Elevated [CO2] and temperature augment gas exchange and shift the fitness landscape in a montane forb.

Climate change is simultaneously increasing carbon dioxide concentrations ([CO2]) and temperature. These factors could interact to influence plant physiology and performance. Alternatively, increased [CO2] may offset costs associated with elevated temperatures. Furthermore, the interaction between elevated temperature and [CO2] may differentially affect populations from along an elevational gradient and disrupt local adaptation. We conducted a multifactorial growth chamber experiment to examine the interactive effects of temperature and [CO2] on fitness and ecophysiology of diverse accessions of Boechera stricta (Brassicaceae) sourced from a broad elevational gradient in Colorado. We tested whether increased [CO2] would enhance photosynthesis across accessions, and whether warmer conditions would depress the fitness of high-elevation accessions owing to steep reductions in temperature with increasing elevation in this system. Elevational clines in [CO2] are not as evident, making it challenging to predict how locally adapted ecotypes will respond to elevated [CO2]. This experiment revealed that elevated [CO2] increased photosynthesis and intrinsic water use efficiency across all accessions. However, these instantaneous responses to treatments did not translate to changes in fitness. Instead, increased temperatures reduced the probability of reproduction for all accessions. Elevated [CO2] and increased temperatures interacted to shift the adaptive landscape, favoring lower elevation accessions for the probability of survival and fecundity. Our results suggest that elevated temperatures and [CO2] associated with climate change could have severe negative consequences, especially for high-elevation populations.

The effect of global change on the expression and evolution of floral traits.

BACKGROUND: Pollinators impose strong selection on floral traits. Indeed, pollinator syndromes are the result of these strong selective forces, but other abiotic and biotic agents also drive the evolution of floral traits and influence plant reproduction. Global change is expected to have widespread effects on biotic and abiotic systems resulting in novel selection on floral traits under future conditions. SCOPE: Global change has depressed pollinator abundance and altered abiotic conditions, thereby exposing flowering plant species to novel suites of selective pressures. Here we consider how biotic and abiotic factors interact to shape the expression and evolution of various floral characteristics (the targets of selection), including floral size, color, physiology, reward quantity and quality, and longevity amongst other traits. We examine cases in which selection imposed by climatic factors conflicts with pollinator-mediated selection. Additionally, we explore how floral traits respond to environmental changes through phenotypic plasticity and how that can alter plant fecundity. In this review, we evaluate how global change may shift the expression and evolution of floral phenotypes. CONCLUSIONS: Floral traits evolve in response to multiple interacting agents of selection. Different agents can sometimes exert conflicting selection. For example, pollinators often prefer large flowers, but drought stress can favor the evolution of smaller flowers, and the size of floral organs can evolve as a trade-off between selection mediated by these opposing actors. Nevertheless, few studies have factorially manipulated abiotic and biotic agents of selection to disentangle their relative strengths and directions of selection. The literature has more often evaluated plastic responses of floral traits to stressors than it has considered how abiotic factors alter selection on these traits. Furthermore, global change will likely alter the selective landscape through changes in the abundance and community compositions of mutualists and antagonists and novel abiotic conditions. We encourage future work to consider a more holistic model of floral evolution, which will enable more robust predictions about floral evolution and plant reproduction as global change progresses.

Phenotypic plasticity and genetic diversity shed light on endemism of rare Boechera perstellata and its potential vulnerability to climate warming.

The rapid pace of contemporary environmental change puts many species at risk, especially rare species constrained by limited capacity to adapt or migrate due to low genetic diversity and/or fitness. But the ability to acclimate can provide another way to persist through change. We compared the capacity of rare Boechera perstellata (Braun's rockcress) and widespread B. laevigata to acclimate to change. We investigated the phenotypic plasticity of growth, biomass allocation, and leaf morphology of individuals of B. perstellata and B. laevigata propagated from seed collected from several populations throughout their ranges in a growth chamber experiment to assess their capacity to acclimate. Concurrently, we assessed the genetic diversity of sampled populations using 17 microsatellite loci to assess evolutionary potential. Plasticity was limited in both rare B. perstellata and widespread B. laevigata, but differences in the plasticity of root traits between species suggest that B. perstellata may have less capacity to acclimate to change. In contrast to its widespread congener, B. perstellata exhibited no plasticity in response to temperature and weaker plastic responses to water availability. As expected, B. perstellata also had lower levels of observed heterozygosity than B. laevigata at the species level, but population-level trends in diversity measures were inconsistent due to high heterogeneity among B. laevigata populations. Overall, the ability of phenotypic plasticity to broadly explain the rarity of B. perstellata versus commonness of B. laevigata is limited. However, some contextual aspects of our plasticity findings compared with its relatively low genetic variability may shed light on the narrow range and habitat associations of B. perstellata and suggest its vulnerability to climate warming due to acclimatory and evolutionary constraints.

The Boechera model system for evolutionary ecology.

Model systems in biology expand the research capacity of individuals and the community. Closely related to Arabidopsis, the genus Boechera has emerged as an important ecological model owing to the ability to integrate across molecular, functional, and eco-evolutionary approaches. Boechera species are broadly distributed in relatively undisturbed habitats predominantly in western North America and provide one of the few experimental systems for identification of ecologically important genes through genome-wide association studies and investigations of selection with plants in their native habitats. The ecologically, evolutionarily, and agriculturally important trait of apomixis (asexual reproduction via seeds) is common in the genus, and field experiments suggest that abiotic and biotic environments shape the evolution of sex. To date, population genetic studies have focused on the widespread species B. stricta, detailing population divergence and demographic history. Molecular and ecological studies show that balancing selection maintains genetic variation in ~10% of the genome, and ecological trade-offs contribute to complex trait variation for herbivore resistance, flowering phenology, and drought tolerance. Microbiome analyses have shown that host genotypes influence leaf and root microbiome composition, and the soil microbiome influences flowering phenology and natural selection. Furthermore, Boechera offers numerous opportunities for investigating biological responses to global change. In B. stricta, climate change has induced a shift of >2 weeks in the timing of first flowering since the 1970s, altered patterns of natural selection, generated maladaptation in previously locally-adapted populations, and disrupted life history trade-offs. Here we review resources and results for this eco-evolutionary model system and discuss future research directions.

Water and nutrient availability exert selection on reproductive phenology.

PREMISE: Global change has changed resource availability to plants, which could shift the adaptive landscape. We hypothesize that novel water and nutrient availability combinations alter patterns of natural selection on reproductive phenology in Boechera stricta (Brassicaceae) and influence the evolution of local adaptation. METHODS: We conducted a multifactorial greenhouse study using 35 accessions of B. stricta sourced from a broad elevational gradient in the Rocky Mountains. We exposed full siblings to three soil water and two nutrient availability treatment levels, reflecting current and projected future conditions. In addition, we quantified fitness (seed count) and four phenological traits: the timing of first flowering, the duration of flowering, and height and leaf number at flowering. RESULTS: Selection favored early flowering and longer duration of flowering, and the genetic correlation between these traits accorded with the direction of selection. In most treatments, we found selection for increased height, but selection on leaf number depended on water availability, with selection favoring more leaves in well-watered conditions and fewer leaves under severe drought. Low-elevation genotypes had the greatest fitness under drought stress, consistent with local adaptation. CONCLUSIONS: We found evidence of strong selection on these heritable traits. Furthermore, the direction and strength of selection on size at flowering depended on the variable measured (height vs. leaf number). Finally, selection often favored both early flowering and a longer duration of flowering. Selection on these two components of phenology can be difficult to disentangle due to tight genetic correlations.

Genetic trade-offs and unexpected life history traits shape local adaptation in Trifolium repens.

Local adaptation has evolved in numerous taxa across the tree of life in response to divergent selection acting on populations that inhabit different environments (Briscoe Runquist et al., 2019; Hargreaves et al., 2019; Hereford, 2009). The genetic basis of local adaptation has intrigued researchers for decades. In their foundational reciprocal transplant study, Clausen and Hiesey (1960) evaluated the genetics of adaptation primarily using hybrid lines derived from crosses of low elevation and alpine Potentilla glandulosa (Rosaceae) ecotypes. Their work revealed that transgressive segregation can lead to a wider range of trait values than expressed by the parents, complex traits are often genetically correlated and evolve in tandem, and local adaptation is typically polygenic, that is, controlled by many loci of small effect (Clausen & Hiesey, 1960). Within the past 15 years, a burgeoning literature has investigated whether local adaptation evolves through genetic trade-offs, such that local alleles at a QTL (quantitative trait locus) or candidate gene have a fitness advantage in their home environment, but suffer a fitness cost when transplanted into a contrasting habitat type (Mitchell-Olds et al., 2007). Alternatively, local adaptation could arise through conditional neutrality, in which an allele native to one habitat type has elevated fitness in its home site relative to foreign alleles, but is not at a fitness disadvantage elsewhere. Conditional neutrality could maintain local adaptation if gene flow is spatially restricted (Hall et al., 2010). In a From the Cover article in this issue of Molecular Ecology, Wright et al. (2022) examined the genetic basis of local adaptation in white clover (Trifolium repens), discovering strong signatures of local adaptation, and revealing that both genetic trade-offs and conditional neutrality contribute to local adaptation. The most surprising and intriguing result to emerge from this study was that variation in a key antiherbivore defence did not appear to influence contemporary patterns of local adaptation. Rather, divergence in life history strategies was crucial, with early reproduction favoured in the southern garden and delayed reproduction and longer lifespans emerging in the north. These findings highlight the challenges of identifying the multivariate targets of divergent selection in locally-adapted systems, and reveal that not all traits that vary across populations contribute to adaptive differentiation. As studies continue to investigate local adaptation, experiments that manipulate environmental conditions and quantify the magnitude and direction of selection on traits will shed light on the processes that drive local adaptation.

Eco-evolutionary causes and consequences of rarity in plants: a meta-analysis.

Species differ dramatically in their prevalence in the natural world, with many species characterized as rare due to restricted geographic distribution, low local abundance and/or habitat specialization. We investigated the ecoevolutionary causes and consequences of rarity with phylogenetically controlled metaanalyses of population genetic diversity, fitness and functional traits in rare and common congeneric plant species. Our syntheses included 252 rare species and 267 common congeners reported in 153 peer-reviewed articles published from 1978 to 2020 and one manuscript in press. Rare species have reduced population genetic diversity, depressed fitness and smaller reproductive structures than common congeners. Rare species also could suffer from inbreeding depression and reduced fertilization efficiency. By limiting their capacity to adapt and migrate, these characteristics could influence contemporary patterns of rarity and increase the susceptibility of rare species to rapid environmental change. We recommend that future studies present more nuanced data on the extent of rarity in focal species, expose rare and common species to ecologically relevant treatments, including reciprocal transplants, and conduct quantitative genetic and population genomic analyses across a greater array of systems. This research could elucidate the processes that contribute to rarity and generate robust predictions of extinction risks under global change.

Global urban environmental change drives adaptation in white clover.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Local adaptation: Causal agents of selection and adaptive trait divergence.

Divergent selection across the landscape can favor the evolution of local adaptation in populations experiencing contrasting conditions. Local adaptation is widely observed in a diversity of taxa, yet we have a surprisingly limited understanding of the mechanisms that give rise to it. For instance, few have experimentally confirmed the biotic and abiotic variables that promote local adaptation, and fewer yet have identified the phenotypic targets of selection that mediate local adaptation. Here, we highlight critical gaps in our understanding of the process of local adaptation and discuss insights emerging from in-depth investigations of the agents of selection that drive local adaptation, the phenotypes they target, and the genetic basis of these phenotypes. We review historical and contemporary methods for assessing local adaptation, explore whether local adaptation manifests differently across life history, and evaluate constraints on local adaptation.

Selection favors adaptive plasticity in a long-term reciprocal transplant experiment.

Spatial and temporal environmental variation can favor the evolution of adaptive phenotypic plasticity, such that genotypes alter their phenotypes in response to local conditions to maintain fitness across heterogeneous landscapes. When individuals show greater fitness in one habitat than another, asymmetric migration can restrict adaptation to the lower quality environment. In these cases, selection is predicted to favor traits that enhance fitness in the higher-quality (source) habitat at the expense of fitness in the marginal (sink) habitat. Here, we test whether plasticity is adaptive in a system regulated by demographic source-sink dynamics. Vaccinium elliottii (Ericaceae) occurs in dry upland and flood-prone bottomland forests throughout the southeastern United States, but has larger populations and higher average individual fitness in upland sites. We conducted a multi-year field experiment to evaluate whether plasticity in foliar morphology increases survival and lifespan. Both across and within habitats, selection favored plasticity in specific leaf area, stomatal density, and leaf size. Stabilizing selection acted on plasticity in stomatal density within habitats, suggesting that extreme levels of plasticity are disadvantageous. Thus, even in systems driven by source-sink dynamics, temporal and spatial variation in conditions across the landscape and within habitat types can favor the evolution of plasticity.

Costs of reproduction under experimental climate change across elevations in the perennial forb Boechera stricta.

Investment in current reproduction can reduce future fitness by depleting resources needed for maintenance, particularly under environmental stress. These trade-offs influence life-history evolution. We tested whether climate change alters the future-fitness costs of current reproduction in a large-scale field experiment of Boechera stricta (Brassicaceae). Over 6 years, we simulated climate change along an elevational gradient in the Rocky Mountains through snow removal, which accelerates snowmelt and reduces soil water availability. Costs of reproduction were greatest in arid, lower elevations, where high initial reproductive effort depressed future fitness. At mid-elevations, initial reproduction augmented subsequent fitness in benign conditions, but pronounced costs emerged under snow removal. At high elevation, snow removal dampened costs of reproduction by prolonging the growing season. In most scenarios, failed reproduction in response to resource limitation depressed lifetime fecundity. Indeed, fruit abortion only benefited high-fitness individuals under benign conditions. We propose that climate change could shift life-history trade-offs in an environment-dependent fashion, possibly favouring early reproduction and short lifespans in stressful conditions.

Review: Plant eco-evolutionary responses to climate change: Emerging directions.

Contemporary climate change is exposing plant populations to novel combinations of temperatures, drought stress, [CO2] and other abiotic and biotic conditions. These changes are rapidly disrupting the evolutionary dynamics of plants. Despite the multifactorial nature of climate change, most studies typically manipulate only one climatic factor. In this opinion piece, we explore how climate change factors interact with each other and with biotic pressures to alter evolutionary processes. We evaluate the ramifications of climate change across life history stages,and examine how mating system variation influences population persistence under rapid environmental change. Furthermore, we discuss how spatial and temporal mismatches between plants and their mutualists and antagonists could affect adaptive responses to climate change. For example, plant-virus interactions vary from highly pathogenic to mildly facilitative, and are partly mediated by temperature, moisture availability and [CO2]. Will host plants exposed to novel, stressful abiotic conditions be more susceptible to viral pathogens? Finally, we propose novel experimental approaches that could illuminate how plants will cope with unprecedented global change, such as resurrection studies combined with experimental evolution, genomics or epigenetics.

Climate change alters plant-herbivore interactions.

Plant-herbivore interactions have evolved in response to coevolutionary dynamics, along with selection driven by abiotic conditions. We examine how abiotic factors influence trait expression in both plants and herbivores to evaluate how climate change will alter this long-standing interaction. The paleontological record documents increased herbivory during periods of global warming in the deep past. In phylogenetically corrected meta-analyses, we find that elevated temperatures, CO2 concentrations, drought stress and nutrient conditions directly and indirectly induce greater food consumption by herbivores. Additionally, elevated CO2 delays herbivore development, but increased temperatures accelerate development. For annual plants, higher temperatures, CO2 and drought stress increase foliar herbivory. Our meta-analysis also suggests that greater temperatures and drought may heighten florivory in perennials. Human actions are causing concurrent shifts in CO2 , temperature, precipitation regimes and nitrogen deposition, yet few studies evaluate interactions among these changing conditions. We call for additional multifactorial studies that simultaneously manipulate multiple climatic factors, which will enable us to generate more robust predictions of how climate change could disrupt plant-herbivore interactions. Finally, we consider how shifts in insect and plant phenology and distribution patterns could lead to ecological mismatches, and how these changes may drive future adaptation and coevolution between interacting species.

Small spaces, big impacts: contributions of micro-environmental variation to population persistence under climate change.

Individuals within natural populations can experience very different abiotic and biotic conditions across small spatial scales owing to microtopography and other micro-environmental gradients. Ecological and evolutionary studies often ignore the effects of micro-environment on plant population and community dynamics. Here, we explore the extent to which fine-grained variation in abiotic and biotic conditions contributes to within-population variation in trait expression and genetic diversity in natural plant populations. Furthermore, we consider whether benign microhabitats could buffer local populations of some plant species from abiotic stresses imposed by rapid anthropogenic climate change. If microrefugia sustain local populations and communities in the short term, other eco-evolutionary processes, such as gene flow and adaptation, could enhance population stability in the longer term. We caution, however, that local populations may still decline in size as they contract into rare microhabitats and microrefugia. We encourage future research that explicitly examines the role of the micro-environment in maintaining genetic variation within local populations, favouring the evolution of phenotypic plasticity at local scales and enhancing population persistence under global change.

Resource availability alters fitness trade-offs: implications for evolution in stressful environments.

PREMISE: Industrialization and human activities have elevated temperatures and caused novel precipitation patterns, altering soil moisture and nutrient availability. Predicting evolutionary responses to climate change requires information on the agents of selection that drive local adaptation and influence resource acquisition and allocation. Here, we examined the contribution of nutrient and drought stress to local adaptation, and we tested whether trade-offs across fitness components constrain or facilitate adaptation under resource stress. METHODS: We exposed 35 families of Boechera stricta (Brassicaceae) to three levels of water and two levels of nutrient supply in a factorial design in the greenhouse. We sourced maternal families from a broad elevational gradient (2499-3530 m a.s.l.), representing disparate soil moisture and nutrient availability. RESULTS: Concordant with local adaptation, maternal families from arid, low-elevation populations had enhanced fecundity under severe drought over those from more mesic, high-elevation sites. Furthermore, fitness trade-offs between growth and reproductive success depended on the environmental context. Under high, but not low, nutrient levels, we found a negative phenotypic relationship between the probability of reproduction and growth rate. Similarly, a negative phenotypic association only emerged between fecundity and growth under severe drought stress, not the benign water treatment levels, indicating that stressful resource environments alter the direction of trait correlations. Genetic covariances were broadly concordant with these phenotypic patterns. CONCLUSIONS: Despite high heritabilities in all fitness components across treatments, trade-offs between growth and reproduction could constrain adaptation to increasing drought stress and novel nutrient levels.

Natural history collections document biological responses to climate change: A commentary on DeLeo et al. (2019), Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana.

Natural history collections can complement and enhance our research programs in a variety of ways. DeLeo et al. (2019) used herbarium records to study the changes in physiology and phenology in Arabidopsis thaliana (Brassicaceae) due to contemporary climate change. Here, we discuss their approach and results as well as highlight other ways in which herbarium and natural history museum records can be leveraged for future studies.The copyright holder of the image (the herbarium sheet of Arabidopsis thaliana) is the first author, Derek Denney. This article is a commentary on DeLeo et al, 26, 523-538.

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.

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.