Cultural innovations influence patterns of genetic diversity in Northwestern Amazonia

Human populations often exhibit contrasting patterns of genetic diversity in the mtDNA and the non-recombining portion of the Y-chromosome (NRY), which reflect sex-specific cultural behaviors and population histories. Here, we sequenced 2.3 Mb of the NRY from 284 individuals representing more than 30 Native-American groups from Northwestern Amazonia (NWA) and compared these data to previously generated mtDNA genomes from the same groups, to investigate the impact of cultural practices on genetic diversity and gain new insights about NWA population history. Relevant cultural practices in NWA include postmarital residential rules and linguistic-exogamy, a marital practice in which men are required to marry women speaking a different language. We identified 2,969 SNPs in the NRY sequences; only 925 SNPs were previously described. The NRY and mtDNA data showed that males and females experienced different demographic histories: the female effective population size has been larger than that of males through time, and both markers show an increase in lineage diversification beginning ~5,000 years ago, with a male-specific expansion occurring ~3,500 years ago. These dates are too recent to be associated with agriculture, therefore we propose that they reflect technological innovations and the expansion of regional trade networks documented in the archaeological evidence. Furthermore, our study provides evidence of the impact of postmarital residence rules and linguistic exogamy on genetic diversity patterns. Finally, we highlight the importance of analyzing high-resolution mtDNA and NRY sequences to reconstruct demographic history, since this can differ considerably between males and females.