ARTÍCULO ORIGINAL

doi: http://dx.doi.org/10.7705/biomedica.v33i3.807

¹ Departamento de Patología, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, D.C., Colombia

² Instituto de Genética, Universidad Nacional de Colombia, Bogotá, D.C., Colombia

³ Servicios Médicos Yunis Turbay y Cía., Bogotá, D.C., Colombia

⁴ Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, D.C., Colombia

Contribución de los autores:

Juan J. Yunis dirigió el proyecto.

Emilio J. Yunis codirigió el proyecto.

Juan J. Yunis, Luis E. Acevedo y David S. Campo: aislamiento ADN y PCR.

Todos los autores participaron en el análisis de resultados y en la escritura del artículo.

Recibido: 31/12/12; aceptado:08/05/13

Introduction: Y chromosome STR haplotypes have been widely used in population studies to establish the origin of diverse populations.

Objective: We analyzed Y chromosome STR haplotypes (8 loci) in 134 Caucasian-mestizo and 137 African-descent Colombian unrelated individuals to correlate the geographical origin with historical data as well as the genetic relationships and possible admixture patterns.

Materials and methods: One hundred samples of African descent and 137 Caucasian-mestizo samples analyzed for Y chromosome STR haplotypes by PCR followed by acrylamide electrophoresis.

Results: No evidence of population substructure was found for the African descent. Two point fifty nine per cent of the haplotypes were shared between the two groups with the possible existence of Caucasian gene flow towards Afro-descendants.

Conclusion: The Caucasian-Mestizo Colombian population is grouped with other populations of the Iberian Peninsula and Europe, while the Afro-Colombian population is grouped with other African populations reported. Key words: Haplotypes, Y chromosome, genetics, Colombia.

doi: http://dx.doi.org/10.7705/biomedica.v33i3.807

Origen geno-geográfico de haplotipos STR del cromosoma Y en una muestra caucásico-mestiza y afrodescendiente de Colombia

Introducción. Los haplotipos STR de cromosoma Y han sido ampliamente utilizados en estudios de poblaciones para establecer el origen de diversas poblaciones.

Objetivo. Se analizaron haplotipos STR del cromosoma Y (8 loci ) en 134 afrodescendientes y caucásico-mestizos no relacionados de Colombia, para correlacionar el origen geográfico con los datos históricos, así como las relaciones genéticas y posibles patrones de mezcla.

Materiales y métodos. Se analizaron los haplotipos STR del cromosoma Y mediante PCR seguidas de electroforesis en acrilamida, de 134 muestras de afrodescendientes y 137 muestras de caucásicos mestizos.

Resultados. No se encontró evidencia de subestructuración de la población afrodescendiente. El 2,59 % de los haplotipos eran compartidos en los dos grupos analizados, con la posible existencia de flujo génico de caucásico-mestizos hacia los afrodescendientes.

Conclusión. La población caucásico-mestiza colombiana se agrupa con otras poblaciones de la península Ibérica y Europa, mientras que la población afrodescendiente colombiana se agrupa con otras poblaciones africanas reportadas.

Palabras clave: haplotipos, cromosoma Y, genética, Colombia.

doi: http://dx.doi.org/10.7705/biomedica.v33i3.807

In recent years, the analysis of Y chromosome polymorphisms has become an important tool for anthropological studies as well as in regular forensic casework (1-6). A set of 8 Y-chromosome specific Short Tandem Repeats found in the nonrecombinant portion of the Y chromosome –the tetranucleotide STR DYS19, DYS385, DYS389-I, DYS389-II, DYS390, DYS391 and DYS393 and the trinucleotide DYS392– conforms the minimal haplotype for forensic casework (7). Several populations from Europe, Asia and the United States have been typed for the Y chromosome minimal haplotype and their haplotype frequencies have been reported to the Y chromosome reference database (YHRD) (8-17). In South America, several non-Amerindian origin populations have been analyzed for the minimal Y-STR haplotype; among them, the population from Buenos Aires, Argentina (15), a population from Medellin (18), another from Valle del Cauca (19), and those reported by us (20). Additional studies have been carried out with the newest platforms (YFiler® Applied Biosystems Palo Alto, CA; PowerPlex Y® and PowerPlex Y23® Promega Corporation, Madison, WI) in some Colombian populations (21-25). Most of these studies have focused their attention on non-Amerindian admixed populations (Mestizo populations)(21-24, 26). None of the studies were carried out in regions with strong presence of African descendant populations, selected unmixed African descendant individuals for analysis (21, 23, 26).Other studies have not analyzed the Y chromosome minimal STR haplotype (27). Due to different genetic background, migrations, culture and admixture processes, additional studies are required to better understand the genetic composition within different regions of each country and between different countries within a continent.

In Colombia, the majority of the population is considered Caucasian-Mestizo, composed mainly of Spanish descent and, in a minor degree, of other European, Arab and Jewish populations. The African descent population is located mainly in the Pacific coast, Caribbean coast and islands. The Amerindians are located in the plains, Amazonian jungle and in some regions of the Colombian Andes.

However, different degrees of admixture have been found in different regions based on blood group analysis (28). In the Pacific and Caribbean coast different degrees of admixture between African descent and Caucasian-Mestizos is present. On the other side, Amerindian admixture is stronger in the southwest and decreases towards the north section of the Andes were the Caucasian component is stronger.

In the present study, we have analyzed the Y-chromosome haplotype data from 271 unrelated individuals, 134 of African descent and 137 Caucasian-Mestizos of Colombia in order to determine the Y chromosome haplotype origin of the two population groups tested. Additional analysis were carried out in order to determine the degree of genetic admixture between these groups and Amerindian populations of Colombia studied by us (unpublished results) and to correlate our findings with previously defined populations of Europe and North America.

Material and methods

One hundred and thirty four (134) unrelated individuals of African descent were collected between 1994-1995, after proper informed consent was obtained, in four different towns (Quibdo n=40, the state capital; Condoto n=34; Istmina n=30; and Tado n=30) of the Choco department in the Pacific region of Colombia. This was part of a research project at the Universidad Nacional de Colombia with the objective to characterize genetically different ethnic groups. In addition, a total of 177 Caucasian-Mestizo individuals from the East-central Andean Region of Colombia (Cundinamarca, n=40, Boyacá,n=40, and Santander, n=40, departments, as well as Bogotá, n=50, the capital city) divided as 45 alleged father/son pairs with known exclusion of paternity, 40 alleged father/son pairs with proven paternity (minimum of 12 STRs and W>99.99%), and 7 unrelated individuals were analyzed, for a total of 137 unrelated Caucasian-Mestizo individuals were provided by Servicios Médicos Yunis Turbay y Cía., after proper informed consent was obtained in order to establish Y STR haplotype frequencies, that could be used for forensic estimations by many laboratories in Colombia and abroad. Generally, a sample size between 120-150 individuals is considered an adequate sample size for forensic frequency estimations.

Whole blood was obtained from all individuals to participate in genetic populations studies. Genomic DNA was extracted by the Quick light DNA isolation kit (Lifecodes Corporation) following manufacturers recommendations or by Chelex 100 as described previously (20,29).

PCR amplification and typing

The tetranucleotide STR DYS19, DYS385, DYS389-I, DYS389-II, DYS390, DYS391 and DYS393 and the trinucleotide DYS392 were analyzed as follow: Primers sequences for DYS19, DYS390, DYS391 and DYS392 were those described previously (3-5). PCR amplifications were carried out as single loci for DYS19, and DYS392 with identical conditions as described (3). A multiplex reaction was performed for DYS390, DYS391 and DYS393 as follow: initial denaturation at 94 °C, for 3 minutes; 5 cycles of 94 o C for 15 seconds, 58 o C for 20 sec., 72 o C for 20 sec., followed by 30 cycles of 94 o C for 15 sec.; 54 o C 20 sec.; 72 o C for 20 sec. For DYS389-I and DYS389-II, Fluorescent labeled primers (FITC) and amplification conditions were identical as previously described (6). For DYS385, Fluorescent labeled primers (TMR) and amplification conditions were identical as described by Schneider et al . (30).

The PCR products were resolved in 4% Acrylamide/bis-acrylamide denaturing gels for DYS19, DYS390, DYS391, DYS392 and DYS393 with silver nitrate staining. For DYS389 and DYS385, typing was carried out in 4% Acrylamide/bis-acrylamide denaturing gels and analyzed in a Hitachi FMBIO II with Internal Lane Standards (CXR 400, Promega Corporation, Madison, WI).

Allele designations were made according to the reference tables with the aid of sequenced allelic ladders provided by Dr. Ángel Carracedo, Instituto de Medicina Legal, Universidad de Santiago de Compostela (Galicia, Spain), and Dr. Daniel Corach, Servicio de Huellas Digitales Genéticas, Universidad de Buenos Aires, (Buenos Aires, Argentina) and from reference samples provided by Dr. Lutz Roewer, Institute of Legal Medicine, Medical Faculty (Charité), Humboldt-University (Berlin, Germany). Proficiency testing for these STRs has been carried out for ystr.charite.de; GEPISFG WG; Collaborative Testing Service (CTS, Sterling, VA); and Sociedad Argentina de Genética Forense (SAGF).

Data analysis

Haplotype and allele frequencies, as well as haplotype diversity, based on eight-locus Y-STR haplotypes were determined with the aid of ARLEQUIN (31). The haplotype frequencies and other parameters of forensic interest have been published earlier (20).

The genetic structure among the African descent population was analyzed considering the molecular difference between individual haplotypes (AMOVA), in addition to differences in haplotype frequencies, resulting in estimates of F st (or R st ), an F st analogue (excluding DYS385) (30). Significance levels of the genetic-variance components as well as F st values were estimated by using 100,000 permutations.

Haplotype sharing between the Caucasian-Mestizo and African descent individuals from Colombia was determined in order to obtain an approximation to the degree of admixture between these groups. For this purpose, numbers of shared haplotypes between the Caucasian-Mestizo and African descent populations of Colombia were determined for each of the haplotypes identified.

Genetic distances (Da) were calculated according to Nei (32) with Populations (Populations Version 1.2.23. Software. http://www.cnrs-gif.fr/pge). A Multi- Dimensional Scaling (MDS) analysis (excluding DYS385) was carried out with the genetic distance matrix obtained previously with the aid of the Statistica for Windows (StatSoft, Inc. Tulsa, Ok). This analysis was carried out for the Caucasian-Mestizo and the African descent (as a whole) populations of Colombia and those previously described by others (33-36); as well as for 698 African descent individuals and 225 individuals from Medellin, Colombia reported in ystr.org. In addition, 254 unrelated individuals belonging to 20 Amerindian tribes of Colombia (Yunis J.J, Campo D.S., Camelo, Z., Acevedo, L., and Yunis, E.J., unpublished results) were included in the MDS analysis.

Results

The haplotype frequencies for the African descent and the Caucasian-Mestizo populations of Colombia have been published before (20). For the African descent population, 110 haplotypes was found out of 134 unrelated individuals tested. Ninety-six out of 110 haplotypes were single instance haplotypes, one haplotype was shared between six individuals, six haplotypes were shared by three individuals and seven haplotypes were shared by two individuals each (table 1).

The genetic structure (excluding DYS385) of the African descent population collected in four different towns of the Choco Department of Colombia, as determined by estimates of F st (or R st ), showed that only 2.6% (p 0.054) of the genetic variation was due to differences between groups (towns) and 97.4% variation was found within the sample collected in each town (100,000 permutations).

For the Caucasian-Mestizo population of Colombia, from a total of 177 individuals analyzed, 45 pairs corresponded to excluded alleged father/son pairs by previous analysis of autosomic STRs, 40 pairs of alleged father/son whose probability of paternity was >99.99% and 7 unrelated individuals, for a total of 137 unrelated individuals were tested. All 40 pairs of compatible paternity by autosomic STRs were also compatible for Y-STR haplotypes. No mutations were detected among these 40 pairs. One out of 45 pairs of excluded paternity by autosomic STRs had an identical Y-STR haplotype. From the 137 unrelated individuals, a total of 122 haplotypes were determined. One hundred and fourteen of the 122 haplotypes were single instance haplotypes, one haplotype was present in five unrelated individuals, 2 haplotypes in four individuals and 5 haplotypes in two unrelated individuals each.

Numbers of shared haplotypes between the Caucasian-Mestizo and African descent populations of Colombia were determined for each of the 232 haplotypes identified. Only six haplotypes were found to be shared between these two ethnic groups (2.59%) as shown in table 2. Three out of these six haplotypes are the most frequent haplotypes in Caucasian-Mestizos.

The multidimensional scaling analysis is presented in figure 1. The Caucasian-mestizo population from Colombia clustered with most of the Caucasian populations included in the analysis. The closest genetic distances (data not shown) were found with the populations form Andalucia (Spain), Medellin (Colombia), and Galician (Spain) populations. On the other hand, the African descent population of Colombia clustered with the African American and Surinam populations. The Amerindian population of Colombia clustered with other Amerindian populations including the Inuit population of Greenland.

Discussion

The analysis of Y-STR haplotypes found in the non-recombinant portion of the Y chromosome (minimal haplotype, DYS19, DYS389-I, DYS389-II, DYS390, DYS391, DYS392, DYS393 and DYS385) were used to determine genetic affinities between groups of male individuals and to detect population structure (36) in 271 unrelated individuals of Colombia, of which 134 were of African descent and 137 were Caucasian-mestizos.

The first immigrants from Spain and Portugal founded the first non-Amerindian villages in present day Colombia in the early 16 th Century (37). The ancestors of the African descent population of Colombia were brought as slaves between 1580 and 1650 (38) from Senegal, Ivory Coast, Mali and the west coast of Guinea. From the Caribbean coast of Colombia, a large proportion of this population was transferred to Popayan, the slave capital located in the southwest section of the country (Cauca department) to be distributed later mainly to Choco, Antioquia, Cauca and Valle del Cauca departments to work in field and mines.

The Amerindian population that inhabited present day Colombia started to be eliminated since the beginning of the conquest. The major Amerindian cultures that existed at the arrival of the Spanish conquerors, located in the Andean region of Colombia, do not longer exist. The present day Amerindian tribes are located in the Amazonian and Orinoquian regions, and some groups in the south and north sections of the country. Based on the 1993 census, around 1.5% of the population was Amerindian (39).

The Colombian Andes have been a strong barrier against free demographic flow within Colombia. In the southwest of Colombia, the Andes divide themselves into three mountain ranges (east, central and west Andes) that extend towards the north covering most of the central portion of the territory (40). Thus, the Andes define five different geographic regions named the Pacific (where the Choco department is located), the Atlantic, the Andean, the Orinoquian and the Amazonian regions. For centuries, demographic growth of different population groups occurred within each region with some degree of isolation, which has generated subcultures within the country. Most of the demographic flow between regions started in the middle to late 20 th century, with some genetic exchange between some regions. Previous studies of the population found in the East-central Andean region of Colombia, based on blood groups analysis, have shown a little contribution of African descent individuals to the genetic makeup of this region (28). In that report, the African descent component was between 2.5% and 5.9% in the three departments where the Caucasian-Mestizo sample was collected for the present study. Our results, based on Y-chromosome haplotypes, showed that only 2.59% (6 out of 232) of the haplotypes were shared between Caucasian-Mestizos and African descent individuals (table 2). Most of the shared Y-STR haplotypes are the most common haplotypes among the Caucasian-mestizo population implying a genetic flow from male Caucasians into African descent individuals. Thus, our results corroborate previous findings of African admixture for the eastcentral region of the Colombian Andes. On the other hand, a similar result was obtained for a sample of 225 unrelated individuals from Medellin (18)(Central-west Andes) when compared to the African descent population reported here. Out of 281 haplotypes (110 African descent and 171 from Medellin), only ten haplotypes were shared between these two groups (2.81%). Once again, the haplotypes shared between these groups are among the most frequent haplotypes found in the Caucasian population. However, based on blood groups, near 15% of the population of Antioquia is of African descent. Although the demographics for the 225 individuals from Medellin was not known, it is possible that it was composed mainly of Caucasian-mestizo individuals (predominant group in the city) and not from other sections of the department like the west section where the African descent component is somewhat stronger. The genetic affinity of the Medellin sample based on genetic distances with other Caucasian populations in the multidimensional scaling analysis provides further support for this assumption.

In a separate report, based on Y chromosome microsatellites and biallelic markers, 94% of male haplotypes found in Antioquia were of European ancestry, 5% of African and 1% Amerindian while around 90% of the mtDNA gene pool was of Amerindian heritage (40) which suggests a Caucasian/Amerindian sex bias. These results are likely true for the Caucasian-mestizo population of Antioquia based on the demographics of the sample selected for that study. However, the genetic Composition of Antioquian population should be somewhat different and the 15% African admixture could probably be a real estimate when considering all the population of that region.

On the other hand, it is likely that a similar Caucasian/Amerindian sex bias will be found for the Caucasian-Mestizo population since historical data indicates a limited female immigration from Spain Thus, the genetic pool was limited to male European Caucasians and Amerindian mtDNA. This admixture process would have generated the Caucasian/ Amerindian sex bias based on Y-Chromosomes and mtDNA, as mentioned earlier, but with various degrees of admixture at the autosomal level which differentiates the present day population from the Amerindian and Spanish populations, as it has been demonstrated for the Caucasian-mestizo population of Colombia and different populations from Spain and Portugal, based on autosomic STR analysis (43-45). In that regard, in another report (26), the analysis of 305 unrelated individuals from the departments located in the Caribbean region of Colombia showed that most of the Y-chromosome haplotypes present in that region of the country, are also of Spanish/European origin that clustered near the populations reported by us and others published in YHRD database. A similar scenario has been found for mestizo samples analyzed in Cartagena (21), Cundinamarca and Boyacá (24), Valle del Cauca, Cauca and Nariño (23).

The genetic structure of the African descent population, collected in four different towns of the Choco Department of Colombia based on the AMOVA, showed that only 2.6% of the genetic variation was due to differences between groups (towns) and 97.4% variation was found within the sample collected in each town. As we have previously reported, these results are likely due to a process of genetic ‘homogenization' carried out by the slavers in Colombia (38). In that process, in order to avoid emancipation movements among the slaves, individuals speaking the same language were separated. A similar process has been reported for African descent populations of Venezuela and Brazil (46).

The African populations have shown the highest genetic heterogeneity based on mtDNA and other autosomic markers studied so far. However, the results obtained in our study, based on Y-Chromosome STR, showed a lower haplotype diversity and discrimination power for the African descent population of Colombia than those obtained for the Caucasian-mestizo population (table 1). Out of 110 haplotypes identified in the African descent population, only 96 were single instance haplotypes as compared to 114 out of 122 in the Caucasianmestizo populations. Thus, several haplotypes among the African descent population might be Identical By Descent (IBD) which leads to a lower haplotype diversity and lower discrimination power. These results are probably true for the population of the Choco department due to several factors. First, a genetic gene pool that has remained unchanged for the last 350 years and the absence of new genetic flow from African populations and other ethnic groups limiting the effective size of Y-chromosomes in this African descent population of Colombia. However, a different picture should be expected in regions were the Caucasian/African admixture process has been stronger as in the Atlantic and the southwest sections of the country.

A multidimensional scaling analysis based on Nei genetic distances was carried out for the Colombian populations described here and several European, American, Asian, Arabs and Amerindian populations in order to determine their genetic affinities.

Although the sample size analyzed here could seem small, 134 haplotypes for African descent and 137 haplotypes for the Caucasian-Mestizo sample, these values are similar to those used in other studies (23-25) to determine the genetic relationship between populations (see footnote of figure 1 for sample sizes from multiple populations analyzed around the globe). The results showed clustering of the Caucasian-Mestizo population of Colombia with other Caucasian populations of Europe and America (Medellin and Buenos Aires). The closest genetic distances were with the population of Andalucia, followed by Medellin and Galicia. Our results are in agreement with historical data indicating that most of the Spanish colonizers of the new world came from Andalucia, Extremadura, and Castilla in that order during the 16 th and 17 th centuries (47). The Caucasian-Mestizo population seems to be genetically distant from the Valencian and Catalunian populations of Spain (both of them belonging to the Aragon province during 16 th century), which corroborates historical data indicating a little contribution of this province to the colonizing force. On the other hand, our sample seems to be genetically distant from the Basque population, a result likely due to the fact that the Basque immigrants to present day Colombia are mainly located in the west section of the country (47).

The African descent population clustered with other African descent populations such as the African- American and the population from Surinam. Based on autosomal STR analyzed for the African descent population of Colombia (43-45) no statistically significant differences were found with the African American population. Our results with Y-STR haplotypes are in agreement with our previous findings, as well as historical data suggesting a common origin in the West coast of Africa for both the African American and Afro-Colombian individuals. The grouping of the population from Surinam, and admixed population, is probably due to the strong African descent component (predominant group) and, a lesser extent, the components derived from Caucasian (Netherlands) and Asian (India and Indonesia) populations of Surinam.

The Arab populations included in the Multidimensional Scaling analysis are very distant from the Caucasian-Mestizo population of Colombia. This result is probably due to the fact that the Arab admixture of the Colombian population has been mainly with Lebanese and Palestinian populations and not with Arab populations of North Africa. In addition, the Lebanese and Palestinian presence is stronger in the Atlantic region of Colombia and, in a lesser extent, in the north Andean region of the country; therefore the Arab ancestry may not be well represented in the sample studied.

Previously, a Jewish ancestry of around 14% for the population of Antioquia was proposed based on 6 loci Y-STR haplotypes (DYS19, DYS388, DYS390, DYS391, DYS392, DYS393) (40). Although our studies did not include the DYS388 loci analyzed in that report, we evaluated the presence of the Cohen modal haplotype based on the remaining 5 STRs analyzed in our sample and in the sample reported for Medellin by Builes et al . The Cohen haplotype (14; 23; 10; 11; 12) was found only in two individuals (2/114, 1.75%) of our sample and in three individuals from Medellin (3/171 haplotypes, 1.75%). In addition, when considering all the haplotypes used to obtain the 14% Jewish ancestry reported by Thomas (48), the number of potential Jewish haplotypes in our sample was 3.5% (4/114) and 3.5% in the sample from Medellin (6/171). Therefore, additional studies are required in order to properly establish the Jewish genetic influence in the population of Colombia.

Taken together, our results showed a limited contribution of Caucasian Y-STR haplotypes in the Afro-Colombian population of the Choco Department as well as a limited contribution of Afro- Colombian Y-STR haplotypes in the Caucasian- Mestizo population of the east-central Andean region of Colombia corroborating previous studies with autosomal markers.

This work was supported by Servicios Médicos Yunis Turbay y Cia., and by a grant from DINAIN, Universidad Nacional de Colombia, D100C377 to J.J. Yunis and Luis E. Acevedo.

All authors declare that there is no conflict of interest. Servicios Médicos Yunis Turbay y Cia provided some of the samples, materials and reagents, and the fluorescent genetic analyzer Hitachi FMBIOII that was used in the present study.

Grant from DINAIN, Universidad Nacional de Colombia, D100C377 to J.J. Yunis and Luis E. Acevedo, and financial support from Servicios Médicos Yunis Turbay y Cía.

Correspondence:

Juan J. Yunis, Departamento de Patología, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, D.C., Colombia Phone: (571) 316 5000, ext. 11605 jjy@yunis.com.co, jjyunisl@unal.edu.co

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