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 highfrequency 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.HapMap ͉ linkage disequilibrium ͉ Neolithic ͉ positive selection H uman populations have increased vastly in numbers during the past 50,000 years or more (1). In theory, more people means more new adaptive mutations (2). Hence, human population growth should have increased in the rate of adaptive substitutions: an acceleration of new positively selected alleles.Can this idea really describe recent human evolution? There are several possible problems. Only a small fraction of all mutations are advantageous; most are neutral or deleterious. Moreover, as a population becomes more and more adapted to its current environment, new mutations should be less and less likely to increase fitness. Because species with large population sizes reach an adaptive peak, their rate of adaptive evolution over geologic time should not greatly exceed that of rare species (3).But humans are in an exceptional demographic and ecological transient. Rapid population growth has been coupled with vast changes in cultures and ecology during the Late Pleistocene and Holocene, creating new opportunities for adaptation. The past 10,000 years have seen rapid skeletal and dental evolution in human populations and the appearance of many new genetic responses to diets and disease (4).In such a transient, large population, size increases the rate and effectiveness of adaptive responses. For example, natural insect populations often produce effective monogenic resistance to pesticides, whereas small laboratory populations under similar selection develop less effective polygenic adaptations (5). Chemostat experiments on Escherichia coli show a continued response to selection (6), with continuous and repeatable responses in large populations but variable and episodic responses in small populations (7). These results are explained by a model in...

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