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Genetic diversity of HLA system in six populations from Jalisco, Mexico: Guadalajara city, Tlajomulco, Tlaquepaque, Tonalá, Zapopan and rural Jalisco
Human Immunology xxx (xxxx) xxx–xxx
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Genetic diversity of HLA system in six populations from Jalisco, Mexico: Guadalajara city, Tlajomulco, Tlaquepaque, Tonalá, Zapopan and rural Jalisco Alicia Bravo-Acevedoa,1, Araceli Escobedo-Ruízb,1, Rodrigo Barquerac,d, ,1, Stephen Claytond,1, Víctor Eduardo García-Ariase,1, Esteban Arrieta-Bolañosf,1, Isis Goné-Vázquezb, Diana Iraíz Hernández-Zaragozac,g, Francia Paulina Arellano-Pradoe, Marla Estefanía Rodríguez-Lópeze, María Guadalupe de Jesús Sánchez-Fernándezh, Mario J. Sandoval-Sandovali, Benjamín Gómez-Navarroj, Joaquín Zúñigak,l, Edmond J. Yunism, ⁎ Carolina Bekker-Méndezn, , Julio Granadoso ⁎
a
Blood Bank, UMAE Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico Histocompatibility Laboratory, Hospital de Especialidades, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico c Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico d Department of Archaeogenetics, Max Planck Institute for the Science of Human History (MPI-SHH), Jena, Germany e Pediatrics Hospital, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico f Institute for Experimental Cellular Therapy, University Hospital Essen, Essen, Germany g Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico h Department of Nephrology and Transplantation Unit, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico i Central Office of Transplantation, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico j Central Office of Nephrology, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico k Laboratory of Immunobiology and Genetics, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Mexico City, Mexico l Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Mexico City, Mexico m Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA, USA n Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional “La Raza”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico o Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán” (INCMNSZ), Mexico City, Mexico b
ARTICLE INFO
ABSTRACT
Keywords: HLA Immunogenetics Population genetics Jalisco Admixture
We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 2046 Mexicans from the state of Jalisco living in the city of Guadalajara (N = 1189), Tlajomulco (N = 30), Tlaquepaque (N = 39), Tonalá (N = 35), Zapopan (N = 168) and rural communities (N = 585), to obtain information regarding allelic and haplotypic frequencies. We find that the most frequent haplotypes found in the state of Jalisco include nine Native American most probable ancestry and three European haplotypes. Admixture estimates revealed that the main genetic components in the state of Jalisco are European (48.45 ± 1.18% by ML; 41.66% of European haplotypes) and Native American (44.02 ± 1.24% by ML; 39.86% of Native American haplotypes), while African genetic component is less apparent (7.53 ± 0.30% by ML; 9.62% of African haplotypes).
Abbreviations: HLA, Human Leukocyte Antigen; MPA, Most-probable ancestry; LD, Linkage Disequilibrium ⁎ Corresponding authors at: Department of Archaeogenetics, Max Planck Institute for the Science of Human History. Kahlaische Strasse 10, 07745 Jena, Germany (R. Barquera), Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional La Raza, Instituto Mexicano del Seguro Social (IMSS), Calzada Vallejo y Jacarandas S/N Colonia La Raza, 02990, Mexico City, Mexico (C.B. Méndez). E-mail addresses: [email protected] (R. Barquera), [email protected] (C. Bekker-Méndez). URLs: http://www.shh.mpg.de/en (R. Barquera), http://www.cienciaimss.org/uim-en-inmunologia-e-infectologia/ (C. Bekker-Méndez). 1 These authors contributed equally to the present work. https://doi.org/10.1016/j.humimm.2019.05.012 Received 30 April 2019; Received in revised form 30 May 2019; Accepted 30 May 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Alicia Bravo-Acevedo, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.05.012
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Jalisco is located in northwestern Mexico, bounded on the north by the states of Nayarit, Zacatecas, Aguascalientes, San Luis Potosí, on the east by Guanajuato, on the south by Michoacán and Colima, and on the west by the Pacific Ocean. It is the third most populated state, and the seventh largest in the territory. The state of Jalisco is composed of 125 municipalities, being the most populated Guadalajara, the capital city, located in the central region of Jalisco, in the geographical area known as Valle de Atemajac, and with a population of 1 495 189 inhabitants [1]. Guadalajara, together with the municipalities of Zapopan, Tlaquepaque, Tonalá, Tlajomulco, El Salto, Ixtahuacán de los Membrillos, Zapotlanejo and Juanacatlán, make up the Metropolitan Area of Guadalajara (GMZ), which is the second largest urban agglomeration in Mexico after the Mexico City. It is from this area that most of the samples for this study came from. By 2010, 78% of the population lived in urban areas and 22% in rural areas [1]. The first settlements of villages date from 1500 years BC, and its settlers were dedicated to hunting, cultivation of corn, beans, potatoes, squash, chili and tomatoes, and the manufacture of ceramics. Radiocarbon dating places occupation of Jalisco beginning from the second century BC until the 5th century AD [2]. The Classic period in northern Jalisco is represented by the Teuchitlan tradition. There are three phases described: the Ahualulco phase (AD 200–400), the Teuchitlan I phase (AD 400–700), and the Teuchitlan II phase (AD 700–1000). In the Teuchitlan tradition, apparently there was a population implosion and the development of the district as a key economic area. Apparently, a statelike organization developed in the Ahualulco phase and a connection was made to Central Mexico during the Teuchitlan phases. Social and political systems were stratified, and political centralization developed [2]. Around the year 600 BC, with the Toltec cultural expansion from the Central Highlands, began the use of metallurgical technique, the installation of irrigation systems, a writing system and the military control of some peoples, particularly Tarascos. However, the indigenous groups in western Mexico did not constitute large states, but rather lordships or cacicazgos, of smaller size [3]. Barra de Navidad is a small coastal site near a saline lagoon in southern coastal Jalisco. The site has been dated tentatively at AD 650-Contact and has been described as either seasonally occupied by inland peoples or permanently occupied by settlers who subsisted mainly on shellfish but who also traded salt, fish, and shellfish to inland peoples for inland products [2]. Metallurgy first appeared in Mesoamerica in Western and Northwestern Mexico in the current states of Jalisco, Michoacan, and Nayarit, probably by AD 800 [4]. Several of the indigenous populations of the region disappeared before the conquest, like the cultures of Capacha and Teuchitlán. The territory of the current state of Jalisco has been inhabited by different ethnic groups: bapames, caxcanes, cocas, cuachichiles, huicholes, cuyutecos, otomíes, nahuas, tecuehuanes, tepehuanes, tecos, purépechas, pinomes, tzaultecas and xilotlantzingas, although at the time of the arrival of the Spaniards to the territory, two main ones existed: Huicholes, or Wixárika people, in the north, and several Nahuas towns in the south. The Spanish, in search of precious minerals, began expeditions to achieve conquest in 1522. During the 16th century, the extermination and subjugation of indigenous peoples was carried out, which resulted in their dissemination or subordination. The Province of Nueva Galicia was established in 1531, with the intention of creating a place that would facilitate the conquest of territories to the north and serve as a link between the mines of Zacatecas and Mexico City, as well as a port of commerce with the far East [5]. The most attractive habitable sites in the Center-West, and therefore generally speaking the areas of densest native population and long-standing centers of economic and political significance after the arrival of the Europeans [6], were the fertile depressions of ancient lakes [among the most important the Bajío region, Morelia, Guadalajara (centered on Lake Chapala), Ameca, Sayula, Tepic, Autlán, and Colima basins, and the Lake Pátzcuaro region]. The Wixárika people have achieved the practice of sustainable
agriculture, in extremely adverse environmental conditions. They are also semi-nomadic, for religious and economic reasons. Its geographic isolation and resistance to Western assimilation has kept this community quite isolated and attached to its cultural practices [7,8]. During the 17th and 18th centuries the indigenous population of Nueva Galicia, a Spanish political entity embracing much of the Center-West, declined from some 850,000 to about 70,000 [6]. In northern Jalisco, due to the debacle of the native population by epidemic diseases, the region was repopulated with people of Iberian origin, which explains the predominance of European genetic background in that area. The Nahua population, in contrast, were not a social group so isolated or so cohesive; In the south of Jalisco, haciendas were established that fragmented their territories and forced their dispersion. Thus, miscegenation, christianization, and in general, a process of “de-Indianization” began in southern Jalisco. The proliferation of ranchos, therefore (except in the Altos de Jalisco and proximate zones, where it was already well under way by 1800 or earlier), seems to have been a mid- to late nineteenth-century phenomenon. The story of this and other agrarian transitions, even if it cannot explain the entire culture history of the Center-West, for sure involved indigenous groups until comparatively recent times [6]. Currently there are two regions inhabited by indigenous people in Jalisco: the Sierra Huichola, mainly in the municipalities of Bolaños, Huejuquilla el Alto and Mezquitic, inhabited by the Wixáritari people (Huichol), and the Sierra de Manantlán, in the municipalities of Tuxpan, Cuautitlán de García Barragán, Zapotitlán de Vadillo and Villa Purificación, inhabited by Nahuas-Otomíes. The region also includes indigenous people from other ethnic groups of different states of the Republic, who reside permanently in the Metropolitan Area of Guadalajara, mainly Purépechas from Michoacán, Zapotecs, Mixtecs and Triquis from Oaxaca, Ñahñu/Otomí from the State of Mexico, Mazahuas from Guerrero, Tzotziles and Tzeltales from Chiapas, Nahuas from Guerrero and Hidalgo, among others [9,10]. Around 0.7% of the population in Jalisco speaks indigenous languages (53 695 people over 3 years old), highlighting the two most prominent native languages in the state: Huichol (18 409 speakers, representing 0.25% of Jalisco's population) and Náhuatl (11 650 speakers, representing 0.15% of the population of Jalisco), but also Purépecha (3 960 speakers, 0.05% of the population of Jalisco) [1]. For the present work, we analyzed HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) PCR-SSP based typings in 684 Mexicans from the state of Jalisco [composed by the following populations: Mexico Jalisco, Mexico Jalisco, Zapopan, N = 168, Allele Frequencies Net Database Identifier (AFND-ID): 3502; Mexico Jalisco, Tonalá, N = 35, AFND-ID: 3503; Tlaquepaque, N = 39, AFND-ID: 3504; Mexico Jalisco, Tlajomulco, N = 30, AFND-ID: 3505; Mexico Jalisco, Guadalajara city, N = 1189, AFND-ID: 3506; Mexico Jalisco Rural, N = 585, AFND-ID: 3579]. In addition to the individual populations we also show data for these combined populations. This latter data is not held on AFND to prevent duplication of data. Maximum-likelihood (ML) frequencies for alleles and four-locus haplotypes were estimated using an ExpectationMaximization algorithm. For a comprehensive review on the methods, such as sample collection, HLA typing and statistical analyses, please refer to [11] in this same issue. For the frequencies of HLA-A, -B, -DRB1 and -DQB1 and haplotypic data for the sample sets of the state of Jalisco please refer to the Supplementary Information: Supplementary Tables 1–11. For data on Hardy-Weinberg equilibrium (HWE) please see Supplementary Information: Supplementary Table 12 of this work and Supplementary Information: Supplementary Table 9 in [11] in this same issue. HLA allelic frequencies in our sample set from Guadalajara show virtually the same frequencies as previous reports for the city [12,13]. We find that the 12 most frequent haplotypes for the state (haplotypic frequency, H.F. ≥ 1.0%, arbitrarily; Supplementary Table 5) include nine Native American most probable ancestry (MPA) (HLA ∼ A*02 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*02 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, 2
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Fig. 1. Geographic situation of Jalisco and admixture proportions for the state of Jalisco [composed by the following populations: Mexico Jalisco Guadalajara, N = 1189, Allele Frequencies Net Database Identifier (AFND-ID): 3506; Mexico Jalisco Tlajomulco, N = 30, AFND-ID: 3505; Mexico Jalisco Tlaquepaque, N = 39, AFND-ID: 3504; Mexico Jalisco Tonalá, N = 35, AFND-ID: 3503; Mexico Jalisco Zapopan, N = 168, AFND-ID: 3502; Mexico Jalisco Rural, N = 585, AFND-ID: 3579]. Admixture proportions were estimated by a Maximum Likelihood method using HLA-A, -B and -DRB1 frequencies as genetic estimators. Green refers to the proportion of European contribution, purple to Native American contribution and yellow depicts African contribution. Map modified from Google Maps Pro [28].
A*24 ∼ B*39 ∼ DRB1*14 ∼ DQB1*03:01, A*68 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*40:02 ∼ DRB1*04 ∼ DQB1*03:02, A*68 ∼ B*48 ∼ DRB1*04 ∼ DQB1*03:02, A*24 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02 and A*24 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02) and three European MPA (HLA ∼ A*01 ∼ B*08 ∼ DRB1*03:01 ∼ DQB1*02, A*33 ∼ B*14:02 ∼ DRB1*01 ∼ DQB1*05 and A*29 ∼ B*44 ∼ DRB1*07 ∼ DQB1*02) haplotypes. Admixture estimates revealed that the main genetic components in the state of Jalisco are European (48.45 ± 1.18% by ML and 41.66% by estimating the proportion of European haplotypes) and Native American (44.02 ± 1.24% by ML and 39.86% by estimating the proportion of Native American haplotypes), while African genetic component is less apparent (7.53 ± 0.30% by ML and 9.62% by estimating the proportion of African haplotypes) (Fig. 1). A genome-wide single-nucleotide polymorphisms (SNPs) admixture estimation for the state of Jalisco [14] found similar admixture estimates of European (45.18%), Native American (50.60%) and African (4.23%) genetic components. These estimations slightly differ from previous reports for the region in which European component was estimated to be 30.8%, Native American estimated at 53.2% and African component was calculated to be 15.9% using 13 CODIS-short tandem repeats (CODIS-STRs) [15]. Uniparental markers show very different proportions: European component has been estimated to be 9% using mitochondrial DNA (mtDNA) [16], 60% using Y chromosome (Y-Chr) SNPs [17] and 67% using Y-Chr-linked STRs [18]; Native American component has been estimated to be 87% using mtDNA [16], 12% using Y-Chr SNPs [17] and 28% using Y-Chrlinked STRs [18]; and African component has been estimated to be 3% using mtDNA [16], 9% using Y-Chr SNPs [17] and 5% using Y-Chr-linked STRs [18]. Regional estimates using STRs estimated the components to be 57.3% European, 41.5% Native American and 1.3% African [19]. The differences between the estimation of the African component could be due to differences in the admixture estimation methods (three loci of HLA vs whole genome SNP data and uniparental markers) or differences in local genomic ancestry: there is an apparent increase in African ancestry in Latin American mixed ancestry populations that could be due to selection of such variants after the conquest and during the colonial period
(discussed in [11] in this issue). The noticeable African genetic component in a state traditionally not linked with African ancestral components may have to do with the important presence of enslaved African individuals in the region in the colonial period; the majority of people self-identified to be of African descent report to live in the peripheral regions of the GMZ [20]. We found that 6.35% of haplotypes are of Asian MPA with their proportion not varying considerably within the GMZ (Tonalá 0.00%, Tlaquepaque 3.85%, Zapopan 5.95%, Guadalajara 6.33%) or the rural areas (6.57%), except for Tlajomulco (10.00%). These results could be explained by the fact that Tlajomulco is one of the fastest-growing municipalities of the GMZ [21], attracting immigrants mainly from northern Mexico [22], which have different genetic components (specially since northern Mexico experienced a great migration flow of Asians in the beginning of the 20th century [23]). Interestingly, the different populations of Jalisco analyzed exhibit very different proportions of ancestral components: the European component ranges from 18.19 ± 7.16% by ML and 34.62% by estimating the proportion of European haplotypes in Tlaquepaque to 72.3 ± 3.08% by ML and 52.86% by estimating the proportion of European haplotypes in Tonalá. The African component goes from 5.11 ± 0.82% by ML and 8.27% by estimating the proportion of African haplotypes in the rural areas to 24.5 ± 7.62% by ML and 10.26% by estimating the proportion of African haplotypes in Tlaquepaque. Finally, the Native American component goes from 21.55 ± 2.94% by ML and 27.14% by estimating the proportion of Native American haplotypes in Tonalá to 57.31 ± 2.18% by ML and 51.29% by estimating the proportion of Native American haplotypes in Tlaquepaque. Important differences in the genetic composition of large metropolitan areas have been reported previously at the HLA genetic level [24]. The GMZ is a migratory concentration center [22] and immigration patterns into the metropolitan zone vary considerably, wih people settling preferentially in peripheral zones (which suffer from different extents of marginalization) such as those in Tlaquepaque, Tonalá and Tlajomulco [10,25]. Since people from other states [26] (some of them with a higher proportion of Native American genetic 3
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components) move into the GMZ, and specifically into this areas, it is expected that the Native American and African components are more prominent in the sample sets from the abovementioned municipalities when compared to Guadalajara and the rest of the state. All data from our sample sets, both frequencies and individual genotypes, can be found at The Allele Frequency Net Database website (www. allelefrequencies.net) [27].
https://doi.org/10.1111/j.1399-0039.2005.00495.x. [13] L.M. Cortes, L.M. Baltazar, M.G. Lopez-Cardona, N. Olivares, C. Ramos, M. Salazar, et al., HLA class II haplotypes in Mexican systemic lupus erythematosus patients, Hum. Immunol. 65 (2004) 1469–1476, https://doi.org/10.1016/j.humimm.2004. 09.008. [14] A. Moreno-Estrada, C.R. Gignoux, J.C. Fernández-López, F. Zakharia, M. Sikora, A.V. Contreras, et al., The genetics of Mexico recapitulates Native American substructure and affects biomedical traits, Science 344 (2014) 1280–1285, https://doi. org/10.1126/science.1251688. [15] R. Rubi-Castellanos, G. Martínez-Cortés, J.F. Muñoz-Valle, A. González-Martín, R.M. Cerda-Flores, M. Anaya-Palafox, et al., Pre-hispanic Mesoamerican demography approximates the present-day ancestry of Mestizos throughout the territory of Mexico, Am. J. Phys. Anthropol. 139 (2009) 284–294, https://doi.org/10.1002/ ajpa.20980. [16] G. Martínez-Cortés, J. Salazar-Flores, J. Haro-Guerrero, R. Rubi-Castellanos, J.S. Velarde-Félix, J.F. Muñoz-Valle, et al., Maternal admixture and population structure in Mexican-Mestizos based on mtDNA haplogroups, Am. J. Phys. Anthropol. 151 (2013) 526–537, https://doi.org/10.1002/ajpa.22293. [17] G. Martínez-Cortés, J. Salazar-Flores, L. Gabriela Fernández-Rodríguez, R. RubiCastellanos, C. Rodríguez-Loya, J.S. Velarde-Félix, et al., Admixture and population structure in Mexican-Mestizos based on paternal lineages, J. Hum. Genet. 57 (2012) 568–574, https://doi.org/10.1038/jhg.2012.67. [18] H. Rangel-Villalobos, J. Salazar-Flores, R. Dondiego, M. Anaya-Palafox, I. NuñoArana, L.M. Canseco-Ávila, et al., South to North increasing gradient of paternal European ancestry throughout the Mexican territory: evidence of Y-linked short tandem repeats, Forensic Sci. Int.: Genet. Suppl. Ser. 2 (2009) 448–450, https://doi. org/10.1016/j.fsigss.2009.08.003. [19] J.A. Aguilar-Velázquez, G. Martínez-Cortés, A. Inclán-Sánchez, A.F. FavelaMendoza, J.S. Velarde-Félix, H. Rangel-Villalobos, Forensic parameters and admixture in Mestizos from five geographic regions of Mexico based on 20 autosomal STRs (Powerplex 21 system), Int. J. Legal Med. 132 (2018) 1293–1296, https://doi. org/10.1007/s00414-018-1810-z. [20] J. Ávila, Afros, invisibles en Jalisco, Guadalajara, 2017. https://www. reporteindigo.com/reporte/afros-invisibles-en-jalisco/. [21] SEDESOL-CONAPO-INEGI, Delimitación de las zonas metropolitanas de México 2005, 2007. [22] J. Sobrino, Migración Interna en México Durante el Siglo XX, 1st Ed., Consejo Nacional de Población, Mexico City, 2010http://www.conapo.gob.mx. [23] J. Buchenau, Small numbers, great impact: Mexico and its immigrants, 1821–1973, J. Am. Ethnic History 20 (2001) 23–49, https://doi.org/10.2307/27502710. [24] E.D. Juárez Cortés, M.A. Sieck Contreras, A.J. Arriaga Perea, R.M. Macías Medrano, A. Balbuena Jaime, P. Everardo Martínez, et al., Genetic differentiation in a sample from northern Mexico city detected by HLA system analysis: impact in the study of population immunogenetics, Hum. Biol. 89 (2017) 181–193, https://doi.org/10. 13110/humanbiology.89.3.02. [25] Consejo Estatal de Población, Análisis Sociodemográfico para la Zona Metropolitana de Guadalajara, Guadalajara, 2008. https://web.archive.org/web/ 20100820205858/http://coepo.jalisco.gob.mx/PDF/Analisissociodemograficos/ Zmg.pdf. [26] A.G. Aguilar, P. Mateos, Demographic differentiation of Urban space in Mexico City | Diferenciación sociodemográfica del espacio urbano de la ciudad de México, Eure 37 (2011) 5–30, https://doi.org/10.4067/S0250-71612011000100001. [27] E.J.M. dos Santos, A. McCabe, F.F. Gonzalez-Galarza, A.R. Jones, D. Middleton, Allele Frequencies Net Database: Improvements for storage of individual genotypes and analysis of existing data, Hum. Immunol. 77 (2016) 238–248, https://doi.org/ 10.1016/j.humimm.2015.11.013. [28] Google, Google Earth Pro ©, (2019). earth.google.com.
Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.humimm.2019.05.012. References: [1] Instituto Nacional de Estadística y Geografía, Tabulados del cuestionario ampliado, Censo de Población y Vivienda 2010. (2011). http://www.beta.inegi.org.mx/ proyectos/ccpv/2010/ (accessed September 6, 2018). [2] S.S. Gorenstein, Western and Northwestern Mexico, in: R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas. Volume II, Mesoamerica, Part 1, Cambridge University Press, Cambridge, 2008, pp. 318–357. [3] D.V. Tetreault, C.F. Lucio López, Diversidad biocultural en el estado de Jalisco: Pueblos indígenas y regiones de alto valor biológico, Espiral: Estudios Sobre Estado y Sociedad (Guadalajara) 18 (2011) 165–199. [4] D. Hosler, Ancient west mexican metallurgy: a technological chronology, J. Field Archaeol. 15 (1988) 191–217, https://doi.org/10.1179/009346988791974475. [5] H. Ortega Villaseñor, Interculturalidad simulada en Jalisco, México, Cuadernos Interculturales 1 (2014) 103–133. [6] E. van Young, The Indigenous Peoples of Western Mexico from the Spanish Invasion to the Present, in: R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas, Mesoamerica, Cambridge University Press, Cambridge, 2008, pp. 136–186. [7] H. Rangel-Villalobos, J.F. Muñoz-Valle, A. González-Martín, A. Gorostiza, M.T. Magaña, L.A. Páez-Riberos, Relaciones genéticas y patrones de estructura entre mestizos y etnias mexicanas revelados por marcadores el cromosoma Y, Estudios de Antropología Biológica XIV (2009) 131–151. [8] R. Guzmán Mejía, M. del C. Anaya Corona, Cultura de maíz-peyote-venado : sustentabilidad del pueblo wixárika, Univ. de Guadalajara, Centro Universitario de Los Altos, Tepatitán de Morelos, Jalisco, 2007. [9] Comisión Estatal Indigena, Pueblos Indígenas. Pueblo Indígena Wixáritari, Comisión Estatal Indigena – CEI. (n.d.). https://cei.jalisco.gob.mx/temas-deinteres/173. [10] F. Domínguez Rueda, La migración indígena a la ciudad de Guadalajara, Tukari. Espacio de Comunicación Intercultural. (2008) 4. http://www.tukari.udg.mx/sites/ default/files/tukari_6.pdf. [11] R. Barquera, D.I. Hernández Zaragoza, A. Bravo Acevedo, E. Arrieta Bolaños, S. Clayton, V. Acuña Alonzo, et al., The immunogenetic diversity of the HLA system in Mexico correlates with underlying population genetic structure, Hum. Immunol. (2019). [12] C.A. Leal, F. Mendoza-Carrera, F. Rivas, S. Rodriguez-Reynoso, E. Portilla-De Buen, HLA-A and HLA-B allele frequencies in a mestizo population from Guadalajara, Mexico, determined by sequence-based typing, Tissue Antigens 66 (2005) 666–673,
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Human Immunology journal homepage: www.elsevier.com/locate/humimm
Genetic diversity of HLA system in six populations from Jalisco, Mexico: Guadalajara city, Tlajomulco, Tlaquepaque, Tonalá, Zapopan and rural Jalisco Alicia Bravo-Acevedoa,1, Araceli Escobedo-Ruízb,1, Rodrigo Barquerac,d, ,1, Stephen Claytond,1, Víctor Eduardo García-Ariase,1, Esteban Arrieta-Bolañosf,1, Isis Goné-Vázquezb, Diana Iraíz Hernández-Zaragozac,g, Francia Paulina Arellano-Pradoe, Marla Estefanía Rodríguez-Lópeze, María Guadalupe de Jesús Sánchez-Fernándezh, Mario J. Sandoval-Sandovali, Benjamín Gómez-Navarroj, Joaquín Zúñigak,l, Edmond J. Yunism, ⁎ Carolina Bekker-Méndezn, , Julio Granadoso ⁎
a
Blood Bank, UMAE Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico Histocompatibility Laboratory, Hospital de Especialidades, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico c Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico d Department of Archaeogenetics, Max Planck Institute for the Science of Human History (MPI-SHH), Jena, Germany e Pediatrics Hospital, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico f Institute for Experimental Cellular Therapy, University Hospital Essen, Essen, Germany g Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico h Department of Nephrology and Transplantation Unit, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico i Central Office of Transplantation, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico j Central Office of Nephrology, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico k Laboratory of Immunobiology and Genetics, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Mexico City, Mexico l Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Mexico City, Mexico m Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA, USA n Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional “La Raza”, Instituto Mexicano del Seguro Social (IMSS), Mexico City, Mexico o Department of Transplantation, Instituto Nacional de Ciencias Médicas y Nutrición “Salvador Zubirán” (INCMNSZ), Mexico City, Mexico b
ARTICLE INFO
ABSTRACT
Keywords: HLA Immunogenetics Population genetics Jalisco Admixture
We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 2046 Mexicans from the state of Jalisco living in the city of Guadalajara (N = 1189), Tlajomulco (N = 30), Tlaquepaque (N = 39), Tonalá (N = 35), Zapopan (N = 168) and rural communities (N = 585), to obtain information regarding allelic and haplotypic frequencies. We find that the most frequent haplotypes found in the state of Jalisco include nine Native American most probable ancestry and three European haplotypes. Admixture estimates revealed that the main genetic components in the state of Jalisco are European (48.45 ± 1.18% by ML; 41.66% of European haplotypes) and Native American (44.02 ± 1.24% by ML; 39.86% of Native American haplotypes), while African genetic component is less apparent (7.53 ± 0.30% by ML; 9.62% of African haplotypes).
Abbreviations: HLA, Human Leukocyte Antigen; MPA, Most-probable ancestry; LD, Linkage Disequilibrium ⁎ Corresponding authors at: Department of Archaeogenetics, Max Planck Institute for the Science of Human History. Kahlaische Strasse 10, 07745 Jena, Germany (R. Barquera), Immunology and Infectology Research Unit, Infectology Hospital, Centro Médico Nacional La Raza, Instituto Mexicano del Seguro Social (IMSS), Calzada Vallejo y Jacarandas S/N Colonia La Raza, 02990, Mexico City, Mexico (C.B. Méndez). E-mail addresses: [email protected] (R. Barquera), [email protected] (C. Bekker-Méndez). URLs: http://www.shh.mpg.de/en (R. Barquera), http://www.cienciaimss.org/uim-en-inmunologia-e-infectologia/ (C. Bekker-Méndez). 1 These authors contributed equally to the present work. https://doi.org/10.1016/j.humimm.2019.05.012 Received 30 April 2019; Received in revised form 30 May 2019; Accepted 30 May 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Alicia Bravo-Acevedo, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.05.012
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Jalisco is located in northwestern Mexico, bounded on the north by the states of Nayarit, Zacatecas, Aguascalientes, San Luis Potosí, on the east by Guanajuato, on the south by Michoacán and Colima, and on the west by the Pacific Ocean. It is the third most populated state, and the seventh largest in the territory. The state of Jalisco is composed of 125 municipalities, being the most populated Guadalajara, the capital city, located in the central region of Jalisco, in the geographical area known as Valle de Atemajac, and with a population of 1 495 189 inhabitants [1]. Guadalajara, together with the municipalities of Zapopan, Tlaquepaque, Tonalá, Tlajomulco, El Salto, Ixtahuacán de los Membrillos, Zapotlanejo and Juanacatlán, make up the Metropolitan Area of Guadalajara (GMZ), which is the second largest urban agglomeration in Mexico after the Mexico City. It is from this area that most of the samples for this study came from. By 2010, 78% of the population lived in urban areas and 22% in rural areas [1]. The first settlements of villages date from 1500 years BC, and its settlers were dedicated to hunting, cultivation of corn, beans, potatoes, squash, chili and tomatoes, and the manufacture of ceramics. Radiocarbon dating places occupation of Jalisco beginning from the second century BC until the 5th century AD [2]. The Classic period in northern Jalisco is represented by the Teuchitlan tradition. There are three phases described: the Ahualulco phase (AD 200–400), the Teuchitlan I phase (AD 400–700), and the Teuchitlan II phase (AD 700–1000). In the Teuchitlan tradition, apparently there was a population implosion and the development of the district as a key economic area. Apparently, a statelike organization developed in the Ahualulco phase and a connection was made to Central Mexico during the Teuchitlan phases. Social and political systems were stratified, and political centralization developed [2]. Around the year 600 BC, with the Toltec cultural expansion from the Central Highlands, began the use of metallurgical technique, the installation of irrigation systems, a writing system and the military control of some peoples, particularly Tarascos. However, the indigenous groups in western Mexico did not constitute large states, but rather lordships or cacicazgos, of smaller size [3]. Barra de Navidad is a small coastal site near a saline lagoon in southern coastal Jalisco. The site has been dated tentatively at AD 650-Contact and has been described as either seasonally occupied by inland peoples or permanently occupied by settlers who subsisted mainly on shellfish but who also traded salt, fish, and shellfish to inland peoples for inland products [2]. Metallurgy first appeared in Mesoamerica in Western and Northwestern Mexico in the current states of Jalisco, Michoacan, and Nayarit, probably by AD 800 [4]. Several of the indigenous populations of the region disappeared before the conquest, like the cultures of Capacha and Teuchitlán. The territory of the current state of Jalisco has been inhabited by different ethnic groups: bapames, caxcanes, cocas, cuachichiles, huicholes, cuyutecos, otomíes, nahuas, tecuehuanes, tepehuanes, tecos, purépechas, pinomes, tzaultecas and xilotlantzingas, although at the time of the arrival of the Spaniards to the territory, two main ones existed: Huicholes, or Wixárika people, in the north, and several Nahuas towns in the south. The Spanish, in search of precious minerals, began expeditions to achieve conquest in 1522. During the 16th century, the extermination and subjugation of indigenous peoples was carried out, which resulted in their dissemination or subordination. The Province of Nueva Galicia was established in 1531, with the intention of creating a place that would facilitate the conquest of territories to the north and serve as a link between the mines of Zacatecas and Mexico City, as well as a port of commerce with the far East [5]. The most attractive habitable sites in the Center-West, and therefore generally speaking the areas of densest native population and long-standing centers of economic and political significance after the arrival of the Europeans [6], were the fertile depressions of ancient lakes [among the most important the Bajío region, Morelia, Guadalajara (centered on Lake Chapala), Ameca, Sayula, Tepic, Autlán, and Colima basins, and the Lake Pátzcuaro region]. The Wixárika people have achieved the practice of sustainable
agriculture, in extremely adverse environmental conditions. They are also semi-nomadic, for religious and economic reasons. Its geographic isolation and resistance to Western assimilation has kept this community quite isolated and attached to its cultural practices [7,8]. During the 17th and 18th centuries the indigenous population of Nueva Galicia, a Spanish political entity embracing much of the Center-West, declined from some 850,000 to about 70,000 [6]. In northern Jalisco, due to the debacle of the native population by epidemic diseases, the region was repopulated with people of Iberian origin, which explains the predominance of European genetic background in that area. The Nahua population, in contrast, were not a social group so isolated or so cohesive; In the south of Jalisco, haciendas were established that fragmented their territories and forced their dispersion. Thus, miscegenation, christianization, and in general, a process of “de-Indianization” began in southern Jalisco. The proliferation of ranchos, therefore (except in the Altos de Jalisco and proximate zones, where it was already well under way by 1800 or earlier), seems to have been a mid- to late nineteenth-century phenomenon. The story of this and other agrarian transitions, even if it cannot explain the entire culture history of the Center-West, for sure involved indigenous groups until comparatively recent times [6]. Currently there are two regions inhabited by indigenous people in Jalisco: the Sierra Huichola, mainly in the municipalities of Bolaños, Huejuquilla el Alto and Mezquitic, inhabited by the Wixáritari people (Huichol), and the Sierra de Manantlán, in the municipalities of Tuxpan, Cuautitlán de García Barragán, Zapotitlán de Vadillo and Villa Purificación, inhabited by Nahuas-Otomíes. The region also includes indigenous people from other ethnic groups of different states of the Republic, who reside permanently in the Metropolitan Area of Guadalajara, mainly Purépechas from Michoacán, Zapotecs, Mixtecs and Triquis from Oaxaca, Ñahñu/Otomí from the State of Mexico, Mazahuas from Guerrero, Tzotziles and Tzeltales from Chiapas, Nahuas from Guerrero and Hidalgo, among others [9,10]. Around 0.7% of the population in Jalisco speaks indigenous languages (53 695 people over 3 years old), highlighting the two most prominent native languages in the state: Huichol (18 409 speakers, representing 0.25% of Jalisco's population) and Náhuatl (11 650 speakers, representing 0.15% of the population of Jalisco), but also Purépecha (3 960 speakers, 0.05% of the population of Jalisco) [1]. For the present work, we analyzed HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) PCR-SSP based typings in 684 Mexicans from the state of Jalisco [composed by the following populations: Mexico Jalisco, Mexico Jalisco, Zapopan, N = 168, Allele Frequencies Net Database Identifier (AFND-ID): 3502; Mexico Jalisco, Tonalá, N = 35, AFND-ID: 3503; Tlaquepaque, N = 39, AFND-ID: 3504; Mexico Jalisco, Tlajomulco, N = 30, AFND-ID: 3505; Mexico Jalisco, Guadalajara city, N = 1189, AFND-ID: 3506; Mexico Jalisco Rural, N = 585, AFND-ID: 3579]. In addition to the individual populations we also show data for these combined populations. This latter data is not held on AFND to prevent duplication of data. Maximum-likelihood (ML) frequencies for alleles and four-locus haplotypes were estimated using an ExpectationMaximization algorithm. For a comprehensive review on the methods, such as sample collection, HLA typing and statistical analyses, please refer to [11] in this same issue. For the frequencies of HLA-A, -B, -DRB1 and -DQB1 and haplotypic data for the sample sets of the state of Jalisco please refer to the Supplementary Information: Supplementary Tables 1–11. For data on Hardy-Weinberg equilibrium (HWE) please see Supplementary Information: Supplementary Table 12 of this work and Supplementary Information: Supplementary Table 9 in [11] in this same issue. HLA allelic frequencies in our sample set from Guadalajara show virtually the same frequencies as previous reports for the city [12,13]. We find that the 12 most frequent haplotypes for the state (haplotypic frequency, H.F. ≥ 1.0%, arbitrarily; Supplementary Table 5) include nine Native American most probable ancestry (MPA) (HLA ∼ A*02 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*02 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, 2
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Fig. 1. Geographic situation of Jalisco and admixture proportions for the state of Jalisco [composed by the following populations: Mexico Jalisco Guadalajara, N = 1189, Allele Frequencies Net Database Identifier (AFND-ID): 3506; Mexico Jalisco Tlajomulco, N = 30, AFND-ID: 3505; Mexico Jalisco Tlaquepaque, N = 39, AFND-ID: 3504; Mexico Jalisco Tonalá, N = 35, AFND-ID: 3503; Mexico Jalisco Zapopan, N = 168, AFND-ID: 3502; Mexico Jalisco Rural, N = 585, AFND-ID: 3579]. Admixture proportions were estimated by a Maximum Likelihood method using HLA-A, -B and -DRB1 frequencies as genetic estimators. Green refers to the proportion of European contribution, purple to Native American contribution and yellow depicts African contribution. Map modified from Google Maps Pro [28].
A*24 ∼ B*39 ∼ DRB1*14 ∼ DQB1*03:01, A*68 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*40:02 ∼ DRB1*04 ∼ DQB1*03:02, A*68 ∼ B*48 ∼ DRB1*04 ∼ DQB1*03:02, A*24 ∼ B*35 ∼ DRB1*04 ∼ DQB1*03:02 and A*24 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02) and three European MPA (HLA ∼ A*01 ∼ B*08 ∼ DRB1*03:01 ∼ DQB1*02, A*33 ∼ B*14:02 ∼ DRB1*01 ∼ DQB1*05 and A*29 ∼ B*44 ∼ DRB1*07 ∼ DQB1*02) haplotypes. Admixture estimates revealed that the main genetic components in the state of Jalisco are European (48.45 ± 1.18% by ML and 41.66% by estimating the proportion of European haplotypes) and Native American (44.02 ± 1.24% by ML and 39.86% by estimating the proportion of Native American haplotypes), while African genetic component is less apparent (7.53 ± 0.30% by ML and 9.62% by estimating the proportion of African haplotypes) (Fig. 1). A genome-wide single-nucleotide polymorphisms (SNPs) admixture estimation for the state of Jalisco [14] found similar admixture estimates of European (45.18%), Native American (50.60%) and African (4.23%) genetic components. These estimations slightly differ from previous reports for the region in which European component was estimated to be 30.8%, Native American estimated at 53.2% and African component was calculated to be 15.9% using 13 CODIS-short tandem repeats (CODIS-STRs) [15]. Uniparental markers show very different proportions: European component has been estimated to be 9% using mitochondrial DNA (mtDNA) [16], 60% using Y chromosome (Y-Chr) SNPs [17] and 67% using Y-Chr-linked STRs [18]; Native American component has been estimated to be 87% using mtDNA [16], 12% using Y-Chr SNPs [17] and 28% using Y-Chrlinked STRs [18]; and African component has been estimated to be 3% using mtDNA [16], 9% using Y-Chr SNPs [17] and 5% using Y-Chr-linked STRs [18]. Regional estimates using STRs estimated the components to be 57.3% European, 41.5% Native American and 1.3% African [19]. The differences between the estimation of the African component could be due to differences in the admixture estimation methods (three loci of HLA vs whole genome SNP data and uniparental markers) or differences in local genomic ancestry: there is an apparent increase in African ancestry in Latin American mixed ancestry populations that could be due to selection of such variants after the conquest and during the colonial period
(discussed in [11] in this issue). The noticeable African genetic component in a state traditionally not linked with African ancestral components may have to do with the important presence of enslaved African individuals in the region in the colonial period; the majority of people self-identified to be of African descent report to live in the peripheral regions of the GMZ [20]. We found that 6.35% of haplotypes are of Asian MPA with their proportion not varying considerably within the GMZ (Tonalá 0.00%, Tlaquepaque 3.85%, Zapopan 5.95%, Guadalajara 6.33%) or the rural areas (6.57%), except for Tlajomulco (10.00%). These results could be explained by the fact that Tlajomulco is one of the fastest-growing municipalities of the GMZ [21], attracting immigrants mainly from northern Mexico [22], which have different genetic components (specially since northern Mexico experienced a great migration flow of Asians in the beginning of the 20th century [23]). Interestingly, the different populations of Jalisco analyzed exhibit very different proportions of ancestral components: the European component ranges from 18.19 ± 7.16% by ML and 34.62% by estimating the proportion of European haplotypes in Tlaquepaque to 72.3 ± 3.08% by ML and 52.86% by estimating the proportion of European haplotypes in Tonalá. The African component goes from 5.11 ± 0.82% by ML and 8.27% by estimating the proportion of African haplotypes in the rural areas to 24.5 ± 7.62% by ML and 10.26% by estimating the proportion of African haplotypes in Tlaquepaque. Finally, the Native American component goes from 21.55 ± 2.94% by ML and 27.14% by estimating the proportion of Native American haplotypes in Tonalá to 57.31 ± 2.18% by ML and 51.29% by estimating the proportion of Native American haplotypes in Tlaquepaque. Important differences in the genetic composition of large metropolitan areas have been reported previously at the HLA genetic level [24]. The GMZ is a migratory concentration center [22] and immigration patterns into the metropolitan zone vary considerably, wih people settling preferentially in peripheral zones (which suffer from different extents of marginalization) such as those in Tlaquepaque, Tonalá and Tlajomulco [10,25]. Since people from other states [26] (some of them with a higher proportion of Native American genetic 3
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components) move into the GMZ, and specifically into this areas, it is expected that the Native American and African components are more prominent in the sample sets from the abovementioned municipalities when compared to Guadalajara and the rest of the state. All data from our sample sets, both frequencies and individual genotypes, can be found at The Allele Frequency Net Database website (www. allelefrequencies.net) [27].
https://doi.org/10.1111/j.1399-0039.2005.00495.x. [13] L.M. Cortes, L.M. Baltazar, M.G. Lopez-Cardona, N. Olivares, C. Ramos, M. Salazar, et al., HLA class II haplotypes in Mexican systemic lupus erythematosus patients, Hum. Immunol. 65 (2004) 1469–1476, https://doi.org/10.1016/j.humimm.2004. 09.008. [14] A. Moreno-Estrada, C.R. Gignoux, J.C. Fernández-López, F. Zakharia, M. Sikora, A.V. Contreras, et al., The genetics of Mexico recapitulates Native American substructure and affects biomedical traits, Science 344 (2014) 1280–1285, https://doi. org/10.1126/science.1251688. [15] R. Rubi-Castellanos, G. Martínez-Cortés, J.F. Muñoz-Valle, A. González-Martín, R.M. Cerda-Flores, M. Anaya-Palafox, et al., Pre-hispanic Mesoamerican demography approximates the present-day ancestry of Mestizos throughout the territory of Mexico, Am. J. Phys. Anthropol. 139 (2009) 284–294, https://doi.org/10.1002/ ajpa.20980. [16] G. Martínez-Cortés, J. Salazar-Flores, J. Haro-Guerrero, R. Rubi-Castellanos, J.S. Velarde-Félix, J.F. Muñoz-Valle, et al., Maternal admixture and population structure in Mexican-Mestizos based on mtDNA haplogroups, Am. J. Phys. Anthropol. 151 (2013) 526–537, https://doi.org/10.1002/ajpa.22293. [17] G. Martínez-Cortés, J. Salazar-Flores, L. Gabriela Fernández-Rodríguez, R. RubiCastellanos, C. Rodríguez-Loya, J.S. Velarde-Félix, et al., Admixture and population structure in Mexican-Mestizos based on paternal lineages, J. Hum. Genet. 57 (2012) 568–574, https://doi.org/10.1038/jhg.2012.67. [18] H. Rangel-Villalobos, J. Salazar-Flores, R. Dondiego, M. Anaya-Palafox, I. NuñoArana, L.M. Canseco-Ávila, et al., South to North increasing gradient of paternal European ancestry throughout the Mexican territory: evidence of Y-linked short tandem repeats, Forensic Sci. Int.: Genet. Suppl. Ser. 2 (2009) 448–450, https://doi. org/10.1016/j.fsigss.2009.08.003. [19] J.A. Aguilar-Velázquez, G. Martínez-Cortés, A. Inclán-Sánchez, A.F. FavelaMendoza, J.S. Velarde-Félix, H. Rangel-Villalobos, Forensic parameters and admixture in Mestizos from five geographic regions of Mexico based on 20 autosomal STRs (Powerplex 21 system), Int. J. Legal Med. 132 (2018) 1293–1296, https://doi. org/10.1007/s00414-018-1810-z. [20] J. Ávila, Afros, invisibles en Jalisco, Guadalajara, 2017. https://www. reporteindigo.com/reporte/afros-invisibles-en-jalisco/. [21] SEDESOL-CONAPO-INEGI, Delimitación de las zonas metropolitanas de México 2005, 2007. [22] J. Sobrino, Migración Interna en México Durante el Siglo XX, 1st Ed., Consejo Nacional de Población, Mexico City, 2010http://www.conapo.gob.mx. [23] J. Buchenau, Small numbers, great impact: Mexico and its immigrants, 1821–1973, J. Am. Ethnic History 20 (2001) 23–49, https://doi.org/10.2307/27502710. [24] E.D. Juárez Cortés, M.A. Sieck Contreras, A.J. Arriaga Perea, R.M. Macías Medrano, A. Balbuena Jaime, P. Everardo Martínez, et al., Genetic differentiation in a sample from northern Mexico city detected by HLA system analysis: impact in the study of population immunogenetics, Hum. Biol. 89 (2017) 181–193, https://doi.org/10. 13110/humanbiology.89.3.02. [25] Consejo Estatal de Población, Análisis Sociodemográfico para la Zona Metropolitana de Guadalajara, Guadalajara, 2008. https://web.archive.org/web/ 20100820205858/http://coepo.jalisco.gob.mx/PDF/Analisissociodemograficos/ Zmg.pdf. [26] A.G. Aguilar, P. Mateos, Demographic differentiation of Urban space in Mexico City | Diferenciación sociodemográfica del espacio urbano de la ciudad de México, Eure 37 (2011) 5–30, https://doi.org/10.4067/S0250-71612011000100001. [27] E.J.M. dos Santos, A. McCabe, F.F. Gonzalez-Galarza, A.R. Jones, D. Middleton, Allele Frequencies Net Database: Improvements for storage of individual genotypes and analysis of existing data, Hum. Immunol. 77 (2016) 238–248, https://doi.org/ 10.1016/j.humimm.2015.11.013. [28] Google, Google Earth Pro ©, (2019). earth.google.com.
Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.humimm.2019.05.012. References: [1] Instituto Nacional de Estadística y Geografía, Tabulados del cuestionario ampliado, Censo de Población y Vivienda 2010. (2011). http://www.beta.inegi.org.mx/ proyectos/ccpv/2010/ (accessed September 6, 2018). [2] S.S. Gorenstein, Western and Northwestern Mexico, in: R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas. Volume II, Mesoamerica, Part 1, Cambridge University Press, Cambridge, 2008, pp. 318–357. [3] D.V. Tetreault, C.F. Lucio López, Diversidad biocultural en el estado de Jalisco: Pueblos indígenas y regiones de alto valor biológico, Espiral: Estudios Sobre Estado y Sociedad (Guadalajara) 18 (2011) 165–199. [4] D. Hosler, Ancient west mexican metallurgy: a technological chronology, J. Field Archaeol. 15 (1988) 191–217, https://doi.org/10.1179/009346988791974475. [5] H. Ortega Villaseñor, Interculturalidad simulada en Jalisco, México, Cuadernos Interculturales 1 (2014) 103–133. [6] E. van Young, The Indigenous Peoples of Western Mexico from the Spanish Invasion to the Present, in: R.E.W. Adams, M.J. MacLeod (Eds.), The Cambridge History of the Native Peoples of the Americas, Mesoamerica, Cambridge University Press, Cambridge, 2008, pp. 136–186. [7] H. Rangel-Villalobos, J.F. Muñoz-Valle, A. González-Martín, A. Gorostiza, M.T. Magaña, L.A. Páez-Riberos, Relaciones genéticas y patrones de estructura entre mestizos y etnias mexicanas revelados por marcadores el cromosoma Y, Estudios de Antropología Biológica XIV (2009) 131–151. [8] R. Guzmán Mejía, M. del C. Anaya Corona, Cultura de maíz-peyote-venado : sustentabilidad del pueblo wixárika, Univ. de Guadalajara, Centro Universitario de Los Altos, Tepatitán de Morelos, Jalisco, 2007. [9] Comisión Estatal Indigena, Pueblos Indígenas. Pueblo Indígena Wixáritari, Comisión Estatal Indigena – CEI. (n.d.). https://cei.jalisco.gob.mx/temas-deinteres/173. [10] F. Domínguez Rueda, La migración indígena a la ciudad de Guadalajara, Tukari. Espacio de Comunicación Intercultural. (2008) 4. http://www.tukari.udg.mx/sites/ default/files/tukari_6.pdf. [11] R. Barquera, D.I. Hernández Zaragoza, A. Bravo Acevedo, E. Arrieta Bolaños, S. Clayton, V. Acuña Alonzo, et al., The immunogenetic diversity of the HLA system in Mexico correlates with underlying population genetic structure, Hum. Immunol. (2019). [12] C.A. Leal, F. Mendoza-Carrera, F. Rivas, S. Rodriguez-Reynoso, E. Portilla-De Buen, HLA-A and HLA-B allele frequencies in a mestizo population from Guadalajara, Mexico, determined by sequence-based typing, Tissue Antigens 66 (2005) 666–673,
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