Toward a new history and geography of human genes informed by ancient DNA

Abstract

Genetic information contains a record of the history of our species, and technological advances have transformed our ability to access this record. Many studies have used genome-wide data from populations today to learn about the peopling of the globe and subsequent adaptation to local conditions. Implicit in this research is the assumption that the geographic locations of people today are informative about the geographic locations of their ancestors in the distant past. However, it is now clear that long-range migration, admixture, and population replacement subsequent to the initial out-of-Africa expansion have altered the genetic structure of most of the world's human populations. In light of this we argue that it is time to critically reevaluate current models of the peopling of the globe, as well as the importance of natural selection in determining the geographic distribution of phenotypes. We specifically highlight the transformative potential of ancient DNA. By accessing the genetic make-up of populations living at archaeologically known times and places, ancient DNA makes it possible to directly track migrations and responses to natural selection.

Figure 1. A negative correlation between heterozygosity and geographic distance from a source population can be generated by qualitatively different, historically plausible demographic models

We simulated genetic data under different demographic models and calculated the average heterozygosity in each simulated population. A. Schematic of a serial founder effect model. B. Schematic of a demographic model with two bottlenecks and extensive admixture. C. Schematic of a demographic model with no bottlenecks and extensive admixture. D,E,F. Average heterozygosity in each population simulated under the demographic models in A,B, and C respectively. Each point represents a population, ordered along the x-axis according as in A.

Figure 2

A rough guide to genetically documented population movements in the history of anatomically modern humans.

Figure 3. A birds-eye view of admixture in human populations

We performed a three-population test for admixture (Reich et al., 2009) on 103 worldwide populations. Circles show the approximate current geographic locations of all tested populations (except for populations in the Americas, which are not plotted for ease of display). Filled circles represent populations identified as admixed, and the colors represent the current geographic labels of the inferred admixing populations. Empty circles represent populations with no statistically-significant evidence for admixture in this test.

Figure 4. Time series allow tests of different models of human history

A. Different scenarios for the dynamics of gene flow. We show idealized time series of admixture proportions in a population under models of continuous gene flow and discrete admixture. B. Selection in the presence of admixture. We show idealized time series of the allele frequencies at a selected allele and admixture proportions in a population. Note that despite selection the allele does not show any net change in frequency.