Eight thousand years of natural selection in Europe

Written by: Stephen Hsu

Primary Source: Information Processing

The latest from the Reich lab at Harvard. The availability of ancient DNA allows for direct comparisons between ancestral and descendant populations. These methods will only become more powerful as technology and access to samples improve.

Note the evidence for polygenic selection on height, over timescales of less than 10k years. (Fig. 3 from paper displayed above.) See also Recent human evolution: European height.

Eight thousand years of natural selection in Europe

The arrival of farming in Europe beginning around 8,500 years ago required adaptation to new environments, pathogens, diets, and social organizations. While evidence of natural selection can be revealed by studying patterns of genetic variation in present-day people, these pattern are only indirect echoes of past events, and provide little information about where and when selection occurred. Ancient DNA makes it possible to examine populations as they were before, during and after adaptation events, and thus to reveal the tempo and mode of selection. Here we report the first genome-wide scan for selection using ancient DNA, based on 83 human samples from Holocene Europe analyzed at over 300,000 positions. We find five genome-wide signals of selection, at loci associated with diet and pigmentation. Surprisingly in light of suggestions of selection on immune traits associated with the advent of agriculture and denser living conditions, we find no strong sweeps associated with immunological phenotypes. We also report a scan for selection for complex traits, and find two signals of selection on height: for short stature in Iberia after the arrival of agriculture, and for tall stature on the Pontic-Caspian steppe earlier than 5,000 years ago. A surprise is that in Scandinavian hunter-gatherers living around 8,000 years ago, there is a high frequency of the derived allele at the EDAR gene that is the strongest known signal of selection in East Asians and that is thought to have arisen in East Asia. These results document the power of ancient DNA to reveal features of past adaptation that could not be understood from analyses of present-day people.

From the paper:

… We also tested for selection on complex traits, which are controlled by many genetic variants, each with a weak effect. Under the pressure of natural selection, these variants are expected to experience small but correlated directional shifts, rather than any single variant changing dramatically in frequency, and recent studies have argued that this may be a predominant mode of natural selection in humans40. The best documented example of this process in humans is height, which has been shown to have been under recent selection in Europe41. At alleles known from GWAS to affect height, northern Europeans have, on average, a significantly higher probability of carrying the height-increasing allele than southern Europeans, which could either reflect selection for increased height in the ancestry of northern Europeans or decreased height in the ancestry of southern Europeans. To test for this signal in our data, we used a statistic that tests whether trait-affecting alleles are more differentiated than randomly sampled alleles, in a way that is coordinated across all alleles consistent with directional selection42. We applied the test to all populations together, as well as to pairs of populations in order to localize the signal (Figure 3, Extended Data Figure 5, Methods).

We detect a significant signal of directional selection on height in Europe (p=0.002), and our ancient DNA data allows us to determine when this occurred and also to determine the direction of selection. Both the Iberian Early Neolithic and Middle Neolithic samples show evidence of selection for decreased height relative to present-day European Americans (Figure 3A; p=0.002 and p < 0.0001, respectively). Comparing populations that existed at the same time (Figure 3B), there is a significant signal of selection between central European and Iberian populations in each of the Early Neolithic, Middle Neolithic and present-day periods (p=0.011, 0.012 and 0.004, respectively). Therefore, the selective gradient in height in Europe has existed for the past 8,000 years. This gradient was established in the Early Neolithic, increased into the Middle Neolithic and decreased at some point thereafter. Since we detect no significant evidence of selection or change in genetic height among Northern European populations, our results further suggest that selection operated mainly on Southern rather than Northern European populations. There is another possible signal in the Yamnaya, related to people who migrated into central Europe beginning at least 4,800 years ago and who contributed about half the ancestry of northern Europeans today9 . The Yamnaya have the greatest predicted genetic height of any population, and the difference between Yamnaya and the Iberian Middle Neolithic is the greatest observed in our data. …

If the analysis leading to the figure below is correct, shifts on the order of 1 SD are possible over timescales less than 10k years, due to natural selection in human populations. Say it with me again: Selection, Not Drift.  (Click for larger version.)

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Stephen Hsu
Stephen Hsu is vice president for Research and Graduate Studies at Michigan State University. He also serves as scientific adviser to BGI (formerly Beijing Genomics Institute) and as a member of its Cognitive Genomics Lab. Hsu’s primary work has been in applications of quantum field theory, particularly to problems in quantum chromodynamics, dark energy, black holes, entropy bounds, and particle physics beyond the standard model. He has also made contributions to genomics and bioinformatics, the theory of modern finance, and in encryption and information security. Founder of two Silicon Valley companies—SafeWeb, a pioneer in SSL VPN (Secure Sockets Layer Virtual Private Networks) appliances, which was acquired by Symantec in 2003, and Robot Genius Inc., which developed anti-malware technologies—Hsu has given invited research seminars and colloquia at leading research universities and laboratories around the world.