Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana

Abstract

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment-specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2-5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.

Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

“…In conclusion, early life stages are known to be under strong selection (15)(16)(17)(18)(19) and to have cascading effects across the whole life cycle (16,20,21), but they are seldom included in studies on the genetic basis of local adaptation (12)(13)(14)(22)(23)(24)(25)(26)(27)(28). By conducting a reciprocal transplant experiment including the whole life cycle and maternal effects, we have shown that selection during early life stages contributes strongly to both the magnitude and the genetic basis of adaptive differentiation among natural populations of A. thaliana.…”

“…For instance, field experiments with plants are usually based on the transplantation of seedlings (12)(13)(14)(22)(23)(24)(25)(26)(27)(28) and therefore do not assess the importance of possible adaptive differentiation and genetic tradeoffs expressed at the seed and germination stage. Indirect evidence suggests that the seed stage may contribute considerably to local adaptation.…”

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

“…We did not directly estimate a fitness proxy such as seed set, but we reasoned that traits shown to have adaptive value in A. thaliana, such as flowering time (87)(88)(89), will be subject to evolutionary forces comparable to those acting directly on fitness. Although flowering time is locally adaptive in A. thaliana, the correlation between flowering time and fitness varies by accession and environment (90)(91)(92). Large-effect mutations in flowering time genes can significantly perturb fitness, but their effect is not directional and varies by genetic background (90,93), providing one possible explanation for variable correlation between these two traits.…”

Gene Regulatory Variation Mediates Flowering Responses to Vernalization along an Altitudinal Gradient in Arabidopsis

“…Most remarkable, though, seems the negligible role of FLC in the adjustment of flowering time along altitude. While MAF2 and MAF3 are known to vary extensively among natural populations (Caicedo et al, 2009;Rosloski et al, 2010) and have repeatedly been identified as important flowering time regulators in quantitative trait locus analyses using wild accessions (Salomé et al, 2011;Silady et al, 2011;Lasky et al, 2012;Fournier-Level et al, 2013;Grillo et al, 2013), the evolutionary properties of AGL19 and its distribution among natural populations will need further investigation.…”

“…For example, AGL19 has been found to promote flowering following vernalization without interacting with FLC (Schönrock et al, 2006), and relatives of FLC, the MADS AFFECTING FLOWERING genes (MAF1-MAF5; MAF1 is also referred to as FLOWERING LOCUS M [FLM]; De Bodt et al, 2003), have been shown to inhibit flowering in a similar way to FLC (Ratcliffe et al, 2003;Scortecci et al, 2003;Werner et al, 2005;Sung et al, 2006;Gu et al, 2013). Genes MAF2 to MAF5 (Ratcliffe et al, 2003) are arranged in a tandem gene array and vary extensively among natural populations (Caicedo et al, 2009;Rosloski et al, 2010), and several recent studies have associated this polymorphic region with natural variation in flowering time (Salomé et al, 2011;Silady et al, 2011;Lasky et al, 2012;Fournier-Level et al, 2013;Grillo et al, 2013), making these genes interesting candidates for studying associations between flowering time and ecological parameters.…”