Range expansion is both slower and more variable with rapid evolution across a spatial gradient in temperature.

Rapid evolution in colonising populations can alter our ability to predict future range expansions. Recent theory suggests that the dynamics of replicate range expansions are less variable, and hence more predictable, with increased selection at the expanding range front. Here, we test whether selection from environmental gradients across space produces more consistent range expansion speeds, using the experimental evolution of replicate duckweed populations colonising landscapes with and without a temperature gradient. We found that the range expansion across a temperature gradient was slower on average, with range-front populations displaying higher population densities, and genetic signatures and trait changes consistent with directional selection. Despite this, we found that with a spatial gradient range expansion speed became more variable and less consistent among replicates over time. Our results therefore challenge current theory, highlighting that chance can still shape the genetic response to selection to influence our ability to predict range expansion speeds.

Density-Dependent Selection during Range Expansion Affects Expansion Load in Life History Traits.

AbstractModels of range expansion have independently explored fitness consequences of life history trait evolution and increased rates of genetic drift-or "allele surfing"-during spatial spread, but no previous model has examined the interactions between these two processes. Here, using spatially explicit simulations, we explore an ecologically complex range expansion scenario that combines density-dependent selection with allele surfing to asses the genetic and fitness consequences of density-dependent selection on the evolution of life history traits. We demonstrate that density-dependent selection on the range edge acts differently depending on the life history trait and can either diminish or enhance allele surfing. Specifically, we show that selection at the range edge is always weaker at sites affecting competitive ability (K-selected traits) than at sites affecting birth rate (r-selected traits). We then link differences in the frequency of deleterious mutations to differences in the efficacy of selection and rate of mutation accumulation across distinct life history traits. Finally, we demonstrate that the observed fitness consequences of allele surfing depend on the population density in which expansion load is measured. Our work highlights the complex relationship between ecology and expressed genetic load, which will be important to consider when interpreting both experimental and field studies of range expansion.

Evolutionary origins for ecological patterns in space.

Historically, many biologists assumed that evolution and ecology acted independently because evolution occurred over distances too great to influence most ecological patterns. Today, evidence indicates that evolution can operate over a range of spatial scales, including fine spatial scales. Thus, evolutionary divergence across space might frequently interact with the mechanisms that also determine spatial ecological patterns. Here, we synthesize insights from 500 eco-evolutionary studies and develop a predictive framework that seeks to understand whether and when evolution amplifies, dampens, or creates ecological patterns. We demonstrate that local adaptation can alter everything from spatial variation in population abundances to ecosystem properties. We uncover 14 mechanisms that can mediate the outcome of evolution on spatial ecological patterns. Sometimes, evolution amplifies environmental variation, especially when selection enhances resource uptake or patch selection. The local evolution of foundation or keystone species can create ecological patterns where none existed originally. However, most often, we find that evolution dampens existing environmental gradients, because local adaptation evens out fitness across environments and thus counteracts the variation in associated ecological patterns. Consequently, evolution generally smooths out the underlying heterogeneity in nature, making the world appear less ragged than it would be in the absence of evolution. We end by highlighting the future research needed to inform a fully integrated and predictive biology that accounts for eco-evolutionary interactions in both space and time.

The role of demographic compensation in stabilising marginal tree populations in North America.

Demographic compensation-the opposing responses of vital rates along environmental gradients-potentially delays anticipated species' range contraction under climate change, but no consensus exists on its actual contribution. We calculated population growth rate (λ) and demographic compensation across the distributional ranges of 81 North American tree species and examined their responses to simulated warming and tree competition. We found that 43% of species showed stable population size at both northern and southern edges. Demographic compensation was detected in 25 species, yet 15 of them still showed a potential retraction from southern edges, indicating that compensation alone cannot maintain range stability. Simulated climatic warming caused larger decreases in λ for most species and weakened the effectiveness of demographic compensation in stabilising ranges. These findings suggest that climate stress may surpass the limited capacity of demographic compensation and pose a threat to the viability of North American tree populations.

Selection on early survival does not explain germination rate clines in Mimulus cardinalis.

PREMISE: Many traits covary with environmental gradients to form phenotypic clines. While local adaptation to the environment can generate phenotypic clines, other nonadaptive processes may also. If local adaptation causes phenotypic clines, then the direction of genotypic selection on traits should shift from one end of the cline to the other. Traditionally, genotypic selection on non-Gaussian traits like germination rate have been hampered because it is challenging to measure their genetic variance. METHODS: Here we used quantitative genetics and reciprocal transplants to test whether a previously discovered cline in germination rate showed additional signatures of adaptation in the scarlet monkeyflower (Mimulus cardinalis). We measured genotypic and population level covariation between germination rate and early survival, a component of fitness. We developed a novel discrete log-normal model to estimate genetic variance in germination rate. RESULTS: Contrary to our adaptive hypothesis, we found no evidence that genetic variation in germination rate contributed to variation in early survival. Across populations, southern populations in both gardens germinated earlier and survived more. CONCLUSIONS: Southern populations have higher early survival but it is not caused by faster germination. This pattern is consistent with nonadaptive forces driving the phenotypic cline in germination rate, but future work will need to assess whether there is selection at other life stages. This statistical framework should help expand quantitative genetic analyses for other waiting-time traits.

Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life-history, and floral traits between scarlet monkeyflower (Mimulus cardinalis) populations.

PREMISE: Across taxa, vegetative and floral traits that vary along a fast-slow life-history axis are often correlated with leaf functional traits arrayed along the leaf economics spectrum, suggesting a constrained set of adaptive trait combinations. Such broad-scale convergence may arise from genetic constraints imposed by pleiotropy (or tight linkage) within species, or from natural selection alone. Understanding the genetic basis of trait syndromes and their components is key to distinguishing these alternatives and predicting evolution in novel environments. METHODS: We used a line-cross approach and quantitative trait locus (QTL) mapping to characterize the genetic basis of twenty leaf functional/physiological, life history, and floral traits in hybrids between annualized and perennial populations of scarlet monkeyflower (Mimulus cardinalis). RESULTS: We mapped both single and multi-trait QTLs for life history, leaf function and reproductive traits, but found no evidence of genetic co-ordination across categories. A major QTL for three leaf functional traits (thickness, photosynthetic rate, and stomatal resistance) suggests that a simple shift in leaf anatomy may be key to adaptation to seasonally dry habitats. CONCLUSIONS: Our results suggest that the co-ordination of resource-acquisitive leaf physiological traits with a fast life-history and more selfing mating system results from environmental selection rather than functional or genetic constraint. Independent assortment of distinct trait modules, as well as a simple genetic basis to leaf physiological traits associated with drought escape, may facilitate adaptation to changing climates.

Local Adaptation to Biotic Interactions: A Meta-analysis across Latitudes.

Adaptation to local conditions can increase species' geographic distributions and rates of diversification, but which components of the environment commonly drive local adaptation-particularly the importance of biotic interactions-is unclear. Biotic interactions should drive local adaptation when they impose consistent divergent selection; if this is common, we expect transplant experiments to detect more frequent and stronger local adaptation when biotic interactions are left intact. We tested this hypothesis using a meta-analysis of transplant experiments from >125 studies (mostly of plants). Overall, local adaptation was common, and biotic interactions affected fitness. Nevertheless, local adaptation was neither more common nor stronger when biotic interactions were left intact, either between experimental treatments within studies (control vs. biotic interactions experimentally manipulated) or between studies that used natural versus biotically altered transplant environments. However, the effect of ameliorating negative interactions varied with latitude, suggesting that interactions may promote local adaptation more often in tropical than in temperate ecosystems, although few tropical studies were available to test this. Our results suggest that biotic interactions often fail to drive local adaptation even though they strongly affect fitness, perhaps because temperate biotic environments are unpredictable at the spatiotemporal scales required for local adaptation.

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.

Geographic variation in reproductive assurance of Clarkia pulchella.

Climate can affect plant populations through direct effects on physiology and fitness, and through indirect effects on their relationships with pollinating mutualists. We therefore expect that geographic variation in climate might lead to variation in plant mating systems. Biogeographic processes, such as range expansion, can also contribute to geographic patterns in mating system traits. We manipulated pollinator access to plants in eight sites spanning the geographic range of Clarkia pulchella to investigate geographic and climatic drivers of fruit production and seed set in the absence of pollinators (reproductive assurance). We examined how reproductive assurance and fruit production varied with the position of sites within the range of the species and with temperature and precipitation. We found that reproductive assurance in C. pulchella was greatest in populations in the northern part of the species' range and was not well explained by any of the climate variables that we considered. In the absence of pollinators, some populations of C. pulchella have the capacity to increase fruit production, perhaps through resource reallocation, but this response is climate dependent. Pollinators are important for reproduction in this species, and recruitment is sensitive to seed input. The degree of autonomous self-pollination that is possible in populations of this mixed-mating species may be shaped by historic biogeographic processes or variation in plant and pollinator community composition rather than variation in climate.

Less favourable climates constrain demographic strategies in plants.

Correlative species distribution models are based on the observed relationship between species' occurrence and macroclimate or other environmental variables. In climates predicted less favourable populations are expected to decline, and in favourable climates they are expected to persist. However, little comparative empirical support exists for a relationship between predicted climate suitability and population performance. We found that the performance of 93 populations of 34 plant species worldwide - as measured by in situ population growth rate, its temporal variation and extinction risk - was not correlated with climate suitability. However, correlations of demographic processes underpinning population performance with climate suitability indicated both resistance and vulnerability pathways of population responses to climate: in less suitable climates, plants experienced greater retrogression (resistance pathway) and greater variability in some demographic rates (vulnerability pathway). While a range of demographic strategies occur within species' climatic niches, demographic strategies are more constrained in climates predicted to be less suitable.

Local Adaptation Interacts with Expansion Load during Range Expansion: Maladaptation Reduces Expansion Load.

The biotic and abiotic factors that facilitate or hinder species range expansions are many and complex. We examine the impact of two genetic processes and their interaction on fitness at expanding range edges: local maladaptation resulting from the presence of an environmental gradient and expansion load resulting from increased genetic drift at the range edge. Results from spatially explicit simulations indicate that the presence of an environmental gradient during range expansion reduces expansion load; conversely, increasing expansion load allows only locally adapted populations to persist at the range edge. Increased maladaptation reduces the speed of range expansion, resulting in less genetic drift at the expanding front and more immigration from the range center, therefore reducing expansion load at the range edge. These results may have ramifications for species being forced to shift their ranges because of climate change or other anthropogenic changes. If rapidly changing climate leads to faster expansion as populations track their shifting climatic optima, populations may suffer increased expansion load beyond previous expectations.

A synthesis of transplant experiments and ecological niche models suggests that range limits are often niche limits.

Global change has made it important to understand the factors that shape species' distributions. Central to this area of research is the question of whether species' range limits primarily reflect the distribution of suitable habitat (i.e. niche limits) or arise as a result of dispersal limitation. Over-the-edge transplant experiments and ecological niche models are commonly used to address this question, yet few studies have taken advantage of a combined approach for inferring the causes of range limits. Here, we synthesise results from existing transplant experiments with new information on the predicted suitability of sites based on niche models. We found that individual performance and habitat suitability independently decline beyond range limits across multiple species. Furthermore, inferences from transplant experiments and niche models were generally concordant within species, with 31 out of 40 cases fully supporting the hypothesis that range limits are niche limits. These results suggest that range limits are often niche limits and that the factors constraining species' ranges operate at scales detectable by both transplant experiments and niche models. In light of these findings, we outline an integrative framework for addressing the causes of range limits in individual species.

The scale of local adaptation in Mimulus guttatus: comparing life history races, ecotypes, and populations.

Fitness trade-offs between environments are central to the evolution of biodiversity. Although transplant studies often document fitness trade-offs consistent with local adaptation (LA), many have also found an advantage of foreign genotypes (foreign advantage (FA)). Understanding the mechanisms driving the magnitude and distribution of fitness variation requires comparative approaches that test the ecological scales at which these different patterns emerge. We used a common garden transplant experiment to compare the relative fitnesses of native vs foreign genotypes at three nested ecological scales within Mimulus guttatus: annual vs perennial life history races, perennial ecotypes across an elevational range, and populations within perennial elevational ecotypes. We integrated fitness across the life-cycle and decomposed LA vs FA into contributions from different fitness components. We found LA, measured as home-site advantage, between annual and perennial races and a trend towards LA among populations within montane habitats. Conversely, we found strong FA of low-elevation perennials in a montane environment. LA between life history races reflects the fitness advantages of adult survival and vegetative growth in a mesic environment. Within the perennial race, recent climate conditions or nonselective processes, such as dispersal limitation or mutational load, could explain FA of low-elevation perennials in a montane environment.

Effects of range-wide variation in climate and isolation on floral traits and reproductive output of Clarkia pulchella.

PREMISE OF THE STUDY: Plant mating systems and geographic range limits are conceptually linked by shared underlying drivers, including landscape-level heterogeneity in climate and in species' abundance. Studies of how geography and climate interact to affect plant traits that influence mating system and population dynamics can lend insight to ecological and evolutionary processes shaping ranges. Here, we examined how spatiotemporal variation in climate affects reproductive output of a mixed-mating annual, Clarkia pulchella. We also tested the effects of population isolation and climate on mating-system-related floral traits across the range. METHODS: We measured reproductive output and floral traits on herbarium specimens collected across the range of C. pulchella. We extracted climate data associated with specimens and derived a population isolation metric from a species distribution model. We then examined how predictors of reproductive output and floral traits vary among populations of increasing distance from the range center. Finally, we tested whether reproductive output and floral traits vary with increasing distance from the center of the range. KEY RESULTS: Reproductive output decreased as summer precipitation decreased, and low precipitation may contribute to limiting the southern and western range edges of C. pulchella. High spring and summer temperatures are correlated with low herkogamy, but these climatic factors show contrasting spatial patterns in different quadrants of the range. CONCLUSIONS: Limiting factors differ among different parts of the range. Due to the partial decoupling of geography and environment, examining relationships between climate, reproductive output, and mating-system-related floral traits reveals spatial patterns that might be missed when focusing solely on geographic position.

Phenotypic lags influence rapid evolution throughout a drought cycle.

Climate anomalies are increasing and posing strong selection, which can lead to rapid evolution. This is occurring on a backdrop of interannual variability that might weaken or even reverse selection. However, the effect of interannual climatic variability on rapid evolution is rarely considered. We study the climatic differences that contribute to rapid evolution throughout a 7-year period, encompassing a severe drought across 12 populations of Mimulus cardinalis (scarlet monkeyflower). Plants were grown in a common greenhouse environment under wet and dry treatments, where specific leaf area and date of flowering were measured. We examine the association between trait values and different climate metrics at different time periods, including the collection year, prior years, and cumulative metrics across sequential years. Of the climatic variables we assessed, we find that anomalies in mean annual precipitation best describe trait differences over our study period. Past climates, of 1-2 years prior, are often related to trait values in a conflicting direction to collection-year climate. Uncovering these complex climatic impacts on evolution is critical to better predict and interpret the impacts of climate change.

Fire sparks upslope range shifts of North Cascades plant species.

As ongoing climate change drives suitable habitats to higher elevations, species ranges are predicted to follow. However, observed range shifts have been surprisingly variable, with most species differing in rates of upward shift and others failing to shift at all. Disturbances such as fires could play an important role in accelerating range shifts by facilitating recruitment in newly suitable habitats (leading edges) and removing adults from areas no longer suited for regeneration (trailing edges). To date, empirical evidence that fires interact with climate change to mediate elevational range shifts is scarce. Resurveying historical plots in areas that experienced climate change and fire disturbance between surveys provides an exciting opportunity to fill this gap. To investigate whether species have tended to shift upslope and if shifts depend on fires, we resurveyed historical vegetation plots in North Cascades National Park, Washington, USA, an area that has experienced warming, drying, and multiple fires since the original surveys in 1983. We quantified range shifts by synthesizing across two lines of evidence: (1) displacement at range edges and the median elevation of species occurrences, and (2) support for the inclusion of interactions among time, fire and elevation in models of species presence with elevation. Among species that experienced fire since the original survey, a plurality expanded into new habitats at their upper edge. In contrast, a plurality of species not experiencing fire showed no evidence of shifts, with the remainder exhibiting responses that were variable in magnitude and direction. Our results suggest that fires can facilitate recruitment at leading edges, while species in areas free of disturbance are more likely to experience stasis.

Phenotypic selection favors missing trait combinations in coexisting annual plants.

Trade-offs among traits are important for maintaining biodiversity, but the role of natural selection in their construction is not often known. It is possible that trade-offs reflect fundamental constraints, negative correlational selection, or directional selection operating on costly, redundant traits. In a Sonoran Desert community of winter annual plants, we have identified a trade-off between relative growth rate and water-use efficiency among species, such that species with high relative growth rate have low water-use efficiency and vice versa. We measured selection on water-use efficiency, relative growth rate, and underlying traits within populations of four species at two study sites with different average climates. Phenotypic trait correlations within species did not match the among-species trade-off. In fact, for two species with high water-use efficiency, individuals with high relative growth rate also had high water-use efficiency. All populations experienced positive directional selection for water-use efficiency and relative growth rate. Selection tended to be stronger on water-use efficiency at the warmer and drier site, and selection on relative growth rate tended to be stronger at the cooler and wetter site. Our results indicate that directional natural selection favors a phenotype not observed among species in the community, suggesting that the among-species trade-off could be due to pervasive genetic constraints, perhaps acting in concert with processes of community assembly.

Water-use efficiency and relative growth rate mediate competitive interactions in Sonoran Desert winter annual plants.

PREMISE OF THE STUDY: A functional approach to investigating competitive interactions can provide a mechanistic understanding of processes driving population dynamics, community assembly, and the maintenance of biodiversity. In Sonoran Desert annual plants, a trade-off between relative growth rate (RGR) and water-use efficiency (WUE) contributes to species differences in population dynamics that promote long-term coexistence. Traits underlying this trade-off explain variation in demographic responses to precipitation as well as life history and phenological patterns. Here, we ask how these traits mediate competitive interactions. • METHODS: We conducted competition trials for three species occupying different positions along the RGR-WUE trade-off axis and compared the effects of competition at high and low soil moisture. We compared competitive effect (ability to suppress neighbors) and competitive response (ability to withstand competition from neighbors) among species. • KEY RESULTS: The RGR-WUE trade-off predicted shifts in competitive responses at different soil moistures. The high-RGR species was more resistant to competition in high water conditions, while the opposite was true for the high-WUE species. The intermediate RGR species tended to have the strongest impact on all neighbors, so competitive effects did not scale directly with differences in RGR and WUE among competitors. • CONCLUSIONS: Our results reveal mechanisms underlying long-term variation in fitness: high-RGR species perform better in years with large, frequent rain events and can better withstand competition under wetter conditions. The opposite is true for high-WUE species. Such resource-dependent responses strongly influence community dynamics and can promote coexistence in variable environments.

Understanding past, contemporary, and future dynamics of plants, populations, and communities using Sonoran Desert winter annuals.

Global change requires plant ecologists to predict future states of biological diversity to aid the management of natural communities, thus introducing a number of significant challenges. One major challenge is considering how the many interacting features of biological systems, including ecophysiological processes, plant life histories, and species interactions, relate to performance in the face of a changing environment. We have employed a functional trait approach to understand the individual, population, and community dynamics of a model system of Sonoran Desert winter annual plants. We have used a comprehensive approach that connects physiological ecology and comparative biology to population and community dynamics, while emphasizing both ecological and evolutionary processes. This approach has led to a fairly robust understanding of past and contemporary dynamics in response to changes in climate. In this community, there is striking variation in physiological and demographic responses to both precipitation and temperature that is described by a trade-off between water-use efficiency (WUE) and relative growth rate (RGR). This community-wide trade-off predicts both the demographic and life history variation that contribute to species coexistence. Our framework has provided a mechanistic explanation to the recent warming, drying, and climate variability that has driven a surprising shift in these communities: cold-adapted species with more buffered population dynamics have increased in relative abundance. These types of comprehensive approaches that acknowledge the hierarchical nature of biology may be especially useful in aiding prediction. The emerging, novel and nonstationary climate constrains our use of simplistic statistical representations of past plant behavior in predicting the future, without understanding the mechanistic basis of change.