Population size changes reshape genomic patterns of diversity

Abstract

Elucidating the forces responsible for genomic variation is critical for understanding evolution. Under standard conditions, X-linked diversity is expected to be three-quarters the level of autosomal diversity. Empirical data often deviate from this prediction, but the reasons for these departures are unclear. We demonstrate that population size changes can greatly alter relative levels of X-linked and autosomal variation: population size reductions lead to particularly low X-linked diversity, whereas growth elevates X-linked relative to autosomal diversity. Genetic variation from a diverse array of taxa supports an important role for this effect in accounting for population differences in the ratio of X-linked to autosomal diversity. Consideration of this effect may improve the inference of population history and other evolutionary processes.

Figure 1. Predictions of the population size change model for X/A diversity ratios

Predicted ratio of X chromosome to autosome diversity for a population with initial N = 10,000 following (A) population reduction, (B) population growth, or (C) population bottleneck lasting 100 generations. In each plot, the x-axis indicates the number of generations since this event (g), the y-axis indicates the magnitude of the size change (in terms of f for population growth, or 1/f for population reductions and bottlenecks; see equations for details), and color depicts the X/A diversity ratio (see scale).

Figure 2. Recovery of variation after a population bottleneck

Expected diversity through time following a population bottleneck (relative to pre-bottleneck levels) is shown separately for autosomal, X-linked, and uniparentally inherited chromosomes (mt/Y). In this bottleneck, a population of N = 10,000 experiences a population size reduction to f = 0.004 times this size, lasting for g₂ = 100 generations until recovery to the initial size.

Figure 3. Reduced X/A diversity ratios in less variable populations

Bars indicate the X/A diversity ratios of more genetically diverse (gray) and less genetically diverse (black) populations of Homo sapiens (Human), Pan Troglodytes (Chimp), Pongo pygmaeus (Orang), Mus musculus castaneus (Mmc), Mus musculus domesticus (Mmd), Mus musculus musculus (Mmm), Drosophila melanogaster (Dmel), and Drosophila simulans (Dsim). Information regarding the data can be found in the Supplemental Text.