Cultural Innovations Influence Patterns of Genetic Diversity in Northwestern Amazonia

Abstract

Human populations often exhibit contrasting patterns of genetic diversity in the mtDNA and the nonrecombining 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 of which were previously described. The NRY and mtDNA data showed different sex-specific demographic histories: female effective population size has been larger than that of males through time, which might reflect larger variance in male reproductive success. Both markers show an increase in lineage diversification beginning ∼5,000 years ago, which may reflect the intensification of agriculture, technological innovations, and the expansion of regional trade networks documented in the archaeological evidence. Furthermore, we find similar excesses of NRY versus mtDNA between-population divergence at both the local and continental scale, suggesting long-term stability of female versus male migration. We also find evidence of the impact of sociocultural practices on diversity patterns. Finally, our study highlights the importance of analyzing high-resolution mtDNA and NRY sequences to reconstruct demographic history, since this can differ considerably between sexes.

Fig. 1.

Molecular diversity indices for the mtDNA and NRY in 17 groups of NWA. (A) Gene diversity. (B) Mean number of pairwise differences. (C) Number of segregating sites. (D) Tajima’s D values. Dotted lines represent the average diversity values across all groups. Population names are color-coded by language family as indicated in the legend. Values for the NRY after removing sequences belonging to haplogroup C2 are shown next to Guayabero and Mur-Uitoto, the only groups carrying these sequences. Stars indicate the matrilocal groups.

Fig. 2.

Distribution of the mean values for: (A) Φ_STs, (B) haplotype diversity, and (C) MPD for all possible triplets (n = 286) of patrilocal groups for the mtDNA (left) and NRY (right). The mean values for matrilocal groups are shown as dotted lines. One-side P values reported after Benjamin–Hochberg correction for multiple comparisons.

Fig. 3.

Shared haplotypes between pairs of populations for the mtDNA (left) and NRY (right).

Fig. 4.

Histograms and cumulative fraction of the number of coalescent events through time for the mtDNA (left) and NRY (right).

Fig. 5.

BSPs for the mtDNA and NRY sequences from NWA. The dotted lines indicate the 95% HPD intervals. Ne was corrected for generation time according to (Fenner 2005), using 26 years for mtDNA and 31 years for NRY.

Fig. 6.

(A) Nucleotide diversity and (B) AMOVA results in NWA and a sample of the Americas (AM) for the mtDNA and the NRY. Dotted lines represent the percentage of among population variation reported by Lippold et al. (2014) for the Americas.