Dissecting the Pre-Columbian Genomic Ancestry of Native Americans along the Andes-Amazonia Divide

Abstract

Extensive European and African admixture coupled with loss of Amerindian lineages makes the reconstruction of pre-Columbian history of Native Americans based on present-day genomes extremely challenging. Still open questions remain about the dispersals that occurred throughout the continent after the initial peopling from the Beringia, especially concerning the number and dynamics of diffusions into South America. Indeed, if environmental and historical factors contributed to shape distinct gene pools in the Andes and Amazonia, the origins of this East-West genetic structure and the extension of further interactions between populations residing along this divide are still not well understood. To this end, we generated new high-resolution genome-wide data for 229 individuals representative of one Central and ten South Amerindian ethnic groups from Mexico, Peru, Bolivia, and Argentina. Low levels of European and African admixture in the sampled individuals allowed the application of fine-scale haplotype-based methods and demographic modeling approaches. These analyses revealed highly specific Native American genetic ancestries and great intragroup homogeneity, along with limited traces of gene flow mainly from the Andes into Peruvian Amazonians. Substantial amount of genetic drift differentially experienced by the considered populations underlined distinct patterns of recent inbreeding or prolonged isolation. Overall, our results support the hypothesis that all non-Andean South Americans are compatible with descending from a common lineage, while we found low support for common Mesoamerican ancestors of both Andeans and other South American groups. These findings suggest extensive back-migrations into Central America from non-Andean sources or conceal distinct peopling events into the Southern Continent.

Keywords: Amazonia; Andes; Native American ancestry; genome-wide SNPs; population genomics.

Fig. 1.

Principal component and ADMIXTURE analyses performed on Native American populations included in the pruned “un-admixed” data set. (a) Plot of PC1 versus PC2 for the 43 un-admixed Native American groups reported in the bottom legends of left and right plots. Individuals are color-coded according to their country of origin (left) or language family affiliation (right). In order to allow continent-wide comparison, we used the same Greenberg’s classification (Greenberg 1987) of languages as in Reich et al. (2012). (b) Results of ADMIXTURE unsupervised cluster-based analysis at K = 8. Average proportions of inferred ancestral components are plotted at population level. Pie charts diameters are proportional to the sample sizes of each considered group ranging from N = 1 to N = 20 (full set of populations, K tested and cross-validation errors are reported in supplementary figs. S3 and S4, Supplementary Material online). The geographical map has been plotted using the R software (v.3.2.4).

Fig. 2.

Intrapopulation patterns of homozygosity and haplotype sharing. (a) ROH calculated for the Native American groups with N ≥ 5 included in the “un-admixed” data set. Top panel shows the distribution of all ROH lengths (black) and their inferred assignment into four bin classes identified by Mclust (blue, red, green, and purple for class 1–4, respectively). Since, class 4 is represented by only three outlier individuals, they were removed from downstream analyses. Bottom panel shows the average length of ROHs over all individuals within each Native American population for each of three considered length classes (i.e., 1–3). (b) Pattern of intrapopulation haplotype sharing measured as the average total length of genome shared IBD between every couple of samples within each population (W_AB). Within-population IBD-sharing was calculated for nine bins of IBD lengths, corresponding to different degrees of relatedness according to Moreno-Estrada et al. (2014). Dashes lines represent the distribution of inferred statistics over the considered length classes (see also supplementary fig. S8, Supplementary Material online). The mode of the distribution is plotted as the corresponding labeled point for each population.

Fig. 3.

fineSTRUCTURE hierarchical clustering dendrogram calculated between pairs of Native American individuals of the “un-admixed” data set. The 26 clusters highlighted with different colors are highly concordant with the actual population labels, with the exclusions of partially overlapping geographically close groups of Costa Rica (i.e., Maleku, Bribri, Teribe, and some Cabecar samples), Chane and Guarani, Wayuu and Kogi, Waunana and Embera, Aymara from Bolivia. In the figure, these samples were thus merged in the same cluster. For detailed annotation of individuals inside each cluster, see supplementary figure S10, Supplementary Material online.

Fig. 4.

Best-fitting AGs obtained with qpGraph. (a) Schematic summary of models testing a topology where the Tzotzils descend from an admixture between a node ancestral to the Zapotec and the non-Andean lineage, while using all possible combinations of Andean and non-Andean populations. (b) Schematic summary of all AGs obtained testing in turn four Peruvian Amazonian groups (i.e., Cashibo, Shipibo, Yanesha, and Ashaninka) as admixed between a non-Andean, specifically Amazonian, lineage and a node ancestral to the Andeans. Dotted lines represent the two-way admixture events tested and the percentages of ancestry on each line denote the proportions of admixture relative to the two admixing lineages. Units along solid lines indicate the measure of drift. Ranges of admixture proportions and drift lengths represent the min and max values reported in supplementary tables S11 and S13, Supplementary Material online, for all of the tests performed. Red nodes represent the two possible events of diffusion into South America hypothesized in the Discussion section.