Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching

Plants evolve defenses against herbivores and pathogens in stressful environments; however, plants that evolve tolerances to other environmental stressors may have compromised defenses. Such tradeoffs involving defenses may depend on limited resources or otherwise stressful environments; however, the effect of stressful environments on defense expression might be different for different genotypes (G×E). To test these predictions, we studied genetic variation and co‐variation of drought stress tolerance and defenses at two levels of genetic variation: between and within closely related species. We did this across an experimental drought stress gradient in a growth room for species for which genetic variation in drought tolerance was likely. In apparent contrast to predictions, the species Boechera holboellii (Brassicaceae) from lower and dryer elevations had slower inherent growth rates and correspondingly higher total defensive glucosinolate concentrations than the closely related species B. stricta from higher elevations. Thus, B. holboellii was both drought tolerant and defended; however, optimality theory does predict tradeoffs between defense and growth. Differences between species in the direct effect of water deficiency on glucosinolate production did not obscure the grow‐or‐defend tradeoff. B. holboellii may also have been more resistant to the specialist herbivore Plutella xylostella; a trend that was less clear because it depended on plant development and water deficient conditions. At finer scales of genetic variation, there was significant variation among families and naturally occurring inbred lines of B. stricta in drought tolerance measured as inherent growth, the reaction norm of growth across drought treatments, shoot water potential, and transpiration rates. Evidence for tradeoffs was also found within B. stricta in genetic correlations between resistance and transpiration rates, or glucosinolates and growth rates. No G×E was detected at these finer scales of genetic variation, although sometimes the tradeoff was dependent on drought conditions. Direct effects of drought stress resulted in an apparent plastic switch between resistance and tolerance to damage, which might be a cost avoidance mechanism because tradeoffs never involved tolerance to damage. Thus, when drought tolerance is manifest as slow inherent growth rates, plants may also have relatively high defense levels, especially in stressful environments. Otherwise, defenses may be compromised by drought‐coping mechanisms, although plastic switches to less costly defenses may alleviate constraints in stressful environments.     

Water deficiency induces evolutionary tradeoff between stress tolerance and chemical defense allocation that may help explain range limits in plants

What causes range limits is a central question in evolutionary ecology. Transplant studies indicate that areas just across range boundaries are often stressful. The recent Defense constraint (DC) hypothesis for plants states that the evolution of tolerance to stressful environments across a range boundary is constrained by allocation to chemical defense because of antagonistic crosstalk between abiotic and biotic stress signaling pathways that otherwise could be co‐opted for range expansion. Abscisic acid (ABA) drought stress tolerance and jasmonic acid/ethylene (JA/ET) defense signaling pathways, for example, are known to be antagonistic to one another in Arabidopsis and other species. To test the DC hypothesis, we examined quantitative genetic variation and co‐variation among marker‐inferred inbred lines and sib‐families of Boechera stricta, a close wild relative of Arabidopsis. The dynamics of the defense‐stress tolerance tradeoff was examined across 1) years that differed in precipitation, 2) drought and ABA treatments, and 3) a NPK nutrient supply gradient. In support of the DC hypothesis, we observed the tradeoff a) in the dry year, and b) in response to water deficiency, which c) was affected by ABA treatments, but the interaction between ABA and glucosinolate (GS) toxin levels was not significant. In contrast to the effects of water deficiency, d) the effect of lower NPK supply to cause the tradeoff was only marginally significant. Because an ABA‐mediated stress response is intrinsic to water deficient conditions and because of the known involvement of JA/ET in GS regulation, we suggest that these results provide circumstantial evidence implicating both of these pathways in the tradeoff and thus in the development of range limits.     

Niche partitioning between close relatives suggests trade‐offs between adaptation to local environments and competition

Niche partitioning among close relatives may reflect trade‐offs underlying species divergence and coexistence (e.g., between stress tolerance and competitive ability). We quantified the effects of habitat and congeneric species interactions on fitness for two closely related herbaceous plant species, Mimulus guttatus and Mimulus laciniatus, in three common habitat types within their sympatric range. Drought stress strongly reduced survival of M. guttatus in fast‐drying seeps occupied by M. laciniatus, suggesting that divergent habitat adaptation maintains this niche boundary. However, neither seedling performance nor congeneric competition explained the absence of M. laciniatus from shady streams where M. guttatus thrives. M. laciniatus may be excluded from this habitat by competition with other species in the community or mature M. guttatus. Species performance and competitive ability were similar in sympatric meadows where plant community stature and the growing season length are intermediate between seeps and streams. Stochastic effects (e.g., dispersal among habitats or temporal variation) may contribute to coexistence in this habitat. Habitat adaptation, species interactions, and stochastic mechanisms influence sympatric distributions for these recently diverged species.     

Evolutionary constraint on low elevation range expansion: Defense‐abiotic stress‐tolerance trade‐off in crosses of the ecological model Boechera stricta

Most transplant experiments across species geographic range boundaries indicate that adaptation to stressful environments outside the range is often constrained. However, the mechanisms of these constraints remain poorly understood. We used extended generation crosses from diverged high and low elevation populations. In experiments across low elevation range boundaries, there was selection on the parental lines for abiotic stress‐tolerance and resistance to herbivores. However, in support of a defense‐tolerance trade‐off, extended generation crosses showed nonindependent segregation of these traits in the laboratory across a drought‐stress gradient and in the field across the low elevation range boundary. Genotypic variation in a marker from a region of the genome containing a candidate gene (MYC2) was associated with change in the genetic trade‐off. Thus, using crosses and forward genetics, we found experimental genetic and molecular evidence for a pleiotropic trade‐off that could constrain the evolution of range expansion.     

Plasticity and local adaptation explain lizard cold tolerance

How does climate variation limit the range of species and what does it take for species to colonize new regions? In this issue of Molecular Ecology, Campbell‐Staton et al. ( 2018 ) address these broad questions by investigating cold tolerance adaptation in the green anole lizard (Anolis carolinensis) across a latitudinal transect. By integrating physiological data, gene expression data and acclimation experiments, the authors disentangle the mechanisms underlying cold adaptation. They first establish that cold tolerance adaptation in Anolis lizards follows the predictions of the oxygen‐ and capacity‐limited thermal tolerance hypothesis, which states that organisms are limited by temperature thresholds at which oxygen supply cannot meet demand. They then explore the drivers of cold tolerance at a finer scale, finding evidence that northern populations are adapted to cooler thermal regimes and that both phenotypic plasticity and heritable genetic variation contribute to cold tolerance. The integration of physiological and gene expression data further highlights the varied mechanisms that drive cold tolerance adaptation in Anolis lizards, including both supply‐side and demand‐side adaptations that improve oxygen economy. Altogether, their work provides new insight into the physiological and genetic mechanisms underlying adaptation to new climatic niches and demonstrates that cold tolerance in northern lizard populations is achieved through the synergy of physiological plasticity and local genetic adaptation for thermal performance.     

Antioxidant activity in the leaves of <Emphasis Type="Italic">Melilotus albus</Emphasis> and <Emphasis Type="Italic">Trifolium medium</Emphasis> from man-made disturbed habitats in the Middle Urals under the influence of copper

Physiological mechanisms of adaptation to copper-induced stress in two widespread legume plants, white sweet clover (Melilotus albus Merik.) and zigzag clover (Trifolium medium L.), growing in habitats differing in the man-made pollution. An antioxidant plant defense system was activated in response to 10 mM CuSO₄, which is a stress factor. Specific biochemical features related to adaptation to soil contamination with copper were observed in tested plant species. Superoxide dismutase was activated in response to stress in both species from various habitats. M. albus from the impact zone manifested the better capacity of proline accumulation as compared with plants from less polluted habitats. T. medium plants from the impact zone contained more active peroxidase. It was suggested that plants growing for a long time under stressful conditions manifest the greater tolerance to copper ions than plants, which did not experience stress or were subjected to the milder stress.     

Restoring native understory to a woodland invaded by Euonymus fortunei: multiple factors affect success

Invasive species are capable of causing change in native plant communities, but invasion is often associated with other anthropogenic impacts on natural areas, such as habitat fragmentation and associated dispersal limitation for native species. Consequently, invasive species removal alone may not always be sufficient to meet restoration objectives. We tested if invasion and dispersal limitation interact to limit plant community restoration within a forest fragment invaded by Euonymus fortunei. Removal of Euonymus alone did not lead to the recolonization of native plant species. However, planting seedlings increased total native cover in invaded, Euonymus removal, and uninvaded control treatments. The consistent establishment of native plant seedlings across all treatments indicates that Euonymus invasion may have limited ability to displace established plants. In contrast, plant species that we added as seed were unable to establish in invaded plots, indicating that Euonymus invasion limits recruitment of native plant species from seed. Over the course of our experiment, a number of setbacks and surprises occurred, including high levels of herbivory, a windstorm, and extreme drought, all of which likely limited restoration success. Overall, our results indicate that Euonymus may contribute to native species declines, but other factors are important. Thus, invasive species removal alone may not be sufficient to reestablish a diverse native plant community. Instead, impacts on natural areas may need to be mitigated along with invasive species removal for restoration to be successful.     

Overexpression of the Arabidopsis photorespiratory pathway gene, serine: glyoxylate aminotransferase (AtAGT1), leads to salt stress tolerance in transgenic duckweed (Lemna minor)

Salt stress has attracted increasing attention due to its toxic ability to restrict plant growth, and the photorespiration pathway has been shown to develop improved plant tolerance to abiotic stress. In this study, an Arabidopsis photorespiratory pathway gene serine: glyoxylate aminotransferase (SGAT), named as AtAGT1, was successfully overexpressed in duckweed (Lemna minor) to investigate the salinity defense capability in three transgenic overexpressed (OE) lines. Increased SGAT activity and decreased endogenous serine levels in these transgenic plant lines under salt stress resulted in enhanced protection against root abscission, higher maximum quantum yield of photosystem II (Fv/Fm), increased defense from cell damage as a result of improved cell membrane integrity, a decrease of reactive oxygen species (ROS) accumulation, and a strengthened antioxidant system. The salt tolerance in these transgenic OE lines indicates that the improvement of photorespiration stimulated the antioxidant system to scavenge ROS. The change of serine level also suggests the role of serine during salt stress. This transgenic engineering in duckweed not only introduced salt tolerance to this aquatic plant but also reveals a significant role of photorespiration during salinity stress.     

Distinct cold tolerance traits independently vary across genotypes in Drosophila melanogaster

Cold tolerance, the ability to cope with low temperature stress, is a critical adaptation in thermally variable environments. An individual's cold tolerance comprises several traits including minimum temperatures for growth and activity, ability to survive severe cold, and ability to resume normal function after cold subsides. Across species, these traits are correlated, suggesting they were shaped by shared evolutionary processes or possibly share physiological mechanisms. However, the extent to which cold tolerance traits and their associated mechanisms covary within populations has not been assessed. We measured five cold tolerance traits—critical thermal minimum, chill coma recovery, short- and long-term cold tolerance, and cold-induced changes in locomotor behavior—along with cold-induced expression of two genes with possible roles in cold tolerance (heat shock protein 70 and frost)—across 12 lines of Drosophila melanogaster derived from a single population. We observed significant genetic variation in all traits, but few were correlated across genotypes, and these correlations were sex-specific. Further, cold-induced gene expression varied by genotype, but there was no evidence supporting our hypothesis that cold-hardy lines would have either higher baseline expression or induction of stress genes. These results suggest cold tolerance traits possess unique mechanisms and have the capacity to evolve independently.     

Seasonal variation in life history traits in two Drosophila species

Seasonal environmental heterogeneity is cyclic, persistent and geographically widespread. In species that reproduce multiple times annually, environmental changes across seasonal time may create different selection regimes that may shape the population ecology and life history adaptation in these species. Here, we investigate how two closely related species of Drosophila in a temperate orchard respond to environmental changes across seasonal time. Natural populations of Drosophila melanogaster and Drosophila simulans were sampled at four timepoints from June through November to assess seasonal change in fundamental aspects of population dynamics as well as life history traits. D. melanogaster exhibit pronounced change across seasonal time: early in the season, the population is inferred to be uniformly young and potentially represents the early generation following overwintering survivorship. D. melanogaster isofemale lines derived from the early population and reared in a common garden are characterized by high tolerance to a variety of stressors as well as a fast rate of development in the laboratory environment that declines across seasonal time. In contrast, wild D. simulans populations were inferred to be consistently heterogeneous in age distribution across seasonal collections; only starvation tolerance changed predictably over seasonal time in a parallel manner as in D. melanogaster. These results suggest fundamental differences in population and evolutionary dynamics between these two taxa associated with seasonal heterogeneity in environmental parameters and associated selection pressures.     

Soil biota composition and the performance of a noxious weed across its invaded range

The success of invasive plant species is driven, in part, by feedback with soil ecosystems. Yet, how variation in belowground communities across latitudinal gradients affects invader distributions remains poorly understood. To determine the effect of soil communities on the performance of the noxious weed Cirsium arvense across its invaded range, we grew seedlings for 40 days in soils collected across a 699 km linear distance from both inside and outside established populations. We also described the mesofaunal and bacterial communities across all soil samples. We found that C. arvense typically performed better when grown in soils sourced from northern populations than from southern locations where it has a longer invasion history. We also found evidence that C. arvense performed best in soils sourced from outside invaded patches, although this was not consistent across all sites. The bacterial community showed a significant increase in the magnitude of compositional change in invaded sites at higher latitudes, while the mesofaunal community showed the opposite pattern. Bacterial community composition was significantly correlated with C. arvense performance, although mesofaunal community composition was not. Our results demonstrate that the interactions between an invasive plant and associated soil communities change across the invaded range, and the bacterial community in particular may affect variation in plant performance. Observed patterns may be caused by C.arvense presence and time since invasion allowing for an accumulation of species‐specific pathogens in southern soils, while the naïveté of northern soils to invasion results in a more responsive bacterial community. Although these interactions are difficult to predict, such effects could possibly facilitate the establishment of this exotic species to novel locations.     

Impact of climate change on migratory birds: community reassembly versus adaptation

Aim Species can respond to global climate change by range shifts or by phenotypic adaptation. At the community level, range shifts lead to a turnover of species, i.e. community reassembly. In contrast, phenotypic adaptation allows species to persist in situ, conserving community composition. So far, community reassembly and adaptation have mostly been studied separately. In nature, however, both processes take place simultaneously. In migratory birds, climate change has been shown to result in both exchange of species and adaptation of migratory behaviour. The aim of our study is to predict the impact of global climate change on migratory bird communities and to assess the extent to which reassembly and adaptation may contribute to alterations. Location Europe. Methods We analysed the relationship between current climate and the proportion of migratory species across bird assemblages in Europe. The magnitude of community reassembly was measured using spatial variation in the proportion of potentially migratory species. Adaptation was inferred from spatial variation in the proportion of potentially migratory species that actually migrate at a specific site. These spatial relationships were used to make temporal predictions of changes in migratory species under global climate change. Results According to our models, increasing winter temperature is expected to lead to declines in the proportion of migratory species, whereas increasing spring temperature and decreasing spring precipitation may lead to increases. Changes in winter and spring temperature are expected to cause mainly adaptation in migratory activity, while changes in spring precipitation may result in both changes in the proportion of potentially migratory species and adaptation of migratory activity. Main conclusions Under current climate change forecasts, changes in the proportion of migratory species will be modest and the communities of migratory birds in Europe are projected to be altered through adaptation of migratory activity rather than through exchange of species.     

Climate change shifts natural selection and the adaptive potential of the perennial forb Boechera stricta in the Rocky Mountains

Heritable genetic variation is necessary for populations to evolve in response to anthropogenic climate change. However, antagonistic genetic correlations among traits may constrain the rate of adaptation, even if substantial genetic variation exists. We examine potential genetic responses to selection by comparing multivariate genetic variance–covariances of traits and fitness (multivariate Robertson–Price identities) across different environments in a reciprocal transplant experiment of the forb Boechera stricta in the Rocky Mountains. By transplanting populations into four common gardens arrayed along an elevational gradient, and exposing populations to control and snow removal treatments, we simulated future and current climates and snowmelt regimes. Genetic variation in flowering and germination phenology declined in plants moved downslope to warmer, drier sites, suggesting that these traits may have a limited ability to evolve under future climates. Simulated climate change via snow removal altered the strength of selection on flowering traits, but we found little evidence that genetic correlations among traits are likely to affect the rate of adaptation to climate change. Overall, our results suggest that climate change may alter the evolutionary potential of B. stricta, but reduced expression of genetic variation may be a larger impediment to adaptation than constraints imposed by antagonistic genetic correlations.     

Climate change disrupts local adaptation and favours upslope migration

Contemporary climate change is proceeding at an unprecedented rate. The question remains whether populations adapted to historical conditions can persist under rapid environmental change. We tested whether climate change will disrupt local adaptation and reduce population growth rates using the perennial plant Boechera stricta (Brassicaceae). In a large‐scale field experiment conducted over five years, we exposed > 106 000 transplants to historical, current, or future climates and quantified fitness components. Low‐elevation populations outperformed local populations under simulated climate change (snow removal) across all five experimental gardens. Local maladaptation also emerged in control treatments, but it was less pronounced than under snow removal. We recovered local adaptation under snow addition treatments, which reflect historical conditions. Our results revealed that low elevation populations risk rapid decline, whereas upslope migration could enable population persistence and expansion at higher elevation locales. Local adaptation to historical conditions could increase vulnerability to climate change, even for geographically widespread species.     

Lipidomic reprogramming associated with drought stress priming‐enhanced heat tolerance in tall fescue (Festuca arundinacea)

Stress priming by exposing plants to a mild or moderate drought could enhance plant tolerance to subsequent heat stress. Lipids play vital roles in stress adaptation, but how lipidomic profiles change, affecting the cross‐stress tolerance, is largely unknown. The objectives of this study were to perform lipidomics, to analyse the content, composition, and saturation levels of lipids in leaves of tall fescue (Festuca arundinacea) following drought priming and subsequent heat stress, and to identify major lipids and molecular species associated with priming‐enhanced heat tolerance. Plants were initially exposed to drought for 8 days by withholding irrigation and subsequently subjected to 25 days of heat stress (38/33°C day/night) in growth chambers. Drought‐primed plants maintained significantly higher leaf relative water content, chlorophyll content, photochemical efficiency, and lower electrolyte leakage than nonprimed plants under heat stress. Drought priming enhanced the accumulation of phospholipids and glycolipids involved in membrane stabilization and stress signalling (phosphatidic acid, phosphatidylcholine, phosphatidylinositol, phosphatidylglycerol, and digalactosyl diacylglycerol) during subsequent exposure to heat stress. The reprogramming of lipid metabolism for membrane stabilization and signalling in response to drought priming and subsequent exposure to heat stress could contribute to drought priming‐enhanced heat tolerance in cool‐season grass species.     

Fine-scale spatio-temporal patterns in a mountain grassland: do species replace each other in a regular fashion?

Abstract. Long-term ‘high spatial resolution’ permanent plot data were used to determine whether fine-scale species replacements in space occur more often than expected on the basis of random processes, and to test whether these replacements are species-specific. Monte Carlo tests were used. There was no indication of significance in associated positive change (species A increased when B increased); the overall number of significant results was not higher than expected on a random basis. For associated negative change, or replacements (species A increased when B decreased) the overall number of significant results was significantly higher than expected. Significant reciprocal replacements between Deschampsia flexuosa, Festuca rubra and Nardus stricta were frequent; changes in Anthoxanthum alpinum and Polygonum bistorta were uncorrelated with changes of the former three. The first three species thus use the ‘same’ space. Both the latter species often reproduce by seeds and their turnover is much higher. The prevalence of negative correlations of changes (i.e. correlation of increase with decrease) supports the concept of an internal structuring within the grassland community.