Lagging adaptation to warming climate in Arabidopsis thaliana

Abstract

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.cliimate adaptation | adaptation lag | local adaptation | provenance test R apid climate change has already caused species range shifts and local extinctions (1) and is predicted to have greater future impacts (2). As the suitable climate space for a species shifts poleward (3), populations previously well adapted to the historical climate in a particular region may experience strong selection to adapt to rapidly warming local temperatures (4-10). Rapid evolutionary response to climate change has already been observed (11, 12), but it remains unclear whether evolutionary response can keep pace with rapidly changing local adaptive optima (6,8,(13)(14)(15). If local adaptation is slower than the rate of climate change, the average fitness of local populations may decline over time (7,14,16,17), possibly resulting in local extinctions and range collapse at the warmer margin. Where such lag exists, we expect that local seeds banked for conservation may no longer be well adapted to their sites of origin (18). However, such adaptational lag may be mitigated by migration or gene flow from populations in historically warmer sites if those populations are better adapted to current conditions in a site than local populations (8,13,19,20). Although adaptational lag has been predicted (4-6, 8, 14, 15, 19, 21, 22), the distinctive signature of mismatch between local p...

Evolution caused by extreme events

“…This question can be addressed by provenance trial experiments in which accessions from a range of climates are planted into common gardens across that climatic range. Wilczek et al [66] used banked seeds from geographically diverse accessions of the annual plant Arabidopsis thaliana to establish common garden experiments spanning the species' European climate range. Although they found evidence of historical adaptation to local climate, the year of the field experiment was unusually warm compared with historical averages.…”

Estimating the ability of plants to plastically track temperature‐mediated shifts in the spring phenological optimum

“…Consequently, observed advances in spring phenology suggest that optimal phenologies have advanced as the climate has warmed. However, little information is available as to whether observed phenologies are advancing at the same rate as optimal phenologies, and what the demographic consequences of any shortfall are (see Wilczek et al, 2014 for an exception). Measuring how optimal phenologies change per unit change in temperature, termed the environmental sensitivity of selection (B) (Chevin et al, 2010), is logistically challenging.…”

Predicting the evolutionary dynamics of seasonal adaptation to novel climates in Arabidopsis thaliana

“…Some populations produce multiple seasonal cohorts per year, including winter annuals as well as rapid cycling cohorts germinating in spring, summer, or early autumn (19). This species shows evidence of adaptation to climate on a broad geographic scale (2,(20)(21)(22) as well as along altitude gradients (23)(24)(25). Populations are large (26) and geographically structured over multiple spatial scales (27), maintaining extensive genetic variation.…”

“…climate change | annual plant | genomic prediction | season O ngoing climate change is causing rapid shifts in environmental selective pressures within local populations (1,2). To persist, populations must track the shifting multivariate trait optimum by phenotypic plasticity or adaptive evolution (3,4), or migrate to keep up with poleward shifts in their original climate niche (1).…”