Outlining the ancestry landscape of Colombian Admixed and Native populations
Humberto Ossa1,2, Juliana Aquino3, Rui Pereira4, Adriana Ibarra5, Rafael H Ossa2,6,Luz Adriana Pérez7, Juan David Granda5, Maria Claudia Lattig7, Helena Groot7, Elizeu Fagundes de Carvalho3, Leonor Gusmão3,4,*
1Pontificia Universidad Javeriana., Facultad de Ciencias, Bogotá, Colombia
2Laboratório de Genética y Biología Molecular, Bogotá, Colombia
3DNA Diagnostic Laboratory (LDD), State University of Rio de Janeiro (UERJ), Brazil
4IPATIMUP (Institute of Pathology and Molecular Immunology from University of Porto), Portugal
5IdentiGEN - Genetic Identification Laboratory and Research Group of Genetic Identification, Institute of Biology, School of Natural and Exact Sciences (FCEN), University of Antioquia, Medellin, Antioquia, Colombia
6Universidad El Bosque, Facultad de Medicina, Bogotá, Colombia
7Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
Keywords: Admixture, Ancestry, AIMs, INDELs, Autosomal markers, Native Americans, Motilón-Barí, Colombia, South America, Population stratification, Substructure
Short title: Ancestry in Colombian populations
*Corresponding author:
Funding: Financial support was granted by DNA Program – State University and Justice Court of Rio de Janeiro (UERJ/TJRJ/MPRJ), Brazil. IPATIMUP is an Associate Laboratory of the Portuguese Ministry of Science, Technology and Higher Education, and is partially supported by FCT, the Portuguese Foundation for Science and Technology.JA was supported through a Doctoral fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil. RP is supported by a postdoctoral fellowship from FCT (SFRH/BPD/81986/2011), Portugal.
Abstract
The ancient background of Colombian population comprises a large number of well differentiated Native communities, belonging to diverse linguistic groups. In the late fifteenth century, a process of admixture was initiated with the arrival of the Europeans, and few years later Africans also became part of the Colombian population. Therefore, the gene pool of current Colombian population results from the admixture between Native Americans, Europeans and Africans, which occurred differently depending on the region of the country, producing a clearly stratified population. Having in mind the importance of population substructure in both clinical and forensic genetics, we sought to investigate and compare patterns of genetics ancestry along the Colombian territory, by studying samples from Native and Non-Native populations, living in the 5 continental regions: Andes, Caribbean, Amazonia, Orinoquía and Pacific. With this purpose, 46 AIM-Indels were genotyped in 761 non-related individuals from current admixed populations; and previously published genotype data from 214 Colombian Natives from five groups were used for population comparisons.
Significant differences were observed among Native and non-Native populations, as well as among admixed populations from different regions and native populations from different ethnic groups. Pacific was the region with the highest African ancestry, Amazonia has the highest Native ancestry and Andean and Orinoquían regions showed the highest proportion of European ancestry. Andean region was further sub-divided in 6 sub-regions: North East, Central West, Central East, West, South West and South East. Among them, the South East region showed a significantly lower European admixture than the remaining. Hardy-Weinberg equilibrium and variance values of ancestry among individuals within populations showed a potential stratification of the Pacific population.
Introduction
In a geographic framework, Colombia occupies the south extreme of the bridge that connects the two American subcontinents. Therefore, since pre historical times that Colombia has been subject to an intense genetic and cultural flow carried by Native American human migrations, which ultimately resulted in a high diversity of ethnic groups that inhabited the country, and to a noticeable heterogeneity between geographic regions (Arango et al. 2006; Cuervo 2000;
Wang 2007; Roewer at al., 2013; DANE censo general 2005; http://www.dane.gov.co).This heterogeneity is still maintained in the current Colombian population, which diversity has been further shaped by the admixture with people from other continents. The Andes represent the region where the Chibcha civilization flourished, the third most developed group of America after the Aztecs and the Incas. The Caribbean region is clearly differentiated from the remaining regions and its territory is inhabited by very diverse ethnic groups. These two regions both before and after the European conquest were and remain the most densely populated and economically active in the country. The other three natural regions include the Pacific region and the forest area that today corresponds to the Orinoquía and Amazon regions, which are the largest in the territory, but the less populated and less economically developed(DANE censo general 2005; http://www.dane.gov.co).
During and after the colonial times, the genetic background of the populations currently inhabiting the Colombian territory was ultimately shaped by different levels of admixture between Native people and European and African incomers, being also associated to different migration patterns, drift effects and a more or less geographic isolation of the populations.
Some studies have been conducted to genetically characterize Colombian populations and to correlate the observed diversity with historic events, using genetic markers with different inheritance patterns and degrees of susceptibility to detect populations’ differentiation by
mutation, drift and admixture(e.g. Rojas et al., 2010; Ibarra et al., 2014a; Salas et al., 2008;
Noguera et al., 2014; Ibarra et al., 2014b).
The ancestral background of Colombia has been investigated using lineage markers. Several studies were published describing the Y chromosome profile of Colombian populations, but most of them were restricted to Y-STRs (e.g. Yunis 2005; Builes 2006; Alonso and Usaquén, 2013), and just few included the slowly evolving Y-SNP markers that allow a more robust analysis of the paternal ancestry in populations (Carvajal-Carmona 2000; Bedoya et al., 2006;
Rojas 2010 (7); Noguera 2013 (8); Xavier 2015 (9). Some of the above mentioned studies also included mtDNA data, revealing an unequal maternal vs. paternal ancestries of the admixed Colombian populations, harbouring a gene pool that is mainly composed by Native American mtDNA and European Y chromosome haplogroups (Carvajal-Carmona 2000 (5);
Bedoya 2006 (6); Rojas 2010 (7); Xavier 2015 (9). European mtDNA haplogroups are the second most represented in admixed populations in Colombia, except for some African descent populations, where the African L-haplotypes are predominant (Salas 2008; Rodas 2003; Yunis and Yunis, 2013).Most Native groups still preserve an almost complete native maternal ancestry, and signs of European admixture can be seen in the Y chromosome gene pool that varies with the degree of cultural and geographic isolation of the group (Mesa 2000;
Usme-romero 2013; Xavier 2015).
If uniparental marker shave been useful to reveal differences in populations concerning paternal and maternal inheritance, they are not the best choice for a more comprehensive description of the genetic profile of populations in terms of ancestry, which can only be achieved with the study of a significant number of recombining markers.
Regarding recombining autosomal markers, the studies available for Colombia are even more fragmentary than for lineage markers, just considering a restrict number of markers and/or population groups (e.g. Bedoya 2006; Wang 2007; Rojas et al., 2010; Reich et al., 2012).Price
et al. (2007) have studied a large set of ancestry-informative markers, however, in this study the “Colombians” were represented by individuals from a single population (Antioquia), and not accounting for the large heterogeneity of the country. On the other hand, a much larger number of population samples across Colombia were examined by Rojas 2010 and Ibarra 2014. However, the study by Rojas 2010 included just a small number of eleven autosomal AIM markers; and the set of 52 SNPs studied by Ibarra 2014 do not present high levels of intercontinental diversity. Therefore, although appropriate to estimates relative differences in the ancestral composition of the populations analysed, data from both studies are not enough to obtain accurate estimates of the ancestry of the Colombians. So far, these studies have shown that Colombia does not present a uniform genetic pool, with a high heterogeneity of African, European and Native American ancestries, depending on the region of the country.
Considering the complex history and the high genetic heterogeneity of the present-day populations in Colombia, more comprehensive studies are still required for a fine scale mapping of the admixture structure of the country, which is crucial in many applied fields, namely clinical and forensic genetics (Tian et al., 2008; Zhivotovsky et al., 2001).
In an attempt to contribute to a better knowledge of the ancestry of Colombians, in the present work we have used 46 autosomal ancestry-informative insertion/deletion markers (AIM- INDELs) to characterize patterns of variation across admixed and Native Colombian populations from different geographic regions.
The AIM-INDELs that we used were previously selected by Pereira et al. (2012) for inference of ancestry and admixture proportions of Asian, African, European and Native American origin; and they were applied to the study of South American populations from Bolivia, Brazil and Colombia (Manta 2013; Vullo et al., 2015; Xavier et al., 2015).
Following the historical settlement of Colombia, genetic variation was investigated in Native and non-Native populations occupying the five continental regions (namely, Andean,
Caribbean, Pacific, Orinoquía and Amazon regions), giving emphasis to the Andean region that currently representsalmost80% of the total population(DANE censo general 2005;
http://www.dane.gov.co). The results obtained revealed a highly stratified population in terms of ancestry that should be taken into account when delineating studies and/or interpreting genetic data in different areas of research.