- Email: [email protected]
Genetic diversity of HLA system in two populations from Nayarit, Mexico: Tepic and rural Nayarit
Human Immunology xxx (xxxx) xxx–xxx
Contents lists available at ScienceDirect
Human Immunology journal homepage: www.elsevier.com/locate/humimm
Genetic diversity of HLA system in two populations from Nayarit, Mexico: Tepic and rural Nayarit Isis Goné-Vázqueza,1, Rodrigo Barquerab,c, ,1, Francia Paulina Arellano-Pradod,1, Diana Iraíz Hernández-Zaragozab,e,1, Araceli Escobedo-Ruíza,1, Stephen Claytonc,1, Esteban Arrieta-Bolañosf,1, Víctor Eduardo García-Ariasd, Marla Estefanía Rodríguez-Lópezd, Alicia Bravo-Acevedog, 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
Histocompatibility Laboratory, Hospital de Especialidades, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico b Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico c Department of Archaeogenetics, Max Planck Institute for the Science of Human History (MPI-SHH), Jena, Germany d Pediatrics Hospital, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico e Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico f Institute for Experimental Cellular Therapy, University Hospital Essen, Essen, Germany g Blood Bank, UMAE Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), 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
ARTICLE INFO
ABSTRACT
Keywords: HLA Immunogenetics Population genetics Nayarit Admixture
We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 161 Mexicans from the state of Nayarit living in Tepic (N = 97) and rural communities (N = 64), to obtain information regarding allelic and haplotypic frequencies. We find that the ten most frequent haplotypes found in the state of Nayarit include eight Native American and two European haplotypes. Admixture estimates revealed that the main genetic components in the state of Nayarit are Native American (50.79 ± 5.03% by ML; 42.24% of Native American haplotypes) and European (37.04 ± 6.21% by ML; 35.72% of European haplotypes), while African genetic component is less apparent but relatively high (12.17 ± 2.50% by ML; 13.36% of African haplotypes).
The state of Nayarit is located in the west of the country, bounded on the north by Sinaloa and Durango, on the east by Zacatecas, on the
east and south by Jalisco and on the west by the Pacific Ocean, where it also has the islands of Islas Marías, Isla Isabel, the Tres Marietas islands
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. Bekker-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.2019.06.008 Received 2 June 2019; Accepted 6 June 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Isis Goné-Vázquez, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.06.008
Human Immunology xxx (xxxx) xxx–xxx
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and Farallón La Peña. With 1 181 050 inhabitants by 2015, it is the fourth least populated state; with 27 815 km2, the ninth least extensive; and with 39.01 inhabitants/km2, the ninth least densely populated. It was founded on January 26, 1917, is divided into 20 municipalities and its capital city is Tepic. In Nayarit there are 52 833 people who spoke an indigenous language, according to INEGI on 2013, the five indigenous languages more commonly spoken are Huichol (47.6%), Cora (39.4%), Tepehuano (3.7%), Nahuatl (3.6%) and Zapotec (0.9%) [1]. It should be noted that the Huichol ethnic group has displaced the Cora, which had the highest demographic weight in Nayarit until before 1995. The main ethnic groups that registered the census of the year 2000 in the state are the Huicholes (16 932 people), the Coras (15 389) and the Tepehuanos (1422); Nahuatl (1422) has initiated an increase caused by immigration from the state of Guerrero and other entities in the center of the country [2]. For the important archaeological site of Ixtlan del Rio, several periods have been described, an Early Period that was aligned with Early Chametla, a Middle Period comparable to Late Chametla 2 and Early Culiacan 2 (Aztatlan complex) and a Late Period, which is related to Late Culiacan and the Autlan Complex. Early Ixtlan is Classic Period, and Middle and Late Ixtlan are Postclassic. A large dense population, the presence of markets and trade in maize and chile can be inferred [3] from conquest period data. The cultural transition zone between semior non-sedentary and settled farming peoples very roughly bisected the Center-West from southeast to northwest, corresponding respectively to the geographic and climatic division between the formidable mountains of upland Nayarit, arid high steppes of central Zacatecas, Bajío plains to the north, the narrow mid-Pacific coastal plain to the west, and neovolcanic lacustrine basins and Michoacán highlands to the south. Coastal Nayarit, on the other hand, was occupied by peoples of Totorame speech (related to Cora) from around the Tropic of Cancer south to about the latitude of present-day Tepic, while Coras, Tecuales, Huicholes, and Tepehuanes held the uplands. These peoples were parttime farmers living in dispersed settlements, but their populations reached fairly high densities [4]. Stone sculpture traditions started showing around 700 CE. The small scale and relative simplicity of these sculptures suggest they were central pieces of village or domestic cults, rather than large public worshipping like those seen in the larger urban centers of central Mesoamerica [5]. Only by the end of the 16th century did the native inhabitants of the eastern Nayarit sierra, southwestern Zacatecas, and the cañones area of Nueva Galicia come under some degree of stable Spanish control. It was not until 1721 that the Cora chieftain met with the viceroy in Mexico City [4]. While the Franciscans missionized the Huicholes, modern Cora culture took definitive shape in the eighteenth century when the Jesuits
concentrated the Indians in their most important population centers. Many Huicholes of the Nayarit sierra at first adhered to the insurgent cause, but later they switched their loyalties to the loyalist side after 1815 in a complex ploy to pursue local indigenous interests. By the time the independence was practically achieved, the Franciscan missionaries left the area. By the mid-nineteenth century many Huichol villages consisted of clusters of huts gathered around abandoned churches, and were held together by simple political structures and subsistence agriculture, tending to remain isolated from Hispanic society except for essential commercial contacts. However, during the first years of the 20th century, privately owned estates were assembled, land concentration reached extreme indices, and by the first third of the 20th century foreigners owned > 50% of the rural areas of the state of Nayarit [4]. The study of population immunogenetics of human groups from Nayarit adds to the growing knowledge on the population genetics of Western Mexico. For the present work, we analyzed HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) PCR-SSP based typings in 161 Mexicans from the state of Nayarit [composed by the following populations: Mexico Nayarit, Tepic, N = 97, Allele Frequencies Net Database Identifier (AFND-ID): 3508; Mexico Nayarit Rural, N = 64, AFND-ID: 3578]. 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 [6] 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 Nayarit please refer to the Supplementary Information: Supplementary Tables 1–7. For data on Hardy-Weinberg equilibrium (HWE) please see Supplementary Information: Supplementary Table 8 of this work and Supplementary Information: Supplementary Table 9 in [6] in this same issue. We find that the most frequent haplotypes for the state (haplotypic frequency, H.F. ≥1.0%, arbitrarily; Supplementary Table 5) include eight Native American most probable ancestry (MPA) (HLA ∼ A*24 ∼ B*40:02 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*68 ∼ B*48 ∼ DRB1*04 ∼ DQB1*03:02, A *24 ∼ B*39 ∼ DRB1*14 ∼ DQB1*03:01, A*24 ∼ B*35 ∼ DRB1* 16 ∼ DQB1*03:01, A*68 ∼ B*40:02 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02 and A*02 ∼ B*35 ∼ DRB1 *04 ∼ DQB1*03:02) and two European MPA haplotypes (A*30 ∼ B*18 ∼ DRB1*03:01 ∼ DQB1*02 and A*02 ∼ B*08 ∼ DRB1 *03:01 ∼ DQB1*02). Admixture estimates (Fig. 1) revealed that the main genetic components in the state of Nayarit are Native American Fig. 1. Geographic situation of Nayarit and admixture proportions for the state of Nayarit [composed by the following populations: Mexico Nayarit, Tepic, N = 97, Allele Frequencies Net Database Identifier (AFND-ID): 3508; Mexico Nayarit Rural, N = 64, AFND-ID: 3578]. Admixture proportions were estimated by ML 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 [12].
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(50.79 ± 5.03% by the maximum likelihood method and 42.24% by estimating the proportion of Native American haplotypes) and European (37.04 ± 6.21% by the maximum likelihood method and 35.72% by estimating the proportion of European haplotypes), while African genetic component is less apparent (12.17 ± 2.50% by the maximum likelihood method and 13.36% by estimating the proportion of African haplotypes). Interestingly, the rural areas of Nayarit have almost twice as much the proportion of African contribution (16.43% ± 6.28% by the maximum likelihood method and 16.41% by estimating the proportion of African haplotypes) as the city of Tepic (9.49% ± 0.90% by the maximum likelihood method and 11.34% by estimating the proportion of African haplotypes). These estimations slightly differ from previous reports for the state of Nayarit in which European component was estimated to be 38.0%, Native American estimated at 56.7% and African component was calculated to be 5.3% using 13 CODIS-short tandem repeats (CODIS-STRs) [7]. When classical markers (i.e. blood groups) were used as genetic estimators in a sample from La Mesa, Nayarit, the proportions of each component were distributed as follows: Native American 79.2%, European 20.0% and African 0.8% [8]. The differences between the estimation of the African component could be due to differences in the admixture estimation methods (three loci of HLA vs. STRs vs. blood groups) 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 [6] in this issue). The New Kingdom of Galicia had, by the end of the 16th century, the third most important population of Africans and the fourth one of Mulattoes [9]. Nayarit was part of that administrative unit, which can partially explain that Nayarit has one of the highest contributions of African ancestry of all states studied in Mexico [6]. The admixture proportions for Tepic and the rural areas of the state don’t show any major shifts to what we found at the state level referring to European and Native American ancestral components (Fig. 1). In concordance with previous reports [10], we found a higher prevalence of African genetic components in the rural areas when compared to urban settlements. We could detect the presence of 6.52% of Asian haplotypes and 2.17% of mixed ancestry haplotypes for the state of Nayarit, with similar proportions both in Tepic (7.22% and 1.55%, respectively) and the rural areas of the state (5.47% and 3.13%, respectively). The admixture estimates and the presence of Native American, European and Asian haplotypes can be explained by the aforementioned historical events that shaped the demographic traits of the
present day state of Nayarit. All data from our sample sets, both frequencies and individual genotypes, can be found at The Allele Frequency Net Database website (www.allelefrequencies.netwww. allelefrequencies.net) [11]. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.humimm.2019.06.008. References [1] Instituto Nacional de Estadística y Geografía (INEGI), Conociendo Nayarit, 2013. Available from: http://internet.contenidos.inegi.org.mx/contenidos/productos/ prod_serv/contenidos/espanol/bvinegi/productos/estudios/conociendo/NAYARIT. pdf. [2] 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). [3] 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. [4] 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, Vol. II, Mesoamerica, Cambridge University Press, Cambridge, 2008, pp. 136–186. [5] E. Williams, The stone sculpture of ancient West Mexico: description and interpretation, Ancient Mesoamerica 2 (1991) 181–192. [6] 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). [7] 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. [8] R. Lisker, V. Babinsky, Admixture estimates in nine Mexican Indian groups and five East Coast localities, Rev. Invest. Clin. 38 (1986) 145–149. [9] G. Aguirre Beltrán, The slave trade in Mexico, Hispanic Am. Hist. Rev. 24 (1944) 412–431. [10] B.Z. González-Sobrino, A.P. Pintado-Cortina, L. Sebastián-Medina, F. MoralesMandujano, A.V. Contreras, Y.E. Aguilar, et al., Genetic diversity and differentiation in urban and indigenous populations of Mexico: patterns of mitochondrial DNA and Y-chromosome lineages, Biodemogr. Social Biol. 62 (2016) 53–72, https://doi.org/ 10.1080/19485565.2015.1117938. [11] 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. [12] Google, Google Earth Pro ©, (2019). earth.google.com.
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Contents lists available at ScienceDirect
Human Immunology journal homepage: www.elsevier.com/locate/humimm
Genetic diversity of HLA system in two populations from Nayarit, Mexico: Tepic and rural Nayarit Isis Goné-Vázqueza,1, Rodrigo Barquerab,c, ,1, Francia Paulina Arellano-Pradod,1, Diana Iraíz Hernández-Zaragozab,e,1, Araceli Escobedo-Ruíza,1, Stephen Claytonc,1, Esteban Arrieta-Bolañosf,1, Víctor Eduardo García-Ariasd, Marla Estefanía Rodríguez-Lópezd, Alicia Bravo-Acevedog, 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
Histocompatibility Laboratory, Hospital de Especialidades, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico b Molecular Genetics Laboratory, Escuela Nacional de Antropología e Historia (ENAH), Mexico City, Mexico c Department of Archaeogenetics, Max Planck Institute for the Science of Human History (MPI-SHH), Jena, Germany d Pediatrics Hospital, Centro Médico Nacional de Occidente (CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, Mexico e Immunogenetics Unit, Técnicas Genéticas Aplicadas a la Clínica (TGAC), Mexico City, Mexico f Institute for Experimental Cellular Therapy, University Hospital Essen, Essen, Germany g Blood Bank, UMAE Hospital de Gineco Obstetricia No. 4 “Luis Castelazo Ayala”, Instituto Mexicano del Seguro Social (IMSS), 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
ARTICLE INFO
ABSTRACT
Keywords: HLA Immunogenetics Population genetics Nayarit Admixture
We studied HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) alleles by PCR-SSP based typing in 161 Mexicans from the state of Nayarit living in Tepic (N = 97) and rural communities (N = 64), to obtain information regarding allelic and haplotypic frequencies. We find that the ten most frequent haplotypes found in the state of Nayarit include eight Native American and two European haplotypes. Admixture estimates revealed that the main genetic components in the state of Nayarit are Native American (50.79 ± 5.03% by ML; 42.24% of Native American haplotypes) and European (37.04 ± 6.21% by ML; 35.72% of European haplotypes), while African genetic component is less apparent but relatively high (12.17 ± 2.50% by ML; 13.36% of African haplotypes).
The state of Nayarit is located in the west of the country, bounded on the north by Sinaloa and Durango, on the east by Zacatecas, on the
east and south by Jalisco and on the west by the Pacific Ocean, where it also has the islands of Islas Marías, Isla Isabel, the Tres Marietas islands
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. Bekker-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.2019.06.008 Received 2 June 2019; Accepted 6 June 2019 0198-8859/ © 2019 American Society for Histocompatibility and Immunogenetics. Published by Elsevier Inc. All rights reserved.
Please cite this article as: Isis Goné-Vázquez, et al., Human Immunology, https://doi.org/10.1016/j.humimm.2019.06.008
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and Farallón La Peña. With 1 181 050 inhabitants by 2015, it is the fourth least populated state; with 27 815 km2, the ninth least extensive; and with 39.01 inhabitants/km2, the ninth least densely populated. It was founded on January 26, 1917, is divided into 20 municipalities and its capital city is Tepic. In Nayarit there are 52 833 people who spoke an indigenous language, according to INEGI on 2013, the five indigenous languages more commonly spoken are Huichol (47.6%), Cora (39.4%), Tepehuano (3.7%), Nahuatl (3.6%) and Zapotec (0.9%) [1]. It should be noted that the Huichol ethnic group has displaced the Cora, which had the highest demographic weight in Nayarit until before 1995. The main ethnic groups that registered the census of the year 2000 in the state are the Huicholes (16 932 people), the Coras (15 389) and the Tepehuanos (1422); Nahuatl (1422) has initiated an increase caused by immigration from the state of Guerrero and other entities in the center of the country [2]. For the important archaeological site of Ixtlan del Rio, several periods have been described, an Early Period that was aligned with Early Chametla, a Middle Period comparable to Late Chametla 2 and Early Culiacan 2 (Aztatlan complex) and a Late Period, which is related to Late Culiacan and the Autlan Complex. Early Ixtlan is Classic Period, and Middle and Late Ixtlan are Postclassic. A large dense population, the presence of markets and trade in maize and chile can be inferred [3] from conquest period data. The cultural transition zone between semior non-sedentary and settled farming peoples very roughly bisected the Center-West from southeast to northwest, corresponding respectively to the geographic and climatic division between the formidable mountains of upland Nayarit, arid high steppes of central Zacatecas, Bajío plains to the north, the narrow mid-Pacific coastal plain to the west, and neovolcanic lacustrine basins and Michoacán highlands to the south. Coastal Nayarit, on the other hand, was occupied by peoples of Totorame speech (related to Cora) from around the Tropic of Cancer south to about the latitude of present-day Tepic, while Coras, Tecuales, Huicholes, and Tepehuanes held the uplands. These peoples were parttime farmers living in dispersed settlements, but their populations reached fairly high densities [4]. Stone sculpture traditions started showing around 700 CE. The small scale and relative simplicity of these sculptures suggest they were central pieces of village or domestic cults, rather than large public worshipping like those seen in the larger urban centers of central Mesoamerica [5]. Only by the end of the 16th century did the native inhabitants of the eastern Nayarit sierra, southwestern Zacatecas, and the cañones area of Nueva Galicia come under some degree of stable Spanish control. It was not until 1721 that the Cora chieftain met with the viceroy in Mexico City [4]. While the Franciscans missionized the Huicholes, modern Cora culture took definitive shape in the eighteenth century when the Jesuits
concentrated the Indians in their most important population centers. Many Huicholes of the Nayarit sierra at first adhered to the insurgent cause, but later they switched their loyalties to the loyalist side after 1815 in a complex ploy to pursue local indigenous interests. By the time the independence was practically achieved, the Franciscan missionaries left the area. By the mid-nineteenth century many Huichol villages consisted of clusters of huts gathered around abandoned churches, and were held together by simple political structures and subsistence agriculture, tending to remain isolated from Hispanic society except for essential commercial contacts. However, during the first years of the 20th century, privately owned estates were assembled, land concentration reached extreme indices, and by the first third of the 20th century foreigners owned > 50% of the rural areas of the state of Nayarit [4]. The study of population immunogenetics of human groups from Nayarit adds to the growing knowledge on the population genetics of Western Mexico. For the present work, we analyzed HLA class I (HLA-A, -B) and class II (HLA-DRB1, -DQB1) PCR-SSP based typings in 161 Mexicans from the state of Nayarit [composed by the following populations: Mexico Nayarit, Tepic, N = 97, Allele Frequencies Net Database Identifier (AFND-ID): 3508; Mexico Nayarit Rural, N = 64, AFND-ID: 3578]. 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 [6] 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 Nayarit please refer to the Supplementary Information: Supplementary Tables 1–7. For data on Hardy-Weinberg equilibrium (HWE) please see Supplementary Information: Supplementary Table 8 of this work and Supplementary Information: Supplementary Table 9 in [6] in this same issue. We find that the most frequent haplotypes for the state (haplotypic frequency, H.F. ≥1.0%, arbitrarily; Supplementary Table 5) include eight Native American most probable ancestry (MPA) (HLA ∼ A*24 ∼ B*40:02 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*35 ∼ DRB1*08 ∼ DQB1*04, A*68 ∼ B*48 ∼ DRB1*04 ∼ DQB1*03:02, A *24 ∼ B*39 ∼ DRB1*14 ∼ DQB1*03:01, A*24 ∼ B*35 ∼ DRB1* 16 ∼ DQB1*03:01, A*68 ∼ B*40:02 ∼ DRB1*04 ∼ DQB1*03:02, A*02 ∼ B*39 ∼ DRB1*04 ∼ DQB1*03:02 and A*02 ∼ B*35 ∼ DRB1 *04 ∼ DQB1*03:02) and two European MPA haplotypes (A*30 ∼ B*18 ∼ DRB1*03:01 ∼ DQB1*02 and A*02 ∼ B*08 ∼ DRB1 *03:01 ∼ DQB1*02). Admixture estimates (Fig. 1) revealed that the main genetic components in the state of Nayarit are Native American Fig. 1. Geographic situation of Nayarit and admixture proportions for the state of Nayarit [composed by the following populations: Mexico Nayarit, Tepic, N = 97, Allele Frequencies Net Database Identifier (AFND-ID): 3508; Mexico Nayarit Rural, N = 64, AFND-ID: 3578]. Admixture proportions were estimated by ML 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 [12].
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(50.79 ± 5.03% by the maximum likelihood method and 42.24% by estimating the proportion of Native American haplotypes) and European (37.04 ± 6.21% by the maximum likelihood method and 35.72% by estimating the proportion of European haplotypes), while African genetic component is less apparent (12.17 ± 2.50% by the maximum likelihood method and 13.36% by estimating the proportion of African haplotypes). Interestingly, the rural areas of Nayarit have almost twice as much the proportion of African contribution (16.43% ± 6.28% by the maximum likelihood method and 16.41% by estimating the proportion of African haplotypes) as the city of Tepic (9.49% ± 0.90% by the maximum likelihood method and 11.34% by estimating the proportion of African haplotypes). These estimations slightly differ from previous reports for the state of Nayarit in which European component was estimated to be 38.0%, Native American estimated at 56.7% and African component was calculated to be 5.3% using 13 CODIS-short tandem repeats (CODIS-STRs) [7]. When classical markers (i.e. blood groups) were used as genetic estimators in a sample from La Mesa, Nayarit, the proportions of each component were distributed as follows: Native American 79.2%, European 20.0% and African 0.8% [8]. The differences between the estimation of the African component could be due to differences in the admixture estimation methods (three loci of HLA vs. STRs vs. blood groups) 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 [6] in this issue). The New Kingdom of Galicia had, by the end of the 16th century, the third most important population of Africans and the fourth one of Mulattoes [9]. Nayarit was part of that administrative unit, which can partially explain that Nayarit has one of the highest contributions of African ancestry of all states studied in Mexico [6]. The admixture proportions for Tepic and the rural areas of the state don’t show any major shifts to what we found at the state level referring to European and Native American ancestral components (Fig. 1). In concordance with previous reports [10], we found a higher prevalence of African genetic components in the rural areas when compared to urban settlements. We could detect the presence of 6.52% of Asian haplotypes and 2.17% of mixed ancestry haplotypes for the state of Nayarit, with similar proportions both in Tepic (7.22% and 1.55%, respectively) and the rural areas of the state (5.47% and 3.13%, respectively). The admixture estimates and the presence of Native American, European and Asian haplotypes can be explained by the aforementioned historical events that shaped the demographic traits of the
present day state of Nayarit. All data from our sample sets, both frequencies and individual genotypes, can be found at The Allele Frequency Net Database website (www.allelefrequencies.netwww. allelefrequencies.net) [11]. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.humimm.2019.06.008. References [1] Instituto Nacional de Estadística y Geografía (INEGI), Conociendo Nayarit, 2013. Available from: http://internet.contenidos.inegi.org.mx/contenidos/productos/ prod_serv/contenidos/espanol/bvinegi/productos/estudios/conociendo/NAYARIT. pdf. [2] 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). [3] 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. [4] 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, Vol. II, Mesoamerica, Cambridge University Press, Cambridge, 2008, pp. 136–186. [5] E. Williams, The stone sculpture of ancient West Mexico: description and interpretation, Ancient Mesoamerica 2 (1991) 181–192. [6] 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). [7] 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. [8] R. Lisker, V. Babinsky, Admixture estimates in nine Mexican Indian groups and five East Coast localities, Rev. Invest. Clin. 38 (1986) 145–149. [9] G. Aguirre Beltrán, The slave trade in Mexico, Hispanic Am. Hist. Rev. 24 (1944) 412–431. [10] B.Z. González-Sobrino, A.P. Pintado-Cortina, L. Sebastián-Medina, F. MoralesMandujano, A.V. Contreras, Y.E. Aguilar, et al., Genetic diversity and differentiation in urban and indigenous populations of Mexico: patterns of mitochondrial DNA and Y-chromosome lineages, Biodemogr. Social Biol. 62 (2016) 53–72, https://doi.org/ 10.1080/19485565.2015.1117938. [11] 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. [12] Google, Google Earth Pro ©, (2019). earth.google.com.
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