Evidence of widespread selection on standing variation in Europe at height-associated SNPs

Abstract

Strong signatures of positive selection at newly arising genetic variants are well-documented in humans1–8, but this form of selection may not be widespread in recent human evolution9. Because many human traits are highly polygenic and partly determined by common, ancient genetic variation, an alternative model for rapid genetic adaptation has been proposed: weak selection acting on many pre-existing (standing) genetic variants, or polygenic adaptation10–12. By studying height, a classic polygenic trait, we demonstrate the first human signature of widespread selection on standing variation. We show that frequencies of alleles associated with increased height, both at known loci and genome-wide, are systematically elevated in Northern Europeans compared with Southern Europeans (p<4.3×10−4). This pattern mirrors intra-European height differences and is not confounded by ancestry or other ascertainment biases. The systematic frequency differences are consistent with the presence of widespread weak selection (selection coefficients ~10−3–10−5 per allele) rather than genetic drift alone (p<10−15).

Does natural selection favour taller stature among the tallest people on earth?

“…Although our findings are suggestive of selection on height, and are in line with genetic evidence regarding past selection on stature in Northern Europe [28], we do not present direct evidence for natural selection. The phenotypic correlation we observe can be caused by both environmental and/or genetic factors, and we can infer the degree of natural selection only to the extent to which genetic effects on both traits correlate [29].…”

Evolutionary and Ecological Responses to Anthropogenic Climate Change

“…Concordant with changes in the climate over that time frame, tropical alleles shifted into temperate populations, potentially representing a genetic response to climate change (Umina et al, 2005). In humans, Turchin et al (2012) found strong evidence for selective changes in allele frequencies at hundreds of height-associated loci in European populations. This study illustrates both the potential for such analyses and the massive work required for successful dissection of complex trait variation.…”

“…For polygenic quantitative traits (Rockman, 2012), genomic approaches could be used to detect subtle changes at multiple loci of small effect (Hansen et al, 2012;Turchin et al, 2012). Continuing advancements in genomic technologies and bioinformatics will improve our understanding of climatic adaptation in model (Fournier-Level et al, 2011;Hancock et al, 2011) and nonmodel (Allendorf et al, 2010) organisms.…”

“…Next-generation sequencing will soon provide researchers with ample molecular markers even in nonmodel organisms to estimate population structure and migration rates more accurately (Allendorf et al, 2010). Although we have sketched an ambitious research program that pushes the limits of current knowledge and technology, rapid progress on similar approaches in human populations (Skoglund et al, 2012;Turchin et al, 2012) illustrates the possibilities for studying genetic responses to climate change.…”

Lakes and ponds as model systems to study parallel evolution

“…This especially in the view that most traits of ecological importance are likely to be polygenic (Falconer and Mackay, 1996;Hill and Kirkpatrick, 2010;Yang et al, 2010), and thereby likely to be weakly selected at the level of individual loci (Turchin et al, 2012). Hence, it seems possible that the likelihood of parallel genetic differentiation in small populations could decrease with the increasing number of genes coding for a given trait.…”