Human Y-chromosome variation in the genome-sequencing era

Nature Reviews Genetics

Volumn 18, Issue 8, 2017, Pages 485-497

  Jobling, Mark A ^a   Tyler Smith, Chris ^b  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANCIENT DNA;

GENETIC VARIATION; HUMAN; MOLECULAR PHYLOGENY; MUTATION RATE; NEXT GENERATION SEQUENCING; POPULATION GENETICS; PRIORITY JOURNAL; REVIEW; WHOLE GENOME SEQUENCING; Y CHROMOSOME; Y CHROMOSOME LINKED DISORDER; CHEMISTRY; DNA SEQUENCE; GENETICS; PHYLOGENY; SINGLE NUCLEOTIDE POLYMORPHISM;

CHROMOSOMES, HUMAN, Y; GENETICS, POPULATION; HUMANS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA;

EID: 85024497631     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg.2017.36     Document Type: Review

References (138)

1. Bachtrog, D. Y-Chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14, 113-124 (2013).
2. Repping, S. et al. High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nat. Genet. 38, 463-467 (2006).
3. Jobling, M. A. Copy number variation on the human Y chromosome. Cytogenet. Genome Res. 123, 253-262 (2008).
4. Poznik, G. D. et al. Punctuated bursts in human male demography inferred from 1,244 worldwide Y chromosome sequences. Nat. Genet. 48, 593-599 (2016).
5. Heyer, E., Chaix, R., Pavard, S. & Austerlitz, F. Sex-specific demographic behaviours that shape human genomic variation. Mol. Ecol. 21, 597-612 (2012).
6. Jobling, M. A., Pandya, A. & Tyler-Smith, C. The Y chromosome in forensic analysis and paternity testing. Int. J. Legal Med. 110, 118-124 (1997).
7. Calafell, F. & Larmuseau, M. H. The Y chromosome as the most popular marker in genetic genealogy benefits interdisciplinary research. Hum. Genet. 136, 559-573 (2017).
8. Ober, C., Loisel, D. A. & Gilad, Y. Sex-specific genetic architecture of human disease. Nat. Rev. Genet. 9, 911-922 (2008).
9. McElreavey, K., Ravel, C., Chantot-Bastaraud, S. & Siffroi, J. P. Y chromosome variants and male reproductive function. Int. J. Androl. 29, 298-303 (2006).
10. Forsberg, L. A., Gisselsson, D. & Dumanski, J. P. Mosaicism in health and disease - clones picking up speed. Nat. Rev. Genet. 18, 128-142 (2016).
11. Jobling, M. A. & Tyler-Smith, C. The human Y chromosome: an evolutionary marker comes of age. Nat. Rev. Genet. 4, 598-612 (2003).
12. Y Chromosome Consortium. A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res. 12, 339-348 (2002).
13. de Knijff, P. Messages through bottlenecks: on the combined use of slow and fast evolving polymorphic markers on the human Y chromosome. Am. J. Hum. Genet. 67, 1055-1061 (2000).
14. Zerjal, T. et al. Genetic relationships of Asians and northern Europeans, revealed by Y-chromosomal DNA analysis. Am. J. Hum. Genet. 60, 1174-1183 (1997).
15. Heyer, E., Puymirat, J., Dieltjes, P., Bakker, E. & de Knijff, P. Estimating Y chromosome specific microsatellite mutation frequencies using deep rooting pedigrees. Hum. Mol. Genet. 6, 799-803 (1997).
16. Zhivotovsky, L. A. et al. The effective mutation rate at Y chromosome short tandem repeats, with application to human population-divergence time. Am. J. Hum. Genet. 74, 50-61 (2004).
17. Hammer, M. F. A recent common ancestry for human Y chromosomes. Nature 378, 376-378 (1995).
18. Whitfield, L. S., Hawkins, T. L., Goodfellow, P. N. & Sulston, J. 41 kilobases of analyzed sequence from the pseudoautosomal and sex-determining regions of the short arm of the human Y chromosome. Genomics 27, 306-311 (1995).
19. Hinds, D. A. et al. Whole-genome patterns of common DNA variation in three human populations. Science 307, 1072-1079 (2005).
20. 1000 Genomes Project Consortium et al. A map of human genome variation from population-scale sequencing. Nature 467, 1061-1073 (2010).
21. Skaletsky, H. et al. The male-specific region of the human Y chromosome: a mosaic of discrete sequence classes. Nature 423, 825-837 (2003).
22. Yan, S. et al. Y chromosomes of 40% Chinese descend from three Neolithic super-grandfathers. PLoS ONE 9, e105691 (2014).
23. Lippold, S. et al. Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences. Investig. Genet. 5, 13 (2014).
24. 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).
25. Wei, W. et al. A calibrated human Y-chromosomal phylogeny based on resequencing. Genome Res. 23, 388-395 (2013).
26. Poznik, G. D. et al. Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341, 562-565 (2013).
27. Karmin, M. et al. A recent bottleneck of Y chromosome diversity coincides with a global change in culture. Genome Res. 25, 459-466 (2015).
28. Francalacci, P. et al. Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y chromosome phylogeny. Science 341, 565-569 (2013).
29. Willems, T. et al. Population-scale sequencing data enable precise estimates of Y-STR mutation rates. Am. J. Hum. Genet. 98, 919-933 (2016).
30. Redon, R. et al. Global variation in copy number in the human genome. Nature 444, 444-454 (2006).
31. Espinosa, J. R., Ayub, Q., Chen, Y., Xue, Y. & Tyler-Smith, C. Structural variation on the human Y chromosome from population-scale resequencing. Croat. Med. J. 56, 194-207 (2015).
32. Massaia, A. & Xue, Y. Human Y chromosome copy number variation in the next generation sequencing era and beyond. Hum. Genet. 136, 591-603 (2017).
33. 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).
34. Balanovsky, O. et al. Deep phylogenetic analysis of haplogroup G1 provides estimates of SNP and STR mutation rates on the human Y-chromosome and reveals migrations of Iranic speakers. PLoS ONE 10, e0122968 (2015).
35. Helgason, A. et al. The Y-chromosome point mutation rate in humans. Nat. Genet. 47, 453-457 (2015).
36. 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).
37. 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).
38. Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445-449 (2014).
39. Kivisild, T. The study of human Y chromosome variation through ancient DNA. Hum. Genet. 136, 529-546 (2017).
40. Moorjani, P., Gao, Z. & Przeworski, M. Human germline mutation and the erratic evolutionary clock. PLoS Biol. 14, e2000744 (2016).
41. Mendez, F. L., Poznik, G. D., Castellano, S. & Bustamante, C. D. The divergence of Neandertal and modern human Y chromosomes. Am. J. Hum. Genet. 98, 728-734 (2016).
42. 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).
43. Underhill, P. A. & Kivisild, T. Use of Y chromosome and mitochondrial DNA population structure in tracing human migrations. Annu. Rev. Genet. 41, 539-564 (2007).
44. Brown, G. R., Laland, K. N. & Mulder, M. B. Bateman's principles and human sex roles. Trends Ecol. Evol. 24, 297-304 (2009).
45. Batini, C. & Jobling, M. A. Detecting past male-mediated expansions using the Y chromosome. Hum. Genet. 136, 547-557 (2017).
46. Zerjal, T. et al. The genetic legacy of the Mongols. Am. J. Hum. Genet. 72, 717-721 (2003).
47. Xue, Y. et al. Recent spread of a Y-chromosomal lineage in northern China and Mongolia. Am. J. Hum. Genet. 77, 1112-1116 (2005).
48. Moore, L. T., McEvoy, B., Cape, E., Simms, K. & Bradley, D. G. A Y-chromosome signature of hegemony in Gaelic Ireland. Am. J. Hum. Genet. 78, 334-338 (2006).
49. Burton, M. L. et al. Regions based on social structure. Curr. Anthropol. 37, 87-123 (1996).
50. Murdock, G. P. Ethnographic Atlas (Univ. of Pittsburgh Press, 1967).
51. Seielstad, M. T., Minch, E. & Cavalli-Sforza, L. L. Genetic evidence for a higher female migration rate in humans. Nat. Genet. 20, 278-280 (1998).
52. Oota, H., Settheetham-Ishida, W., Tiwawech, D., Ishida, T. & Stoneking, M. Human mtDNA and Y chromosome variation is correlated with matrilocal versus patrilocal residence. Nat. Genet. 29, 20-21 (2001).
53. Wilkins, J. F. Unraveling male and female histories from human genetic data. Curr. Opin. Genet. Dev. 16, 611-617 (2006).
54. Alves-Silva, J. et al. The ancestry of Brazilian mtDNA lineages. Am. J. Hum. Genet. 67, 444-461 (2000).
55. Rojas, W. et al. Genetic make up and structure of Colombian populations by means of uniparental and biparental DNA markers. Am. J. Phys. Anthropol. 143, 13-20 (2010).
56. Corach, D. et al. Inferring continental ancestry of Argentineans from autosomal, Y-chromosomal and mitochondrial DNA. Ann. Hum. Genet. 74, 65-76 (2010).
57. Redd, A. J. et al. Gene flow from the Indian subcontinent to Australia: evidence from the Y chromosome. Curr. Biol. 12, 673-677 (2002).
58. Bergstrom, A. et al. Deep roots for Aboriginal Australian Y chromosomes. Curr. Biol. 26, 809-813 (2016).
59. Wei, W., Ayub, Q., Xue, Y. & Tyler-Smith, C. A comparison of Y-chromosomal lineage dating using either resequencing or Y-SNP plus Y-STR genotyping. Forensic Sci. Int. Genet. 7, 568-572 (2013).
60. Ilumae, A. M. et al. Human Y chromosome haplogroup N: a non-trivial time-resolved phylogeography that cuts across language families. Am. J. Hum. Genet. 99, 163-173 (2016).
61. Batini, C. et al. Large-scale recent expansion of European patrilineages shown by population resequencing. Nat. Commun. 6, 7152 (2015).
62. Balaresque, P. et al. A predominantly Neolithic origin for European paternal lineages. PLoS Biol. 8, e1000285 (2010).
63. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167-172 (2015).
64. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211 (2015).
65. Foster, E. A. et al. Jefferson fathered slave's last child. Nature 396, 27-28 (1998).
66. King, T. E. & Jobling, M. A. Founders, drift and infidelity: the relationship between Y chromosome diversity and patrilineal surnames. Mol. Biol. Evol. 26, 1093-1102 (2009).
67. Martinez-Cadenas, C. et al. The relationship between surname frequency and Y chromosome variation in Spain. Eur. J. Hum. Genet. 24, 120-128 (2016).
68. Sole-Morata, N., Bertranpetit, J., Comas, D. & Calafell, F. Y-Chromosome diversity in Catalan surname samples: insights into surname origin and frequency. Eur. J. Hum. Genet. 23, 1549-1557 (2015).
69. McEvoy, B. & Bradley, D. G. Y-Chromosomes and the extent of patrilineal ancestry in Irish surnames. Hum. Genet. 119, 212-219 (2006).
70. Greeff, J. M. & Erasmus, J. C. Three hundred years of low non-paternity in a human population. Heredity 115, 396-404 (2015).
71. Larmuseau, M. H. et al. Low historical rates of cuckoldry in a Western European human population traced by Y-chromosome and genealogical data. Proc. Biol. Sci. 280, 20132400 (2013).
72. King, T. E., Ballereau, S. J., Schürer, K. & Jobling, M. A. Genetic signatures of coancestry within surnames. Curr. Biol. 16, 384-388 (2006).
73. Gymrek, M., McGuire, A. L., Golan, D., Halperin, E. & Erlich, Y. Identifying personal genomes by surname inference. Science 339, 321-324 (2013).
74. King, T. E. & Jobling, M. A. What's in a name? Y chromosomes, surnames and the genetic genealogy revolution. Trends Genet. 25, 351-360 (2009).
75. Rocca, R. A. et al. Discovery of Western European R1b1a2 Y chromosome variants in 1000 genomes project data: an online community approach. PLoS ONE 7, e41634 (2012).
76. Balanovsky, O. et al. Phylogeography of human Y-chromosome haplogroup Q3-L275 from an academic/citizen science collaboration. BMC Evol. Biol. 17, 18 (2017).
77. Sinclair, A. H. et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240-244 (1990).
78. Berta, P. et al. Genetic evidence equating SRY and the testis-determining factor. Nature 348, 448-450 (1990).
79. Vogt, P. H. et al. Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11. Hum. Mol. Genet. 5, 933-943 (1996).
80. Tyler-Smith, C. & Krausz, C. The will-o'-the-wisp of genetics - hunting for the azoospermia factor gene. N. Engl. J. Med. 360, 925-927 (2009).
81. Ramathal, C. et al. DDX3Y gene rescue of a Y chromosome AZFa deletion restores germ cell formation and transcriptional programs. Sci. Rep. 5, 15041 (2015).
82. Wang, Q. J. et al. Y Linked inheritance of non-syndromic hearing impairment in a large Chinese family. J. Med. Genet. 41, E80 (2004).
83. Wang, Q. et al. Genetic basis of Y-linked hearing impairment. Am. J. Hum. Genet. 92, 301-306 (2013).
84. Charchar, F. J. et al. Inheritance of coronary artery disease in men: an analysis of the role of the Y chromosome. Lancet 379, 915-922 (2012).
85. Giachini, C. et al. TSPY1 copy number variation influences spermatogenesis and shows differences among Y lineages. J. Clin. Endocrinol. Metab. 94, 4016-4022 (2009).
86. Shen, Y. et al. A significant effect of the TSPY1 copy number on spermatogenesis efficiency and the phenotypic expression of the gr/gr deletion. Hum. Mol. Genet. 22, 1679-1695 (2013).
87. Giachini, C. et al. Partial AZFc deletions and duplications: clinical correlates in the Italian population. Hum. Genet. 124, 399-410 (2008).
88. Rozen, S. G. et al. AZFc deletions and spermatogenic failure: a population-based survey of 20,000 Y chromosomes. Am. J. Hum. Genet. 91, 890-896 (2012).
89. Sato, Y. et al. Y chromosome gr/gr subdeletion is associated with lower semen quality in young men from the general Japanese population but not in fertile Japanese men. Biol. Reprod. 90, 116 (2014).
90. Nathanson, K. L. et al. The Y deletion gr/gr and susceptibility to testicular germ cell tumor. Am. J. Hum. Genet. 77, 1034-1043 (2005).
91. Printzlau, F., Wolstencroft, J. & Skuse, D. H. Cognitive, behavioral, and neural consequences of sex chromosome aneuploidy. J. Neurosci. Res. 95, 311-319 (2017).
92. Schoemaker, M. J. et al. Mortality in women with Turner syndrome in Great Britain: a national cohort study. J. Clin. Endocrinol. Metab. 93, 4735-4742 (2008).
93. Higgins, C. D., Swerdlow, A. J., Schoemaker, M. J., Wright, A. F. & Jacobs, P. A. Mortality and cancer incidence in males with Y polysomy in Britain: a cohort study. Hum. Genet. 121, 691-696 (2007).
94. Fisher, E. M. C. et al. Homologous ribosomal protein genes on the human X and Y chromosomes: escape from inactivation and possible implications for Turner syndrome. Cell 63, 1205-1218 (1990).
95. Jacobs, P. A., Brunton, M., Court Brown, W. M., Doll, R. & Goldstein, H. Change of human chromosome count distribution with age: evidence for a sex differences. Nature 197, 1080-1081 (1963).
96. Forsberg, L. A. et al. Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer. Nat. Genet. 46, 624-628 (2014).
97. Dumanski, J. P. et al. Mutagenesis. Smoking is associated with mosaic loss of chromosome Y. Science 347, 81-83 (2015).
98. Dumanski, J. P. et al. Mosaic loss of chromosome Y in blood is associated with Alzheimer disease. Am. J. Hum. Genet. 98, 1208-1219 (2016).
99. Ganster, C. et al. New data shed light on Y-loss-related pathogenesis in myelodysplastic syndromes. Genes Chromosomes Cancer 54, 717-724 (2015).
100. Noveski, P. et al. Loss of Y chromosome in peripheral blood of colorectal and prostate cancer patients. PLoS ONE 11, e0146264 (2016).
101. Zhou, W. et al. Mosaic loss of chromosome Y is associated with common variation near TCL1A. Nat. Genet. 48, 563-568 (2016).
102. Wright, D. J. et al. Genetic variants associated with mosaic Y chromosome loss highlight cell cycle genes and overlap with cancer susceptibility. Nat. Genet. 49, 674-679 (2017).
103. Wong, H. Y. et al. TMSB4Y is a candidate tumor suppressor on the Y chromosome and is deleted in male breast cancer. Oncotarget 6, 44927-44940 (2015).
104. Santos, F. R., Pandya, A. & Tyler-Smith, C. Reliability of DNA-based sex tests. Nat. Genet. 18, 103 (1998).
105. Jobling, M. A. et al. Structural variation on the short arm of the human Y chromosome: recurrent multigene deletions encompassing Amelogenin Y. Hum. Mol. Genet. 16, 307-316 (2007).
106. Wei, W. et al. Copy number variation in the human Y chromosome in the UK population. Hum. Genet. 134, 789-800 (2015).
107. Fernandes, S. et al. A large AZFc deletion removes DAZ3/DAZ4 and nearby genes from men in Y haplogroup N. Am. J. Hum. Genet. 74, 180-187 (2004).
108. Repping, S. et al. A family of human Y chromosomes has dispersed throughout northern Eurasia despite a 1.8-Mb deletion in the azoospermia factor c region. Genomics 83, 1046-1052 (2004).
109. Wilson Sayres, M. A., Lohmueller, K. E. & Nielsen, R. Natural selection reduced diversity on human Y chromosomes. PLoS Genet. 10, e1004064 (2014).
110. Rozen, S., Marszalek, J. D., Alagappan, R. K., Skaletsky, H. & Page, D. C. 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 (2009).
111. Jobling, M. A. et al. A selective difference between human Y-chromosomal DNA haplotypes. Curr. Biol. 8, 1391-1394 (1998).
112. Goodwin, S., McPherson, J. D. & McCombie, W. R. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17, 333-351 (2016).
113. Chaisson, M. J., Wilson, R. K. & Eichler, E. E. Genetic variation and the de novo assembly of human genomes. Nat. Rev. Genet. 16, 627-640 (2015).
114. Haber, M., Mezzavilla, M., Xue, Y. & Tyler-Smith, C. Ancient DNA and the rewriting of human history: be sparing with Occam's razor. Genome Biol. 17, 1 (2016).
115. Balanovsky, O. et al. Genetic differentiation between upland and lowland populations shapes the Y chromosomal landscape of West Asia. Hum. Genet. 36, 437-450 (2017).
116. Wise, A. L., Gyi, L. & Manolio, T. A. eXclusion: toward integrating the X chromosome in genome-wide association analyses. Am. J. Hum. Genet. 92, 643-647 (2013).
117. Ledford, H. Astra Zeneca launches project to sequence 2 million genomes. Nature 532, 427 (2016).
118. Marx, V. The DNA of a nation. Nature 524, 503-505 (2015).
119. Sekido, R. & Lovell-Badge, R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934 (2008).
120. Cortez, D. et al. Origins and functional evolution of Y chromosomes across mammals. Nature 508, 488-493 (2014).
121. Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome. Science 286, 964-967 (1999).
122. Page, D. C., Harper, M. E., Love, J. & Botstein, D. Occurrence of a transposition from the X-chromosome long arm to the Y-chromosome short arm during human evolution. Nature 311, 119-122 (1984).
123. Repping, S. et al. Polymorphism for a 1.6-Mb deletion of the human Y chromosome persists through balance between recurrent mutation and haploid selection. Nat. Genet. 35, 247-251 (2003).
124. Ross, M. T. et al. The DNA sequence of the human X chromosome. Nature 434, 325-337 (2005).
125. Rozen, S. et al. Abundant gene conversion between arms of massive palindromes in human and ape Y chromosomes. Nature 423, 873-876 (2003).
126. Hallast, P., Balaresque, P., Bowden, G. R., Ballereau, S. J. & Jobling, M. A. Recombination dynamics of a human Y-chromosomal palindrome: rapid GC-biased gene conversion, multi-kilobase conversion tracts, and rare inversions. PLoS Genet. 9, e1003666 (2013).
127. Balaresque, P. et al. Gene conversion violates the stepwise mutation model for microsatellites in Y chromosomal palindromic repeats. Hum. Mutat. 35, 609-617 (2014).
128. Trombetta, B., Cruciani, F., Underhill, P. A., Sellitto, D. & Scozzari, R. Footprints of X-to-Y gene conversion in recent human evolution. Mol. Biol. Evol. 27, 714-725 (2010).
129. Rosser, Z. H., Balaresque, P. & Jobling, M. A. 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 (2009).
130. 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. 31, 2108-2123 (2014).
131. Berg, I. L. et al. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat. Genet. 42, 859-863 (2010).
132. Crow, J. F. The origins, patterns and implications of human spontaneous mutation. Nat. Rev. Genet. 1, 40-47 (2000).
133. Segurel, L., Wyman, M. J. & Przeworski, M. Determinants of mutation rate variation in the human germline. Annu. Rev. Genomics Hum. Genet. 15, 47-70 (2014).
134. Kayser, M. Forensic use of Y-chromosome DNA: a general overview. Hum. Genet. 136, 621-635 (2017).
135. Prinz, M., Ishii, A., Coleman, A., Baum, H. J. & Shaler, R. C. Validation and casework application of a Y chromosome specific STR multiplex. Forensic Sci. Int. 120, 177-188 (2001).
136. Ballantyne, K. N. et al. Mutability of Y-chromosomal microsatellites: rates, characteristics, molecular bases, and forensic implications. Am. J. Hum. Genet. 87, 341-353 (2010).
137. Ballantyne, K. N. et al. 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 (2012).
138. 1000 Genomes Project Consortium et al. A global reference for human genetic variation. Nature 526, 68-74 (2015).