Genomic insight into the origins and dispersal of the Brazilian coastal natives

Abstract

In the 15th century, ∼900,000 Native Americans, mostly Tupí speakers, lived on the Brazilian coast. By the end of the 18th century, the coastal native populations were declared extinct. The Tupí arrived on the east coast after leaving the Amazonian basin ∼2,000 y before present; however, there is no consensus on how this migration occurred: toward the northern Amazon and then directly to the Atlantic coast, or heading south into the continent and then migrating to the coast. Here we leveraged genomic data from one of the last remaining putative representatives of the Tupí coastal branch, a small, admixed, self-reported Tupiniquim community, as well as data of a Guaraní Mbyá native population from Southern Brazil and of three other native populations from the Amazonian region. We demonstrated that the Tupiniquim Native American ancestry is not related to any extant Brazilian Native American population already studied, and thus they could be considered the only living representatives of the extinct Tupí branch that used to settle the Atlantic Coast of Brazil. Furthermore, these data show evidence of a direct migration from Amazon to the Northeast Coast in pre-Columbian time, giving rise to the Tupí Coastal populations, and a single distinct migration southward that originated the Guaraní people from Brazil and Paraguay. This study elucidates the population dynamics and diversification of the Brazilian natives at a genomic level, which was made possible by recovering data from the Brazilian coastal population through the genomes of mestizo individuals.

Genetic admixture in Brazil

“…These demographic differences between Andeans (Quechuans and Aymarans) and other South American indigenous populations have been recurrently corroborated by different studies (Barbieri et al, 2014, 2019; Jota et al, 2011, 2016), and are part of a complex population dynamics in pre‐Columbian times involving fission‐fusion processes (Neel & Salzano, 1967), demographic expansions (Castro e Silva et al, 2020; Ramallo et al, 2013) and differentiation in isolation associated to culture (Hünemeier et al, 2012).…”

“…Tarazona-Santos et al (2001) suggested that cultural differences like farming and the complex hierarchy of the Andean civilization should have driven a larger gene flow between populations located even 4,000 km apart, while this contact was more restrict in other landscapes, like Amazonia. These demographic differences between Andeans (Quechuans and Aymarans) and other South American indigenous populations have been recurrently corroborated by different studies (Barbieri et al, 2014(Barbieri et al, , 2019Jota et al, 2011Jota et al, , 2016, and are part of a complex population dynamics in pre-Columbian times involving fission-fusion processes (Neel & Salzano, 1967), demographic expansions (Castro e Silva et al, 2020;Ramallo et al, 2013) and differentiation in isolation associated to culture (Hünemeier et al, 2012).…”

“…Unfortunately, most of the pre‐Columbian diversity of peoples (and history) was lost in the last 500 years (Denevan, 1992; Rodrigues, 1993). Some entire indigenous groups and their languages were almost completely lost, as exemplified by the sad story of the once very numerous Tupi speakers of the Brazilian coast, who have been reduced to few remaining Guarani speakers in southeastern Brazil (Castro e Silva et al, 2020).…”

Roadmap for Establishing Large-Scale Genomic Medicine Initiatives in Low- and Middle-Income Countries

“…With a ; yellow, Epigen-Brazil initiative; 28 gray, Baependi Heart Study; 29 red, Native American/ Tupí-Guarani. 30 limited budget available in resourcelimited settings, it would also be highly recommended that in parallel with the genomes that are sequenced, the rest of the interested participants could be genotyped by high-definition microarrays that would allow researchers to evaluate the common genomic structure, to create selected pharmacogenomics data, and to model disease polygenic scores. This genomic information can be readily applicable in primary care and first line interventions, such as in screening programs.…”

“…Geographic Distribution of Some of the Ongoing Cohort Studies within BrazilColored circles indicate states where cohorts of Brazilians are followed in the different studies. Blue, ELSA-Brazil;26 green, Brazilian Longitudinal Study of Aging (ELSI-Brazil 27 ); yellow, Epigen-Brazil initiative;28 gray, Baependi Heart Study;29 red, Native American/ Tupí-Guarani 30.…”