Genetic analysis of ancestry, admixture and selection in Bolivian and Totonac populations of the New World

Abstract

Background: Populations of the Americas were founded by early migrants from Asia, and some have experienced recent genetic admixture. To better characterize the native and non-native ancestry components in populations from the Americas, we analyzed 815,377 autosomal SNPs, mitochondrial hypervariable segments I and II, and 36 Y-chromosome STRs from 24 Mesoamerican Totonacs and 23 South American Bolivians.

Results and conclusions: We analyzed common genomic regions from native Bolivian and Totonac populations to identify 324 highly predictive Native American ancestry informative markers (AIMs). As few as 40-50 of these AIMs perform nearly as well as large panels of random genome-wide SNPs for predicting and estimating Native American ancestry and admixture levels. These AIMs have greater New World vs. Old World specificity than previous AIMs sets. We identify highly-divergent New World SNPs that coincide with high-frequency haplotypes found at similar frequencies in all populations examined, including the HGDP Pima, Maya, Colombian, Karitiana, and Surui American populations. Some of these regions are potential candidates for positive selection. European admixture in the Bolivian sample is approximately 12%, though individual estimates range from 0-48%. We estimate that the admixture occurred ~360-384 years ago. Little evidence of European or African admixture was found in Totonac individuals. Bolivians with pre-Columbian mtDNA and Y-chromosome haplogroups had 5-30% autosomal European ancestry, demonstrating the limitations of Y-chromosome and mtDNA haplogroups and the need for autosomal ancestry informative markers for assessing ancestry in admixed populations.

Figure 1

Sampling locations and the distribution of major mtDNA and Y-chromosome haplogroups for Mesoamerican Totonacs and South American Bolivians.

Figure 2

a) Principal components plot of individual pairwise genetic distance estimates. Panel 1 – most New World Totonac and Bolivian individuals are clustered and have smaller estimated distances to the HapMap CHB/JPT than to the CEU or YRI (~815 K SNPs). Panel 2 – data merged with five Native American HGDP populations typed on the Affymetrix 6.0 platform (~470 K SNPs). Each individual (+) is color coded by population. The percent variance accounted for by each principal component is indicated on the axes. b) Population structure analysis of Totonac and Bolivian individuals at K inferred ancestral populations using a genome-wide panel of 120,958 SNPs (r² ≤ 0.2). Each individual is shown as a vertical bar with proportionate ancestry indicated by color. The top two panels show European attributable ancestry in ten Bolivians at K = 2, 3. The bottom two panels demonstrate greater similarity between the Totonacs and Bolivians than between other World populations (K = 4, 5), including CHB and JPT samples.

Figure 3

Estimate for the age of admixture in Bolivians. The Hapmix log likelihoods summed over all individuals and chromosomes is plotted for generations 2 through 35.

Figure 4

Structure analysis of Bolivians and Totonacs using a panel of 324 AIMs.a) New World ancestry is predicted for all Bolivians and Totonacs. A non-New World ancestry component is correctly distinguished in the ten Bolivians with European admixture. b) A subset of 173 AIMs present in the merged genome-wide data set (this study, [9] and [20]) identifies New World ancestry in other unrelated Native American populations and demonstrates transferability to other New World populations that were not used to ascertain the AIMs. c) 47 AIMs from Kosoy et al. present in the merged data.

Figure 5

Accuracy and performance of the 324 AIMs. The root mean square error (RMSE) between Native American ancestry estimates using AIMs and the ancestry estimate using 120,598 genome-wide markers. (Note: the full AIMs panel (324 markers) produces ancestry estimates slightly lower than the genome-wide marker set, and thus the RMSE cannot achieve zero error with respect to the high-density genome-wide marker set.) AIMs are ordered from more informative (left) to less informative.