Inferring the demographic history and rate of adaptive substitution in Drosophila

Abstract

An important goal of population genetics is to determine the forces that have shaped the pattern of genetic variation in natural populations. We developed a maximum likelihood method that allows us to infer demographic changes and detect recent positive selection (selective sweeps) in populations of varying size from DNA polymorphism data. Applying this approach to single nucleotide polymorphism data at more than 250 noncoding loci on the X chromosome of Drosophila melanogaster from an (ancestral) African population and a (derived) European, we found that the African population expanded about 60,000 y ago and that the European population split off from the African lineage about 15,800 y ago, thereby suffering a severe population size bottleneck. We estimated that about 160 beneficial mutations (with selection coefficients s between 0.05% and 0.5%) were fixed in the euchromatic portion of the X in the African population since population size expansion, and about 60 mutations (with s around 0.5%) in the diverging European lineage.

Figure 1. Demographic Models of the African and European Populations

(A) The demographic histories are plotted together. (B) The demographic histories are plotted for both populations separately. (C) The joint MFS for an example genealogy where the sample size of European lines (indicated by E) is 3, and that of African lines (A) is 4. ω_ij is the number of mutations carried by i chromosomes of the African sample and by j chromosomes of the European sample.

Figure 2. Watterson's θ_W versus Divergence between D. melanogaster and D. simulans

Pearson's r = 0.65, p < 0.01 in the African sample; Pearson's r = 0.40, p < 0.01 in the European sample. In the African sample, 13 loci are circled because of their high divergence and low θ_W.

Figure 3. Comparisons of MFS

For the European population, the expected MFSs under our estimated bottleneck scenario and a previously proposed bottleneck scenario [24] are plotted.

Figure 4. Evaluation of the Demographic Scenarios for the African and European Populations

The standard deviation (SD) of a summary statistic is calculated as the standard deviation among loci. The values of the solid bars are obtained from the data. VMR, varying mutation rate model; CMR, constant mutation rate model. The 95% CI of the SD of each summary statistic obtained from 10³ simulated datasets is also given.

Figure 5. The Frequency Spectrum of Selection Coefficients (s) for Recent Positive Selection in the African and European Populations

The y-axis shows the rate of adaptive substitution with an s value in (s₁, s₂) if all selectively driven substitutions occur in coding regions. The 95% likelihood-based CIs are given as error bars.