TRANSPLANTED MALE GENOMES IN THREE VENEZUELAN POPULATIONS

Dinorah Castro de Guerra, Esteban Arroyo, Francisco Mauro Salzano and Maria Cátira Bortolini

Dinorah Castro de Guerra. M.Sc and Ph.Sc., Instituto Venezolano de Investigaciones Científicas (IVIC). Associate Researcher, Laboratory of Human Genetics, Centro de Medicina Experimental IVIC. Address: IVIC, Apartado 21827, Caracas 1020A, Venezuela. e-mail: dcastro@ivic.ve

Esteban Arroyo. Anthropologist, Universidad Central de Venezuela (UCV). Assistant Student, Laboratory of Human Genetics IVIC. e-mail: earroyo@ivic.ve

Francisco Mauro Salzano. Ph.D., Universidade de São Paulo. Emeritus Professor, Departament of Genetics, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Brazil. e-mail: francisco.salzano@ufrgs.br

Maria Cátira Bortolini. Ph.D., UFRGS. Associate Professor, Departament of Genetics, UFRGS, Porto Alegre, Brazil. e-mail: maria.bortolini@ufrgs.br

Resumen

Las migraciones desde las Islas Canarias a Venezuela han sido constantes desde la época colonial, presentando algunas regiones del país una importante influencia de ese origen. Algunos estudios han demostrado el mantenimiento de las características genéticas fundadoras en tres poblaciones semi-aisladas de la región nor-central de Venezuela. Este trabajo reporta sobre el origen del cromosoma Y en esas poblaciones, a través del análisis de cuatro marcadores bi-alélicos y tres microsatélites ubicados en su región no recombinante. Los haplogrupos Q-M3 y E-M2 , no están en esas poblaciones reflejando el origen predominantemente europeo de sus fundadores. El uso combinado de los polimorfismos bi-alélicos y los microsatélites corrobora este postulado; además, el cromosoma YAP detectado en dos de esas poblaciones está asociado con el alelo 13 del locus DYS19 el cual presenta las mas elevadas frecuencias en los Beréberes del norte de África, revelando la importancia de los hombres Beréberes en la formación de población canaria y/o la introducción de cromosomas Y Beréberes en el sur-este de España durante los siete siglos de dominación musulmana. El origen predominantemente europeo de los cromosomas Y ha sido reportado en otras áreas de América, sugiriendo que el reemplazo del cúmulo de genes aborígenes masculinos parece representar la tendencia general en el proceso de conquista y colonización del Nuevo Mundo. Tomando en consideración la clasificación propuesta por Darcy Ribeiro, nosotros proponemos la expresión genomas masculinos transplantados que refiere a la sustitución de los cromosomas Y nativos en Sur América.

Summary

Migration from the Canary Islands to Venezuela has been continuous since Colonial times, some regions of the country presenting an important Canarian influence. Earlier studies demonstrated the maintenance of the original Canarian gene pool in three north-central semi-isolated Venezuelan populations. The present study investigates the origin of the Y-chromosomes in these populations, through the analysis of four biallelic markers and three microsatellite loci located at its nonrecombining region. Haplogroups Q-M3 and E-M2 do not occur in these populations, reflecting the predominantly European origin of their male founders. The combined use of biallelic and microsatellite polymorphisms corroborated this postulation; moreover, the YAP chromosomes detected in two of these Venezuelan populations was associated with allele 13 at the DYS19 locus, which occurs with highest frequencies in Berbers from North Africa, revealing the importance of Berber males in the formation of the Canarian population and/or Berber Y-chromosome introgression during the seven centuries of the Muslim domination of Southern Spain. The predominantly European origin of the Y-chromosome had also been reported for other areas of the Americas, suggesting that the replacement of the aboriginal male background seems to represent a general trend in the process of Conquest and Colonization of the New World. Therefore, and taking into consideration the classification of the American peoples proposed by Darcy Ribeiro, we coined the expression transplanted male genome for the substitution of Native Y-chromosomes in South America.

Resumo

Movimentos migratórias das Ilhas Canárias para a Venezuela têm sido constantes desde os tempos coloniais, resultando que em algumas regiões deste país Sul-americano há considerável influência Canária. Anteriormente, nós conduzimos alguns estudos que demonstraram a manutenção de um pool gênico canário original em três populações Venezuelanas semi-isoladas localizadas na região centro-norte do país. Aqui, nós investigamos a origem dos cromossomos Y nestas mesmas três populações através do estudo de quatro marcadores bialélicos e três locos de microsatélites localizados na região não recombinante do cromossomo Y. Haplogrupos Q-M3 e E-M2 não foram detectados, refletindo a origem européia dos homens que fundaram estas populações. Analises combinadas utilizando os locos bialélicos juntamente com os microsatélites corroborou este achado. Cromossomos YAP detectados em duas destas populações venezuelanas mostraram estar associados com o alelo 13 do loco DYS19, sendo que esta composição apresenta suas mais altas freqüências entre os Berberes do norte da África. Este fato revela a importância dos homens Berberes na formação da população contemporânea das Ilhas Canárias e/ou a introgressão destes cromossomos no sul da Espanha durante a ocupação muçulmana da Península Ibérica.

A predominância de cromossomos Y de origem européia, juntamente com a substituição do background nativo, tem também sido reportada em outras áreas do continente, sugerindo que esta é uma tendência generalizada no processo de conquista e colonização do Novo Mundo. Assim, e levando-se em consideração a classificação dos povos proposto por Darcy Ribeiro (Ribeiro, 1970), nós cunhamos a expressão "genoma masculino transplantado" para o fenômeno da substituição dos cromossomos Y nativos americanos que ocorreu na América do Sul.

Keywords / Venezuelan Population / Y-chromosome / Haplotypes / Haplogroups / Transplanted Male Genomes /

Received: 11/08/2002. Modified: 03/24/2003. Accepted: 03/27/2003

Since the Conquest and Colonization of the New World, Native American history has been strongly influenced by important migrations from Europe and Africa. The arrival of immigrants led to the establishment of a rapidly growing admixed population and a concomitant decline in the Amerind groups (Salzano and Bortolini, 2002). Among the Spaniard migrants, those from the Canary Islands have arrived continuously to Venezuela since the Colonial period, some Venezuelan regions having a well-known Canarian influence (Castillo Lara, 1980; Cunill Grau, 1987; Lynch, 1987). Cultural aspects of this influence have been reported (Báez Gutiérrez, 1995, Rodríguez, 1995), but little is known about their biological contribution. Recently published studies have demonstrated the maintenance of the original Canarian gene pool in three semi-isolated Venezuelan populations: San Antonio de Los Altos, San Diego de Los Altos and Hoyo de La Cumbre. Using classical genetic polymorphisms Castro de Guerra and Zambrano (2000) found that the European genetic contribution is majoritarian, with values ranging from 78% (San Diego) to 92% (Hoyo de La Cumbre). On the other hand, genetic distance analyses suggested that this component is mainly of Canarian origin in Hoyo de La Cumbre and San Antonio, whereas in San Diego other European influences should also be considered.

Some aspects of the gender-specific gene flow from the Canary Islands to these three Canarian-derived populations were also evaluated considering the DYS19 locus (Castro de Guerra et al., 2001). The results suggested that the Canarian male contribution ranged from 73% in San Diego to 100% in Hoyo de La Cumbre. The proportion of non European Y-chromosomes in San Antonio and San Diego is difficult to support historically and could be related to the known homoplasy associated to the DYS19 locus, which leads to sharing of alleles just by recurrent mutations, not by descent (Kniff et al., 1997).

The paternally inherited nonrecombining portion of the Y chromosome (NRY) includes polymorphisms that mutate relatively frequently (microsatellites, like the DYS19 locus) and biallelic polymorphisms (the YAP Alu insert and single nucleotide substitutions) that are unlikely to have arisen more than once in human evolution (Thomas et al., 2000, Underhill et al., 2001). In recent years, the power of the combination of these two sets of NRY polymorphisms in resolving evolutionary histories of human populations has been recognized (Carvajal-Carmona et al., 2000; Mesa et al., 2000; Thomas et al., 2000; Bortolini et al., 2002, 2003; Lell et al., 2002). To obtain more precise information about the origin of the Y-chromosomes in the three above-indicated Canarian-derived populations, four biallelic and three microsatellite loci located in that region were investigated. The results were also compared with those reported in the literature, considering their potential parental groups, as well as other Latin American populations.

Subjects and Methods

Samples were collected from 53 individuals living in three small and semi-isolated Venezuelan populations localized in the north-central region, near Caracas. Two of them (San Antonio de Los Altos and Hoyo de La Cumbre) were founded by Spanish-Canarian families at the end of the seventeenth and nineteenth centuries respectively. Previous investigations revealed that both communities have an important degree of isolation and endogamy (Villarroel, 1994; Castro de Guerra and Zambrano, 1997). San Diego de Los Altos, geographically near San Antonio, was an "encomienda town" in early times, a basically Native American settlement established by Spaniards for religious instruction. However, it also had inhabitants commonly identified as White, who came mainly from San Antonio de Los Altos and the Canary Islands, as well as a small population of African origin (initially slaves). The isolation of this population had been lower than that of the others (Chacón, 1980; Castro de Guerra and Zambrano, 1996).

DNA of 21 samples from San Antonio, 19 from Hoyo de La Cumbre, and 13 from San Diego, were isolated from 3ml of whole blood using the Debomoy and Nurnberger (1991) procedure.

Haplogroups were defined through four bi-allelic markers that were typed as reported in the following references: YAP or DYS287, Hammer and Horai (1995); sY81 or DYS271, Seielstad et al. (1994); 92R7, Hurles et al. (1999); and DYS199, Underhill et al. (1996). Additionally, three microsatellite loci were examined: DYS19, as reported by Castro de Guerra et al. (2001), while DYS390 and DYS393 were amplified using primers and conditions reported by Kayser et al. (1997). PCR products were loaded in 8% polyacrilamide/0.4 bisacrylamide gels in TBE buffer (50mM tris borate/EDTA 10mM, pH 8.3) and submitted to polyacrylamide gel electrophoresis (PAGE). The gel was visualized by silver-staining and fragments were identified according to previously identified allelic patterns (Ruíz-Linares et al., 1999; Bortolini et al., 2002). Following common usage, we refer to microsatellite lineages as haplotypes to distinguish them from biallelic haplogroups, which were defined according to the nomenclature established by the Y-Chromosome Consortium (http://ycc.biosci.arizona.edu/nomenclature_system/ frontpage.html).

The ARLEQUIN program (Schneider et al., 2000) was used to estimate allele and haplotype frequencies, gene diversity indices, and pairwise FST genetic distances. Admixture values were obtained using the least squares method and ADMIX computer program (Long, 1991).

Results and Discussion

The haplogroup frequencies identified in the three Venezuelan Canarian-derived populations and in their potential parental groups, as well as in two other Latin American populations, are shown in Table I. Overall, the haplogroup frequencies in Venezuelans are closer to those seen in Gran Canaria and Spain. E-M2 and Q-M3, which are unequivocally Sub-Saharan African and Amerindian markers, respectively, were not observed in the three Venezuelan communities. YAP, present in West Africa (25%), Spain (5%), and which has its highest distribution in Berbers (83%), is absent in San Diego, but was present in low (5%) and moderate frequencies (19%) in Hoyo de La Cumbre and San Antonio, respectively.

The haplogroup analysis also reveals a major genetic similarity between San Antonio and San Diego, and between these two populations and Gran Canaria and Spain, whereas Hoyo de La Cumbre shows a different distribution. This difference is mainly represented by the high frequency of Null (ancestral alleles for 92R7, DYS287, DYS271 and DYS199) and may be explained by a founder effect or genetic drift, since this population is the smallest and most isolated of the three.

Table II shows the genetic distances between these Venezuelan populations and the others, based on the above-indicated haplogroup distributions. Considering the potential parental populations, the smallest distances were observed in relation to Gran Canaria and Spain, with the exception of Hoyo de La Cumbre, which has a significant difference with these two populations. High similarity was observed with the previously tested Colombian and Brazilian mixed populations. Among Venezuelans, the smallest distance is between San Antonio and San Diego, and the highest between San Diego and Hoyo de La Cumbre, but the last number is not significantly different from zero.

Admixture estimations based on the haplogroup frequencies (Table III) suggest that the Y-chromosomes of these Venezuelan populations have an exclusively Canarian and/or Spaniard origin, while the autosome markers indicate some Amerindian and African ancestry (Castro de Guerra and Zambrano, 2000).

To refine the assessment of Y-chromosome origins in the three Venezuelan populations, the microsatellite haplotypes obtained were grouped considering simultaneously the biallelic data (Table IV). An important proportion of the haplotypes observed in Gran Canaria and Spain, 76% and 78% respectively, is present in at least one of the Venezuelan populations. Haplotype 1, the most commonly detected in Hoyo de La Cumbre and San Antonio, is also the most frequent in Gran Canaria and Spain. In San Diego, the most frequent haplotype (4) differs by just one mutational step from haplotype 1. This haplotype is also frequent in San Antonio, but it is absent or has a low frequency in the other populations. Considering haplotype 1 and its one-step derivatives (2, 3, 4, 5, 6 and 7) as a modal cluster, it can be seen that it represents more than half of the chromosomes in all populations, except for Berbers. The most frequent (47%) haplotype in Berbers (24; alleles 13, 24 and 13 for DYS19, DYS390, and DYS393, respectively), occurs in low frequency (9%) in San Antonio only. These results allow to discard an Amerindian origin for the DYS19-13 allele, as well as a Sub-Saharan Africa origin for the YAP chromosomes in these Venezuelans. In Amerindians DYS19-13 allele is associated with Q-M3 chromosomes, while in Sub-Saharan Africans they are associated to alleles with 15 or more repeats (Ruíz-Linares et al., 1999; Bravi et al., 2000). However, rather than any direct migration from North Africa to America, these data reveal the importance of the Berber male contribution to the formation of the Canarian population and/or of Berber Y-chromosome introgression between the VII and XV centuries, during the Muslim occupation of the Iberian Peninsula (Bortolini et al., 2003). Table IV shows that about 5% and 15% of haplotypes associated with P-M45 in San Antonio and San Diego, respectively, and 15% and 16% of haplotypes identified with the Null haplogroup in San Diego and Hoyo de La Cumbre, respectively, are not shared with Spain, Gran Canaria and/or Berber populations. A distinct European and/or a low Sub-Saharan African male influence can be suggested to explain these findings.

The results presented, as a whole, suggest that the Sub-Saharan African and Amerind contributions to the three Venezuelan populations considered seem to have been introduced mainly by females, although of course, the introduction of non-Y alleles through the males cannot be excluded.

The predominantly European origin of Y-chromosomes has also been reported for other areas of America, like Antioquia in Colombia (Carvajal- Carmona et al., 2000), Northern Chile (Rocco et al., 2002) and Brazil in general (Carvalho-Silva et al., 2001), although regional differences occur due to the different processes of conquest carried out by the Spaniards and Portuguese.

In many American countries or in areas within them, populations were subjected to the phenomena of replacement of their cultural or morphological traits by European characteristics. They were named by Ribeiro (1970) as transplanted peoples. Here it is proposed that the substitution of their Y-chromosomes be characterized as cases of transplanted male genomes.

ACKNOWLEDGMENTS

The authors thank the members of the populations that agreed to participate in this study. This research was supported by Venezuela´s CONICIT (Grant S1-95000717), while the investigations in Brazil are supported by PRONEX (Programa de Apoio a Núcleos de Excelência), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul), and PROPESQ/UFRGS (Pró-Reitoria de Pesquisa da Universidade Federal do Rio Grande do Sul).

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