Natural Selection in the Great Apes

Abstract

Natural selection is crucial for the adaptation of populations to their environments. Here, we present the first global study of natural selection in the Hominidae (humans and great apes) based on genome-wide information from population samples representing all extant species (including most subspecies). Combining several neutrality tests we create a multi-species map of signatures of natural selection covering all major types of natural selection. We find that the estimated efficiency of both purifying and positive selection varies between species and is significantly correlated with their long-term effective population size. Thus, even the modest differences in population size among the closely related Hominidae lineages have resulted in differences in their ability to remove deleterious alleles and to adapt to changing environments. Most signatures of balancing and positive selection are species-specific, with signatures of balancing selection more often being shared among species. We also identify loci with evidence of positive selection across several lineages. Notably, we detect signatures of positive selection in several genes related to brain function, anatomy, diet and immune processes. Our results contribute to a better understanding of human evolution by putting the evidence of natural selection in humans within its larger evolutionary context. The global map of natural selection in our closest living relatives is available as an interactive browser at http://tinyurl.com/nf8qmzh.

Keywords: adaptation; comparative genomics; evolution; primates..

Fig. 1.

Timescale of neutrality tests. Hominidae phylogeny with the approximate time ranges where each neutrality test has power to detect signatures of natural selection. (a) The lineages with the number of genomes used in this study are shown on the right. The X-axis shows the timescale, in units of millions of years. Split times of lineages from Prado-Martinez et al. (2013). For FWH, MK and HKA, the approximate time range where the tests are inferred to have most power to detect selection are represented by color intensity. For ELS, we label in green the branches where the test has power to detect selection. n: number of individuals in each lineage. Ne: estimates of effective population size in units of thousands of individuals according to Watterson’s estimator, taken from Prado-Martinez et al. (2013).

Fig. 2.

Summary of the neutrality tests used. Each box presents the input (the information used), the analysis strategy (how each test was applied on the genome-wide data), the pattern (the signatures of selection explored), the criteria to select selection candidates (the top candidates for each test) and the criteria to select candidates for GO analyses (the candidate used for gene ontology analyses).

Fig. 3.

Percentage of windows overlapping protein coding exons. Percentage of windows overlapping protein coding exons for noncumulative bins of the HKA empirical distribution (X-axis). Each lineage is plotted as a shaded line. The Pearson’s correlation (R) between the percentage of windows overlapping protein coding exons and Ne within each HKA bin and across all lineages is shown on the right Y-axis. Pearson’s correlation coefficient was computed both with an estimate of short- and long-term Ne (from Prado-Martinez et al. 2013). Only R values with significant P values (P <0.05) are shown.

Fig. 4.

Correlation between rate of adaptive substitutions (α) and effective population size (Ne). The X-axis shows the effective population size. On the Y-axis, the rate of adaptive substitutions is plotted as α. Correlations were calculated while controlling for the phylogenetic nonindependence using a generalized least square approach and a random walk/maximum likelihood method (see Supplementary Materials MK 2.3, Supplementary Material online).

Fig. 5.

Venn Diagram of shared targets of balancing and positive selection among Pan troglodytes lineages. Overlap of the number of putative target genes of balancing and positive selection as inferred by the HKA test for all P. troglodytes lineages.