Plasticity in functional traits in the context of climate change: a case study of the subalpine forb Boechera stricta (Brassicaceae)

Environmental variation often induces shifts in functional traits, yet we know little about whether plasticity will reduce extinction risks under climate change. As climate change proceeds, phenotypic plasticity could enable species with limited dispersal capacity to persist in situ, and migrating populations of other species to establish in new sites at higher elevations or latitudes. Alternatively, climate change could induce maladaptive plasticity, reducing fitness, and potentially stalling adaptation and migration. Here, we quantified plasticity in life history, foliar morphology, and ecophysiology in Boechera stricta (Brassicaceae), a perennial forb native to the Rocky Mountains. In this region, warming winters are reducing snowpack and warming springs are advancing the timing of snow melt. We hypothesized that traits that were historically advantageous in hot and dry, low‐elevation locations will be favored at higher elevation sites due to climate change. To test this hypothesis, we quantified trait variation in natural populations across an elevational gradient. We then estimated plasticity and genetic variation in common gardens at two elevations. Finally, we tested whether climatic manipulations induce plasticity, with the prediction that plants exposed to early snow removal would resemble individuals from lower elevation populations. In natural populations, foliar morphology and ecophysiology varied with elevation in the predicted directions. In the common gardens, trait plasticity was generally concordant with phenotypic clines from the natural populations. Experimental snow removal advanced flowering phenology by 7 days, which is similar in magnitude to flowering time shifts over 2–3 decades of climate change. Therefore, snow manipulations in this system can be used to predict eco‐evolutionary responses to global change. Snow removal also altered foliar morphology, but in unexpected ways. Extensive plasticity could buffer against immediate fitness declines due to changing climates.     

Evolutionary potential of Chamaecrista fasciculata in relation to climate change. II. Genetic architecture of three populations reciprocally planted along an environmental gradient in the great plains

Climate change will test the evolutionary potential of populations. Information regarding the genetic architecture within and among populations is essential for prediction of evolutionary outcomes. However, little is known about the distribution of genetic variation for relevant traits in natural populations or alteration of genetic architecture in a changing environment. In this study, pedigreed families from three populations of the annual prairie legume Chamaecrista fasciculata were reciprocally transplanted in three environments across a broad latitudinal range in the Great Plains. The underlying premise of this work is that northern populations will in the future experience climates similar to current-day climates further south. Estimates of narrow-sense heritability ranged from 0.053 to 0.481, suggesting the potential for evolutionary change is possible for most traits. In general, the northern population harbored less genetic variation and had lower heritability for traits than the southern population. This population also experienced large reductions in fitness, as measured by estimated lifetime fecundity, when raised in either the intermediate or the southern climate, whereas the difference between the intermediate and southern population was less extreme. For fecundity, the pattern of cross-environment additive genetic correlations was antagonistic to evolutionary change in four of six cases when native and nonnative sites were compared. Six additional antagonistic positive correlations were found for the rate of phenological development and leaf thickness. Overall, the data suggest that if climate changes as predicted, the northern population will face a severe evolutionary challenge in the future because of low heritabilities, cross-environment genetic correlations antagonistic to selection, and demographic instability due to lower seed production in a hotter and drier climate.     

Evolutionary constraints mediate extinction risk under climate change

Mounting evidence suggests that rapid evolutionary adaptation may rescue some organisms from the impacts of climate change. However, evolutionary constraints might hinder this process, especially when different aspects of environmental change generate antagonistic selection on genetically correlated traits. Here, we use individual-based simulations to explore how genetic correlations underlying the thermal physiology of ectotherms might influence their responses to the two major components of climate change—increases in mean temperature and thermal variability. We found that genetic correlations can influence population dynamics under climate change, with declines in population size varying three-fold depending on the type of correlation present. Surprisingly, populations whose thermal performance curves were constrained by genetic correlations often declined less rapidly than unconstrained populations. Our results suggest that accurate forecasts of the impact of climate change on ectotherms will require an understanding of the genetic architecture of the traits under selection.     

Similarity in G matrix structure among natural populations of Arabidopsis lyrata

Understanding the stability of the G matrix in natural populations is fundamental for predicting evolutionary trajectories; yet, the extent of its spatial variation and how this impacts responses to selection remain open questions. With a nested paternal half‐sib crossing design and plants grown in a field experiment, we examined differences in the genetic architecture of flowering time, floral display, and plant size among four Scandinavian populations of Arabidopsis lyrata. Using a multivariate Bayesian framework, we compared the size, shape, and orientation of G matrices and assessed their potential to facilitate or constrain trait evolution. Flowering time, floral display and rosette size varied among populations and significant additive genetic variation within populations indicated potential to evolve in response to selection. Yet, some characters, including flowering start and number of flowers, may not evolve independently because of genetic correlations. Using a multivariate framework, we found few differences in the genetic architecture of traits among populations. G matrices varied mostly in size rather than shape or orientation. Differences in multivariate responses to selection predicted from differences in G were small, suggesting overall matrix similarity and shared constraints to trait evolution among populations.     

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.     

Antagonistic selection and pleiotropy constrain the evolution of plant chemical defenses

When pleiotropy is present, genetic correlations may constrain the evolution of ecologically important traits. We used a quantitative genetics approach to investigate constraints on the evolution of secondary metabolites in a wild mustard, Boechera stricta. Much of the genetic variation in chemical composition of glucosinolates in B. stricta is controlled by a single locus, BCMA1/3. In a large‐scale common garden experiment under natural conditions, we quantified fitness and glucosinolate profile in two leaf types and in fruits. We estimated genetic variances and covariances (the G ‐matrix) and selection on chemical profile in each tissue. Chemical composition of defenses was strongly genetically correlated between tissues. We found antagonistic selection between defense composition in leaves and fruits: compounds that were favored in leaves were disadvantageous in fruits. The positive genetic correlations and antagonistic selection led to strong constraints on the evolution of defenses in leaves and fruits. In a hypothetical population with no genetic variation at BCMA1/3, we found no evidence for genetic constraints, indicating that pleiotropy affecting chemical profile in multiple tissues drives constraints on the evolution of secondary metabolites.     

Revealing hidden evolutionary capacity to cope with global change

The extent to which global change will impact the long‐term persistence of species depends on their evolutionary potential to adapt to future conditions. While the number of studies that estimate the standing levels of adaptive genetic variation in populations under predicted global change scenarios is growing all the time, few studies have considered multiple environments simultaneously and even fewer have considered evolutionary potential in multivariate context. Because conditions will not be constant, adaptation to climate change is fundamentally a multivariate process so viewing genetic variances and covariances over multivariate space will always be more informative than relying on bivariate genetic correlations between traits. A multivariate approach to understanding the evolutionary capacity to cope with global change is necessary to avoid misestimating adaptive genetic variation in the dimensions in which selection will act. We assessed the evolutionary capacity of the larval stage of the marine polychaete Galeolaria caespitosa to adapt to warmer water temperatures. Galeolaria is an important habitat‐forming species in Australia, and its earlier life‐history stages tend to be more susceptible to stress. We used a powerful quantitative genetics design that assessed the impacts of three temperatures on subsequent survival across over 30 000 embryos across 204 unique families. We found adaptive genetic variation in the two cooler temperatures in our study, but none in the warmest temperature. Based on these results, we would have concluded that this species has very little capacity to evolve to the warmest temperature. However, when we explored genetic variation in multivariate space, we found evidence that larval survival has the potential to evolve even in the warmest temperatures via correlated responses to selection across thermal environments. Future studies should take a multivariate approach to estimating evolutionary capacity to cope with global change lest they misestimate a species’ true adaptive potential.     

Evolutionary dynamics of the leaf phenological cycle in an oak metapopulation along an elevation gradient

It has been predicted that environmental changes will radically alter the selective pressures on phenological traits. Long‐lived species, such as trees, will be particularly affected, as they may need to undergo major adaptive change over only one or a few generations. The traits describing the annual life cycle of trees are generally highly evolvable, but nothing is known about the strength of their genetic correlations. Tight correlations can impose strong evolutionary constraints, potentially hampering the adaptation of multivariate phenological phenotypes. In this study, we investigated the evolutionary, genetic and environmental components of the timing of leaf unfolding and senescence within an oak metapopulation along an elevation gradient. Population divergence, estimated from in situ and common‐garden data, was compared to expectations under neutral evolution, based on microsatellite markers. This approach made it possible (1) to evaluate the influence of genetic correlation on multivariate local adaptation to elevation and (2) to identify traits probably exposed to past selective pressures due to the colder climate at high elevation. The genetic correlation was positive but very weak, indicating that genetic constraints did not shape the local adaptation pattern for leaf phenology. Both spring and fall (leaf unfolding and senescence, respectively) phenology timings were involved in local adaptation, but leaf unfolding was probably the trait most exposed to climate change‐induced selection. Our data indicated that genetic variation makes a much smaller contribution to adaptation than the considerable plastic variation displayed by a tree during its lifetime. The evolutionary potential of leaf phenology is, therefore, probably not the most critical aspect for short‐term population survival in a changing climate.     

PLEIOTROPY CAUSES LONG-TERM GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION IN BRASSICA RAPA

Fundamental, long-term genetic trade-offs constrain life-history evolution in wild crucifer populations. I studied patterns of genetic constraint in Brassica rapa by estimating genetic correlations among life-history components by quantitative genetic analyses among ten wild populations, and within four populations. Genetic correlations between age and size at first reproduction were always greater than +0.8 within and among all populations studied. Although quantitative genetics might provide insight about genetic constraints if genetic parameters remain approximately constant, little evidence has been available to determine the constancy of genetic correlations. I found strong and consistent estimates of genetic correlations between life-history components, which were very similar within four natural populations. Population differentiation also showed these same trade-offs, resulting from long-term genetic constraint. For some traits, evolutionary changes among populations were incompatible with a model of genetic drift. Historical patterns of natural selection were inferred from population differentiation, suggesting that correlated response to selection has caused some traits to evolve opposite to the direct forces of natural selection. Comparison with Arabidopsis suggests that these life-history trade-offs are caused by genes that regulate patterns of resource allocation to different components of fitness. Ecological and energetic models may correctly predict these trade-offs because there is little additive genetic variation for rates of resource acquisition, but resource allocation is genetically variable.     

SEXUAL CONFLICT AND THE MAINTENANCE OF MULTIVARIATE GENETIC VARIATION

Mate choice should erode additive genetic variation in sexual displays, yet these traits often harbor substantial genetic variation. Nevertheless, recent developments in quantitative genetics have suggested that multivariate genetic variation in the combinations of traits under selection may still be depleted. Accordingly, the erosion and maintenance of variation may only be detectable by studying whole suites of traits. One potential process favoring the maintenance of genetic variance in multiple trait combinations is the modification of sexual selection via sexually antagonistic interactions between males and females. Here we consider how interlocus sexual conflict can shape the genetic architecture of male sexual traits in the cricket, Teleogryllus commodus. In this species, the ability of each sex to manipulate insemination success significantly alters the selection acting on male courtship call properties. Using a quantitative genetic breeding design we estimated the additive genetic variation in these traits and then predicted the change in variation due to previously documented patterns of sexual selection. Our results indicate that female choice should indeed deplete multivariate genetic variance, but that sexual conflict over insemination success may oppose this loss of variance. We suggest that changes in the direction of selection due to sexually antagonistic interactions will be an important and potentially widespread factor in maintaining multivariate genetic variation.     

In situ marker‐based assessment of leaf trait evolutionary potential in a marginal European beech population

Evolutionary processes are expected to be crucial for the adaptation of natural populations to environmental changes. In particular, the capacity of rear edge populations to evolve in response to the species limiting conditions remains a major issue that requires to address their evolutionary potential. In situ quantitative genetic studies based on molecular markers offer the possibility to estimate evolutionary potentials manipulating neither the environment nor the individuals on which phenotypes are measured. The goal of this study was to estimate heritability and genetic correlations of a suite of leaf functional traits involved in climate adaptation for a natural population of the tree Fagus sylvatica, growing at the rear edge of the species range. Using two marker‐based quantitative genetics approaches, we obtained consistent and significant estimates of heritability for leaf phenological (phenology of leaf flush), morphological (mass, area, ratio mass/area) and physiological (δ¹³C, nitrogen content) traits. Moreover, we found only one significant positive genetic correlation between leaf area and leaf mass, which likely reflected mechanical constraints. We conclude first that the studied population has considerable genetic diversity for important ecophysiological traits regarding drought adaptation and, second, that genetic correlations are not likely to impose strong genetic constraints to future population evolution. Our results bring important insights into the question of the capacity of rear edge populations to evolve.     

The role of ecology,neutral processes and antagonistic coevolution in an apparent sexual arms race

Some of the strongest examples of a sexual ‘arms race’ come from observations of correlated evolution in sexually antagonistic traits among populations. However, it remains unclear whether these cases truly represent sexually antagonistic coevolution; alternatively, ecological or neutral processes might also drive correlated evolution. To investigate these alternatives, we evaluated the contributions of intersex genetic correlations, ecological context, neutral genetic divergence and sexual coevolution in the correlated evolution of antagonistic traits among populations of Gerris incognitus water striders. We could not detect intersex genetic correlations for these sexually antagonistic traits. Ecological variation was related to population variation in the key female antagonistic trait (spine length, a defence against males), as well as body size. Nevertheless, population covariation between sexually antagonistic traits remained substantial and significant even after accounting for all of these processes. Our results therefore provide strong evidence for a contemporary sexual arms race.     

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.     

Will phenotypic plasticity affecting flowering phenology keep pace with climate change?

Rising temperatures have begun to shift flowering time, but it is unclear whether phenotypic plasticity can accommodate projected temperature change for this century. Evaluating clines in phenological traits and the extent and variation in plasticity can provide key information on assessing risk of maladaptation and developing strategies to mitigate climate change. In this study, flower phenology was examined in 52 populations of big sagebrush (Artemisia tridentata) growing in three common gardens. Flowering date (anthesis) varied 91 days from late July to late November among gardens. Mixed‐effects modeling explained 79% of variation in flowering date, of which 46% could be assigned to plasticity and genetic variation in plasticity and 33% to genetics (conditional R² = 0.79, marginal R² = 0.33). Two environmental variables that explained the genetic variation were photoperiod and the onset of spring, the Julian date of accumulating degree‐days >5 °C reaching 100. The genetic variation was mapped for contemporary and future climates (decades 2060 and 2090), showing flower date change varies considerably across the landscape. Plasticity was estimated to accommodate, on average, a ±13‐day change in flowering date. However, the examination of genetic variation in plasticity suggests that the magnitude of plasticity could be affected by variation in the sensitivity to photoperiod and temperature. In a warmer common garden, lower‐latitude populations have greater plasticity (+16 days) compared to higher‐latitude populations (+10 days). Mapped climatypes of flowering date for contemporary and future climates illustrate the wide breadth of plasticity and large geographic overlap. Our research highlights the importance of integrating information on genetic variation, phenotypic plasticity and climatic niche modeling to evaluate plant responses and elucidate vulnerabilities to climate change.     

Grow with the flow: a latitudinal cline in physiology is associated with more variable precipitation in Erythranthe cardinalis

Local adaptation is commonly observed in nature: organisms perform well in their natal environment, but poorly outside it. Correlations between traits and latitude, or latitudinal clines, are among the most common pieces of evidence for local adaptation, but identifying the traits under selection and the selective agents is challenging. Here, we investigated a latitudinal cline in growth and photosynthesis across 16 populations of the perennial herb Erythranthe cardinalis (Phrymaceae). Using machine learning methods, we identify interannual variation in precipitation as a likely selective agent: southern populations from more variable environments had higher photosynthetic rates and grew faster. We hypothesize that selection may favour a more annualized life history – grow now rather than save for next year – in environments where severe droughts occur more often. Thus, our study provides insight into how species may adapt if Mediterranean climates become more variable due to climate change.     

Local selection modifies phenotypic divergence among Rana temporaria populations in the presence of gene flow

In ectotherms, variation in life history traits among populations is common and suggests local adaptation. However, geographic variation itself is not a proof for local adaptation, as genetic drift and gene flow may also shape patterns of quantitative variation. We studied local and regional variation in means and phenotypic plasticity of larval life history traits in the common frog Rana temporaria using six populations from central Sweden, breeding in either open‐canopy or partially closed‐canopy ponds. To separate local adaptation from genetic drift, we compared differentiation in quantitative genetic traits (Q_ST) obtained from a common garden experiment with differentiation in presumably neutral microsatellite markers (F_ST). We found that R. temporaria populations differ in means and plasticities of life history traits in different temperatures at local, and in F_ST at regional scale. Comparisons of differentiation in quantitative traits and in molecular markers suggested that natural selection was responsible for the divergence in growth and development rates as well as in temperature‐induced plasticity, indicating local adaptation. However, at low temperature, the role of genetic drift could not be separated from selection. Phenotypes were correlated with forest canopy closure, but not with geographical or genetic distance. These results indicate that local adaptation can evolve in the presence of ongoing gene flow among the populations, and that natural selection is strong in this system.     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

Picturing local adaptation: Spectral and structural traits from drone remote sensing reveal clinal responses to climate transfer in common-garden trials of interior spruce (Picea engelmannii × glauca)

Common-garden trials of forest trees provide phenotype data used to assess growth and local adaptation; this information is foundational to tree breeding programs, genecology, and gene conservation. As jurisdictions consider assisted migration strategies to match populations to suitable climates, in situ progeny and provenance trials provide experimental evidence of adaptive responses to climate change. We used drone technology, multispectral imaging, and digital aerial photogrammetry to quantify spectral traits related to stress, photosynthesis, and carotenoids, and structural traits describing crown height, size, and complexity at six climatically disparate common-garden trials of interior spruce (Picea engelmannii × glauca) in western Canada. Through principal component analysis, we identified key components of climate related to temperature, moisture, and elevational gradients. Phenotypic clines in remotely sensed traits were analyzed as trait correlations with provenance climate transfer distances along principal components (PCs). We used traits showing clinal variation to model best linear unbiased predictions for tree height (R² = .98–.99, root mean square error [RMSE] = 0.06–0.10 m) and diameter at breast height (DBH, R² = .71–.97, RMSE = 2.57–3.80 mm) and generated multivariate climate transfer functions with the model predictions. Significant (p < .05) clines were present for spectral traits at all sites along all PCs. Spectral traits showed stronger clinal variation than structural traits along temperature and elevational gradients and along moisture gradients at wet, coastal sites, but not at dry, interior sites. Spectral traits may capture patterns of local adaptation to temperature and montane growing seasons which are distinct from moisture-limited patterns in stem growth. This work demonstrates that multispectral indices improve the assessment of local adaptation and that spectral and structural traits from drone remote sensing produce reliable proxies for ground-measured height and DBH. This phenotyping framework contributes to the analysis of common-garden trials towards a mechanistic understanding of local adaptation to climate.     

Clinal adaptation and adaptive plasticity in Artemisia californica: implications for the response of a foundation species to predicted climate change

Local adaptation and plasticity pose significant obstacles to predicting plant responses to future climates. Although local adaptation and plasticity in plant functional traits have been documented for many species, less is known about population‐level variation in plasticity and whether such variation is driven by adaptation to environmental variation. We examined clinal variation in traits and performance – and plastic responses to environmental change – for the shrub Artemisia californica along a 700 km gradient characterized (from south to north) by a fourfold increase in precipitation and a 61% decrease in interannual precipitation variation. Plants cloned from five populations along this gradient were grown for 3 years in treatments approximating the precipitation regimes of the north and south range margins. Most traits varying among populations did so clinally; northern populations (vs. southern) had higher water‐use efficiencies and lower growth rates, C : N ratios and terpene concentrations. Notably, there was variation in plasticity for plant performance that was strongly correlated with source site interannual precipitation variability. The high‐precipitation treatment (vs. low) increased growth and flower production more for plants from southern populations (181% and 279%, respectively) than northern populations (47% and 20%, respectively). Overall, precipitation variability at population source sites predicted 86% and 99% of variation in plasticity in growth and flowering, respectively. These striking, clinal patterns in plant traits and plasticity are indicative of adaptation to both the mean and variability of environmental conditions. Furthermore, our analysis of long‐term coastal climate data in turn indicates an increase in interannual precipitation variation consistent with most global change models and, unexpectedly, this increased variation is especially pronounced at historically stable, northern sites. Our findings demonstrate the critical need to integrate fundamental evolutionary processes into global change models, as contemporary patterns of adaptation to environmental clines will mediate future plant responses to projected climate change.