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.

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.

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.

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.

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.

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.

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.

Quantifying the impact of gene flow on phenotype-environment mismatch: a demonstration with the scarlet monkeyflower Mimulus cardinalis.

Geographic range margins offer testing grounds for limits to adaptation. If range limits are concordant with niche limits, range expansions require the evolution of new phenotypes that can maintain populations beyond current range margins. However, many species' range margins appear static over time, suggesting limits on the ability of marginal populations to evolve appropriate phenotypes. A potential explanation is the swamping gene flow hypothesis, which posits that asymmetrical gene flow from large, well-adapted central populations prevents marginal populations from locally adapting. We present an empirical framework for combining gene flow, environment, and fitness-related phenotypes to infer the potential for maladaptation, and we demonstrate its application using the scarlet monkeyflower Mimulus cardinalis. We grew individuals sampled from populations on a latitudinal transect under varied temperatures and determined the phenotypic deviation (PD), the mismatch between phenotype and local environment. We inferred gene flow among populations and predicted that populations receiving the most temperature- or latitude-weighted immigration would show the greatest PD and that these populations were likely marginal. We found asymmetrical gene flow from central to marginal populations. Populations with more latitude-weighted immigration had significantly greater PD but were not necessarily marginal. Gene flow may limit local adaptation in this species, but swamping gene flow is unlikely to explain its northern range limit.

Incorporating population-level variation in thermal performance into predictions of geographic range shifts.

Determining how species' geographic ranges are governed by current climates and how they will respond to rapid climatic change poses a major biological challenge. Geographic ranges are often spatially fragmented and composed of genetically differentiated populations that are locally adapted to different thermal regimes. Tradeoffs between different aspects of thermal performance, such as between tolerance to high temperature and tolerance to low temperature or between maximal performance and breadth of performance, suggest that the performance of a given population will be a subset of that of the species. Therefore, species-level projections of distribution might overestimate the species' ability to persist at any given location. However, current approaches to modeling distributions often do not consider variation among populations. Here, we estimated genetically-based differences in thermal performance curves for growth among 12 populations of the scarlet monkeyflower, Mimulus cardinalis, a perennial herb of western North America. We inferred the maximum relative growth rate (RGR(max)), temperature optimum (T(opt)), and temperature breadth (T(breadth)) for each population. We used these data to test for tradeoffs in thermal performance, generate mechanistic population-level projections of distribution under current and future climates, and examine how variation in aspects of thermal performance influences forecasts of range shifts. Populations differed significantly in RGR(max) and had variable, but overlapping, estimates of T(opt) and T(breadth). T(opt) declined with latitude and increased with temperature of origin, consistent with tradeoffs between performances at low temperatures versus those at high temperatures. Further, T(breadth) was negatively related to RGR(max), as expected for a specialist-generalist tradeoff. Parameters of the thermal performance curve influenced properties of projected distributions. For both current and future climates, T(opt) was negatively related to latitudinal position, while T(breadth) was positively related to projected range size. The magnitude and direction of range shifts also varied with T(opt) and T(breadth), but sometimes in unexpected ways. For example, the fraction of habitat remaining suitable increased with T(opt) but decreased with T(breadth). Northern limits of all populations were projected to shift north, but the magnitude of shift decreased with T(opt) and increased with T(breadth). Median latitude was projected to shift north for populations with high T(breadth) and low T(opt), but south for populations with low T(breadth) and high T(opt). Distributions inferred by integrating population-level projections did not differ from a species-level projection that ignored variation among populations. However, the species-level approach masked the potential array of divergent responses by populations that might lead to genotypic sorting within the species' range. Thermal performance tradeoffs among populations within the species' range had important, but sometimes counterintuitive, effects on projected responses to climatic change.

Palaeococcus helgesonii sp. nov., a facultatively anaerobic, hyperthermophilic archaeon from a geothermal well on Vulcano Island, Italy.

A novel, hyperthermophilic archaeon was isolated from a shallow geothermal well that taps marine waters on the Island of Vulcano in the southern Tyrrhenian Sea, Italy. The cells were irregular cocci, 0.6-1.5 microm in diameter, with multiple polar flagella. Growth was observed at temperatures from 45 to 85 degrees C (optimum at approximately 80 degrees C), pH 5-8 (optimum at 6.5), and 0.5-6.0% NaCl (optimum at approximately 2.8%). The minimum doubling time was 50 min. The isolate was obligately chemoheterotrophic, utilizing complex organic compounds including yeast or beef extract, peptone, tryptone, or casein for best growth. The presence of elemental sulfur enhanced growth. The isolate grew anaerobically as well as microaerobically. The G+C content of the genomic DNA was 42.5 mol%. The 16S rRNA sequence indicated that the new isolate was a member of the Thermococcales within the euryarchaeota, representing the second species in the genus Palaeococcus. Its physiology and phylogeny differed in several key characteristics from those of Palaeococcus ferrophilus, justifying the establishment of a new species; the name Palaeococcus helgesonii sp. nov. is proposed, type strain PI1 (DSM 15127).