Recent acceleration of human adaptive evolution

Abstract

Genomic surveys in humans identify a large amount of recent positive selection. Using the 3.9-million HapMap SNP dataset, we found that selection has accelerated greatly during the last 40,000 years. We tested the null hypothesis that the observed age distribution of recent positively selected linkage blocks is consistent with a constant rate of adaptive substitution during human evolution. We show that a constant rate high enough to explain the number of recently selected variants would predict (i) site heterozygosity at least 10-fold lower than is observed in humans, (ii) a strong relationship of heterozygosity and local recombination rate, which is not observed in humans, (iii) an implausibly high number of adaptive substitutions between humans and chimpanzees, and (iv) nearly 100 times the observed number of high-frequency linkage disequilibrium blocks. Larger populations generate more new selected mutations, and we show the consistency of the observed data with the historical pattern of human population growth. We consider human demographic growth to be linked with past changes in human cultures and ecologies. Both processes have contributed to the extraordinarily rapid recent genetic evolution of our species.

Fig. 1.

Age distribution of ascertained selected alleles. Each point represents the number of variants dated to a single 10-generation bin. Fitted curves are the number of ascertained variants predicted by Eq. 2 under a constant population size and constant s̄ = 0.022 for YRI and s̄ = 0.034 for CEU. The distribution drops to zero approaching the present, because all alleles have frequencies >22% today. The 2,965 (YRI) and 2,246 (CEU) selection ages shown have had 509 alleles removed that are likely examples of ongoing balanced selection (SI Appendix). Including these alleles in the analysis does not change the overall conclusion of acceleration of selection.

Fig. 2.

Historic and prehistoric population size estimates for human populations (SI Appendix). Key features are the larger ancestral African population size and the earlier Neolithic growth in core agricultural areas.

Fig. 3.

Tip of the iceberg. Both the demographic and constant-rate models can account for the age distribution of ascertained variants (CEU data shown), but they differ greatly in the expected number of variants above the ascertainment frequency (fixed or near-fixed). The demographic model predicts a low long-term substitution rate and few alleles >78%, consistent with the observed data.