Populations of western North American monkeyflowers accrue niche breadth primarily via genotypic divergence in environmental optima.

Niche breadth, the range of environments that individuals, populations, and species can tolerate, is a fundamental ecological and evolutionary property, yet few studies have examined how niche breadth is partitioned across biological scales. We use a published dataset of thermal performance for a single population from each of 10 closely related species of western North American monkeyflowers (genus Mimulus) to investigate whether populations achieve broad thermal niches through general purpose genotypes, specialized genotypes with divergent environmental optima, and/or variation among genotypes in the degree of generalization. We found the strongest relative support for the hypothesis that populations with greater genetic variation for thermal optimum had broader thermal niches, and for every unit increase in among-family variance in thermal optimum, population-level thermal breadth increased by 0.508°C. While the niche breadth of a single genotype represented up to 86% of population-level niche breadth, genotype-level niche breadth had a weaker positive effect on population-level breadth, with every 1°C increase in genotypic thermal breadth resulting in a 0.062°C increase in population breadth. Genetic variation for thermal breadth was not predictive of population-level thermal breadth. These findings suggest that populations of Mimulus species have achieved broad thermal niches primarily through genotypes with divergent thermal optima and to a lesser extent via general-purpose genotypes. Future work examining additional biological hierarchies would provide a more comprehensive understanding of how niche breadth partitioning impacts the vulnerabilities of individuals, populations, and species to environmental change.

A viewpoint on ecological and evolutionary study of plant thermal performance curves in a warming world.

We can understand the ecology and evolution of plant thermal niches through thermal performance curves (TPCs), which are unimodal, continuous reaction norms of performance across a temperature gradient. Though there are numerous plant TPC studies, plants remain under-represented in syntheses of TPCs. Further, few studies quantify plant TPCs from fitness-based measurements (i.e. growth, survival and reproduction at the individual level and above), limiting our ability to draw conclusions from the existing literature about plant thermal adaptation. We describe recent plant studies that use a fitness-based TPC approach to test fundamental ecological and evolutionary hypotheses, some of which have uncovered key drivers of climate change responses. Then, we outline three conceptual questions in ecology and evolutionary biology for future plant TPC studies: (i) Do populations and species harbour genetic variation for TPCs? (ii) Do plant TPCs exhibit plastic responses to abiotic and biotic factors? (iii) Do fitness-based TPCs scale up to population-level thermal niches? Moving forward, plant ecologists and evolutionary biologists can capitalize on TPCs to understand how plasticity and adaptation will influence plant responses to climate change.

The evolution of thermal performance in native and invasive populations of Mimulus guttatus.

The rise of globalization has spread organisms beyond their natural range, allowing further opportunity for species to adapt to novel environments and potentially become invaders. Yet, the role of thermal niche evolution in promoting the success of invasive species remains poorly understood. Here, we use thermal performance curves (TPCs) to test hypotheses about thermal adaptation during the invasion process. First, we tested the hypothesis that if species largely conserve their thermal niche in the introduced range, invasive populations may not evolve distinct TPCs relative to native populations, against the alternative hypothesis that thermal niche and therefore TPC evolution has occurred in the invasive range. Second, we tested the hypothesis that clines of TPC parameters are shallower or absent in the invasive range, against the alternative hypothesis that with sufficient time, standing genetic variation, and temperature-mediated selection, invasive populations would re-establish clines found in the native range in response to temperature gradients. To test these hypotheses, we built TPCs for 18 native (United States) and 13 invasive (United Kingdom) populations of the yellow monkeyflower, Mimulus guttatus. We grew clones of multiple genotypes per population at six temperature regimes in growth chambers. We found that invasive populations have not evolved different thermal optima or performance breadths, providing evidence for evolutionary stasis of thermal performance between the native and invasive ranges after over 200 years post introduction. Thermal optimum increased with mean annual temperature in the native range, indicating some adaptive differentiation among native populations that was absent in the invasive range. Further, native and invasive populations did not exhibit adaptive clines in thermal performance breadth with latitude or temperature seasonality. These findings suggest that TPCs remained unaltered post invasion, and that invasion may proceed via broad thermal tolerance and establishment in already climatically suitable areas rather than rapid evolution upon introduction.

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.

Spatial variation in high temperature-regulated gene expression predicts evolution of plasticity with climate change in the scarlet monkeyflower.

A major way that organisms can adapt to changing environmental conditions is by evolving increased or decreased phenotypic plasticity. In the face of current global warming, more attention is being paid to the role of plasticity in maintaining fitness as abiotic conditions change over time. However, given that temporal data can be challenging to acquire, a major question is whether evolution in plasticity across space can predict adaptive plasticity across time. In growth chambers simulating two thermal regimes, we generated transcriptome data for western North American scarlet monkeyflowers (Mimulus cardinalis) collected from different latitudes and years (2010 and 2017) to test hypotheses about how plasticity in gene expression is responding to increases in temperature, and if this pattern is consistent across time and space. Supporting the genetic compensation hypothesis, individuals whose progenitors were collected from the warmer-origin northern 2017 descendant cohort showed lower thermal plasticity in gene expression than their cooler-origin northern 2010 ancestors. This was largely due to a change in response at the warmer (40°C) rather than cooler (20°C) treatment. A similar pattern of reduced plasticity, largely due to a change in response at 40°C, was also found for the cooler-origin northern versus the warmer-origin southern population from 2017. Our results demonstrate that reduced phenotypic plasticity can evolve with warming and that spatial and temporal changes in plasticity predict one another.

Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off.

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

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

Evolutionary rescue can prevent populations from declining under climate change, and should be more likely at high-latitude, "leading" edges of species' ranges due to greater temperature anomalies and gene flow from warm-adapted populations. Using a resurrection study with seeds collected before and after a 7-year period of record warming, we tested for thermal adaptation in the scarlet monkeyflower Mimulus cardinalis. We grew ancestors and descendants from northern-edge, central, and southern-edge populations across eight temperatures. Despite recent climate anomalies, populations showed limited evolution of thermal performance curves. However, one southern population evolved a narrower thermal performance breadth by 1.31°C, which matches the direction and magnitude of the average decrease in seasonality experienced. Consistent with the climate variability hypothesis, thermal performance breadth increased with temperature seasonality across the species' geographic range. Inconsistent with performance trade-offs between low and high temperatures across populations, we did not detect a positive relationship between thermal optimum and mean temperature. These findings fail to support the hypothesis that evolutionary response to climate change is greatest at the leading edge, and suggest that the evolution of thermal performance is unlikely to rescue most populations from the detrimental effects of rapidly changing climate.

Context Dependence of Local Adaptation to Abiotic and Biotic Environments: A Quantitative and Qualitative Synthesis.

Understanding how spatially variable selection shapes adaptation is an area of long-standing interest in evolutionary ecology. Recent meta-analyses have quantified the extent of local adaptation, but the relative importance of abiotic and biotic factors in driving population divergence remains poorly understood. To address this gap, we combined a quantitative meta-analysis and a qualitative metasynthesis to (1) quantify the magnitude of local adaptation to abiotic and biotic factors and (2) characterize major themes that influence the motivation and design of experiments that seek to test for local adaptation. Using local-foreign contrasts as a metric of local adaptation (or maladaptation), we found that local adaptation was greater in the presence than in the absence of a biotic interactor, especially for plants. We also found that biotic environments had stronger effects on fitness than abiotic environments when ignoring whether those environments were local versus foreign. Finally, biotic effects were stronger at low latitudes, and abiotic effects were stronger at high latitudes. Our qualitative analysis revealed that the lens through which local adaptation has been examined differs for abiotic and biotic factors. It also revealed biases in the design and implementation of experiments that make quantitative results challenging to interpret and provided directions for future research.

Determinants of geographic range size in plants.

Geographic range size has long fascinated ecologists and evolutionary biologists, yet our understanding of the factors that cause variation in range size among species and across space remains limited. Not only does geographic range size inform decisions about the conservation and management of rare and nonindigenous species due to its relationship with extinction risk, rarity, and invasiveness, but it also provides insights into fundamental processes such as dispersal and adaptation. There are several features unique to plants (e.g. polyploidy, mating system, sessile habit) that may lead to distinct mechanisms explaining variation in range size. Here, we highlight key studies testing intrinsic and extrinsic hypotheses about geographic range size under contrasting scenarios where species' ranges are static or change over time. We then present results from a meta-analysis of the relative importance of commonly hypothesized determinants of range size in plants. We show that our ability to infer the relative importance of these determinants is limited, particularly for dispersal ability, mating system, ploidy, and environmental heterogeneity. We highlight avenues for future research that merge approaches from macroecology and evolutionary ecology to better understand how adaptation and dispersal interact to facilitate niche evolution and range expansion.

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

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

Range edges in heterogeneous landscapes: Integrating geographic scale and climate complexity into range dynamics.

The impacts of climate change have re-energized interest in understanding the role of climate in setting species geographic range edges. Despite the strong focus on species' distributions in ecology and evolution, defining a species range edge is theoretically and empirically difficult. The challenge of determining a range edge and its relationship to climate is in part driven by the nested nature of geography and the multidimensionality of climate, which together generate complex patterns of both climate and biotic distributions across landscapes. Because range-limiting processes occur in both geographic and climate space, the relationship between these two spaces plays a critical role in setting range limits. With both conceptual and empirical support, we argue that three factors-climate heterogeneity, collinearity among climate variables, and spatial scale-interact to shape the spatial structure of range edges along climate gradients, and we discuss several ways that these factors influence the stability of species range edges with a changing climate. We demonstrate that geographic and climate edges are often not concordant across species ranges. Furthermore, high climate heterogeneity and low climate collinearity across landscapes increase the spectrum of possible relationships between geographic and climatic space, suggesting that geographic range edges and climatic niche limits correspond less frequently than we may expect. More empirical explorations of how the complexity of real landscapes shapes the ecological and evolutionary processes that determine species range edges will advance the development of range limit theory and its applications to biodiversity conservation in the context of changing climate.

Community turnover by composition and climatic affinity across scales in an alpine system.

PREMISE: Examining community turnover across climate gradients at multiple scales is vital to understanding biogeographic response to climate change. This approach is especially important for alpine plants in which the relative roles of topographic complexity and nonclimatic or stochastic factors vary across spatial scales. METHODS: We examined the structure of alpine plant communities across elevation gradients in the White Mountains, California. Using community climatic niche means (CCNMs) and measures of community dissimilarity, we explored the relation between community composition and elevation gradients at three scales: the mountain range, individual peaks, and within elevation contours. RESULTS: At the mountain range scale, community turnover and CCNMs showed strongly significant relations with elevation, with an increase in the abundance of cooler and wetter-adapted species at higher elevations. At the scale of single peaks, we found weak and inconsistent relations between CCNMs and elevation, but variation in community composition explained by elevation increased. Within the elevation contours, the range of CCNMs was weakly positively correlated with turnover in species identity, likely driven by microclimate and other site-specific factors. CONCLUSIONS: Our results suggest that there is strong environmental sorting of alpine plant communities at broad scales, but microclimatic and site-specific, nonclimatic factors together shape community turnover at finer scales. In the context of climate change, our results imply that community-climate relations are scale-dependent, and predictions of local alpine plant range shifts are limited by a lack of topoclimatic and habitat information.

Additive genetic variance for lifetime fitness and the capacity for adaptation in an annual plant.

The immediate capacity for adaptation under current environmental conditions is directly proportional to the additive genetic variance for fitness, VA (W). Mean absolute fitness, W¯ , is predicted to change at the rate VA(W)W¯ , according to Fisher's Fundamental Theorem of Natural Selection. Despite ample research evaluating degree of local adaptation, direct assessment of VA (W) and the capacity for ongoing adaptation is exceedingly rare. We estimated VA (W) and W¯ in three pedigreed populations of annual Chamaecrista fasciculata, over three years in the wild. Contrasting with common expectations, we found significant VA (W) in all populations and years, predicting increased mean fitness in subsequent generations (0.83 to 6.12 seeds per individual). Further, we detected two cases predicting "evolutionary rescue," where selection on standing VA (W) was expected to increase fitness of declining populations ( W¯ < 1.0) to levels consistent with population sustainability and growth. Within populations, inter-annual differences in genetic expression of fitness were striking. Significant genotype-by-year interactions reflected modest correlations between breeding values across years, indicating temporally variable selection at the genotypic level that could contribute to maintaining VA (W). By directly estimating VA (W) and total lifetime W¯ , our study presents an experimental approach for studies of adaptive capacity in the wild.

Expression of additive genetic variance for fitness in a population of partridge pea in two field sites.

Despite the importance of adaptation in shaping biological diversity over many generations, little is known about populations' capacities to adapt at any particular time. Theory predicts that a population's rate of ongoing adaptation is the ratio of its additive genetic variance for fitness, VA(W) , to its mean absolute fitness, W¯ . We conducted a transplant study to quantify W¯ and standing VA(W) for a population of the annual legume Chamaecrista fasciculata in one field site from which we initially sampled it and another site where it does not currently occur naturally. We also examined genotype-by-environment interactions, G × E, as well as its components, differences between sites in VA(W) and in rank of breeding values for fitness. The mean fitness indicated population persistence in both sites, and there was substantial VA(W) for ongoing adaptation at both sites. Statistically significant G × E indicated that the adaptive process would differ between sites. We found a positive correlation between fitness of genotypes in the "home" and "away" environments, and G × E was more pronounced as the life-cycle proceeds. This study exemplifies an approach to assessing whether there is sufficient VA(W) to support evolutionary rescue in populations that are declining.

Detrimental effects of rhizobial inoculum early in the life of partridge pea, Chamaecrista fasciculata.

PREMISE OF THE STUDY: Mutualistic relationships with microbes may aid plants in overcoming environmental stressors and increase the range of abiotic environments where plants can persist. Rhizobia, nitrogen-fixing bacteria associated with legumes, often confer fitness benefits to their host plants by increasing access to nitrogen in nitrogen-limited soils, but effects of rhizobia on host fitness under other stresses, such as drought, remain unclear. METHODS: In this greenhouse study, we varied the application of rhizobia (Bradyrhizobium sp.) inoculum and drought to examine whether the fitness benefits of rhizobia to their host, partridge pea (Chamaecrista fasciculata), would differ between drought and well-watered conditions. Plants were harvested 9 weeks after seeds were sown. KEY RESULTS: Young C. fasciculata plants that had been inoculated had lower biomass, leaf relative growth rate, and stem relative growth rate compared to young uninoculated plants in both drought and well-watered environments. CONCLUSIONS: Under the conditions of this study, the rhizobial interaction imposed a net cost to their hosts early in development. Potential reasons for this cost include allocating more carbon to nodule and root development than to aboveground growth and a geographic mismatch between the source populations of host plants and rhizobia. If developing plants incur such costs from rhizobia in nature, they may suffer an early disadvantage relative to other plants, whether conspecifics lacking rhizobia or heterospecifics.

Demographic compensation does not rescue populations at a trailing range edge.

Species' geographic ranges and climatic niches are likely to be increasingly mismatched due to rapid climate change. If a species' range and niche are out of equilibrium, then population performance should decrease from high-latitude "leading" range edges, where populations are expanding into recently ameliorated habitats, to low-latitude "trailing" range edges, where populations are contracting from newly unsuitable areas. Demographic compensation is a phenomenon whereby declines in some vital rates are offset by increases in others across time or space. In theory, demographic compensation could increase the range of environments over which populations can succeed and forestall range contraction at trailing edges. An outstanding question is whether range limits and range contractions reflect inadequate demographic compensation across environmental gradients, causing population declines at range edges. We collected demographic data from 32 populations of the scarlet monkeyflower (Erythranthe cardinalis) spanning 11° of latitude in western North America and used integral projection models to evaluate population dynamics and assess demographic compensation across the species' range. During the 5-y study period, which included multiple years of severe drought and warming, population growth rates decreased from north to south, consistent with leading-trailing dynamics. Southern populations at the trailing range edge declined due to reduced survival, growth, and recruitment, despite compensatory increases in reproduction and faster life-history characteristics. These results suggest that demographic compensation may only delay population collapse without the return of more favorable conditions or the contribution of other buffering mechanisms such as evolutionary rescue.

Artificial Selection Reveals High Genetic Variation in Phenology at the Trailing Edge of a Species Range.

Species responses to climate change depend on the interplay of migration and adaptation, yet we know relatively little about the potential for adaptation. Genetic adaptations to climate change often involve shifts in the timing of phenological events, such as flowering. If populations at the edge of a species range have lower genetic variation in phenological traits than central populations, then their persistence under climate change could be threatened. To test this hypothesis, we performed artificial selection experiments using the scarlet monkeyflower (Mimulus cardinalis) and compared genetic variation in flowering time among populations at the latitudinal center, northern edge, and southern edge of the species range. We also assessed whether selection on flowering time yielded correlated responses in functional traits, potentially representing a cost associated with early or late flowering. Contrary to prediction, southern populations exhibited greater responses to selection on flowering time than central or northern populations. Further, selection for early flowering resulted in correlated increases in specific leaf area and leaf nitrogen, whereas selection for late flowering led to decreases in these traits. These results provide critical insights about how spatial variation in the potential for adaptation may affect population persistence under changing climates.

The evolution of environmental tolerance and range size: a comparison of geographically restricted and widespread Mimulus.

The geographic ranges of closely related species can vary dramatically, yet we do not fully grasp the mechanisms underlying such variation. The niche breadth hypothesis posits that species that have evolved broad environmental tolerances can achieve larger geographic ranges than species with narrow environmental tolerances. In turn, plasticity and genetic variation in ecologically important traits and adaptation to environmentally variable areas can facilitate the evolution of broad environmental tolerance. We used five pairs of western North American monkeyflowers to experimentally test these ideas by quantifying performance across eight temperature regimes. In four species pairs, species with broader thermal tolerances had larger geographic ranges, supporting the niche breadth hypothesis. As predicted, species with broader thermal tolerances also had more within-population genetic variation in thermal reaction norms and experienced greater thermal variation across their geographic ranges than species with narrow thermal tolerances. Species with narrow thermal tolerance may be particularly vulnerable to changing climatic conditions due to lack of plasticity and insufficient genetic variation to respond to novel selection pressures. Conversely, species experiencing high variation in temperature across their ranges may be buffered against extinction due to climatic changes because they have evolved tolerance to a broad range of temperatures.

Randomized, double-blind, placebo controlled pilot study of intradetrusor injections of onabotulinumtoxinA for the treatment of refractory overactive bladder persisting following surgical management of benign prostatic hyperplasia.

INTRODUCTION: We assessed the efficacy of onabotulinumtoxinA (BOTOX, Allergan Inc., Irvine, CA, USA) in patients with refractory overactive bladder (OAB) after treatment for benign prostatic hyperplasia (BPH). MATERIALS AND METHODS: This was a two-center, randomized, double-blinded pilot study conducted in patients with OAB secondary to bladder outlet obstruction (BOO), refractory to anticholinergic medication and persistent for greater than 3 months after surgical intervention to relieve obstruction, with an International Prostate Symptom Score (IPSS) > 12. Patients were randomized in 1:1 fashion to either 200 units of onabotulinumtoxinA versus placebo. Fifteen patients received onabotulinumtoxinA versus 13 who received placebo. Follow up was performed at 1 week and then 1, 3, 6, and 9 months. The primary endpoint was reduction in the frequency of micturition per 24 hours by 3-day voiding diary. Secondary endpoints were maximum flow rate (Qmax), post-void residual (PVR), and IPSS scores. RESULTS: Patients receiving onabotulinumtoxinA demonstrated significantly improved quality of life scores at 180 and 270 days after treatment (p = 0.02 and 0.03, respectively) as well as significantly lower International Consultation on Incontinence Questionnaire (ICIQ) scores (p < 0.05). Baseline urinary frequency was 10.5 versus 11.0 voids/day (p = 0.47). Frequency episodes improved from 11 episodes per day to 8 episodes per day in the treatment arm. The placebo arm did not have a decrease in frequency episodes. This response was durable up to 90 days, although this was not statistically significant. IPSS, PVR, and urgency were unchanged postoperatively in both groups. CONCLUSIONS: OnabotulinumtoxinA was safe in patients with refractory irritative lower urinary tracts symptoms after surgical treatment of BPH. There were improvements in daily frequency, although the results were not statistically significant. Larger trials are needed to help characterize the utility of onabotulinumtoxinA in the treatment of OAB secondary to BPH.