Spatio‐temporal variation in fitness responses to contrasting environments in Arabidopsis thaliana

The evolutionary response of organisms to global climate change is expected to be strongly conditioned by preexisting standing genetic variation. In addition, natural selection imposed by global climate change on fitness‐related traits can be heterogeneous over time. We estimated selection of life‐history traits of an entire genetic lineage of the plant Arabidopsis thaliana occurring in north‐western Iberian Peninsula that were transplanted over multiple years into two environmentally contrasting field sites in southern Spain, as southern environments are expected to move progressively northwards with climate change in the Iberian Peninsula. The results indicated that natural selection on flowering time prevailed over that on recruitment. Selection favored early flowering in six of eight experiments and late flowering in the other two. Such heterogeneity of selection for flowering time might be a powerful mechanism for maintaining genetic diversity in the long run. We also found that north‐western A. thaliana accessions from warmer environments exhibited higher fitness and higher phenotypic plasticity for flowering time in southern experimental facilities. Overall, our transplant experiments suggested that north‐western Iberian A. thaliana has the means to cope with increasingly warmer environments in the region as predicted by trends in global climate change models.     

Natural variation,differentiation, and genetic trade‐offs of ecophysiological traits in response to water limitation in Brachypodium distachyon and its descendent allotetraploid B. hybridum (Poaceae)

Differences in tolerance to water stress may underlie ecological divergence of closely related ploidy lineages. However, the mechanistic basis of physiological variation governing ecogeographical cytotype segregation is not well understood. Here, using Brachypodium distachyon and its derived allotetraploid B. hybridum as model, we test the hypothesis that, for heteroploid annuals, ecological divergence of polyploids in drier environments is based on trait differentiation enabling drought escape. We demonstrate that under water limitation allotetraploids maintain higher photosynthesis and stomatal conductance and show earlier flowering than diploids, concordant with a drought‐escape strategy to cope with water stress. Increased heterozygosity and greater genetic variability and plasticity of polyploids could confer a superior adaptive capability. Consistent with these predictions, we document (1) greater standing within‐population genetic variation in water‐use efficiency (WUE) and flowering time in allotetraploids, and (2) the existence of (nonlinear) environmental clines in physiology across allotetraploid populations. Increased gas exchange and diminished WUE occurred at the driest end of the gradient, consistent with a drought‐escape strategy. Finally, we found that allotetraploids showed weaker genetic correlations than diploids congruous with the expectation of relaxed pleiotropic constraints in polyploids. Our results suggest evolutionary divergence of ecophysiological traits in each ploidy lineage.     

Quantitative variation in water-use efficiency across water regimes and its relationship with circadian, vegetative, reproductive, and leaf gas-exchange traits

Drought limits light harvesting, resulting in lower plant growth and reproduction. One trait important for plant drought response is water-use efficiency (WUE). We investigated (1) how the joint genetic architecture of WUE, reproductive characters, and vegetative traits changed across drought and well-watered conditions, (2) whether traits with distinct developmental bases (e.g. leaf gas exchange versus reproduction) differed in the environmental sensitivity of their genetic architecture, and (3) whether quantitative variation in circadian period was related to drought response in Brassica rapa. Overall, WUE increased in drought, primarily because stomatal conductance, and thus water loss, declined more than carbon fixation. Genotypes with the highest WUE in drought expressed the lowest WUE in well-watered conditions, and had the largest vegetative and floral organs in both treatments. Thus, large changes in WUE enabled some genotypes to approach vegetative and reproductive trait optima across environments. The genetic architecture differed for gas-exchange and vegetative traits across drought and well-watered conditions, but not for floral traits. Correlations between circadian and leaf gas-exchange traits were significant but did not vary across treatments, indicating that circadian period affects physiological function regardless of water availability. These results suggest that WUE is important for drought tolerance in Brassica rapa and that artificial selection for increased WUE in drought will not result in maladaptive expression of other traits that are correlated with WUE.     

Variation in and adaptive plasticity of flower size and drought-coping traits

Although phenotypic plasticity of morphological and physiological traits in response to drought could be adaptive, there have been relatively few tests of plasticity variation or of adaptive plasticity in drought-coping traits across populations with different moisture availabilities. We measured floral size, vegetative size, and physiological traits in four field populations of Leptosiphon androsaceus (Polemoniaceae) that were distributed across a rainfall gradient in California, USA. Measurements were made over 5 years that varied in precipitation. We also conducted a growth chamber experiment in which half-sibs from three populations were divided equally among a well-watered and a drought treatment. We tested for selection on traits in each of the watering treatments, and evaluated whether traits exhibited plasticity. In the field, plant traits exhibited substantial variation across populations and years. Flower size, leaf size, and water-use efficiency (WUE) were generally higher for populations that received greater average rainfall. However, in dry years, we observed a decrease in flower and leaf size, but an increase in WUE across the populations. In the growth chamber experiment, leaf and physiological traits exhibited plasticity, with smaller leaves and higher WUE found in the drought, as compared to the well-watered treatment. Only specific leaf area exhibited differentiation in plasticity among populations. Although there was no observed plasticity in floral size, selection favored smaller flowers in the drought treatment and larger flowers in the well-watered treatment. Our results suggest that moisture availability has led to trait variation in L. androsaceus via a combination of selection and phenotypic plasticity.     

Tests for the joint evolution of mating system and drought escape in Mimulus

Background and Aims

Self-fertilizing taxa are often found at the range margins of their progenitors, where sub-optimal habitats may select for alternative physiological strategies. The extent to which self-fertilization is favoured directly vs. arising indirectly through correlations with other adaptive life history traits is unclear. Trait responses to selection depend on genetic variation and covariation, as well as phenotypic and genetic responses to altered environmental conditions. We tested predictions of the hypothesis that self-fertilization in Mimulus arises through direct selection on physiological and developmental traits that allow seasonal drought escape.

Methods

Phenotypic selection on mating system and drought escape traits was estimated in field populations of M. guttatus. In addition, trait phenotype and phenotypic selection were compared between experimental wet and dry soil in two greenhouse populations each of M. guttatus and M. nasutus. Finally, genetic variation and covariation for traits were compared between wet and dry soil treatments in a greenhouse population of M. guttatus.

Key Results

Consistent with predictions, selection for early flowering was generally stronger than for mating system traits, and selection for early flowering was stronger in dry soil. Inconsistent with predictions, selection for water-use efficiency was largely absent; selection for large flowers was stronger than for drought escape in the field; and most drought escape and mating system traits were not genetically correlated. A positive genetic correlation between flowering time and flower size, which opposed the adaptive contour, emerged only in wet soil, suggesting that variation in water availability may maintain variation in these traits. Plastic responses to soil moisture treatments supported the idea that taxonomic divergence could have been facilitated by plasticity in flowering time and selfing.

Conclusions

The hypothesis that plant mating systems may evolve indirectly via selection on correlated life history characteristics is plausible and warrants increased attention.     

The adaptive significance of drought escape in Avena barbata, an annual grass

Drought strongly influences plant productivity, suggesting that water limitation has shaped the evolution of many plant physiological traits. One functional strategy that plants employ to cope with decreasing water availability is drought escape. For drought-escaping species, high metabolic activity (gas exchange) and rapid growth are hypothesized to confer a fitness advantage, because this enables a plant to complete its life cycle before the most intense period of drought. By growing an annual grass species (Avena barbata) under well-watered or water-limited conditions in a greenhouse, we directly tested whether high photosynthesis, increased stomatal opening, and early flowering are adaptive under drought. We measured phenotypic selection on instantaneous gas exchange and flowering time as well as the underlying biochemical traits that regulate photosynthesis. We found strong selection for earlier flowering in the dry environment, but no evidence that increased photosynthesis was adaptive under drought. Photosynthetic rate (A) and stomatal conductance (gs) were both adaptively neutral in the dry environment. Increased photosynthetic capacity (Amax) was maladaptive in the dry environment, perhaps because of the respiratory cost associated with maintaining excess enzyme and substrate capacity. There was no correlational selection on the combination of physiology and flowering time in the dry environment, suggesting that accelerated development and high gas exchange may not need to be tightly linked to promote drought escape. In contrast, there was selection for both high photosynthetic function (Amax and A) and early flowering in the well-watered environment. These combinations of traits may have been favored because they maximize both energy and time available for reproduction. Our results suggest that the benefit of increased photosynthesis for plant fitness may be strongest in the absence of drought stress.     

Plasticity Regulators Modulate Specific Root Traits in Discrete Nitrogen Environments

Plant development is remarkably plastic but how precisely can the plant customize its form to specific environments? When the plant adjusts its development to different environments, related traits can change in a coordinated fashion, such that two traits co-vary across many genotypes. Alternatively, traits can vary independently, such that a change in one trait has little predictive value for the change in a second trait. To characterize such “tunability” in developmental plasticity, we carried out a detailed phenotypic characterization of complex root traits among 96 accessions of the model Arabidopsis thaliana in two nitrogen environments. The results revealed a surprising level of independence in the control of traits to environment – a highly tunable form of plasticity. We mapped genetic architecture of plasticity using genome-wide association studies and further used gene expression analysis to narrow down gene candidates in mapped regions. Mutants in genes implicated by association and expression analysis showed precise defects in the predicted traits in the predicted environment, corroborating the independent control of plasticity traits. The overall results suggest that there is a pool of genetic variability in plants that controls traits in specific environments, with opportunity to tune crop plants to a given environment.     

A resurrection study reveals limited evolution of phenology in response to recent climate change across the geographic range of the scarlet monkeyflower

Premise of the studyAs global climate change alters drought regimes, rapid evolution of traits that facilitate adaptation to drought can rescue populations in decline. The evolution of phenological advancement can allow plant populations to escape drought, but evolutionary responses in phenology can vary across a species'' range due to differences in drought intensity and standing genetic variation.Methods Mimulus cardinalis, a perennial herb spanning a broad climatic gradient, recently experienced a period of record drought. Here, we used a resurrection study comparing flowering time and stem height at first flower of pre‐drought ancestors and post‐drought descendants from northern‐edge, central, and southern‐edge populations in a common environment to examine the evolution of drought escape across the latitudinal range.Key resultsContrary to the hypothesis of the evolution of advanced phenology in response to recent drought, flowering time did not advance between ancestors and descendants in any population, though storage condition and maternal effects could have impacted these results. Stem height was positively correlated with flowering time, such that plants that flowered earlier were shorter at first flower. This correlation could constrain the evolution of earlier flowering time if selection favors flowering early at a large size.ConclusionsThese findings suggest that rapid evolution of phenology will not rescue these populations from recent climate change. Future work is needed to examine the potential for the evolution of alternative drought strategies and phenotypic plasticity to buffer M. cardinalis populations from changing climate.     

Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana

The temporal control or timing of the life cycle of annual plants is presumed to provide adaptive strategies to escape harsh environments for survival and reproduction. This is mainly determined by the timing of germination, which is controlled by the level of seed dormancy, and of flowering initiation. However, the environmental factors driving the evolution of plant life cycles remain largely unknown. To address this question we have analysed nine quantitative life history traits, in a native regional collection of 300 wild accessions of Arabidopsis thaliana. Seed dormancy and flowering time were negatively correlated, indicating that these traits have coevolved. In addition, environmental–phenotypic analyses detected strong altitudinal and climatic clines for most life history traits. Overall, accessions showing life cycles with early flowering, small seeds, high seed dormancy and slow germination rate were associated with locations exposed to high temperature, low summer precipitation and high radiation. Furthermore, we analysed the expression level of the positive regulator of seed dormancy DELAY OF GERMINATION 1 (DOG1), finding similar but weaker altitudinal and climatic patterns than seed dormancy. Therefore, DOG1 regulatory mutations are likely to provide a quantitative molecular mechanism for the adaptation of A. thaliana life cycle to altitude and climate.     

Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers

Plant water-use efficiency (WUE) is expected to affect plant fitness and thus be under natural selection in arid habitats. Although many natural population studies have assessed plant WUE, only a few related WUE to fitness. The further determination of whether selection on WUE is direct or indirect through functionally related traits has yielded no consistent results. For natural populations of two desert annual sunflowers, Helianthus anomalus and H. deserticola, we used phenotypic selection analysis with vegetative biomass as the proxy for fitness to test (1) whether there was direct and indirect selection on WUE (carbon isotope ratio) and related traits (leaf N, area, succulence) and (2) whether direct selection was consistent with hypothesized drought/dehydration escape and avoidance strategies. There was direct selection for lower WUE in mesic and dry H. anomalus populations, consistent with dehydration escape, even though it is the longer lived of the two species. For mesic H. anomalus, direct selection favored lower WUE and higher N, suggesting that plants may be “wasting water” to increase N delivery via the transpiration stream. For the shorter lived H. deserticola in the direr habitat, there was indirect selection for lower WUE, inconsistent with drought escape. There was also direct selection for higher leaf N, succulence and leaf size. There was no direct selection for higher WUE consistent with dehydration avoidance in either species. Thus, in these natural populations of two desert dune species higher fitness was associated with some combination direct and indirect selection for lower WUE, higher leaf N and larger leaf size. Our understanding of the adaptive value of plant ecophysiological traits will benefit from further consideration of related traits such as leaf nitrogen and more tests in natural populations.     

Genetic determinism of reproductive fitness traits under drought stress in the model legume <Emphasis Type="Italic">Medicago truncatula</Emphasis>

Fitness traits that determine the reproductive ability of individuals and the persistence of populations are affected by drought stress. Medicago truncatula that commonly encounters drought stress in its natural area, and for which large natural diversity and genetic tools are available, is a suitable species to investigate genetic determinism of fitness traits under stress. In a common garden, three successive cycles of short drought stress were applied after flowering, during the reproductive stage that is the most susceptible to drought for that species. Ten genotypes derived from natural populations and a mapping population were used to investigate the genetic determinism of vegetative and reproductive traits as components of fitness. A large genetic variation was observed and transgressive genotypes (more resistant or more susceptible than the parental genotypes) were found in the mapping population. Fitness traits were reduced by 5–74% in drought condition compared to well-watered condition. The most affected characters were total pod number per plant and total pod weight per plant. A total of 49 QTL, explaining between 6 and 38% of phenotypic variation for vegetative and reproductive fitness traits, were detected on all chromosomes except chromosome 6. A major QTL for flowering date (R ² of 19 and 38%) that co-located with QTL for reproductive fitness traits were found on chromosome 7. In this study, no major QTL specific to drought-stressed or well-watered conditions were detected. We, thus, showed that QTL explaining fitness traits were numerous with small effects, in accordance with the genetic determinism of a complex trait.     

Natural variation in stomatal abundance of Arabidopsis thaliana includes cryptic diversity for different developmental processes

Background and Aims

Current understanding of stomatal development in Arabidopsis thaliana is based on mutations producing aberrant, often lethal phenotypes. The aim was to discover if naturally occurring viable phenotypes would be useful for studying stomatal development in a species that enables further molecular analysis.

Methods

Natural variation in stomatal abundance of A. thaliana was explored in two collections comprising 62 wild accessions by surveying adaxial epidermal cell-type proportion (stomatal index) and density (stomatal and pavement cell density) traits in cotyledons and first leaves. Organ size variation was studied in a subset of accessions. For all traits, maternal effects derived from different laboratory environments were evaluated. In four selected accessions, distinct stomatal initiation processes were quantitatively analysed.

Key Results and Conclusions

Substantial genetic variation was found for all six stomatal abundance-related traits, which were weakly or not affected by laboratory maternal environments. Correlation analyses revealed overall relationships among all traits. Within each organ, stomatal density highly correlated with the other traits, suggesting common genetic bases. Each trait correlated between organs, supporting supra-organ control of stomatal abundance. Clustering analyses identified accessions with uncommon phenotypic patterns, suggesting differences among genetic programmes controlling the various traits. Variation was also found in organ size, which negatively correlated with cell densities in both organs and with stomatal index in the cotyledon. Relative proportions of primary and satellite lineages varied among the accessions analysed, indicating that distinct developmental components contribute to natural diversity in stomatal abundance. Accessions with similar stomatal indices showed different lineage class ratios, revealing hidden developmental phenotypes and showing that genetic determinants of primary and satellite lineage initiation combine in several ways. This first systematic, comprehensive natural variation survey for stomatal abundance in A. thaliana reveals cryptic developmental genetic variation, and provides relevant relationships amongst stomatal traits and extreme or uncommon accessions as resources for the genetic dissection of stomatal development.     

Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis (Balsaminaceae)

For longer lived annual plants, high water-use efficiency (WUE) and low stomatal conductance are hypothesized to confer a fitness advantage under drought stress. To directly test the adaptive significance of WUE and stomatal conductance under drought stress, inbred lines of Impatiens capensis were grown in two field environments (watered and not-watered), in a year of unusual early-season drought. In contrast to the results from a previous study of late-season drought in the same system, selection was detected for lower WUE, increased stomatal conductance, and early flowering time. These findings suggest that early-season drought conditions may select for drought avoidance traits such as low WUE and early reproduction, whereas later drought selects for tolerance traits such as high WUE.     

QTL analysis and QTL-based prediction of flowering phenology in recombinant inbred lines of barley

Combining ecophysiological modelling and genetic mapping has increasingly received attention from researchers who wish to predict complex plant or crop traits under diverse environmental conditions. The potential for using this combined approach to predict flowering time of individual genotypes in a recombinant inbred line (RIL) population of spring barley (Hordeum vulgare L.) was examined. An ecophysiological phenology model predicts preflowering duration as affected by temperature and photoperiod, based on the following four input traits: f(o) (the minimum number of days to flowering at the optimum temperature and photoperiod), theta1 and theta2 (the development stages for the start and the end of the photoperiod-sensitive phase, respectively), and delta (the photoperiod sensitivity). The model-input trait values were obtained from a photoperiod-controlled greenhouse experiment. Assuming additivity of QTL effects, a multiple QTL model was fitted for the model-input traits using composite interval mapping. Four to seven QTL were identified for each trait. Each trait had at least one QTL specific to that trait alone. Other QTL were shared by two or all traits. Values of the model-input traits predicted for the RILs from the QTL model were fed back into the ecophysiological model. This QTL-based ecophysiological model was subsequently used to predict preflowering duration (d) for eight field trial environments. The model accounted for 72% of the observed variation among 94 RILs and 94% of the variation among the two parents across the eight environments, when observations in different environments were pooled. However, due to the low percentage (34-41%) of phenotypic variation accounted for by the identified QTL for three model-input traits (theta1, theta2 and delta), the QTL-based model accounted for somewhat less variation among the RILs than the model using original phenotypic input trait values. Nevertheless, days to flowering as predicted from the QTL-based ecophysiological model were highly correlated with days to flowering as predicted from QTL-models per environment for days to flowering per se. The ecophysiological phenology model was thus capable of extrapolating (QTL) information from one environment to another.     

Selection on QTL and complex traits in complex environments

Understanding genetic variation for complex traits in heterogeneous environments is a fundamental problem in biology. In this issue of Molecular Ecology, Fournier‐Level et al. ( 2013 ) analyse quantitative trait loci (QTL) influencing ecologically important phenotypes in mapping populations of Arabidopsis thaliana grown in four habitats across its native European range. They used causal modelling to quantify the selective consequences of life history and morphological traits and QTL on components of fitness. They found phenology QTL colocalizing with known flowering time genes as well as novel loci. Most QTL influenced fitness via life history and size traits, rather than QTL having direct effects on fitness. Comparison of phenotypes among environments found no evidence for genetic trade‐offs for phenology or growth traits, but genetic trade‐offs for fitness resulted because flowering time had opposite fitness effects in different environments. These changes in QTL effects and selective consequences may maintain genetic variation among populations.     

Assortative mating by flowering time and its effect on correlated traits in variable environments

Reproductive timing is a key life‐history trait that impacts the pool of available mates, the environment experienced during flowering, and the expression of other traits through genetic covariation. Selection on phenology, and its consequences on other life‐history traits, has considerable implications in the context of ongoing climate change and shifting growing seasons. To test this, we grew field‐collected seed from the wildflower Mimulus guttatus in a greenhouse to assess the standing genetic variation for flowering time and covariation with other traits. We then created full‐sib families through phenological assortative mating and grew offspring in three photoperiod treatments representing seasonal variation in daylength. We find substantial quantitative genetic variation for the onset of flowering time, which covaried with vegetative traits. The assortatively‐mated offspring varied in their critical photoperiod by over two hours, so that families differed in their probability of flowering across treatments Allocation to flowering and vegetative growth changed across the daylength treatments, with consistent direction and magnitude of covariation among flowering time and other traits. Our results suggest that future studies of flowering time evolution should consider the joint evolution of correlated traits and shifting seasonal selection to understand how environmental variation influences life histories.     

Dependence of functional traits related to growth rates and their CO<Subscript>2</Subscript> response on multiple habitat climate factors across <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> populations

The values of many plant traits are often different even within a species as a result of local adaptation. Here, we studied how multiple climate variables influence trait values in Arabidopsis thaliana grown under common conditions. We examined 9 climate variables and 29 traits related to vegetative growth rate in 44 global A. thaliana accessions grown at ambient or elevated CO₂ concentration ([CO₂]) and applied a multiple regression analysis. We found that genetic variations in the traits related to growth rates were associated with various climate variables. At ambient [CO₂], plant size was positively correlated with precipitation in the original habitat. This may be a result of larger biomass investment in roots at the initial stage in plants adapting to a lower precipitation. Stomatal conductance and photosynthetic nitrogen use efficiency were negatively correlated with vapor pressure deficit, probably as a result of the trade-off between photosynthetic water- and nitrogen-use efficiency. These results suggest that precipitation and air humidity influence belowground and aboveground traits, respectively. Elevated [CO₂] altered climate dependences in some of the studied traits. The CO₂ response of relative growth rate was negatively correlated with altitude, indicating that plants inhabiting a higher altitude have less plasticity to changing [CO₂]. These results are useful not only for understanding evolutionary process but also to predict the plant species that are favored under future global change.     

Independent FLC Mutations as Causes of Flowering-Time Variation in Arabidopsis thaliana and Capsella rubella

Capsella rubella is an inbreeding annual forb closely related to Arabidopsis thaliana, a model species widely used for studying natural variation in adaptive traits such as flowering time. Although mutations in dozens of genes can affect flowering of A. thaliana in the laboratory, only a handful of such genes vary in natural populations. Chief among these are FRIGIDA (FRI) and FLOWERING LOCUS C (FLC). Common and rare FRI mutations along with rare FLC mutations explain a large fraction of flowering-time variation in A. thaliana. Here we document flowering time under different conditions in 20 C. rubella accessions from across the species’ range. Similar to A. thaliana, vernalization, long photoperiods and elevated ambient temperature generally promote flowering. In this collection of C. rubella accessions, we did not find any obvious loss-of-function FRI alleles. Using mapping-by-sequencing with two strains that have contrasting flowering behaviors, we identified a splice-site mutation in FLC as the likely cause of early flowering in accession 1408. However, other similarly early C. rubella accessions did not share this mutation. We conclude that the genetic basis of flowering-time variation in C. rubella is complex, despite this very young species having undergone an extreme genetic bottleneck when it split from C. grandiflora a few tens of thousands of years ago.     

Selection and plasticity both account for interannual variation in life‐history phenology in an annual prairie legume

As the environment changes, so too must plant communities and populations if they are to persist. Life‐history transitions and their timing are often the traits that are most responsive to changing environmental conditions. To compare the contributions of plasticity and natural selective response to variation in germination and flowering phenology, we performed a quantitative genetic study of phenotypic selection on Chamaecrista fasciculata (Fabaceae) across two consecutive years in a restored tallgrass prairie. The earliest dates of germination and flowering were recorded for two parental cohorts and one progeny cohort in an experimental garden. Environmental differences between years were the largest contributors to phenological variation in this population. In addition, there was substantial heritability for flowering time and statistically significant selection for advancement of flowering. Comparison between a progeny cohort and its preselection parental cohort indicated a change in mean flowering time consistent with the direction of selection. Selection on germination time was weaker than that on flowering time, while environmental effects on germination time were stronger. The response to selection on flowering time was detectable when accounting for the effect of the environment on phenotypic differences, highlighting the importance of controlling for year‐to‐year environmental variation in quantitative genetic studies.