A Nonparametric Test Reveals Selection for Rapid Flowering in the Arabidopsis Genome

Abstract

The detection of footprints of natural selection in genetic polymorphism data is fundamental to understanding the genetic basis of adaptation, and has important implications for human health. The standard approach has been to reject neutrality in favor of selection if the pattern of variation at a candidate locus was significantly different from the predictions of the standard neutral model. The problem is that the standard neutral model assumes more than just neutrality, and it is almost always possible to explain the data using an alternative neutral model with more complex demography. Today's wealth of genomic polymorphism data, however, makes it possible to dispense with models altogether by simply comparing the pattern observed at a candidate locus to the genomic pattern, and rejecting neutrality if the pattern is extreme. Here, we utilize this approach on a truly genomic scale, comparing a candidate locus to thousands of alleles throughout the Arabidopsis thaliana genome. We demonstrate that selection has acted to increase the frequency of early-flowering alleles at the vernalization requirement locus FRIGIDA. Selection seems to have occurred during the last several thousand years, possibly in response to the spread of agriculture. We introduce a novel test statistic based on haplotype sharing that embraces the problem of population structure, and so should be widely applicable.

GWAPP: A Web Application for Genome-Wide Association Mapping in Arabidopsis

“…from Sweepfinder (Nielsen et al, 2005); (3) the pairwise haplotypesharing score (PHS) (Toomajian et al, 2006); (4) a recombination estimate (rho) (McVean et al, 2004); and (5) sequence similarity with Arabidopsis lyrata (Hu et al, 2011). Four of these statistics, Fst, CLR, PHS, and the recombination rate estimate, were calculated using the data set of Horton et al (2012) and may not be representative for the subset being analyzed.…”

Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus

“…The ability to flower at the appropriate time given local environmental conditions can strongly affect plant fitness (2,17). Studies of the molecular variation in FRI support the idea that the molecular variation at this locus has been shaped by adaptive evolution (6,18,19). These studies show that nonfunctional alleles of FRI that result in early flowering have evolved from late-flowering functional alleles through a number of independent loss-of-function mutations (20)(21)(22).…”

“…Although the hypothesis that FRI ⌬ has evolved through adaptive selection to reduce flowering time has strong support from molecular studies (19), the expected latitudinal clines in flowering time mediated by FRI or in its allele frequency are not evident (15). Furthermore, direct evidence for selection at the FRI locus through its effect on flowering time remains elusive (28).…”

Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation

“…Excess nonsynonymous substitutions suggest either that P5CS1 is a recurrent target of selection across the range of Arabidopsis or that selection on the intron 2 and 3 polymorphisms associated with high exon 3-skip P5CS1 has reduced the strength of purifying selection on tightly linked variants. Because tests based on models of sequence evolution can be sensitive to the effects of population structure, we also used the test of Toomajian et al (21) that compares the haplotype structure at a given locus to a genomewide distribution of haplotype lengths. This test provides evidence that selection has acted to increase the frequency of a P5CS1 haplotype in the recent past (pair-wise haplotype sharing score = 1.834, P = 0.059).…”