Y-Chromosome Diversity in Native Mexicans Reveals Continental
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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 148:395–405 (2012) Y-Chromosome Diversity in Native Mexicans Reveals Continental Transition of Genetic Structure in the Americas Karla Sandoval,1,2 Andres Moreno-Estrada,2 Isabel Mendizabal,1 Peter A. Underhill,2 Maria Lopez-Valenzuela,1 Rosenda Pen˜ aloza-Espinosa,1,3 Marisol Lopez-Lopez,1,3 Leonor Buentello-Malo,4 Heriberto Avelino,5 Francesc Calafell,1 and David Comas1* 1Institut de Biologia Evolutiva (UPF-CSIC), CEXS-UPF-PRBB, Barcelona, Catalonia, Spain 2Department of Genetics, Stanford University, Stanford, CA 94305 3Departamento de Sistemas Biolo´gicos, Universidad Auto´noma Metropolitana, Mexico City, Mexico 4Instituto de Investigaciones Antropolo´gicas, Universidad Nacional Auto´noma de Me´xico, Mexico City, Mexico 5Department of Linguistics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany KEY WORDS Y-chromosome haplogroups; native Mexican populations; Mesoamerica; genetic diversity; male lineages ABSTRACT The genetic characterization of Native paternal lineages reveal different narratives of their Mexicans is important to understand multiethnic based population history, with sex-biased continental contribu- features influencing the medical genetics of present tions and different admixture proportions. At a conti- Mexican populations, as well as to the reconstruct the nental scale, we found that Arctic populations and the peopling of the Americas. We describe the Y-chromosome northernmost groups from North America cluster to- genetic diversity of 197 Native Mexicans from 11 popu- gether, but we did not find a clear differentiation within lations and 1,044 individuals from 44 Native American Mesoamerica and the rest of the continent, which populations after combining with publicly available coupled with the fact that the majority of individuals data. We found extensive heterogeneity among Native from Central and South American samples are re- Mexican populations and ample segregation of Q-M242* stricted to the Q-M3 branch, supports the notion that (46%) and Q-M3 (54%) haplogroups within Mexico. The most Native Americans from Mesoamerica southwards northernmost sampled populations falling outside Meso- are descendants from a single wave of migration. This america (Pima and Tarahumara) showed a clear differ- observation is compatible with the idea that present day entiation with respect to the other populations, which is Mexico might have constituted an area of transition in in agreement with previous results from mtDNA line- the diversification of paternal lineages during the coloni- ages. However, our results point toward a complex zation of the Americas. Am J Phys Anthropol 148:395– genetic makeup of Native Mexicans whose maternal and 405, 2012. VC 2012 Wiley Periodicals, Inc. The ability to reconstruct human population history well as Y-chromosome markers (Rangel-Villalobos et al., using uniparental systems has motivated a deluge of 2000, 2001a,b, 2008; Tarazona-Santos et al., 2001; Luna- genetic studies during the last decades. However, several Vazquez et al., 2003, 2005, 2008; Hernandez-Gutierrez et geographic regions remain underrepresented in compre- hensive surveys of human genetic variation. One such region is Mesoamerica, a wide area covering central- Additional Supporting Information may be found in the online southern Mexico and part of Central America (including version of this article. regions from Guatemala, Belize, El Salvador, Honduras, Nicaragua, and Costa Rica). Despite different civiliza- Grant sponsor: Agencia Espan˜ ola de Cooperacio´n Internacional tions arising in this region, Mesoamerica comprised an (AECI, Programa de Cooperacio´n Interuniversitaria e Investigacio´n interrelated cultural area that constituted one of the two Cientı´fica entre Espan˜a e Iberoame´rica); Grant number: A/7694/07. Grant sponsor: Direccio´n General de Investigacio´n, Ministerio de centers of the New World civilization (Carmack et al., Ciencia e Innovacio´n, Spain; Grant number: CGL2010-14944/BOS. 1996; Lo´pez-Austin and Lo´pez-Luja´n, 2001). The impact Grant sponsor: Direccio´ General de Recerca, Generalitat de Catalu- of post-Columbian European and African admixture with nya; Grant number: 2009SGR1101. Grant sponsor: Basque Govern- Native Mexicans is of great interest to understand dis- ment (Hezkuntza, Unibertsitate eta Ikerketa Saila, Eusko Jaurlar- ease susceptibility in Mexican populations (Bryc et al., itza); Grant number: BFI107.4. 2010), as well as to reconstruct the history of Mesoamer- ica and the peopling of the Americas (Mulligan et al., *Correspondence to: David Comas. E-mail: [email protected] 2008). Numerous studies on this region have focused on Mes- Received 26 July 2011; accepted 29 February 2012 tizo populations using autosomal markers (Rangel-Villa- lobos et al., 1999; Cerda-Flores et al., 1987, 2002a,b; DOI 10.1002/ajpa.22062 Cerda-Flores and Garza-Chapa, 1989; Felix-Lopez et al., Published online 11 May 2012 in Wiley Online Library 2006; Wang et al., 2008; Silva-Zolezzi et al., 2009) as (wileyonlinelibrary.com). VC 2012 WILEY PERIODICALS, INC. 396 K. SANDOVAL ET AL. al., 2005; Licea-Cadena et al., 2006; Torres-Rodriguez et individuals from 44 Native American populations to al., 2006; Gorostiza et al., 2007; Gutierrez-Alarcon et al., determine the distribution of paternal lineages within 2007; Rubi-Castellanos et al., 2009a,b; Salazar-Flores et Mexico in contrast with the continental landscape and al., 2010). These studies have shown a substantial con- evaluated its correlation to geographical, cultural, and tribution of Native American ancestry to extant Mexican linguistic factors. In addition, we contrasted our results Mestizo populations, supported by additional studies with the female counterpart for the same populations as based on mtDNA sequences (Torroni et al., 1994; Green revealed by mtDNA analysis (Sandoval et al., 2009) and et al., 2000; Gonza´lez-Oliver et al., 2001; Pen˜ aloza-Espi- found a remarkable differential contribution between nosa et al., 2007; Sandoval et al., 2009; Kemp et al., maternal and paternal lineages in Mesoamerica. 2010). Other studies have also described the paternal genetic diversity in Mexican indigenous groups (Rangel- MATERIALS AND METHODS Villalobos et al., 2000; Barrot et al., 2005; Felix-Lopez et al., 2006; Paez-Riberos et al., 2006; Kemp et al., 2010); Populations studied however, a better understanding could be gained by put- A total of 197 Native Mexican male individuals were ting this characterization into context with the continen- analyzed: 22 Triquis, 18 Tarahumaras, 2 Mixtecs, 7 Oto- tal landscape. Previous studies on continental genetic mis, 22 Nahuas from Xochimilco, 22 Nahuas from structure identified by autosomal markers (Wang et al., Zitlala, 9 Nahuas from San Pedro Atocpan, 17 Nahuas 2007; Yang et al., 2010), have reported a North-to-South from Santo Domingo Ocotitlan, 8 Purepechas, 19 Yucatec reduction of diversity in the Americas, consistent with Mayas, and 51 Pimas. An additional sample of 11 Que- early studies based on Y-chromosome diversity showing chuas from Peru were also analyzed and used for inter patterns of low haplotype diversity in Native American population comparisons. DNAs from Pima, Yucatec Maya populations (Ruiz-Linares et al., 1999; Underhill et al., and Quechua were provided by the laboratory of Judith 2001; Salzano, 2002). Concerning Y-chromosome varia- R. Kidd and Kenneth K. Kidd (Yale University, New Ha- tion, components of both Q1a3 and C3 subhaplogroups ven, Conn) where lymphoblastoid cell lines are main- are viewed as prehistoric Native paternal lineages in the tained. All samples were collected with the appropriate Americas while all other haplogroups are considered to informed consent and all individuals were native speak- reflect the consequences of post-Columbian contact. The ers with local ancestors; their geographic location is nearest molecular ancestors to Q and C subhaplogroups shown in Figure 1. in Native Americans are rare elsewhere, with the excep- tion of northern Asia, where they reach frequencies of 28 Y chromosome genotyping and 18%, respectively (Mulligan et al., 2004). With the identification of the haplogroup Q defining M242 SNP DNA concentration of all samples was normalized to 1 (Seielstad et al., 2003), the age of Q haplotypes in the ng/ll using the QuantifilerTM Human DNA Quantifica- Americas was estimated at 15,000–18,000 ybp (Bortolini tion Kit (Applied Biosystems). Three SNPs (M45, which et al., 2003). Although haplogroup Q is present in 76% of defines the major haplogroup P; M242, which defines Native Americans (Zegura et al., 2004), the Native haplogroup Q; and M207, which defines haplogroup R) American C3-M217 associated haplogroups have only were genotyped in all individuals in 5ll reactions. The been detected among the Na-Dene-speaking Tanana, reactions contained 1 ll of DNA template, 0.25 llof203 Navajo, Chipewyan, and the Amerindian Cheyenne SNP Genotyping Assay, 1.25 ll of sterile-filtered water (Bergen et al., 1999; Karafet et al., 1999; Bortolini et al., and 2.5 ll of TaqMan1 Universal PCR Master Mix. Each 2002, 2003; Zegura et al., 2004). The higher haplotypic individual was amplified under standard conditions with diversity of C-M130 lineages in eastern Siberians and TaqMan1 probes (Applied Biosystems). Those individu- Asians (Lell et al., 2002) and an estimated coalescent for als not assigned within the major haplogroup P, were C-M130 of 25,000–30,000 ybp (Karafet et al., 1999; genotyped for marker M130 (which defines haplogroup