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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Transgenerational and Within-Generation Plasticity in Response to Climate Change: Insights from a Manipulative Field Experiment across an Elevational Gradient.

Parental environmental effects-or transgenerational plasticity-can influence an individual's phenotype or fitness yet remain underexplored in the context of global change. Using the perennial self-pollinating plant Boechera stricta, we explored the effects of climate change on transgenerational and within-generation plasticity in dormancy, germination, growth, and survival. We first conducted a snow removal experiment in the field, in which we transplanted 16 families of known origin into three common gardens at different elevations and exposed half of the siblings to contemporary snow dynamics and half to early snow removal. We planted the offspring of these individuals in a factorial manipulation of temperature and water level in the growth chamber and reciprocally transplanted them across all parental environments in the field. The growth chamber experiment revealed that the effects of transgenerational plasticity persist in traits expressed after establishment, even when accounting for parental effects on seed mass. The field experiment showed that transgenerational and within-generation plasticity can interact and that plasticity varies clinally in populations distributed across elevations. These findings demonstrate that transgenerational plasticity can influence fitness-related traits and should be incorporated in studies of biological responses to climate change.

Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment.

Climate change has induced pronounced shifts in the reproductive phenology of plants, yet we know little about which environmental factors contribute to interspecific variation in responses and their effects on fitness. We integrate data from a 43 yr record of first flowering for six species in subalpine Colorado meadows with a 3 yr snow manipulation experiment on the perennial forb Boechera stricta (Brassicaceae) from the same site. We analyze shifts in the onset of flowering in relation to environmental drivers known to influence phenology: the timing of snowmelt, the accumulation of growing degree days, and photoperiod. Variation in responses to climate change depended on the sequence in which species flowered, with early-flowering species reproducing faster, at a lower heat sum, and under increasingly disparate photoperiods relative to later-flowering species. Early snow-removal treatments confirm that the timing of snowmelt governs observed trends in flowering phenology of B. stricta and that climate change can reduce the probability of flowering, thereby depressing fitness. Our findings suggest that climate change is decoupling historical combinations of photoperiod and temperature and outpacing phenological changes for our focal species. Accurate predictions of biological responses to climate change require a thorough understanding of the factors driving shifts in phenology.

Ecological causes and consequences of flower color polymorphism in a self-pollinating plant (Boechera stricta).

Intraspecific variation in flower color is often attributed to pollinator-mediated selection, yet this mechanism cannot explain flower color polymorphisms in self-pollinating species. Indirect selection mediated via biotic and abiotic stresses could maintain flower color variation in these systems. The selfing forb, Boechera stricta, typically displays white flowers, but some individuals produce purple flowers. We quantified environmental correlates of flower color in natural populations. To disentangle plasticity from genotypic variation, we performed a multiyear field experiment in five gardens. In controlled conditions, we evaluated herbivore preferences and the effects of drought stress and soil pH on flower color expression. In natural populations, purple-flowered individuals experienced lower foliar herbivory than did their white-flowered counterparts. This pattern also held in the common gardens. Additionally, low-elevation environments induced pigmented flowers (plasticity), and the likelihood of floral pigmentation decreased with source elevation of maternal families (genetic cline). Viability selection favored families with pigmented flowers. In the laboratory, herbivores exerted greater damage on tissue derived from white- vs purple-flowered individuals. Furthermore, drought induced pigmentation in white-flowered lineages, and white-flowered plants had a fecundity advantage in the well-watered control. Flower color variation in selfing species is probably maintained by herbivory, drought stress, and other abiotic factors that vary spatially.

Unifying genetic canalization, genetic constraint, and genotype-by-environment interaction: QTL by genomic background by environment interaction of flowering time in Boechera stricta.

Natural populations exhibit substantial variation in quantitative traits. A quantitative trait is typically defined by its mean and variance, and to date most genetic mapping studies focus on loci altering trait means but not (co)variances. For single traits, the control of trait variance across genetic backgrounds is referred to as genetic canalization. With multiple traits, the genetic covariance among different traits in the same environment indicates the magnitude of potential genetic constraint, while genotype-by-environment interaction (GxE) concerns the same trait across different environments. While some have suggested that these three attributes of quantitative traits are different views of similar concepts, it is not yet clear, however, whether they have the same underlying genetic mechanism. Here, we detect quantitative trait loci (QTL) influencing the (co)variance of phenological traits in six distinct environments in Boechera stricta, a close relative of Arabidopsis. We identified nFT as the QTL altering the magnitude of phenological trait canalization, genetic constraint, and GxE. Both the magnitude and direction of nFT's canalization effects depend on the environment, and to our knowledge, this reversibility of canalization across environments has not been reported previously. nFT's effects on trait covariance structure (genetic constraint and GxE) likely result from the variable and reversible canalization effects across different traits and environments, which can be explained by the interaction among nFT, genomic backgrounds, and environmental stimuli. This view is supported by experiments demonstrating significant nFT by genomic background epistatic interactions affecting phenological traits and expression of the candidate gene, FT. In contrast to the well-known canalization gene Hsp90, the case of nFT may exemplify an alternative mechanism: Our results suggest that (at least in traits with major signal integrators such as flowering time) genetic canalization, genetic constraint, and GxE may have related genetic mechanisms resulting from interactions among major QTL, genomic backgrounds, and environments.

Stability and generalization in seed dispersal networks: a case study of frugivorous fish in Neotropical wetlands.

When species within guilds perform similar ecological roles, functional redundancy can buffer ecosystems against species loss. Using data on the frequency of interactions between fish and fruit, we assessed whether co-occurring frugivores provide redundant seed dispersal services in three species-rich Neotropical wetlands. Our study revealed that frugivorous fishes have generalized diets; however, large-bodied fishes had greater seed dispersal breadth than small species, in some cases, providing seed dispersal services not achieved by smaller fish species. As overfishing disproportionately affects big fishes, the extirpation of these species could cause larger secondary extinctions of plant species than the loss of small specialist frugivores. To evaluate the consequences of frugivore specialization for network stability, we extracted data from 39 published seed dispersal networks of frugivorous birds, mammals and fish (our networks) across ecosystems. Our analysis of interaction frequencies revealed low frugivore specialization and lower nestedness than analyses based on binary data (presence-absence of interactions). In that case, ecosystems may be resilient to loss of any given frugivore. However, robustness to frugivore extinction declines with specialization, such that networks composed primarily of specialist frugivores are highly susceptible to the loss of generalists. In contrast with analyses of binary data, recently developed algorithms capable of modelling interaction strengths provide opportunities to enhance our understanding of complex ecological networks by accounting for heterogeneity of frugivore-fruit interactions.

Plant fitness in a rapidly changing world.

Modern reliance on fossil fuels has ushered in extreme temperatures globally and abnormal precipitation patterns in many regions. Although the climate is changing rapidly, other agents of natural selection such as photoperiod remain constant. This decoupling of previously reliable environmental cues shifts adaptive landscapes, favors novel suites of traits and likely increases the extinction risk of local populations. Here, I examine the fitness consequences of changing climates. Meta-analyses demonstrate that simulated future climates depress viability and fecundity components of fitness for native plant species in the short term, which could reduce population growth rates. Contracting populations that cannot adapt or adjust plastically to new climates might not be capable of producing sufficient migrants to track changing conditions.

3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture.

Identification of genes that control root system architecture in crop plants requires innovations that enable high-throughput and accurate measurements of root system architecture through time. We demonstrate the ability of a semiautomated 3D in vivo imaging and digital phenotyping pipeline to interrogate the quantitative genetic basis of root system growth in a rice biparental mapping population, Bala × Azucena. We phenotyped >1,400 3D root models and >57,000 2D images for a suite of 25 traits that quantified the distribution, shape, extent of exploration, and the intrinsic size of root networks at days 12, 14, and 16 of growth in a gellan gum medium. From these data we identified 89 quantitative trait loci, some of which correspond to those found previously in soil-grown plants, and provide evidence for genetic tradeoffs in root growth allocations, such as between the extent and thoroughness of exploration. We also developed a multivariate method for generating and mapping central root architecture phenotypes and used it to identify five major quantitative trait loci (r(2) = 24-37%), two of which were not identified by our univariate analysis. Our imaging and analytical platform provides a means to identify genes with high potential for improving root traits and agronomic qualities of crops.