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Y-Chromosome Diversity in Native Mexicans

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Y-Chromosome Diversity in Native Mexicans American Journal of Physical Anthropology Y-chromosome diversit y in Native Mexicans reveals continental transition of genetic structure in the Americas Journal: American Journal of Physical Anthropology Manuscript ID: AJPA-2011-00227.R1 Wiley - Manuscript type: Research Article Date Submitted by the Author: n/a Complete List of Authors: Sandoval, Karla; Stanford University, Department of Genetics; Institut de Biologia Evolutiva, Moreno, Andrés; Stanford University, Genetics Mendizabal, Isabel; Institute of Evolutionary Biology (UPF-CSIC), CEXS- UPF-PRBB, Underhill, Peter; Stanford University, Genetics Lopez-Valenzuela, Maria; Institut de Biologia Evolutiva, Peñaloza-Espinosa, Rosenda; Centro Medico Nacional, Buentello-Malo, Leonora; Universidad Nacional Autonoma de Mexico, Avelino, Heriberto; Max Planck Institute for Evolutionary Anthropology, Calafell, Francesc; Universitat Pompeu Fabra, Unitat de Biologia Evolutiva; Comas, David; Institut de Biologia Evolutiva, Y-chromosome haplogroups, Native Mexican populations, Mesoamerica, Key Words: genetic diversity, male lineages John Wiley & Sons, Inc. Page 1 of 33 American Journal of Physical Anthropology 1 2 3 Y-chromosome diversity in Native Mexicans reveals continental 4 5 6 transition of genetic structure in the Americas 7 8 9 10 Karla Sandoval 1,2 , Andres Moreno-Estrada 2, Isabel Mendizabal 1, Peter A. Underhill 2, 11 12 1 3 4 13 Maria Lopez-Valenzuela , Rosenda Peñaloza-Espinosa , Leonor Buentello-Malo , 14 5 1 1 15 Heriberto Avelino , Francesc Calafell , David Comas 16 17 18 19 1Institut de Biologia Evolutiva (UPF-CSIC), CEXS-UPF-PRBB, Barcelona, Catalonia, 20 21 Spain. 22 23 2 24 Department of Genetics, Stanford University, Stanford, CA 94305 25 3 26 Unidad de Investigación Médica en Genética Humana, Centro Médico Nacional, Siglo 27 28 XXI, IMSS, 06703 Mexico City, Mexico. 29 30 4Instituto de Investigaciones Antropológicas, Universidad Nacional Autónoma de 31 32 33 México, Mexico City, Mexico. 34 5 35 Department of Linguistics, Max Planck Institute for Evolutionary Anthropology, 36 37 Leipzig, Germany. 38 39 Corresponding author: David Comas 40 41 Tel. +34 93 316 0843 42 43 44 Fax. +34 93 316 0901 45 46 E-mail: [email protected] 47 48 Key words: Y-chromosome haplogroups, Native Mexican populations, Mesoamerica, 49 50 genetic diversity, male lineages 51 52 53 Running headline: Y-chromosome diversity of Native Mexican Populations 54 55 56 57 58 59 60 John Wiley & Sons, Inc. 1 American Journal of Physical Anthropology Page 2 of 33 1 2 3 Abstract 4 5 6 7 8 The genetic characterization of Native Mexicans is important to understand 9 10 multi-ethnic based features influencing the medical genetics of present Mexican 11 12 13 populations, as well as to the reconstruct the peopling of the Americas. We describe the 14 15 Y-chromosome genetic diversity of 197 Native Mexicans from eleven populations and 16 17 1044 individuals from 44 Native American populations after combining with publicly 18 19 available data. We found extensive heterogeneity among Native Mexican populations 20 21 and ample segregation of Q-M242* (46%) and Q-M3 (54%) haplogroups within 22 23 24 Mexico. The northernmost sampled populations falling outside Mesoamerica (Pima and 25 26 Tarahumara) showed a clear differentiation with respect to the other populations, which 27 28 is in agreement with previous results from mtDNA lineages. However, our results point 29 30 towards a complex genetic makeup of Native Mexicans whose maternal and paternal 31 32 33 lineages reveal different narratives of their population history, with sex-biased 34 35 continental contributions and different admixture proportions. At a continental scale we 36 37 found that Arctic populations and the northernmost groups from North America cluster 38 39 together, but we did not find a clear differentiation within Mesoamerica and the rest of 40 41 the continent, which coupled with the fact that the majority of individuals from Central 42 43 44 and South American samples are restricted to the Q-M3 branch, supports the notion that 45 46 most Native Americans from Mesoamerica southwards are descendants from a single 47 48 wave of migration. This observation is compatible with the idea that present day 49 50 Mexico might have constituted an area of transition in the diversification of paternal 51 52 53 lineages during the colonization of the Americas. 54 55 56 57 58 59 60 John Wiley & Sons, Inc. 2 Page 3 of 33 American Journal of Physical Anthropology 1 2 3 Introduction 4 5 The ability to reconstruct human population history using uniparental systems 6 7 8 has motivated a deluge of genetic studies during the last decades. However, several 9 10 geographic regions remain underrepresented in comprehensive surveys of human 11 12 genetic variation. One such region is Mesoamerica, a wide area covering central- 13 14 southern Mexico and part of Central America (including regions from Guatemala, 15 16 17 Belize, El Salvador, Honduras, Nicaragua and Costa Rica). Despite different 18 19 civilizations arising in this region, Mesoamerica comprised an interrelated cultural area 20 21 that constituted one of the two centers of the New World civilization (Carmack et al. 22 23 1996; López-Austin and López- Luján 2001). The impact of post-Columbian European 24 25 and African admixture with Native Mexicans is of great interest to understand disease 26 27 28 susceptibility in Mexican populations (Bryc et al. 2010), as well as to reconstruct the 29 30 history of Mesoamerica and the peopling of the Americas (Mulligan et al. 2008). 31 32 Numerous studies on this region have focused on Mestizo populations using 33 34 autosomal markers (Cerda-Flores et al. 2002a; 1989; 1987; 2002b; Felix-Lopez et al. 35 36 37 2006; Rangel-Villalobos et al. 1999; Silva-Zolezzi et al. 2009; Wang et al. 2008) as well 38 39 as Y-chromosome markers (Gorostiza et al. 2007; Gutierrez-Alarcon et al. 2007; 40 41 Hernandez-Gutierrez et al. 2005; Licea-Cadena et al. 2006; Luna-Vazquez et al. 2008; 42 43 2005; and 2003; Rangel-Villalobos et al. 2001a; 2001b; 2008; and 2000; Rubi- 44 45 Castellanos et al. 2009a; 2009b; Salazar-Flores et al. 2010; Tarazona-Santos et al. 2001; 46 47 48 Torres-Rodriguez et al. 2006). These studies have shown a substantial contribution of 49 50 Native American ancestry to extant Mexican Mestizo populations, supported by 51 52 additional studies based on mtDNA sequences (González-Oliver et al. 2001; Green et al. 53 54 2000; Kemp et al. 2010; Peñaloza-Espinosa et al. 2007; Sandoval et al. 2009; Torroni et 55 56 57 al. 1994). Other studies have also described the paternal genetic diversity in Mexican 58 59 60 John Wiley & Sons, Inc. 3 American Journal of Physical Anthropology Page 4 of 33 1 2 3 indigenous groups (Barrot et al. 2005; Felix-Lopez et al. 2006; Kemp et al. 2010; Paez- 4 5 Riberos et al. 2006; Rangel-Villalobos et al. 2000); however, a better understanding 6 7 could be gained by putting this characterization into context with the continental 8 9 10 landscape. Previous studies on continental genetic structure identified by autosomal 11 12 markers (Wang et al. 2007; Yang et al. 2010), have reported a North-to-South reduction 13 14 of diversity in the Americas, consistent with early studies based on Y-chromosome 15 16 diversity showing patterns of low haplotypic diversity in Native American populations 17 18 (Ruiz-Linares et al. 1999; Salzano 2002; Underhill et al. 2001). Concerning Y- 19 20 21 chromosome variation, components of both Q1a3 and C3 sub-haplogroups are viewed 22 23 as prehistoric Native paternal lineages in the Americas while all other haplogroups are 24 25 considered to reflect the consequences of post-Columbian contact. The nearest 26 27 molecular ancestors to Q and C sub-haplogroups in Native Americans are rare 28 29 30 elsewhere, with the exception of northern Asia, where they reach frequencies of 28% 31 32 and 18%, respectively (Mulligan et al. 2004). With the identification of the haplogroup 33 34 Q defining M242 SNP (Seielstad et al. 2003), the age of Q haplotypes in the Americas 35 36 was estimated at 15,000–18,000 ybp (Bortolini et al. 2003). Although haplogroup Q is 37 38 present in 76% of Native Americans (Zegura et al. 2004), the Native American C3- 39 40 41 M217 associated haplogroups have only been detected among the Na-Dene-speaking 42 43 Tanana, Navajo, Chipewyan, and the Amerindian Cheyenne (Bergen et al. 1999; 44 45 Bortolini et al. 2002; 2003; Karafet et al. 1999; Zegura et al. 2004). The higher 46 47 haplotypic diversity of C-M130 lineages in eastern Siberians and Asians (Lell et al. 48 49 50 2002) and an estimated coalescent for C-M130 of ~25,000–30,000 ybp (Karafet et al. 51 52 1999; Underhill et al. 2000), is consistent with an Asian origin for C-M130, This 53 54 inference is bolstered by other age estimates for the entire C lineage and the Native 55 56 57 58 59 60 John Wiley & Sons, Inc. 4 Page 5 of 33 American Journal of Physical Anthropology 1 2 3 American-specific C3-P39 as 27,500±10,100 and 2,550±1910 ybp, respectively 4 5 (Hammer and Zegura 2002; Karafet et al. 2002). 6 7 Here, we report the haplogroup composition based on Y-chromosome STR and 8 9 10 SNP data for 197 unrelated individuals from eleven native populations from Mexico 11 12 belonging to two independent cultural and geographical areas: Tarahumara and Pima 13 14 from northern Mexico (outside Mesoamerica); and Triqui, Mixtec, Otomi, Xochimilco 15 16 Nahua, Zitlala Nahua, Atocpan Nahua, Ocotitlan Nahua, Purepecha, and Yucatec Maya, 17 18 all from Central-South Mexico and within the Mesoamerican area. These populations 19 20 21 belong to four different linguistic families (Campbell 1997; 1986; and Mithun 1990; 22 23 1999), Uto-Aztecan including Tarahumara, Pima and the Nahua languages; 24 25 Otomanguean including Triqui, Mixtec and Otomi; Mayan including Yucatec Maya, 26 27 and finally Tarascan including the isolate Purepecha.
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