. Hum Mol Genet. 16: 307-316.
26. Jobling MA, Tyler-Smith C. 2003. The human Y chromosome: An evolutionary marker comes of age. Nat Rev Genet. 4: 598-612.
27. Karafet TM, Mendez FL, Meilerman M, Underhill PA, Zegura SL, Hammer MF. 2008. New binary polymorphisms reshape and increase resolution of the human Y-chromosomal haplogroup tree. Genome Res. 18: 830-838.
28. Karafet TM, Zegura SL, Posukh O, Osipova L, Bergen A, Long J, Goldman D, KlitzW, Harihara S, de Knijff P. 1999. Ancestral Asian source(s) of New World Y-chromosome founder haplotypes. Am J Hum Genet. 64: 817-831.
29. King TE, Parkin EJ, Swinfield G, Cruciani F, Scozzari R, Rosa A, Lim SK, Xue Y, Tyler-Smith C, Jobling MA. 2007. Africans in Yorkshire? The deepest-rooting clade of the Y phylogeny within an English genealogy. Eur J Hum Genet. 15: 288-293.
30. Kuroki Y, Toyoda A, Noguchi H, Taylor TD, Itoh T, Kim DS, Kim DW, Choi SH, Kim IC, Choi HH. 2006. Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nat Genet. 38: 158-167.
31. Larmuseau MH, Vanderheyden N, Van Geystelen A, van Oven M, de Knijff P, Decorte R. 2014. Recent radiation within Y-chromosomal haplogroup R-M269 resulted in high Y-STR haplotype resemblance. Ann Hum Genet. 78: 92-103.
32. Mendez FL, Krahn T, Schrack B, Krahn AM, Veeramah KR, Woerner AE, Fomine FL, Bradman N, Thomas MG, Karafet TM. 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.
33. Mendizabal I, Valente C, Gusmao A, Alves C, Gomes V, Goios A, Parson W, Calafell F, Alvarez L, Amorim A. 2011. Reconstructing the Indian origin and dispersal of the European Roma: A maternal genetic perspective. PLoS One 6: E15988.
34. Poznik GD, Henn BM, Yee MC, Sliwerska E, Euskirchen GM, Lin AA, Snyder M, Quintana-Murci L, Kidd JM, Underhill PA. 2013. Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341: 562-565.
35. Purps JS, Siegert S,Willuweit S, Nagy M, Alves C, Salazar R, Angustia SM, Santos LH, Anslinger K, Bayer B. 2014. A global analysis of Y-chromosomal haplotype diversity for 23 STR loci. Forensic Sci Int Genet. 12C: 12-23.
36. Rambaut A 2006-2012. Fig.Tree. Tree figure drawing tool. Version 1.4.0. Available from: Http://tree.bio.ed.ac.uk/software/figtree/.
37. Repping S, van Daalen SK, Brown LG, Korver CM, Lange J, Marszalek JD, Pyntikova T, van der Veen F, Skaletsky H, Page DC. 2006. High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nat Genet. 38: 463-467.
38. Rocca RA, Magoon G, Reynolds DF, Krahn T, Tilroe VO, Op den Velde Boots PM, Grierson AJ. 2012. Discovery of Western European R1b1a2 Y chromosome variants in 1000 genomes project data: An online community approach. PLoS One 7: E41634.
39. Rosser ZH, Balaresque P, Jobling MA. 2009. Gene conversion between the X chromosome and the male-specific region of the Y chromosome at a translocation hotspot. Am J Hum Genet. 85: 130-134.
40. Rozen S, Marszalek JD, Alagappan RK, Skaletsky H, Page DC. 2009. Remarkably little variation in proteins encoded by the Y chromosome's single-copy genes, implying effective purifying selection. Am J Hum Genet. 85: 923-928.
41. Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Page DC. 2003. Abundant gene conversion between arms of massive palindromes in human and ape Y chromosomes. Nature 423: 873-876.
42. Saillard J, Forster P, Lynnerup N, Bandelt H-J, Nørby S. 2000. mtDNA variation among Greenland Eskimos: The edge of the Beringian expansion. Am J Hum Genet. 67: 718-726.
43. Scozzari R, Massaia A, Trombetta B, Bellusci G,Myres NM, Novelletto A, Cruciani F. 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.
44. Sezgin E, Lind JM, Shrestha S, Hendrickson S, Goedert JJ, Donfield S, Kirk GD, Phair JP, Troyer JL, O'Brien SJ. 2009. Association of Y chromosome haplogroup I with HIV progression, and HAART outcome. Hum Genet. 125: 281-294.
45. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova R, Ali J, Bieri T. 2003. The male-specific region of the human Y chromosome: A mosaic of discrete sequence classes. Nature 423: 825-837.
46. Trombetta B, Cruciani F, Underhill PA, Sellitto D, Scozzari R. 2010. Footprints of X-to-Y gene conversion in recent human evolution. Mol Biol Evol. 27: 714-725.
47. Trombetta B, Sellitto D, Scozzari R, Cruciani F. 2014. Inter-and intraspecies phylogenetic analyses reveal extensive x-y gene conversion in the evolution of gametologous sequences of human sex chromosomes. Mol Biol Evol. 31: 2108-2123.
48. Underhill PA, Shen P, Lin AA, Jin L, Passarino G, Yang WH, Kauffman E, Bonn-e-Tamir B, Bertranpetit J, Francalacci P. 2000. Y chromosome sequence variation and the history of human populations. Nat Genet. 26: 358-361.
49. Van Geystelen A, Decorte R, Larmuseau MH. 2013a. AMY-tree: An algorithm to use whole genome SNP calling for Y chromosomal phylogenetic applications. BMC Genomics 14: 101.
50. Van Geystelen A, Decorte R, Larmuseau MH. 2013b. Updating the Y-chromosomal phylogenetic tree for forensic applications based on whole genome SNPs. Forensic Sci Int Genet. 7: 573-580.
51. van Oven M, Van Geystelen A, Kayser M, Decorte R, Larmuseau MH. 2014. Seeing the wood for the trees: A minimal reference phylogeny for the human Y chromosome. Hum Mutat. 35: 187-191.
52. Wei W, Ayub Q, Chen Y, McCarthy S, Hou Y, Carbone I, Xue Y, Tyler-Smith C. 2013. A calibrated human Y-chromosomal phylogeny based on resequencing. Genome Res. 23: 388-395.
53. Wei W, Ayub Q, Xue Y, Tyler-Smith C. 2013. A comparison of Ychromosomal lineage dating using either resequencing or Y-SNP plus Y-STR genotyping. Forensic Sci Int Genet. 7: 568-572.
54. Wilson Sayres MA, Lohmueller KE, Nielsen R. 2014. Natural selection reduced diversity on human Y chromosomes. PLoS Genet. 10: E1004064.
55. Xue Y,Wang Q, Long Q, Ng BL, Swerdlow H, Burton J, Skuce C, Taylor R, Abdellah Z, Zhao Y. 2009. Human Y chromosome base-substitution mutation rate measured by direct sequencing in a deep-rooting pedigree. Curr Biol. 19: 1453-1457.
56. Y Chromosome Consortium. 2002. A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res. 12: 339-348.
57. Zhivotovsky LA, Underhill PA, Cinnioglu C, Kayser M, Morar B, Kivisild T, Scozzari R, Cruciani F, Destro-Bisol G, Spedini G. 2004. The effective mutation rate at Y chromosome short tandem repeats, with application to human population-divergence time. Am J Hum Genet. 74: 50-61.