Indigenous peoples in eastern Brazil: insights from 19^th century genomes and metagenomes

Abstract

Although Brazil was inhabited by more than 3,000 Indigenous populations prior to European colonization, today’s Indigenous peoples represent less than 1% of Brazil’s census population. Some of the decimated communities belonged to the so-called “Botocudos” from central-eastern Brazil. These peoples are thought to represent a case of long-standing genetic continuity bearing a strong craniometric resemblance to that of the oldest Indigenous Americans (“Paleoamericans”). Yet, little is known about their origins and genetic relationship to other Native Americans, as only two “Botocudo” genomes have been sequenced so far and those were surprisingly of Polynesian ancestry. To deepen our knowledge on the genomic history of pre-contact Indigenous Americans and the pathogens they were exposed to, we carbon-dated and sequenced 24 ancient Brazilians (including 22 “Botocudos”) whose remains were hosted at the National Museum of Rio de Janeiro and recovered prior to the tragic 2018 fire. The resulting genomes’ depth of coverage ranged from 0.001× to 24×. Their genetic ancestry was found to be Indigenous American without gene flow from external populations such as Europeans, Africans or Polynesians. Unlike Mesoamericans, the “Botocudos” and Amazonians do not seem to have experienced a population expansion once in the Americas. Moreover, remarkably, their genomes exhibit amongst the lowest levels of heterozygosity worldwide and long runs of homozygosity, which could be explained by unique social practices or a very small effective size. Finally, whole genomes of likely ancient pathogens were recovered, including lineages of Human parvovirus B19 that were possibly introduced after the European contact.