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A Continental Perspective on Y-Chromosome Diversity

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A Continental Perspective on Y-Chromosome Diversity The Eurasian Heartland: A continental perspective on Y-chromosome diversity R. Spencer Wellsa,b, Nadira Yuldashevaa,c, Ruslan Ruzibakievc, Peter A. Underhilld, Irina Evseevae, Jason Blue-Smithd, Li Jinf, Bing Suf, Ramasamy Pitchappang, Sadagopal Shanmugalakshmig, Karuppiah Balakrishnang, Mark Readh, Nathaniel M. Pearsoni, Tatiana Zerjalj, Matthew T. Websterk, Irakli Zholoshvilil, Elena Jamarjashvilil, Spartak Gambarovm, Behrouz Nikbinn, Ashur Dostievo, Ogonazar Aknazarovp, Pierre Zallouaq, Igor Tsoyr, Mikhail Kitaevs, Mirsaid Mirrakhimovs, Ashir Charievt, and Walter F. Bodmera,u aImperial Cancer Research Fund Cancer and Immunogenetics Laboratory and Wellcome Trust Centre for Human Genetics, University of Oxford, Headington OX3 9DS, United Kingdom; cInstitute of Immunology, Academy of Sciences, Tashkent, Uzbekistan; dDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305; eDepartment of Medical Genetics, Archangelsk State Medical Academy, Archangelsk, Russia; fDepartment of Human Genetics, School of Public Health, University of Texas, Houston, TX 77030; gCentre for Advanced Studies in Functional Genomics, School of Biological Sciences, Madurai Kamaraj University, Madurai, India; hMark Read Photography, 2 Beatty Road, London N16 8EB, United Kingdom; iDepartment of Ecology and Evolution, University of Chicago, Chicago, IL 60637; jDepartment of Biochemistry, University of Oxford, Oxford OX3 1QU, United Kingdom; kInstitute of Molecular Medicine, University of Oxford, Headington OX3 9DS, United Kingdom; lDepartment of Pediatrics, State Medical Institute, Tbilisi, Georgia; mImmunology Laboratory, Mikaelin Surgical Institute, Yerevan, Armenia; nDepartment of Immunology, University of Medical Sciences, Tehran 14496, Iran; oTajik State Medical Institute, Dushanbe, Tajikistan; pPamir Biological Laboratory, Khorog, Tajikistan; qGenetics Research Laboratory, Chronic Care Center, Hazmieh, Lebanon; rInstitute of Nutrition, Almaty, Kazakstan; sInstitute of Cardiology, Bishkek, Kyrgyzstan; and tState Medical Institute, Ashgabad, Turkmenistan Contributed by Walter F. Bodmer, June 15, 2001 The nonrecombining portion of the human Y chromosome has analysis of other genetic markers. In particular, the Y data may proven to be a valuable tool for the study of population history. shed some light on the path(s) followed by anatomically modern The maintenance of extended haplotypes characteristic of partic- humans after they left Africa and settled other continents. In this ular geographic regions, despite extensive admixture, allows com- paper we present the analysis of 23 NRY biallelic polymorphisms plex demographic events to be deconstructed. In this study we in a sample of 1,935 men from 49 Eurasian populations. These report the frequencies of 23 Y-chromosome biallelic polymorphism results are compared with data from other populations in an haplotypes in 1,935 men from 49 Eurasian populations, with a effort to reconstruct the history of early human migrations in particular focus on Central Asia. These haplotypes reveal traces of Eurasia, as well as more recent events in the region of Central historical migrations, and provide an insight into the earliest Asia. patterns of settlement of anatomically modern humans on the Eurasian continent. Central Asia is revealed to be an important Methods reservoir of genetic diversity, and the source of at least three major Samples. Samples were collected from healthy adult men, pri- waves of migration leading into Europe, the Americas, and India. marily during three expeditions in 1996, 1998, and 2000 (see The genetic results are interpreted in the context of Eurasian http:͞͞popgen.well.ox.ac.uk͞eurasia for details). Informed con- linguistic patterns. sent was obtained from all donors. We made an effort to sample a variety of linguistic groups, including those speaking languages uman population genetics uses the distribution of genetic belonging to the Afro-Asiatic, Indo-European, Dravidian, South Hmarkers in extant human populations to gain an insight into Caucasian, North Caucasian, Altaic, Uralic, and Sino-Tibetan demographic and migrational history. Population studies of language families. The Sourashtran, Yadhava, and Kallar sam- protein (‘‘classical’’) polymorphisms, HLA variation, and mito- ples were collected as described elsewhere (S.S., R.S.W., K.B., chondrial DNA have all contributed greatly to our understand- and R.P., unpublished work). The Nenets, Northern Russian, ing of human origins and early dispersals (1). New molecular Pomor, and Saami samples were collected in 1996 and 1998, the biological techniques, including surveys of autosomal microsat- Tuvinian in 1996, and the Orkney samples in 1994. For some ellite diversity (2) and single nucleotide polymorphism (SNP) samples, cell lines were prepared by Epstein–Barr virus trans- haplotypes (3, 4) have revealed similar patterns. The genetic formation of peripheral blood leukocytes. For most, however, evidence has consistently pointed to a recent common origin in blood was collected by venipuncture, and the red cells were lysed Africa, with subsequent dispersal(s) of modern humans through- by two rounds of osmotic shock and centrifugation in 115 mM out the rest of the world. NH4Cl. The resulting white cell pellet was resuspended in a white ⅐ ͞ ͞ Recently, diversity on the nonrecombining portion of the Y cell lysis buffer (100 mM Tris CL, pH 7.6 50 mM NaCl 40 mM ͞ ͞ chromosome (NRY) has been applied to the study of human EDTA, pH 8.0 0.2% SDS 0.5% sodium azide), rendering the history (5, 6). Two features of the NRY make it particularly well DNA stable for several weeks under field conditions. After suited for these investigations. First, like mtDNA, it is passed returning to the laboratory, the DNA was purified by using a from parent to offspring (in this case, father to son) without the standard salting-out procedure (9). ‘‘shuffling’’ effect of recombination; this allows the evolution and retention of a wide variety of stable haplotypes with varying Genotyping. The polymorphisms typed in this study are shown in ages, related through a clear, stepwise mutational process. The Table 1 and in the supplemental data (Tables 2 and 3), which are second feature is the highly specific geographic pattern of NRY variation: NRY diversity within populations is lower than that Abbreviation: NRY, nonrecombining portion of the Y chromosome. seen for other markers, and variation among populations is b higher (7). Thus, the Y chromosome provides anthropologists To whom correspondence should be addressed. E-mail: [email protected]. and geneticists with an extremely powerful tool for historical and uTo whom reprint requests should be addressed at: Imperial Cancer Research Fund Cancer and Immunogenetics Laboratory, Institute of Molecular Medicine, John Radcliffe Hospital, demographic studies. Oxford OX3 9DS, United Kingdom. E-mail: [email protected]. The ease with which recently described biallelic NRY markers The publication costs of this article were defrayed in part by page charge payment. This (8) can be typed and assigned to haplotypes promises to reveal article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. many details of human history that were unclear from the §1734 solely to indicate this fact. 10244–10249 ͉ PNAS ͉ August 28, 2001 ͉ vol. 98 ͉ no. 18 www.pnas.org͞cgi͞doi͞10.1073͞pnas.171305098 Downloaded by guest on September 27, 2021 Table 1. Y-chromosome haplotype frequencies in 49 Eurasian populations, listed according to geographic region Haplotypes are defined in Table 2. published on the PNAS web site, www.pnas.org; the nomencla- on the relationships presented by Underhill et al. (8); ‘‘ancestral’’ ture is that of Underhill et al. (8), and marker details are and ‘‘derived’’ states were determined from comparisons to GENETICS available on dbSNP (http:͞͞www.ncbi.nlm.nih.gov͞SNP). The non-human primate sequences. Every sample was analyzed in a polymorphism M3, not found in our samples, was typed by using ‘‘first round’’ typing plate containing all primer sets for the dHPLC with the analysis conditions described (10). YAP was following markers: M20A (primers specific for the ancestral typed by using the method of Hammer and Horai (11). All other state), M9G, M17del, M45A, M89T, RPS4YT, M173C, and polymorphisms were typed by using allele-specific PCR, with M175del (all specific for the derived state). Thus, an M20G primers designed to amplify only in the presence of the particular derived sample would show no band for the M20A ancestral polymorphism; the primer sets are given in Table 3. PCR primer set, but would show bands for the M9G and M89T reactions were carried out in a 10 ␮l reaction volume, containing derived sets. All subsequent typing for further resolution (‘‘sub- 10 pmol of each primer, 30 ng of genomic DNA, 0.2 units typing’’) was carried out with the most evolutionarily derived AmpliTaq Gold (Perkin–Elmer), 175 ␮M of each dNTP, 1X marker from the first round, as well as additional primer sets AmpliTaq Gold PCR buffer, and 2.3 mM MgCl2. Primers were specific for the new markers. For example, individuals typed as optimized to allow the use of the following cycling conditions for M89T in the first round would be further subtyped for M52C, all markers: 95° for 10 min, followed by 29 cycles of 95° for 30s, M170C, and M172G, in addition to M89T (see Table 2). Positive 62° for 30s, and 72° for 30s, followed by a 10 min extension at and negative control samples were included
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