Statistical evaluation of alternative models of human evolution

Abstract

An appropriate model of recent human evolution is not only important to understand our own history, but it is necessary to disentangle the effects of demography and selection on genome diversity. Although most genetic data support the view that our species originated recently in Africa, it is still unclear if it completely replaced former members of the Homo genus, or if some interbreeding occurred during its range expansion. Several scenarios of modern human evolution have been proposed on the basis of molecular and paleontological data, but their likelihood has never been statistically assessed. Using DNA data from 50 nuclear loci sequenced in African, Asian and Native American samples, we show here by extensive simulations that a simple African replacement model with exponential growth has a higher probability (78%) as compared with alternative multiregional evolution or assimilation scenarios. A Bayesian analysis of the data under this best supported model points to an origin of our species approximately 141 thousand years ago (Kya), an exit out-of-Africa approximately 51 Kya, and a recent colonization of the Americas approximately 10.5 Kya. We also find that the African replacement model explains not only the shallow ancestry of mtDNA or Y-chromosomes but also the occurrence of deep lineages at some autosomal loci, which has been formerly interpreted as a sign of interbreeding with Homo erectus.

Fig. 1.

Alternative scenarios of human evolution. (A) African replacement models: AFRIG, African replacement with instantaneous population growth; AFREG, African replacement with exponential population growth. (B) Assimilation models: ASIG, assimilation with instantaneous population growth; ASEG, assimilation with exponential population growth. (C) Multiregional evolution (MRE) models: MRE1S, MRE with constant population size in Africa/Asia; MRE2S, MRE with two population sizes in Africa/Asia; MREBIG, MRE with bottleneck and instantaneous population growth; MREBEG, MRE with bottleneck and exponential population growth. For all models, the dark grays represent modern human populations, and lighter grays represent archaic populations. AF, Africa; AS, Asia; AM, Americas. A more detailed description of these models is provided in Materials and Methods and in SI Fig. 3. The posterior probability of different models within each major scenario is given below each model. The posterior probabilities of the best model selected under each scenario are reported within boxes.

Fig. 2.

Empirical TMRCA distribution obtained by simulation under different models. Parameter values were set to the median of the estimated marginal posterior distributions. Each distribution combines a mirrored estimated density surface in gray with a standard boxplot representation. Boxplots display the median of the distribution as a white dot, the interquartile range (IQR, 25–75%) as a thick line, and the region of ±1.5 IQR as a thin line ending with vertical whiskers. To facilitate the comparison among models, all distributions (apart those from MREBIG model) were cut after the 99th percentile (full distributions are available in SI Tables 6, 7, and 8). (A) Autosomal loci. (B) Autosomal loci under the best model (AFREG), where only the samples of each of the three regions are considered. (C) mtDNA and Y-chromosome. For these markers, simulations were performed by using estimates of effective sizes four times smaller than those obtained for autosomal loci to reflect the smaller population sizes of these uniparentally inherited markers.