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 Biology and Evolution

Volumn 7, Issue 7, 2015, Pages 1940-1950

  Trombetta, Beniamino ^a   D'Atanasio, Eugenia ^a   Massaia, Andrea ^a,i   Ippoliti, Marco ^a   Coppa, Alfredo ^a   Candilio, Francesca ^a   Coia, Valentina ^b   Russo, Gianluca ^c   Dugoujon, Jean Michel ^d   Moral, Pedro ^e   Akar, Nejat ^f   Sellitto, Daniele ^g   Valesini, Guido ^a   Novelletto, Andrea ^h   Scozzari, Rosaria ^a   Cruciani, Fulvio ^a,g  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b INSTITUTE FOR RENEWABLE ENERGY   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITÉ PAUL SABATIER   (France)

^e UNIVERSITY OF BARCELONA   (Spain)

^f TOBB UNIVERSITY OF ECONOMICS AND TECHNOLOGY   (Turkey)

^g CNR   (Italy)

^h UNIVERSITY OF ROME TOR VERGATA   (Italy)

ⁱ WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

African prehistory; dispersal of early pastoralists; human Y chromosome; MSY phylogeny; next generation sequencing; SNP based dating

Indexed keywords

AFRICA; CLASSIFICATION; GENOTYPING TECHNIQUE; HAPLOTYPE; HUMAN; MALE; MIGRATION; MOLECULAR EVOLUTION; MUTATION; PHYLOGENY; PHYLOGEOGRAPHY; SINGLE NUCLEOTIDE POLYMORPHISM; Y CHROMOSOME;

AFRICA; CHROMOSOMES, HUMAN, Y; EVOLUTION, MOLECULAR; GENOTYPING TECHNIQUES; HAPLOTYPES; HUMAN MIGRATION; HUMANS; MALE; MUTATION; PHYLOGENY; PHYLOGEOGRAPHY; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84941989054     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv118     Document Type: Article

References (67)

1. Abu-Amero, et al. 2009. Saudi Arabian Y-chromosome diversity and its relationship with nearby regions. BMC Genet. 10:59-68.
2. Adams SM, et al. 2008. The genetic legacy of religious diversity and intolerance: paternal lineages of Christians, Jews, and Muslims in the Iberian Peninsula. Am J Hum Genet. 83:725-736.
3. Arredi B, et al. 2004. A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa. Am J Hum Genet. 75:338-345.
4. Bandelt HJ, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48.
5. Battaglia V, et al. 2009. Y-chromosomal evidence of the cultural diffusion of agriculture in Southeast Europe. Eur J Hum Genet. 17:820-830.
6. Bučková J, Černý V, Novelletto A. 2013. Multiple and differentiated contributions to the male gene pool of pastoral and farmer populations of the African Sahel. Am J Phys Anthropol. 151:10-21.
7. Chiaroni J, Underhill PA, Cavalli-Sforza LL. 2009. Y chromosome diversity, human expansion, drift, and cultural evolution. Proc Natl Acad Sci U S A. 107:2174-2179.
8. Cressie NAC. 1991. Statistics for spatial data. New York: John Wiley and Sons Inc.
9. Cruciani F, et al. 2002. A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes. Am J Hum Genet. 70:1197-1214.
10. Cruciani F, et al. 2004. Phylogeographic analysis of haplogroup E3b (E-M215) Y chromosomes reveals multiple migratory events within and out of Africa. Am J Hum Genet. 74:1014-1022.
11. Cruciani F, et al. 2007. Tracing past human male movements in Northern/Eastern Africa and Western Eurasia: new clues from Y-chromosomal haplogroups E-M78 and J-M12. Mol Biol Evol. 24:1300-1311.
12. Cruciani F, et al. 2011. Strong intra- and inter-continental differentiation revealed by Y chromosome SNPs M269, U106 and U152. Forensic Sci Int Genet. 5:e49-e52.
13. Cruciani F, La Fratta R, Torroni A, Underhill PA, Scozzari R. 2006. Molecular dissection of the Y chromosome haplogroup E-M78 (E3b1a): a posteriori evaluation of a microsatellite-network-based approach through six new biallelic markers. Hum Mutat. 27:831-832.
14. Drmanac R, et al. 2010. Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays. Science 327:78-81.
15. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214.
16. Ehret C. 2002. The civilizations of Africa: a history to 1800. Charlottesville (VA): The University Press of Virginia.
17. Forster P, Harding R, Torroni A, Bandelt HJ. 1996. Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet. 59:935-945.
18. Francalacci P, et al. 2013. Low-pass DNA sequencing of 1200 Sardinians reconstructs European Y-chromosome phylogeny. Science 341:565-569.
19. Fu Q, et al. 2014. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514:445-449.
20. Gebremeskel EI, Ibrahim ME. 2014. Y-chromosome E haplogroups: their distribution and implication to the origin of Afro-Asiatic languages and pastoralism. Eur J Hum Genet. 22:1387-1392.
21. Geppert M, et al. 2015. Identification of new SNPs in native South American populations by resequencing the Y chromosome. Forensic Sci Int Genet. 15:111-114.
22. Gomes V, Sánchez-Diz P, Amorim A, Carracedo Á, Gusmão L. 2010. Digging deeper into East African human Y chromosome lineages. Hum Genet. 127:603-613.
23. Hallast P, 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.
24. Hammer MF, et al. 1998. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol. 15:427-441.
25. Henn BM, et al. 2008. Y-chromosomal evidence of a pastoralist migration through Tanzania to southern Africa. Proc Natl Acad Sci U S A. 105:10693-10698.
26. Ingram CJ, et al. 2007. A novel polymorphism associated with lactose tolerance in Africa: multiple causes for lactase persistence? Hum Genet 120:779-788.
27. Ingram CJ, et al. 2009. Multiple rare variants as a cause of a common phenotype: several different lactase persistence associated alleles in a single ethnic group. J Mol Evol. 69:579-588.
28. Jobling MA. 2001. Y-chromosomal SNP haplotype diversity in forensic analysis. Forensic Sci Int. 118:158-162.
29. Jobling MA, Hurles ME, Tyler-Smith C. 2004. Human evolutionary genetics. New York: Garland Science.
30. Jobling MA, Tyler-Smith C. 2003. The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet. 4:598-612.
31. Jones BL, et al. 2013. Diversity of lactase persistence alleles in Ethiopia: signature of a soft selective sweep. Am J Hum Genet. 93:538-544.
32. Karafet TM, et al. 2008. New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res. 18:830-838.
33. Kayser M, et al. 2007. Relating two deep-rooted pedigrees from Central Germany by high-resolution Y-STR haplotyping. Forensic Sci Int Genet. 1:125-128.
34. King TE, et al. 2007. Thomas Jefferson's Y chromosome belongs to a rare European lineage. Am J Phys Anthropol. 132:584-589.
35. Lancaster A. 2009. Y haplogroups, archaeological cultures and language families: a review of the possibility of multidisciplinary comparisons using the case of haplogroup E-M35. J Genet Geneal. 5:35-65.
36. Larmuseau MH, et al. 2011. Micro-geographic distribution of Y-chromosomal variation in the central-western European region Brabant. Forensic Sci Int Genet. 5:95-99.
37. Larmuseau MH, et al. 2012. Temporal differentiation across a West-European Y-chromosomal cline: genealogy as a tool in human population genetics. Eur J Hum Genet. 20:434-440.
38. Lazaridis I, et al. 2014. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513:409-413.
39. Lesur J, Hildebrand E, Abawa G, Gutherz X. 2014. The advent of herding in the Horn of Africa: new data from Ethiopia, Djibouti and Somaliland. Quat Int. 343:148-158.
40. Lippold S, et al. 2014. Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences. Investig Genet. 5:13.
41. Maiquilla SM, et al. 2011. Y-STR DNA analysis of 154 female child sexual assault cases in the Philippines. Int J Legal Med. 125:817-824.
42. Marshall F, Hildebrand E. 2002. Cattle before crops: the beginnings of food production in Africa. J World Prehist. 16:99-143.
43. Mizuno N, et al. 2010. A forensic method for the simultaneous analysis of biallelic markers identifying Y chromosome haplogroups inferred as having originated in Asia and the Japanese archipelago. Forensic Sci Int Genet. 4:73-79.
44. Poznik GD, et al. 2013. Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341:562-565.
45. Ralf A, van Oven M, Zhong K, Kayser M. 2014. Simultaneous analysis of hundreds of Y-chromosomal SNPs for high-resolution paternal lineage classification using targeted semiconductor sequencing. Hum Mutat. 36:151-159.
46. Ranciaro A, et al. 2014. Genetic origins of lactase persistence and the spread of pastoralism in Africa. Am J Hum Genet. 94:496-510.
47. Roewer L, Willuweit S, Stoneking M, Nasidze I. 2009. A Y-STR database of Iranian and Azerbaijanian minority populations. Forensic Sci Int Genet. 4:e53-e55.
48. Rootsi S, et al. 2013. Phylogenetic applications of whole Y-chromosome sequences and the Near Eastern origin of Ashkenazi Levites. Nat Commun. 4:2928.
49. Scozzari R, 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.
50. Semino O, et al. 2004. 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.
51. Tamura K, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739.
52. Tishkoff SA, et al. 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 39:31-40.
53. Trombetta B, Cruciani F, Sellitto D, Scozzari R. 2011. A new topology of the human Y chromosome haplogroup E1b1 (E-P2) revealed through the use of newly characterized binary polymorphisms. PLoS One 6:e16073.
54. Underhill PA, et al. 2000. Y chromosome sequence variation and the history of human populations. Nat Genet. 26:358-361.
55. Underhill PA, et al. 2015. The phylogenetic and geographic structure of Y-chromosome haplogroup R1a. Eur J Hum Genet. 23:124-131.
56. Underhill PA, Kivisild T. 2007. Use of Y chromosome and mitochondrial DNA population structure in tracing human migrations. Annu Rev Genet. 41:539-564.
57. Van Geystelen A, Wenseleers T, Decorte R, Caspers MJ, Larmuseau MH. 2014. In silico detection of phylogenetic informative Y-chromosomal single nucleotide polymorphisms from whole genome sequencing data. Electrophoresis 35:3102-3210.
58. van Oven M, Toscani K, van den Tempel N, Ralf A, Kayser M. 2013. Multiplex genotyping assays for fine-resolution subtyping of the major human Y-chromosome haplogroups E, G, I, J, and R in anthropological, genealogical, and forensic investigations. Electrophoresis 34:3029-3038.
59. 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.
60. Wei W, Ayub Q, Chen Y, et al. 2013. A calibrated human Y-chromosomal phylogeny based on resequencing. Genome Res. 23:388-395.
61. Wei W, Ayub Q, Xue Y, Tyler-Smith C. 2013. A comparison of Y-chromosomal lineage dating using either resequencing or Y-SNP plus Y-STR genotyping. Forensic Sci Int Genet. 7:568-572.
62. Wetton JH, Tsang KW, Khan H. 2005. Inferring the population of origin of DNA evidence within the UK by allele-specific hybridization of Y-SNPs. Forensic Sci Int. 152:45-53.
63. Wright DK. 2014. East and southern Africa Neolithic: geography and overview. In: Smith C, editor. Encyclopedia of global archaeology. New York: Springer. p. 2281-2298.
64. Xue Y, et al. 2009. Human Y chromosome base-substitution mutation rate measured by direct sequencing in a deep-rooting pedigree. Curr Biol. 19:1453-1457.
65. Xue Y, Tyler-Smith C. 2010. The hare and the tortoise: one small step for four SNPs, one giant leap for SNP-kind. Forensic Sci Int Genet. 4:59-61.
66. Yan S, et al. 2014. Y chromosomes of 40% Chinese descend from three Neolithic super-grandfathers. PLoS One 9:e105691.
67. Yu Y, Harris AJ, He X. 2010. S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol. 56:848-850.