Regional differences in the accumulation of SNPs on the male-specific portion of the human y chromosome replicate autosomal patterns: Implications for genetic dating

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Trombetta, Beniamino ^a   D'Atanasio, Eugenia ^a   Massaia, Andrea ^a,e   Myres, Natalie M ^b   Scozzari, Rosaria ^a   Cruciani, Fulvio ^a,c   Novelletto, Andrea ^d  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Ancestry   (United States)

^c CNR   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ARTICLE; AUTOSOME; BIOACCUMULATION; CHROMOSOME; CHROMOSOME REPLICATION; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; GENETIC DATING; GENETIC PROCEDURES; GENETIC VARIABILITY; HUMAN; MALE; MUTATION RATE; PHYLOGENY; SINGLE NUCLEOTIDE POLYMORPHISM; Y CHROMOSOME; MUTATION;

CHROMOSOMES, HUMAN, Y; HUMANS; MALE; MUTATION; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84941975657     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134646     Document Type: Article

References (65)

1. Rito T, Richards MB, Fernandes V, Alshamali F, Cerny V, Pereira L, et al. The first modern human dispersals across Africa. PLoS ONE. 2013; 8:e80031. doi: 10.1371/journal.pone.0080031 PMID: 24236171
2. Underhill PA, Shen P, Lin AA, Jin L, Passarino G, Yang WH, et al. Y chromosome sequence variation and the history of human populations. Nat Genet. 2000; 26:358-61. PMID: 11062480
3. Poznik GD, Henn BM, Yee M-C, Sliwerska E, Euskirchen GM, Lin AA, et al. Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science. 2013; 341:562-5. doi: 10.1126/science.1237619 PMID: 23908239
4. Scozzari R, Massaia A, Trombetta B, Bellusci G, Myres NM, Novelletto A, 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. 2014; 24:535-44. doi: 10.1101/gr.160788.113 PMID: 24395829
5. Wei W, Ayub Q, Chen Y, McCarthy S, Hou Y, Carbone I, et al. A calibrated human Y-chromosomal phylogeny based on resequencing. Genome Res. 2013; 23:388-95. doi: 10.1101/gr.143198.112 PMID: 23038768
6. Francalacci P, Morelli L, Angius A, Berutti R, Reinier F, Atzeni R, et al. Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y-chromosome phylogeny. Science. 2013; 341:565-9. doi: 10.1126/science.1237947 PMID: 23908240
7. Lippold S, Xu H, Ko A, Li M, Renaud G, Butthof A, et al. Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences. Investig Genet. 2014; 5:13. doi: 10.1186/2041-2223-5-13 PMID: 25254093
8. Karmin M, Saag L, Vicente M, Wilson Sayres MA, Järve M, Talas UG, et al. A recent bottleneck of Y chromosome diversity coincides with a global change in culture. Genome Res. 2015; 25:459-66. doi: 10.1101/gr.186684.114 PMID: 25770088
9. Hallast P, Batini C, Zadik D, Maisano Delser P, Wetton J, Arroyo-Pardo E, et al. The Y-chromosome tree bursts into leaf: 13,000 high confidence SNPs covering the majority of known clades. Mol Biol Evol. 2015; 32:661-73. doi: 10.1093/molbev/msu327 PMID: 25468874
10. Batini C, Hallast P, Zadik D, Delser PM, Benazzo A, Ghirotto S, et al. Large-scale recent expansion of European patrilineages shown by population resequencing. Nat Commun. 2015; 6.
11. Mendez FL, Krahn T, Schrack B, Krahn A-M, Veeramah KR, Woerner AE, et al. An African American paternal lineage adds an extremely ancient root to the human Y chromosome phylogenetic tree. Am J Hum Genet. 2013; 92:454-9. doi: 10.1016/j.ajhg.2013.02.002 PMID: 23453668
12. Awadalla P, Gauthier J, Myers RA, Casals F, Hamdan FF, Griffing AR, et al. Direct measure of the de novo mutation rate in autism and schizophrenia cohorts. Am J Hum Genet. 2010; 87:316-24. doi: 10.1016/j.ajhg.2010.07.019 PMID: 20797689
13. Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, et al. Rate of de novo mutations and the importance of father's age to disease risk. Nature. 2012; 488:471-5. doi: 10.1038/nature11396 PMID: 22914163
14. Roach JC, Glusman G, Smit AF, Huff CD, Hubley R, Shannon PT, et al. Analysis of genetic inheritance in a family quartet by whole-genome sequencing. Science. 2010; 328:636-9. doi: 10.1126/science.1186802 PMID: 20220176
15. Elhaik E, Tatarinova TV, Klyosov AA, 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. 2014:1-6.
16. Mendez FL, Veeramah KR, Thomas MG, Karafet T, Hammer MF. Reply to 'The'extremely ancient' chromosomome that ins't'. Eur J Hum Genet. 2014.
17. Elhaik E, Tatarinova TV, Klyosov AA, Graur D. Reply to Mendez et al: the extremely ancient' chromosome that still isn't. Eur J Hum Genet. 2015; 23:567-8. doi: 10.1038/ejhg.2014.227 PMID: 25315661
18. Helgason A, Einarsson AW, Guomundsdóttir VB, Sigurosson Á, Gunnarsdóttir ED, Jagadeesan A, et al. The Y-chromosome point mutation rate in humans. Nat Genet. 2015:Epub ahead of print.
19. Ségurel L, Wyman MJ, Przeworski M. Determinants of mutation rate variation in the human germline. Annu Rev Genomics Hum Genet. 2014; 15:47-70. doi: 10.1146/annurev-genom-031714-125740 PMID: 25000986
20. Makova KD, Hardison RC. The effects of chromatin organization on variation in mutation rates in the genome. Nat Rev Genet. 2015; 16:213-23. doi: 10.1038/nrg3890 PMID: 25732611
21. Michaelson JJ, Shi Y, Gujral M, Zheng H, Malhotra D, Jin X, et al. Whole-genome sequencing in autism identifies hot spots for de novo germline mutation. Cell. 2012; 151:1431-42. doi: 10.1016/j.cell.2012.11.019 PMID: 23260136
22. Hellmann I, Prüfer K, Ji H, Zody MC, Paabo S, Ptak SE. Why do human diversity levels vary at a megabase scale? Genome Res. 2005; 15:1222-31. PMID: 16140990
23. Francioli LC, Polak PP, Koren A, Menelaou A, Chun S, Renkens I, et al. Genome-wide patterns and properties of de novo mutations in humans. Nat Genet. 2015.
24. Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SKM, Minx PJ, et al. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature. 2010; 463:536-9. doi: 10.1038/nature08700 PMID: 20072128
25. Wolfe KH, Sharp PM, Li W-H. Mutation rates differ among regions of the mammalian genome. Nature. 1989; 337:283-5. PMID: 2911369
26. O'Fallon B. Purifying selection causes widespread distortions of genealogical structure on the human X chromosome. Genetics. 2013; 194:485-92. doi: 10.1534/genetics.113.152074 PMID: 23589459
27. Fu Q, Li H, Moorjani P, Jay F, Slepchenko SM, Bondarev AA, et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature. 2014; 514:445-9. doi: 10.1038/nature13810 PMID: 25341783
28. Lazaridis I, Patterson N, Mittnik A, Renaud G, Mallick S, Kirsanow K, et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature. 2014; 513:409-13. doi: 10.1038/nature13673 PMID: 25230663
29. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28:2731-9. doi: 10.1093/molbev/msr121 PMID: 21546353
30. Bandelt HJ, Forster P, Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999; 16:37-48. PMID: 10331250
31. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007; 7:214. PMID: 17996036
32. Hamilton MJ, Burger O, DeLong JP, Walker RS, Moses ME, Brown JH. Population stability, cooperation, and the invasibility of the human species. Proc Natl Acad Sci USA. 2009; 106:12255-60. doi: 10.1073/pnas.0905708106 PMID: 19592508
33. Ammerman AJ, Cavalli-Sforza LL. The Neolithic transition and the genetics of populations in Europe. Princeton: Princeton University Press 1984.
34. Boone JL. Subsistence strategies and early human population history: an evolutionary ecological perspective World Archaeol. 2002; 34:6-25. PMID: 16475305
35. Weddington N, Stuy A, Hiratani I, Ryba T, Yokochi T, Gilbert DM. ReplicationDomain: a visualization tool and comparative database for genome-wide replication timing data. BMC Bioinformatics. 2008; 9:530. doi: 10.1186/1471-2105-9-530 PMID: 19077204
36. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, et al. The DNA sequence of the human X chromosome. Nature. 2005; 434:325-37. PMID: 15772651
37. Lahn BT, Page DC. Four evolutionary strata on the human X chromosome. Science. 1999; 286:964-7. PMID: 10542153
38. Koren A, Polak P, Nemesh J, Michaelson JJ, Sebat J, Sunyaev SR, et al. Differential relationship of DNA replication timing to different forms of human mutation and variation. Am J Hum Genet. 2012; 91:1033-40. doi: 10.1016/j.ajhg.2012.10.018 PMID: 23176822
39. Stamatoyannopoulos JA, Adzhubei I, Thurman RE, Kryukov GV, Mirkin SM, Sunyaev SR. Human mutation rate associated with DNA replication timing. Nat Genet. 2009; 41:393-5. doi: 10.1038/ng.363 PMID: 19287383
40. Niederstätter H, Berger B, Erhart D, Willuweit S, Geppert M, Gassner C, et al. Multiple recurrent mutations at four human Y-chromosomal single nucleotide polymorphism sites in a 37 bp sequence tract on the ARSDP1 pseudogene. Forensic Sci Intl: Genetics. 2013; 7:593-600.
41. Rosser ZH, Balaresque P, Jobling MA. Gene conversion between the X chromosome and the malespecific region of the Y chromosome at a translocation hotspot. Am J Hum Genet 2009; 85:130-4. doi: 10.1016/j.ajhg.2009.06.009 PMID: 19576564
42. Cruciani F, Trombetta B, Macaulay V, Scozzari R. About the X-to-Y gene conversion rate. Am J Hum Genet. 2011; 86:495-7.
43. Trombetta B, Cruciani F, Underhill PA, Sellitto D, Scozzari R. Footprints of X-to-Y gene conversion in recent human evolution. Mol Biol Evol. 2010; 27:714-25. doi: 10.1093/molbev/msp231 PMID: 19812029
44. Trombetta B, Sellitto D, Scozzari R, Cruciani F. Inter-and intraspecies phylogenetic analyses reveal extensive X-Y gene conversion in the evolution of gametologous sequences of human sex chromosomes. Mol Biol Evol. 2014; 31:2108-23. doi: 10.1093/molbev/msu155 PMID: 24817545
45. Rozen S, Marszalek JD, Alagappan RK, Skaletsky H, Page DC. Remarkably little variation in proteins encoded by the Y chromosome's single-copy genes, implying effective purifying selection. Am J Hum Genet. 2009; 85:923-8. doi: 10.1016/j.ajhg.2009.11.011 PMID: 20004767
46. Wilson Sayres MA, Lohmueller KE, Nielsen R. Natural selection reduced diversity on human Y chromosomes. PLoS Genet. 2014; 10:e1004064. doi: 10.1371/journal.pgen.1004064 PMID: 24415951
47. Montano V, Ferri G, Marcari V, Batini C, Anyaele O, Destro-Bisol G, et al. The Bantu expansion revisited: a new analysis of Y chromosome variation in Central Western Africa. Mol Ecol. 2011; 20:2693-708. doi: 10.1111/j.1365-294X.2011.05130.x PMID: 21627702
48. Underhill P, Poznik GD, Rootsi S, Järve M, Lin A, Wang J, et al. The phylogenetic and geographic structure of Y-chromosome haplogroup R1a. Eur J Hum Genet. 2014; 23:124-31. doi: 10.1038/ejhg.2014.50 PMID: 24667786
49. Underhill PA, Myres NM, Rootsi S, Metspalu M, Zhivotovsky LA, King RJ, et al. Separating the post-Glacial coancestry of European and Asian Y chromosomes within haplogroup R1a. Eur J Hum Genet. 2010; 18:479-84. doi: 10.1038/ejhg.2009.194 PMID: 19888303
50. Balaresque P, Bowden GR, Adams SM, Leung H-Y, King TE, Rosser ZH, et al. A predominantly Neolithic origin for European paternal lineages. PLoS Biol. 2010; 8:e1000285. doi: 10.1371/journal.pbio.1000285 PMID: 20087410
51. Myres NM, Rootsi S, Lin AA, Järve M, King RJ, Kutuev I, et al. A major Y-chromosome haplogroup R1b Holocene era founder effect in Central and Western Europe. Eur J Hum Genet. 2011; 19:95-101. doi: 10.1038/ejhg.2010.146 PMID: 20736979
52. Ralph P, Coop G. The geography of recent genetic ancestry across Europe. PLoS Biol. 2013; 11: e1001555. doi: 10.1371/journal.pbio.1001555 PMID: 23667324
53. Keinan A, Clark AG. Recent explosive human population growth has resulted in an excess of rare genetic variants. Science. 2012; 336:740-3. doi: 10.1126/science.1217283 PMID: 22582263
54. Elango N, Kim S-H, Vigoda E, Yi SV, Nisc Comparative Sequencing Program. Mutations of different molecular origins exhibit contrasting patterns of regional substitution rate variation. PLoS Comput Biol. 2008; 4:e1000015. doi: 10.1371/journal.pcbi.1000015 PMID: 18463707
55. Schaibley VM, Zawistowski M, Wegmann D, Ehm MG, Nelson MR, St Jean PL, et al. The influence of genomic context on mutation patterns in the human genome inferred from rare variants. Genome Res. 2013; 23:1974-84. doi: 10.1101/gr.154971.113 PMID: 23990608
56. Hodgkinson A, Ladoukakis E, Eyre-Walker A. Cryptic variation in the human mutation rate. PLoS Biology. 2009; 7:e27.
57. Wang CC, Gilbert MTP, Jin L, Li H. Evaluating the Y chromosomal timescale in human demographic and lineage dating. Investig Genet. 2014; 5:12. doi: 10.1186/2041-2223-5-12 PMID: 25215184
58. Henn BM, Gignoux CR, Feldman MW, Mountain JL. Characterizing the time dependency of human mitochondrial DNA mutation rate estimates. Mol Biol Evol. 2009; 26:217-30. doi: 10.1093/molbev/msn244 PMID: 18984905
59. Zhivotovsky LA, Underhill PA, Feldman MW. Difference between evolutionarily effective and germ-line mutation rate due to stochastically varying haplogroup size. Mol Biol Evol. 2006; 23:2268-70. PMID: 16956974
60. Soares P, Alshamali F, Pereira JB, Fernandes V, Silva NM, Afonso C, et al. The expansion of mtDNA haplogroup L3 within and out of Africa. Mol Biol Evol. 2011; 29:915-27. doi: 10.1093/molbev/msr245 PMID: 22096215
61. Rowley-Conwy P. Westward Ho! Curr Anthrop. 2011; 52:S431-S51.
62. Allentoft ME, Sikora M, Sjogren K-G, Rasmussen S, Rasmussen M, Stenderup J, et al. Population genomics of Bronze Age Eurasia. Nature. 2015; 522:167-72. doi: 10.1038/nature14507 PMID: 26062507
63. Haak W, Lazaridis I, Patterson N, Rohland N, Mallick S, Llamas B, et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature. 2015; 522:207-11. doi: 10.1038/nature14317 PMID: 25731166
64. van Oven M, Van Geystelen A, Kayser M, Decorte R, Lermuseau MH. Seeing the wood for the trees: a minimal reference phylogeny for the human Y chromosome. Hum Mut. 2014; 35:187-91. doi: 10.1002/humu.22468 PMID: 24166809
65. Trombetta B, D'Atanasio E, Massaia A, Ippoliti M, Coppa A, Candilio F, et al. Phylogeographic refinement and large scale genotyping of human Y chromosome haplogroup E provide new insights into the dispersal of early pastoralists in the African continent. Genome Biol Evol. 2015:Jun 24. pii: evv118. [Epub ahead of print].