Life‐history variation and adaptation in the historically mobile plant <i>Arabidopsis thaliana</i> (Brassicaceae) in North America

Griffith, Converse; Kim, Eunsuk; Donohue, Kathleen

doi:10.3732/ajb.91.6.837

Cited by 70 publications

(90 citation statements)

References 48 publications

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“…This study provides, to our knowledge, the first direct field test of regional climate adaptation in A. thaliana, although several previous studies have measured the fitness of natural accessions in the field in this species (26,28,39,41,(46)(47)(48)(49)(50)(51). Reciprocal transplant experiments between northern and southern sites show evidence of local adaptation but were not designed to distinguish the role of climate (41).…”

Section: Discussionmentioning

confidence: 99%

Lagging adaptation to warming climate in Arabidopsis thaliana

Wilczek

Cooper

Korves

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

171

219

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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...

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Section: Discussionmentioning

confidence: 99%

Lagging adaptation to warming climate in Arabidopsis thaliana

Wilczek

Cooper

Korves

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

171

219

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“…While small amounts of spring germination have been observed in typically winterannual populations of A. thaliana (Baskin and Baskin 1983), populations in New England have been observed to have high frequencies of spring germination, possibly because of their ability to set seeds in the autumn (Griffith et al 2004). We predict therefore that adaptive plastic responses to germination season would evolve most easily in such populations.…”

Section: Natural Selection On Life History and Its Plasticitymentioning

confidence: 99%

Niche Construction Through Germination Cueing: Life-History Responses to Timing of Germination in Arabidopsis Thaliana

et al. 2005

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Abstract. Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life-history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life-history traits, and whether germination timing influenced the expression of genetic variation for life-history traits. Adult life-history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life-history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life-history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life-history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life-history traits and the genetic variation of these traits.Key words. Dormancy, maternal effects, natural selection, phenotypic plasticity, seasonal cues.Received October 25, 2004. Accepted January 16, 2005 The timing of seed germination is highly responsive to environmental conditions. For a seed to germinate, certain environmental conditions must be present to break dormancy, and additional environmental conditions must exist subsequently to permit germination (Simpson 1990;Bewley 1997;Baskin and Baskin 1998). The timing of germination can therefore be a precise mechanism of habitat selection or niche construction that determines the environment experienced by the plant (Donohue 2003(Donohue , 2005. If the environmental conditions that elicit germination accurately predict the environment experienced by adults, germination behavior has the potential to influence the environment experienced by the plant throughout its life. It can thereby influence the phenotypic expression of plastic postgermination characters and the mode and strength of natural selection on those characters (Donohue 2002).Niche construction occurs when organisms alter the environment they experience (Odling-Smee et al. 1996), either through direct habitat modification, habitat choice, or resource garnering and depletion (Bazzaz 1991; de Kroon and Hutchins 1995;Huber et al. 1999). The environme...

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“…In KY, germination timing alone accounted for 72% of the variation in fitness among genotypes. Many studies have demonstrated strong natural selection on naturally segregating germination variants (Miller 1987;Kalisz 1989;Biere 1991;Gross and Smith 1991;Masuda and Washitani 1992;Donohue 2002;Griffith et al 2004). This study shows just how strong natural selection on germination timing can be on a range of potential segregants derived from natural genotypes.…”

Section: The Strength Of Natural Selection On Germinationmentioning

confidence: 99%

“…Transgressive segregation after hybridization between distinct lineages creates novel genotypes that can contribute to adaptive evolution and ecological diversification in hybrid species (Lexer et al 2003;Rieseberg et al 2003a,b), and hybridization is also hypothesized to contribute to invasiveness (Ellstrand and Schierenbeck 2000). Hybridization of colonizing lineages and the resulting creation of novel genotypes followed by lineage sorting may be an especially effective process for the rapid creation and subsequent preservation of adaptive gene complexes in selfing species (Weinig et al 2003;Griffith et al 2004). We simulated this sort of dynamic of novel genotypes in novel environments by experimentally creating a set of recombinant inbred lines to measure natural selection on germination timing and other life-history traits in two geographic locations.…”

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confidence: 99%

The Evolutionary Ecology of Seed Germination of Arabidopsis Thaliana: Variable Natural Selection on Germination Timing

et al. 2005

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Abstract. Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14-h and 10-h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June-dispersed seeds in RI, but only 4% in November-dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.Key words. Dormancy, maternal effects, natural selection, phenotypic plasticity, seasonal cues. Timing of seed germination is critical to the lifetime performance of the resulting plant. The conditions that elicit germination are the same conditions with which the young seedlings must contend, and those conditions can determine or predict conditions experienced throughout the life of a plant. Germination timing strongly influences seedling survivorship (Biere 1991;Gross and Smith 1991), total lifetime fitness (Miller 1987;Kalisz 1989;Masuda and Washitani 1992), life-history expression (Chouard 1960;Venable 1985;Kalisz 1989;Kalisz and Wardle 1994;Nordborg and Bergelson 1999;Galloway 2001Galloway , 2002, and selection on postgermination characters (Evans and Cabin 1995;Weinig 2000;Donohue 2002). An appropriate germination response to environmental cues is thereby the first requirement for establishment of plants in a location; before plants can display adaptive phenotypes for any adult character, they must first survive through germination.The timing of seed germination stro...

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Life‐history variation and adaptation in the historically mobile plant Arabidopsis thaliana (Brassicaceae) in North America

Cited by 70 publications

References 48 publications

Lagging adaptation to warming climate in Arabidopsis thaliana

Lagging adaptation to warming climate in Arabidopsis thaliana

Niche Construction Through Germination Cueing: Life-History Responses to Timing of Germination in Arabidopsis Thaliana

The Evolutionary Ecology of Seed Germination of Arabidopsis Thaliana: Variable Natural Selection on Germination Timing

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