Continent-Wide Decoupling of Y-Chromosomal Genetic Variation from Language and Geography in Native South Americans

Lutz Roewer, Michael Nothnagel, Leonor Gusmão, Veronica Gomes, Miguel González, Daniel Corach, Andrea Sala, Evguenia Alechine, Teresinha Palha, Ney Santos, Andrea Ribeiro-dos-Santos, Maria Geppert, Sascha Willuweit, Marion Nagy, Sarah Zweynert, Miriam Baeta, Carolina Núñez, Begoña Martínez-Jarreta, Fabricio González-Andrade, Elizeu Fagundes de CarvalhoDayse Aparecida da Silva, Juan José Builes, Daniel Turbón, Ana Maria Lopez Parra, Eduardo Arroyo-Pardo, Ulises Toscanini, Lisbeth Borjas, Claudia Barletta, Elizabeth Ewart, Sidney Santos, Michael Krawczak

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Abstract

Numerous studies of human populations in Europe and Asia have revealed a concordance between their extant genetic structure and the prevailing regional pattern of geography and language. For native South Americans, however, such evidence has been lacking so far. Therefore, we examined the relationship between Y-chromosomal genotype on the one hand, and male geographic origin and linguistic affiliation on the other, in the largest study of South American natives to date in terms of sampled individuals and populations. A total of 1,011 individuals, representing 50 tribal populations from 81 settlements, were genotyped for up to 17 short tandem repeat (STR) markers and 16 single nucleotide polymorphisms (Y-SNPs), the latter resolving phylogenetic lineages Q and C. Virtually no structure became apparent for the extant Y-chromosomal genetic variation of South American males that could sensibly be related to their inter-tribal geographic and linguistic relationships. This continent-wide decoupling is consistent with a rapid peopling of the continent followed by long periods of isolation in small groups. Furthermore, for the first time, we identified a distinct geographical cluster of Y-SNP lineages C-M217 (C3*) in South America. Such haplotypes are virtually absent from North and Central America, but occur at high frequency in Asia. Together with the locally confined Y-STR autocorrelation observed in our study as a whole, the available data therefore suggest a late introduction of C3* into South America no more than 6,000 years ago, perhaps via coastal or trans-Pacific routes. Extensive simulations revealed that the observed lack of haplogroup C3* among extant North and Central American natives is only compatible with low levels of migration between the ancestor populations of C3* carriers and non-carriers. In summary, our data highlight the fact that a pronounced correlation between genetic and geographic/cultural structure can only be expected under very specific conditions, most of which are likely not to have been met by the ancestors of native South Americans. © 2013 Roewer et al.
Original languageAmerican English
JournalPLoS Genetics
DOIs
StatePublished - 1 Apr 2013

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    Roewer, L., Nothnagel, M., Gusmão, L., Gomes, V., González, M., Corach, D., Sala, A., Alechine, E., Palha, T., Santos, N., Ribeiro-dos-Santos, A., Geppert, M., Willuweit, S., Nagy, M., Zweynert, S., Baeta, M., Núñez, C., Martínez-Jarreta, B., González-Andrade, F., ... Krawczak, M. (2013). Continent-Wide Decoupling of Y-Chromosomal Genetic Variation from Language and Geography in Native South Americans. PLoS Genetics. https://doi.org/10.1371/journal.pgen.1003460