Lagging adaptation to warming climate in Arabidopsis thaliana.

If climate change outpaces the rate of adaptive evolution within a site, populations previously well adapted to local conditions may decline or disappear, and banked seeds from those populations will be unsuitable for restoring them. However, if such adaptational lag has occurred, immigrants from historically warmer climates will outperform natives and may provide genetic potential for evolutionary rescue. We tested for lagging adaptation to warming climate using banked seeds of the annual weed Arabidopsis thaliana in common garden experiments in four sites across the species' native European range: Valencia, Spain; Norwich, United Kingdom; Halle, Germany; and Oulu, Finland. Genotypes originating from geographic regions near the planting site had high relative fitness in each site, direct evidence for broad-scale geographic adaptation in this model species. However, genotypes originating in sites historically warmer than the planting site had higher average relative fitness than local genotypes in every site, especially at the northern range limit in Finland. This result suggests that local adaptive optima have shifted rapidly with recent warming across the species' native range. Climatic optima also differed among seasonal germination cohorts within the Norwich site, suggesting that populations occurring where summer germination is common may have greater evolutionary potential to persist under future warming. If adaptational lag has occurred over just a few decades in banked seeds of an annual species, it may be an important consideration for managing longer-lived species, as well as for attempts to conserve threatened populations through ex situ preservation.

Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field.

To date, the effect of natural selection on candidate genes underlying complex traits has rarely been studied experimentally, especially under ecologically realistic conditions. Here we report that the effect of selection on the flowering time gene FRIGIDA (FRI) reverses depending on the season of germination and allelic variation at the interacting gene FLOWERING LOCUS C (FLC). In field studies of 136 European accessions of Arabidopsis thaliana, accessions with putatively functional FRI alleles had higher winter survival in one FLC background in a fall-germinating cohort, but accessions with deletion null FRI alleles had greater seed production in the other FLC background in a spring-germinating cohort. Consistent with FRI's role in flowering, selection analyses suggest that the difference in winter survival can be attributed to time to bolting. However, in the spring cohort, the fitness difference was associated with rosette size. Our analyses also reveal that controlling for population structure with estimates of inferred ancestry and a geographical restriction was essential for detecting fitness associations. Overall, our results suggest that the combined effects of seasonally varying selection and epistasis could explain the maintenance of variation at FRI and, more generally, may be important in the evolution of genes underlying complex traits.

A developmental response to pathogen infection in Arabidopsis.

We present evidence that susceptible Arabidopsis plants accelerate their reproductive development and alter their shoot architecture in response to three different pathogen species. We infected 2-week-old Arabidopsis seedlings with two bacterial pathogens, Pseudomonas syringae and Xanthomonas campestris, and an oomycete, Peronospora parasitica. Infection with each of the three pathogens reduced time to flowering and the number of aerial branches on the primary inflorescence. In the absence of competition, P. syringae and P. parasitica infection also increased basal branch development. Flowering time and branch responses were affected by the amount of pathogen present. Large amounts of pathogen caused the most dramatic changes in the number of branches on the primary inflorescence, but small amounts of P. syringae caused the fastest flowering and the production of the most basal branches. RPS2 resistance prevented large changes in development when it prevented visible disease symptoms but not at high pathogen doses and when substantial visible hypersensitive response occurred. These experiments indicate that phylogenetically disparate pathogens cause similar changes in the development of susceptible Arabidopsis. We propose that these changes in flowering time and branch architecture constitute a general developmental response to pathogen infection that may affect tolerance of and/or resistance to disease.