ARTÍCULOS ORIGINALES

Ancestral genetic composition of a human population from the Colombian southwest using autosomal AIM-InDels

Composición genética ancestral de una población humana del sudoeste de Colombia usando AIM-InDels autosómicos

 

Urbano L.^1,2, Portilla E.C.^1,2, Builes J.J.³, Gusmão L.^4,5, Sierra-Torres C.H.^1,2,*

¹ Human Genetics Laboratory, Department of Physiological Sciences, Faculty of Health Sciences, University of Cauca, Popayán, Colombia.
² Molecular Diagnostics Unit, Innovagen Foundation, Popayán, Colombia.
³ Genes Ltda., Medellín Colombia.
⁴ IPATIMUP-Institute of Molecular Pathology and Immunology of the University of Porto, Porto, Portugal.
⁵ DNA Diagnostic Laboratory (LDD), State University of Rio de Janeiro (UERJ), Rio de Janeiro, Brazil.
*Corresponding author: hsierra@unicauca.edu.co

Fecha de recepción: 26/04/2015
Fecha de aceptación de versión final: 11/09/2016

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ABSTRACT

Genetic markers with allele distribution differences in human populations provide human ancestry information that can be used to evaluate admixture proportions in different ethnic groups, including stratification in genetic association studies. The aim of this study was to determine the African, European and Native American admixture proportion by making use of 46 insertion-deletion informative ancestry record markers set in 500 Latin American people in the Department of Cauca, Colombia. Allelic frequencies were established, Hardy Weinberg test was performed, comparisons in genetic distances among population groups were estimated using Arlequin v 3.5, and STRUCTURE v 2.3.4 software was used to determine the population's ancestry admixture. The results revealed a diverse genetic base, resulting from the three continental populations tested. The average ancestry observed in the Cauca population was: 48 % Native American, 39 % European, and 14 % African. This study reveals the complex population stratification of the Department of Cauca, which is the result of the genetic admixture of three continental populations.

Key words: Genetic ancestry; InDels; AIMs; Latin America; Human populations.

RESUMEN

Los marcadores genéticos con diferencias en la distribución de alelos en las poblaciones humanas proporcionan información de ancestría que se puede utilizar para evaluar las proporciones de mezcla de diferentes grupos étnicos, incluyendo la estratificación en los estudios de asociación genética. El objetivo de este estudio fue determinar las proporciones de mezcla Africana, Europea y Nativo Americana utilizando un conjunto de 46 marcadores informativos de ancestría de inserción-deleción en una población de 500 sujetos Latino-Americanos del Departamento del Cauca, Colombia. Se estimaron las frecuencias alélicas, la prueba de Hardy Weinberg, se realizaron comparaciones de distancias genéticas entre poblaciones utilizando Arlequin v 3.5. Se utilizó El programa STRUCTURE v 2.3.4 para determinar la mezcla ancestral de la población. Los resultados mostraron una base genética muy diversa producto de las tres poblaciones continentales evaluadas. La ancestría promedio observada en la población del Cauca fue del 48 % de Nativos Americanos, el 39 % Europeos y el 14 % de Africanos. Este estudio revela la compleja estratificación poblacional del Departamento del Cauca, la cual es el resultado de la mezcla genética de tres poblaciones continentales.

Palabras clave: Ancestría genética; InDels; AIMs; América Latina; Poblaciones humanas.

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INTRODUCTION

The genetic composition of the Colombian population, like most Latin American populations, is the result of complex admixture processes among European, Native American and African ancestors that took place during the Spanish conquest of America (Chacón-Duque et al., 2014). In addition to the Spaniards, an important number of Afro-descendants were brought to the continent as slaves. Throughout the last 500 years of history, the Colombian population has undergone genetic mixture and, as a consequence, the Colombian Native American population has been notably reduced (Acosta et al., 2009). The population with mixed ancestry is mainly concentrated in the urban areas of the country, particularly in the Colombian Andes; the Afro-Colombian population lives mainly in the Caribbean and Pacific coasts and the islands, whereas the Native American populations are located predominantly in the East and in rural areas of the Southwest and North of the country (Rojas et al., 2010). The population from the Department of Cauca is well known for its highly multiethnic background as a result of the admixture of parental populations (Córdoba et al., 2012). According to data from the National Administrative Department of Statistics, Cauca has 1,182,022 inhabitants, of whom 56.25 % are white and "Mestizo" and are located mainly in the central area of the Department; 21.55 % are Native Americans located in the East; and 22.2 % are Afro-descendants who reside in the Pacific Coast (DANE, 2005). Genetic ancestry studies of human populations from highly admixed regions such as the Department of Cauca is currently considered a powerful tool to determine their admixture patterns (Neves Manta et al., 2013). The implementation and use of polymorphic markers such as Ancestry Informative Markers (AIMs)-InDels, which present high intercontinental allelic differentiation across populations, allows the identification of allele frequency differences among populations and to infer their ancestral origin (Bastos-Rodrigues et al., 2006; et al., 2009; Pena et al., 2009; Tishkoff et al., 2009; Pena et al., 2011; Manta et al., 2013; Neves Manta et al., 2013; Pepinski et al., 2013; Zaumsegel et al., 2013; LaRue et al., 2014; Shi et al., 2015).
The aim of this study was to determine the admixture proportions of a population sample from the Department of Cauca based on the evaluation of ancestral contributions of three different continental populations, Native Americans, Europeans and Africans, using autosomal AIMs-InDels.

MATERIALS AND METHODS

Ethics statement
The questionnaires, procedures, and protocols used were reviewed and approved by the Ethics Committee for Scientific Research at the University of Cauca; following guidelines and bioethical principles established in the Helsinki declaration of the 206 World Medical Association and the parameters outlined in Resolution 8430 of 1993 by the Colombian Ministry of Health. Sample collection and DNA extraction During this study, a total of 500 samples were collected from unrelated individuals from 23 municipalities of the Department of Cauca, Colombia, as follows: 67.2 % were collected in the central region and 1.2 %, 26.6 % and 5.0 % were collected from the north, south and east regions, respectively. According to 2005 census by the National Administrative Department of Statistics, the Department of Cauca had a 68.3 % of inhabitants in the central zone, 3.5 % in the north zone, 23 % in the south zone, and 5.2 % in the east zone. Therefore, the population sample included in this study represents the general population (DANE, 2005). The genetic markers information was obtained from Marshfield Diallelic Insertion/Deletion Polymorphisms database website (Weber et al., 2002) and GENES Ltda. Blood samples were collected in tubes containing EDTA and coded with internal control codes to protect the identity of each participant. Then, DNA was extracted using the standard salting-out procedure (Miller et al., 1988). A DNA concentration of 30 ng/µl, measured with a NanoDrop 2000c Spectrophotometer, was used for the analysis (Desjardins et al., 2010).

Genotyping
We used a set of 46 autosomal AIMs-InDels (Table 1), previously reported and validated for human population groups of Africans, Europeans and Native Americans (Shriver et al., 1997; Pereira et al., 2009). Amplification and genotyping of the 46 AIM-InDels was performed using the QIAGEN Multiplex PCR kit (Qiagen) combined with a mixture of 0.1 μM of all primers and 5 ng of genomic DNA to complete a 6 μL of final reaction solution. The amplified products were separated by electrophoresis in 5 % polyacrylamide gels and visualized with a FMBIO IIe Genetic Analyzer (HITACHI GENETIC Systems, Alameda, CA, USA).

Table 1. InDels allele frequency, in HGDP-CEPH diversity panel population samples from Africa (AFR), Europe (EUR) and Native America (NAM).

Polymerase Chain Reaction
PCR reaction admixture calculus were done multiplying a sample volume (µL) by the total number of individuals; following, the 46 InDels panel markers were prepared according to the Genes laboratory protocol; the final volume per sample was 6 µL. For each assembly, a negative control under the same condition was considered (Tables 2 and 3).

Table 2. Reactive mixture for PCR (polymerase chain reaction).

Table 3. Multiplex PCR profile.

Statistical analysis
Estimation of allele frequencies, Hardy Weinberg Equilibrium testing and population comparisons by pairwise genetic distances (FST) were carried out using Arlequin v 3.5 (Excoffier et al., 2010) (Schneider et al., 2009). For an easier visualization of the observed genetic distances, a multidimensional scaling (MSD) plot of the pairwise FST was performed using STATISTICA v7.0.
The software STRUCTURE v 2.3.4 was used to determine the ancestral admixture of the population under study and to infer the population structure (Pritchard et al., 2000). The evaluation of the ancestral proportions was performed by using published information on the geographic origin of the reference samples. PDGH-CEPH were used as reference samples (Pereira et al., 2012), and a tri-hybrid contribution from Native Americans, Europeans and Africans (K= 3) to the current genetic makeup of Cauca population was assumed. Furthermore, 100,000 burning steps followed by 100,000 Markov Chain Monte Carlo iterations, using both "Admixture Model" and only the reference individual with POPFLAG=1, were considered in the STRUCTURE analysis (Pritchard et al., 2000). The option "Use population Information to test for migrants" was used in the Admixture Model.

RESULTS

Allele frequencies
The allele frequencies and expected heterozygosities estimated for the 46 AIM-InDels are presented in Table 4. The generated data from all samples were used to test Hardy Weinberg Equilibrium and p values were corrected by Bonferroni´s correction for multiple tests (Bland et al., 1995). The InDels frequency distribution showed no statistically significant deviations from HWE within Cauca population.

Table 4. Frequencies of 46 insertion/deletion polymorphisms, obtained in individuals from the Department of Cauca.

Genetic distance analysis
A two-dimensional MDS plot was drawn to improve the visualization of genetic distances (Figure 1). It can be observed that Cauca and Manaus populations are neighbors and that these two populations are the result of the Native Americans and Europeans admixture, as other Brazilian populations.

Figure 1. Multidimensional scaling plot of the pairwise Fst genetic distances calculated for samples from Native Americans, European, African and Cauca populations, including samples of Brazil; SI: Santa Isabel do Rio Negro; MA: Manaus; PE: Pernambuco; AL: Alagoas; MT: Mato Grosso do Sul; TE: Terena; MI: Minas Gerais; ES: Espírito Santo; RJ: Rio de Janeiro; SP: São Paulo; PR: Paraná; SC: Santa Catarina; RG: Rio Grande do Sul).

Analysis of admixture
The ancestry proportions from the admixture analysis are shown in Figures 2A and 2B. The average ancestry of the studied population is 48 % Native American, 14 % African and 39 % European (Figure 3).

Figure 2A. Bar plot showing individual ancestry estimates obtained from Cauca population and parental populations. Based on STRUCTURE analysis with 100,000 burning steps followed by 100,000 MCMC iterations and k= 3 with POPFLAG= 1, treated in CLUMPP and plotted with destruct (AFR: Africa; EUR: Europe; NAM: Native America). Panels 1, 2 and 3 present the distribution of the African, European and Native American populations, respectively. On the other hand, panel 4 shows the distribution of individuals from the Department of Cauca evidencing a homogeneous contribution from both the Native American and European populations; notice that the largest proportion corresponds to "mestizo". The African contribution is present in a low proportion.
Figure 2B. Triangle plot representation to distinguish individuals from different parental populations. Based on STRUCTURE results from the run with highest -lnP(D) (left: admixture model; right: using population information; red: Africa; green: European; blue: Native American; yellow: Cauca). For each individual, the values of the three ancestry coefficients are indicated by the distance to the edges of the triangle. Each individual is represented by a colored point and a homogenous distribution of the population from Cauca in both clusters of European and Native American population is shown. Furthermore, a lower proportion of individuals from Cauca in the African population cluster are observed.

Figure 3. Map of regions studied from the Department of Cauca showing African, European and Native American ancestry contribution. Principal Component Analysis Plot

Principal component analysis
Principal component analysis was done to reduce the data dimension (Figure 4). It can be observed that the studied population is composed of European and Amerindian populations (biplot's right side); on the other hand, a minority arrangement towards the African population is also observed (biplot's left side). These findings set the Department of Cauca as a mixed race population territory (Figure 4).

Figure 4. Principal Component Analysis, Biplot right side shows that the studied population is spread and compounded by the European and Amerindian origin, in contrast, in the biplot left side there is a minority population of African origin.

DISCUSSION

The estimation of the genetic composition of populations resulting from admixtures has been important in genetic analyses of many human populations (Lai et al., 2009; Lee et al., 2010; Lins et al., 2010; Wang et al., 2010; Avena et al., 2012; Crouch et al., 2012; Campos-Sánchez et al., 2013; Heinz et al., 2013; Shahabi et al., 2013; Parolin et al., 2014). A set of 46 AIMs-InDels reported by Pereira et al. (2012) was used to characterize the composition of genetic ancestry proportions of a population sample of 500 individuals from 23 out of 42 municipalities representing the central, northern, southern and eastern regions of the Department of Cauca (DANE, 2005). Individuals from western municipalities were not included in this study because jungle and maritime barriers limited the access to this part of the State. Thus, a random assessment of the genetic composition of the most representative regions from Cauca was accomplished.
The pairwise genetic distances analysis of the studied population showed a higher number of individuals closer to both Native American and European parental populations and a lower frequency closer to African population. The lower frequency of African population could be explained by the occurrence of cultural and geographic barriers which have resulted in the isolation of this ethnic group. These results are consistent with the admixture composition analysis conducted by STRUCTURE, which indicates that the ancestry genetic composition of the Cauca population is predominantly "Mestizo", resulting from the genetic contributions of both Native American and European populations and, to a lesser extent, the African population. The observed differences in ancestry proportions are the result of the admixture by both, European and African populations with the existent Native American population of Cauca. Our findings are consistent with previous genetic composition studies carried out in individuals from several municipalities of Cauca using different AIMs. The study by Acosta et al. showed a high percentage of European contribution in the Caucasian-Mestizo population and a high influence of African ancestry in Afro-Colombian individuals (Acosta et al., 2009). Furthermore, it has been indicated that the Native American and European populations have contributed to a greater proportion to the current gene pool of Cauca population than the African (Rojas et al., 2010; Córdoba et al., 2012). A previous study conducted in Cauca suggest that the DNAmt linage and Y chromosome ancestry did not contribute in the same way to the admixture process, as only 72.8 % of Y chromosomes comes from an European origin, but just a 0.65 % of DNAmt comes from such origin (Cordoba et al., 2012).
In this study, a 17 % paternal contribution against an 89 % maternal contribution in the Amerindian component was also observed. In the African people an opposite phenomenon is observed, as there is a greater paternal contribution. These results suggest that there is a sexual bias in the studied population admixture process due to interethnic reproduction mainly between European conquerors and native women, which could also explain the results found in the present study. The Department of Cauca harbors the highest percentage of Native American population in Colombia. About 20 % of the Cauca population belongs to this ethnic group; moreover, there are eight officially recognized indigenous groups which are established in 26 of the 42 municipalities (Zaumsegel et al., 2013). The admixture analysis in our study revealed greater proportions of Native Americans in both eastern and southern regions of Cauca. This distribution is explained by the fact that numerous Native Americans tribes have inhabited predominantly in the municipalities of the eastern region (Caldono, Puracé, Totoró) since the Pre-Colombian period. Furthermore, several Native American tribes (e.g. Yanacona) are located predominantly in the South of the Department. On the other hand, the admixture proportions of Africans were significantly higher in the northern Region compared to the others. Despite the fact that the North of Cauca is inhabited mainly by Afro-Colombians, Native American and "Mestizo" populations exhibit a wide ethnic diversity. The various hard-labor activities carried out in this region, such as mining and agriculture, contribute to the large concentration of male Afro-descendants linked to them (DANE, 2005).
The population of the Department of Cauca according to the estimates of the National Administrative Department of Statistics -based on the census carried out at the national level in 2005- is constituted by 1,330,756 inhabitants who are spread over a territory of 30,169 km². According to this census, 20.50 % of the population is classified as indigenous. However, our study reveals that according to InDels markers the Amerindian ancestry is 48 %, being twice of that reported by the government. On the other hand, our study reveals a 14 % of the population having an African ancestry, while the government reports 21 %; and the European ancestry is not establish by the government. Data discrepancies are obviously the result of self-reported ethnicity that people provide during census interviewing, while genetic studies provide a more precise approach to ancestry origin.

CONCLUSIONS

All populations presented identical European and Native American contributions, which were slightly higher than the African contribution. Therefore it was determined that the Department of Cauca has a mixed population.

ACKNOWLEDGEMENTS

We are indebted to all the volunteers who participated in the study from the municipalities of El Tambo, Puracé, Silvia, Mercaderes, Rosas, Timbio, Bolivar, La Sierra, La Vega, Cajibio, Argelia, Tunia, Sotará, Piendamó, Miranda, El Bordo, Santander de Quilichao, Totoró, Almaguer, Inzá, Puerto Tejada, Balboa, Morales, San Sebastián, Belalcazar, Coconuco, Sucre, and Popayán. Finally, we acknowledge the collaboration of the administrative personnel of the Human Genetics Laboratory and the Vice-presidency for Research of the University of Cauca.

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