Origin and dynamics of admixture in Brazilians and its effect on the pattern of deleterious mutations

Significance

The EPIGEN Brazil Project is the largest Latin-American initiative to study the genomic diversity of admixed populations and its effect on phenotypes. We studied 6,487 Brazilians from three population-based cohorts with different geographic and demographic backgrounds. We identified ancestry components of these populations at a previously unmatched geographic resolution. We broadened our understanding of the African diaspora, the principal destination of which was Brazil, by revealing an African ancestry component that likely derives from the slave trade from Bantu/eastern African populations. In the context of the current debate about how the pattern of deleterious mutations varies between Africans and Europeans, we use whole-genome data to show that continental admixture is the main and complex determinant of the amount of deleterious genotypes in admixed individuals.

Continental admixture and kinship analysis of the EPIGEN Brazil populations. (A) Kinship coefficient for each pair of individuals and the probability that they share zero identity by descent (IBD) alleles (IBD = 0). Horizontal lines represent a kinship coefficient threshold used to consider individuals as relatives. (B) Brazilian regions, the studied populations, and their continental individual ancestry bar plots. N represents the numbers of EPIGEN individuals in the Original Dataset (including relatives; detailed in SI Appendix, section 6). (C) PCA representation, including worldwide populations and the EPIGEN populations, using only unrelated individuals (Dataset U; explained in SI Appendix, section 6). The three graphics derive from the same analysis and are different only for the plotting of the EPIGEN individuals. AP, admixed population; ASW, Americans of African ancestry in USA; CEU, Utah residents with Northern and Western European ancestry; CLM, Colombians from Medellin, Colombia; EAFR, east Africa; FIN, Finnish in Finland; French B, Basque; GBR, British in England and Scotland; IBS, Iberian population in Spain; LWK, Luhya in Webuye, Kenya; ME, Middle East; MXL/MEX, Mexican ancestry from Los Angeles; N., (North) Italian; NAT, Native American; NE, northeast; NEUR, north Europe; PC, principal component; PUR, Puerto Ricans from Puerto Rico; S, south; SE, southeast; SEUR, south Europe; TSI, Toscani in Italia; YRI, Yoruba in Ibadan, Nigeira; WAFR, west Africa.

Abstract

While South Americans are underrepresented in human genomic diversity studies, Brazil has been a classical model for population genetics studies on admixture. We present the results of the EPIGEN Brazil Initiative, the most comprehensive up-to-date genomic analysis of any Latin-American population. A population-based genome-wide analysis of 6,487 individuals was performed in the context of worldwide genomic diversity to elucidate how ancestry, kinship, and inbreeding interact in three populations with different histories from the Northeast (African ancestry: 50%), Southeast, and South (both with European ancestry >70%) of Brazil. We showed that ancestry-positive assortative mating permeated Brazilian history. We traced European ancestry in the Southeast/South to a wider European/Middle Eastern region with respect to the Northeast, where ancestry seems restricted to Iberia.

By developing an approximate Bayesian computation framework, we infer more recent European immigration to the Southeast/South than to the Northeast. Also, the observed low Native-American ancestry (6–8%) was mostly introduced in different regions of Brazil soon after the European Conquest. We broadened our understanding of the African diaspora, the major destination of which was Brazil, by revealing that Brazilians display two within-Africa ancestry components: one associated with non-Bantu/western Africans (more evident in the Northeast and African Americans) and one associated with Bantu/eastern Africans (more present in the Southeast/South). Furthermore, the whole-genome analysis of 30 individuals (42-fold deep coverage) shows that continental admixture rather than local post-Columbian history is the main and complex determinant of the individual amount of deleterious genotypes.

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