Selection for population-specific adaptation shaped patterns of variation in the photoperiod pathway genes in Arabidopsis lyrata during post-glacial colonization.

Spatially varying selection can lead to population-specific adaptation, which is often recognized at the phenotypic level; however, the genetic evidence is weaker in many groups of organisms. In plants, environmental shifts that occur due to colonization of a novel environment may require adaptive changes in the timing of growth and flowering, which are often governed by location-specific environmental cues such as day length. We studied locally varying selection in 19 flowering time loci in nine populations of the perennial herb Arabidopsis lyrata, which has a wide but patchy distribution in temperate and boreal regions of the northern hemisphere. The populations differ in their recent population demographic and colonization histories and current environmental conditions, especially in the growing season length. We searched for population-specific molecular signatures of directional selection by comparing a set of candidate flowering time loci with a genomic reference set within each population using multiple approaches and contrasted the patterns of different populations. The candidate loci possessed approximately 20% of the diversity of the reference loci. On average the flowering time loci had more rare alleles (a smaller Tajima's D) and an excess of highly differentiated sites relative to the reference, suggesting positive selection. The strongest signal of selection was detected in photoperiodic pathway loci in the colonizing populations of Northwestern Europe, whereas no evidence of positive selection was detected in the Central European populations. These findings emphasized the population-specific nature of selection and suggested that photoperiodic adaptation was important during postglacial colonization of the species.

A recent local sweep at the PHYA locus in the Northern European Spiterstulen population of Arabidopsis lyrata.

Northern and central European Arabidopsis lyrata ssp. petraea populations are locally adapted to prevailing climatic conditions through differences in timing of life history events. The timing of flowering and, in perennials, the timing of growth cessation influence fitness. Phytochrome A may have an important role in regulating these life history traits as it perceives changes in daylength. We asked whether PHYA has contributed to local adaptation to the northern conditions in A. l. petraea. To search for signals of directional selection at the PHYA locus, we resequenced PHYA and 9 short fragments around PHYA from a 57-kb region from a German (Plech) and a Norwegian (Spiterstulen) population and compared patterns of differentiation and diversity to a set of 19 reference loci around the genome. First, we found that the populations were highly differentiated: there were three nonsynonymous fixed differences at the PHYA locus, which was in stark contrast with the total four fixed differences in the 19 reference loci. Compatible with a sweep hypothesis, variation was almost completely removed from the 9.4-kb region around PHYA in the northern Spiterstulen population. The overall level of linkage disequilibrium (LD) was higher in Spiterstulen, but there was no LD across the PHYA locus in the population, which is also a known consequence of a selective sweep. The sweep has likely occurred after the last glacial maximum, which suggests that it has contributed to adaptation to the northern conditions.

Role of vernalization and of duplicated FLOWERING LOCUS C in the perennial Arabidopsis lyrata.

FLOWERING LOCUS C (FLC) is one of the main genes influencing the vernalization requirement and natural flowering time variation in the annual Arabidopsis thaliana. Here we studied the effects of vernalization on flowering and its genetic basis in the perennial Arabidopsis lyrata. Two tandemly duplicated FLC genes (FLC1 and FLC2) were compared with respect to expression and DNA sequence. The effect of vernalization on flowering and on the expression of FLC1 was studied in three European populations. The genetic basis of the FLC1 expression difference between two of the populations was further studied by expression quantitative trait locus (eQTL) mapping and sequence analysis. FLC1 was shown to have a likely role in the vernalization requirement for flowering in A. lyrata. Vernalization decreased its expression and the northern study populations showed higher FLC1 expression than the southern one. eQTL mapping between two of the populations revealed one eQTL affecting FLC1 expression in the genomic region containing the FLC genes. Most FLC1 sequence differences between the study populations were found in the promoter region and in the first intron. Variation in the FLC1 sequence may cause differences in FLC1 expression between late- and early-flowering A. lyrata populations.

Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism.

Species share homologous genes to a large extent, but it is not yet known to what degree the same loci have been targets for natural selection in different species. Natural variation in flowering time is determined to a large degree by 2 genes, FLOWERING LOCUS C and FRIGIDA, in Arabidopsis thaliana. Here, we examine whether FRIGIDA has a role in differences in flowering time between and within natural populations of Arabidopsis lyrata, a close outcrossing perennial relative of A. thaliana. We found 2 FRIGIDA sequence variants producing potentially functional proteins but with a length difference of 14 amino acids. These variants conferred a 15-day difference in flowering time in an association experiment in 2 Scandinavian populations. The difference in flowering time between alleles was confirmed with transformation to A. thaliana. Because the north European late-flowering populations harbor both late- and early sequence variants at intermediate frequencies and the late-flowering variant is most frequent in the southern early flowering European population, other genetic factors must be responsible for the flowering time differences between the populations. The length polymorphism occurs at high frequencies also in several North American populations. The occurrence of functional variants at intermediate frequencies in several populations suggests that the variation may be maintained by balancing selection. This is in contrast to A. thaliana, where independent loss-of-function mutations at the FRIGIDA gene are responsible for differences between populations and local adaptation.

Cryptic population genetic structure: the number of inferred clusters depends on sample size.

Clustering methods have been used extensively to unravel cryptic population genetic structure. We investigated the effect of the number of individuals sampled in each location on the resulting number of clusters. Our study was motivated by recent results in Arabidopsis thaliana: studies in which more than one individual was sampled per location apparently have led to a much higher number of clusters than studies where only one individual was sampled in each location, as is generally done in this species. We show, using computer simulations and microsatellite data in A. thaliana, that the number of sampled individuals indeed has a strong impact on the number of resulting clusters. This effect is smaller if the sampled populations have a hierarchical structure. In most cases, sampling 5-10 individuals per population should be enough. The results argue for abandoning the concept of 'accessions' in partially selfing organisms.