Abstract
Although human Y chromosomes belonging to haplogroup R1b are quite rare in Africa, being found mainly in Asia and Europe, a group of chromosomes within the paragroup R-P25* are found concentrated in the central-western part of the African continent, where they can be detected at frequencies as high as 95%. Phylogenetic evidence and coalescence time estimates suggest that R-P25* chromosomes (or their phylogenetic ancestor) may have been carried to Africa by an Asia-to-Africa back migration in prehistoric times. Here, we describe six new mutations that define the relationships among the African R-P25* Y chromosomes and between these African chromosomes and earlier reported R-P25 Eurasian sub-lineages. The incorporation of these new mutations into a phylogeny of the R1b haplogroup led to the identification of a new clade (R1b1a or R-V88) encompassing all the African R-P25* and about half of the few European/west Asian R-P25* chromosomes. A worldwide phylogeographic analysis of the R1b haplogroup provided strong support to the Asia-to-Africa back-migration hypothesis. The analysis of the distribution of the R-V88 haplogroup in >1800 males from 69 African populations revealed a striking genetic contiguity between the Chadic-speaking peoples from the central Sahel and several other Afroasiatic-speaking groups from North Africa. The R-V88 coalescence time was estimated at 9200–5600 kya, in the early mid Holocene. We suggest that R-V88 is a paternal genetic record of the proposed mid-Holocene migration of proto-Chadic Afroasiatic speakers through the Central Sahara into the Lake Chad Basin, and geomorphological evidence is consistent with this view.
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References
Brooks N, Chiapello I, Di Lernia S et al: The climate-environment-society nexus in the Sahara from prehistoric times to the present day. J North Afr Stud 2005; 10: 253–292.
Talbot MR : Late Pleistocene rainfall and dune building in the Sahel. Palaeoecol Afr 1983; 16: 203–213.
Burroughs WJ : Climate Change in Prehistory. The End of the Reign of Chaos. Cambridge University Press: Cambridge, 2005.
Damnati B : Holocene lake records in the northern hemisphere of Africa. J Afr Earth Sci 2000; 31: 253–262.
Drake N, Bristow C : Shorelines in the Sahara: geomorphological evidence for an enhanced monsoon from palaeolake Megachad. Holocene 2006; 16: 901–911.
Breunig P, Neumann K, Van Neer W : New research on the Holocene settlement and environment of the Chad Basin in Nigeria. Afr Archaeol Rev 1996; 13: 111–145.
Huysecom E, Ozainne S, Raeli F, Ballouche A, Rasse M, Stokes S : Ounjougou (Mali): a history of Holocene settlement at the southern edge of the Sahara. Antiquity 2004; 78: 579–593.
Kuper R, Kröpelin S : Climate-controlled Holocene occupation in the Sahara: motor of Africa's evolution. Science 2006; 313: 803–807.
Tafuri MA, Bentley RA, Manzi G, Di Lernia S : Mobility and kinship in the prehistoric Sahara: strontium isotope analysis of Holocene human skeletons from the Acacus Mts. (southwestern Libya). J Anthropol Archaeol 2006; 25: 390–402.
Sereno PC, Garcea EAA, Jousse H et al: Lakeside cemeteries in the Sahara: 5000 years of Holocene population and environmental change. PLoS One 2008; 3: e2995.
Krings M, Salem AH, Bauer K et al: mtDNA analysis of Nile River Valley populations: a genetic corridor or a barrier to migration? Am J Hum Genet 1999; 64: 1166–1176.
Cruciani F, La Fratta R, Santolamazza P et al: Phylogeographic analysis of haplogroup E3b (E-M215) Y chromosomes reveals multiple migratory events within and out of Africa. Am J Hum Genet 2004; 74: 1014–1022.
Cruciani F, La Fratta R, Trombetta B et al: 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 2007; 24: 1300–1311.
Tofanelli S, Ferri G, Bulayeva K et al: J1-M267 Y lineage marks climate-driven pre-historical human displacements. Eur J Hum Genet 2009; 17: 1520–1524.
Scozzari R, Cruciani F, Santolamazza P et al: Combined use of biallelic and microsatellite Y-chromosome polymorphisms to infer affinities among African populations. Am J Hum Genet 1999; 65: 829–846.
Underhill PA, Shen P, Lin AA et al: Y chromosome sequence variation and the history of human populations. Nat Genet 2000; 26: 358–361.
Bosch E, Calafell F, Comas D, Oefner PJ, Underhill PA, Bertranpetit J : High-resolution analysis of human Y-chromosome variation shows a sharp discontinuity and limited gene flow between northwestern Africa and the Iberian Peninsula. Am J Hum Genet 2001; 68: 1019–1029.
Cruciani F, Santolamazza P, Shen P et al: A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes. Am J Hum Genet 2002; 70: 1197–1214.
Arredi B, Poloni ES, Paracchini S et al: A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa. Am J Hum Genet 2004; 75: 338–345.
Luis JR, Rowold DJ, Regueiro M et al: The Levant versus the Horn of Africa: evidence for bidirectional corridors of human migrations. Am J Hum Genet 2004; 74: 532–544.
Semino O, Magri C, Benuzzi G et al: 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 2004; 74: 1023–1034.
Beleza S, Gusmão L, Amorim A, Carracedo A, Salas A : The genetic legacy of western Bantu migrations. Hum Genet 2005; 117: 366–375.
Wood ET, Stover DA, Ehret C et al: Contrasting patterns of Y chromosome and mtDNA variation in Africa: evidence for sex-biased demographic processes. Eur J Hum Genet 2005; 13: 867–876.
Rosa A, Ornelas C, Jobling MA, Brehm A, Villems R : Y-chromosomal diversity in the population of Guinea-Bissau: a multiethnic perspective. BMC Evol Biol 2007; 7: 124.
Berniell-Lee G, Calafell F, Bosch E et al: Genetic and demographic implications of the Bantu expansion: insights from human paternal lineages. Mol Biol Evol 2009; 26: 1581–1589.
Robino C, Crobu F, Di Gaetano C et al: Analysis of Y-chromosomal SNP haplogroups and STR haplotypes in an Algerian population sample. Int J Legal Med 2008; 122: 251–255.
Hassan HY, Underhill PA, Cavalli-Sforza LL, Ibrahim ME : Y-chromosome variation among Sudanese: restricted gene flow, concordance with language, geography, and history. Am J Phys Anthropol 2008; 137: 316–323.
Cinnioǧlu C, King R, Kivisild T et al: Excavating Y-chromosome haplotype strata in Anatolia. Hum Genet 2004; 114: 127–148.
Cann HM, de Toma C, Cazes L et al: A human genome diversity cell line panel. Science 2002; 296: 261–262.
Hammer MF, Karafet TM, Redd AJ et al: Hierarchical patterns of global human Y-chromosome diversity. Mol Biol Evol 2001; 18: 1189–1203.
Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL, Hammer MF : New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res 2008; 18: 830–838.
Underhill PA, Jin L, Lin AA et al: Detection of numerous Y chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography. Genome Res 1997; 7: 996–1005.
Underhill PA, Passarino G, Lin AA et al: The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann Hum Genet 2001; 65: 43–62.
Adams SM, King TE, Bosch E, Jobling MA : The case of the unreliable SNP: recurrent back-mutation of Y-chromosomal marker P25 through gene conversion. Forensic Sci Int 2006; 159: 14–20.
Myres NM, Ritchie KH, Lin AA, Hughes RH, Woodward SR, Underhill PA : Y-chromosome short tandem repeat intermediate variant alleles DYS392.2, DYS449.2, and DYS385.2 delineate new phylogenetic substructure in human Y-chromosome haplogroup tree. Croat Med J 2009; 50: 239–249.
Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW : Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 1995; 92: 6723–6727.
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: 2268–2270.
Bandelt H-J, Forster P, Sykes BC, Richards MB : Mitochondrial portraits of human populations using median networks. Genetics 1995; 141: 743–753.
Bandelt H-J, Forster P, Röhl A : Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999; 16: 37–48.
Cressie NAC : Statistics for Spatial Data. John Wiley and Sons Inc: New York, 1991.
Semino O, Santachiara-Benerecetti AS, Falaschi F, Cavalli-Sforza LL, Underhill PA : Ethiopians and Khoisan share the deepest clades of the human Y-chromosome phylogeny. Am J Hum Genet 2002; 70: 265–268.
Sanchez JJ, Hallenberg C, Børsting C, Hernandez A, Morling N : High frequencies of Y chromosome lineages characterized by E3b1, DYS19-11, DYS392-12 in Somali males. Eur J Hum Genet 2005; 13: 856–866.
King TE, Bowden GR, Balaresque PL, Adams SM, Shanks ME, Jobling MA : Thomas Jefferson's Y chromosome belongs to a rare European lineage. Am J Phys Anthropol 2007; 132: 584–589.
Lewis MP (ed): Ethnologue: Languages of the World, 16th Edn. SIL International: Dallas Tex, 2009, Online version: http://www.ethnologue.com/.
Tishkoff SA, Reed FA, Friedlaender FR et al: The genetic structure and history of Africans and African Americans. Science 2009; 324: 1035–1044.
Ehret C : Reconstructing Proto-Afroasiatic (Proto-Afrasian). Vowels, Tone, Consonants, and Vocabulary. University of California Press: Berkeley, 1995.
Ehret C : The Civilizations of Africa: A History to 1800. James Currey: Oxford, 2002.
Blench R : The westward wandering of Cushitic pastoralists. Explorations in the prehistory of Central Africa. In: Baroin C, Boutrais J (eds) L’Homme et l’animal dans le bassin du lac Tchad. IRD Edn. Paris, 1999, pp 39–80.
Černý V, Fernandes V, Costa MD, Hájek M, Mulligan CJ, Pereira L : Migration of Chadic speaking pastoralists within Africa based on population structure of Chad Basin and phylogeography of mitochondrial L3f haplogroup. BMC Evol Biol 2009; 9: 63.
Acknowledgements
We are grateful to all the donors for providing DNA samples and to the people that contributed to the sample collection. In particular, we thank Laurent Varesi (for the Corsican samples), Farha El Chennawi, Anne Cambon-Thomsen, MS Issad, Eric Crubézy, Abdellatif Baali, Mohammed Cherkaoui, and Mohammed Melhaoui for their help in the collection of the Moroccan, Algerian, and Egyptian Berbers samples. This research received support from Grandi Progetti Ateneo, Università di Roma ‘La Sapienza,’ and the Italian Ministry of the University (Progetti di Ricerca di Interesse Nazionale 2007), both to RS. The sampling of the Berbers was made within the framework of the Inserm ‘Réseau Nord/Sud’ N°490NS1 (Mozabite Berbers), ‘The Origin of Man, Language and Languages’ (OMLL), EUROCORES Programme and benefited from funding by the Région Midi-Pyrénées (Toulouse, France), the CNRS (Centre National de la Recherche Scientifique), and the E.C. Sixth Framework Programme under Contract ERASCT-2003-980409.
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Cruciani, F., Trombetta, B., Sellitto, D. et al. Human Y chromosome haplogroup R-V88: a paternal genetic record of early mid Holocene trans-Saharan connections and the spread of Chadic languages. Eur J Hum Genet 18, 800–807 (2010). https://doi.org/10.1038/ejhg.2009.231
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DOI: https://doi.org/10.1038/ejhg.2009.231
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