A reevaluation of the Native American mtDNA genome diversity and its bearing on the models of early colonization of Beringia

Abstract

The Americas were the last continents to be populated by humans, and their colonization represents a very interesting chapter in our species' evolution in which important issues are still contentious or largely unknown. One difficult topic concerns the details of the early peopling of Beringia, such as for how long it was colonized before people moved into the Americas and the demography of this occupation. A recent work using mitochondrial genome (mtDNA) data presented evidence for a so called "three-stage model" consisting of a very early expansion into Beringia followed by approximately 20,000 years of population stability before the final entry into the Americas. However, these results are in disagreement with other recent studies using similar data and methods. Here, we reanalyze their data to check the robustness of this model and test the ability of Native American mtDNA to discriminate details of the early colonization of Beringia. We apply the Bayesian Skyline Plot approach to recover the past demographic dynamic underpinning these events using different mtDNA data sets. Our results refute the specific details of the "three-stage model", since the early stage of expansion into Beringia followed by a long period of stasis could not be reproduced in any mtDNA data set cleaned from non-Native American haplotypes. Nevertheless, they are consistent with a moderate population bottleneck in Beringia associated with the Last Glacial Maximum followed by a strong population growth around 18,000 years ago as suggested by other recent studies. We suggest that this bottleneck erased the signals of ancient demographic history from recent Native American mtDNA pool, and conclude that the proposed early expansion and occupation of Beringia is an artifact caused by the misincorporation of non-Native American haplotypes.

Figure 1. Bayesian Skyline Plots using different sequence sets.

BSPs estimated with 100 million MCMC iterations sampled every 2,500 steps using log-normal relaxed clock and HKY model plus gamma (eight categories) with the standard substitution rate of 1.26×10⁻⁸ sites/yr and a generation time of 25 yr. The y axis represents the female effective population size in a log scale and the x axis shows time in thousands of years ago (kya). The thicker blue lines are the median for population size and the thinner black lines represent the 95% higher posterior density (HPD) intervals. (A) BSP using the original 77 individuals from . (B) BSP for the nine misincorporated non-Native American sequences. (C) BSP for the 68 confirmed Native American haplotypes in in blue and black; and the BSP from in red dashed (median) and gray lines (95% HPD interval).

Figure 2. Bayesian Skyline Plot for ten replicates of nine random non-African haplotypes.

Ten BSPs using random samples of nine non-African individuals from belonging to macrohaplogroups M and N, showing a similar pattern of expansion between ∼80 and ∼40 kya. All BSPs were calculated with 100 million MCMC generations sampling every 2,500 using the same model applied to the BSPs in Figure 1. Axes and lines are as in Figure 1.