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.

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.

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.

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.

The evolution of plasticity at geographic range edges.

Phenotypic plasticity enables rapid responses to environmental change, and could facilitate range shifts in response to climate change. What drives the evolution of plasticity at range edges, and the capacity of range-edge individuals to be plastic, remain unclear. Here, we propose that accurately predicting when plasticity itself evolves or mediates adaptive evolution at expanding range edges requires integrating knowledge on the demography and evolution of edge populations. Our synthesis shows that: (i) the demography of edge populations can amplify or attenuate responses to selection for plasticity through diverse pathways, and (ii) demographic effects on plasticity are modified by the stability of range edges. Our spatially explicit synthesis for plasticity has the potential to improve predictions for range shifts with climate change.

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.

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.

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.

Regional differences in rapid evolution during severe drought.

Climate change is increasing drought intensity, threatening biodiversity. Rapid evolution of drought adaptations might be required for population persistence, particularly in rear-edge populations that may already be closer to physiological limits. Resurrection studies are a useful tool to assess adaptation to climate change, yet these studies rarely encompass the geographic range of a species. Here, we sampled 11 populations of scarlet monkeyflower (Mimulus cardinalis), collecting seeds across the plants' northern, central, and southern range to track trait evolution from the lowest to the greatest moisture anomaly over a 7-year period. We grew families generated from these populations across well-watered and terminal drought treatments in a greenhouse and quantified five traits associated with dehydration escape and avoidance. When considering pre-drought to peak-drought phenotypes, we find that later date of flowering evolved across the range of M. cardinalis, suggesting a shift away from dehydration escape. Instead, traits consistent with dehydration avoidance evolved, with smaller and/or thicker leaves evolving in central and southern regions. The southern region also saw a loss of plasticity in these leaf traits by the peak of the drought, whereas flowering time remained plastic across all regions. This observed shift in traits from escape to avoidance occurred only in certain regions, revealing the importance of geographic context when examining adaptations to climate change.

Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion.

Every species experiences limits to its geographic distribution. Some evolutionary models predict that populations at range edges are less well adapted to their local environments due to drift, expansion load, or swamping gene flow from the range interior. Alternatively, populations near range edges might be uniquely adapted to marginal environments. In this study, we use a database of transplant studies that quantify performance at broad geographic scales to test how local adaptation, site quality, and population quality change from spatial and climatic range centers toward edges. We find that populations from poleward edges perform relatively poorly, both on average across all sites (15% lower population quality) and when compared to other populations at home (31% relative fitness disadvantage), consistent with these populations harboring high genetic load. Populations from equatorial edges also perform poorly on average (18% lower population quality) but, in contrast, outperform foreign populations (16% relative fitness advantage), suggesting that populations from equatorial edges have strongly adapted to unique environments. Finally, we find that populations from sites that are thermally extreme relative to the species' niche demonstrate strong local adaptation, regardless of their geographic position. Our findings indicate that both nonadaptive processes and adaptive evolution contribute to variation in adaptation across species' ranges.

On the Origin of Coexisting Species.

Speciation is frequently initiated but rarely completed, a phenomenon hypothesized to arise due to the failure of nascent lineages to persist. Although a failure to persist often has ecological causes, key gaps exist between ecological and evolutionary theories that, if filled, would clarify when and why speciation succeeds or fails. Here, we apply ecological coexistence theory to show how the alignment between different forms of niche opportunity and niche use shape the initiation, progression, and completion of speciation. Niche evolution may drive coexistence or competitive exclusion, and an ability to coexist ecologically may help or hinder speciation. Our perspective allows progress towards unifying the origin and maintenance of species diversity across the tree of life.

Eco-evolutionary dynamics of range expansion.

Understanding the movement of species' ranges is a classic ecological problem that takes on urgency in this era of global change. Historically treated as a purely ecological process, range expansion is now understood to involve eco-evolutionary feedbacks due to spatial genetic structure that emerges as populations spread. We synthesize empirical and theoretical work on the eco-evolutionary dynamics of range expansion, with emphasis on bridging directional, deterministic processes that favor evolved increases in dispersal and demographic traits with stochastic processes that lead to the random fixation of alleles and traits. We develop a framework for understanding the joint influence of these processes in changing the mean and variance of expansion speed and its underlying traits. Our synthesis of recent laboratory experiments supports the consistent role of evolution in accelerating expansion speed on average, and highlights unexpected diversity in how evolution can influence variability in speed: results not well predicted by current theory. We discuss and evaluate support for three classes of modifiers of eco-evolutionary range dynamics (landscape context, trait genetics, and biotic interactions), identify emerging themes, and suggest new directions for future work in a field that stands to increase in relevance as populations move in response to global change.

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.

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.

Evolution of an inferior competitor increases resistance to biological invasion.

Biodiversity is imperilled by the spatial homogenization of life on Earth. As new species invade ecological communities, there is urgent need to understand when native species might resist or succumb to interactions with new species. In the California Floristic Province, a global biodiversity hotspot, we show that populations of a native grass (Vulpia microstachys) have evolved to resist the competitive impacts of a dominant European invader (Bromus hordeaceus). Contrary to classic theory, which predicts that competing species co-evolve to differentiate their niches, our evidence is instead most consistent with the native species having evolved to better compete for those resources used by the invader, curtailing the invader's spread. Evolution to resist an invader was achieved despite populations interacting within a diverse background community (22 species 0.5 m-2 on average), refuting the oft-cited hypothesis that high diversity precludes the evolution of pairwise species interactions. Lastly, unlike studies that have explored the demographic consequences of evolution under competition, ours does so with naturally evolved populations. Our study highlights evolution as an underappreciated coexistence mechanism, acting to buffer species from extinction in the face of biological invasion.

Experimental migration upward in elevation is associated with strong selection on life history traits.

One of the strongest biological impacts of climate change has been the movement of species poleward and upward in elevation. Yet, what is not clear is the extent to which the spatial distribution of locally adapted lineages and ecologically important traits may also shift with continued climate change. Here, we take advantage of a transplant experiment mimicking up-slope seed dispersal for a suite of ecologically diverse populations of yellow monkeyflower (Mimulus guttatus sensu lato) into a high-elevation common garden during an extreme drought period in the Sierra Nevada mountains, California, USA. We use a demographic approach to quantify fitness and test for selection on life history traits in local versus lower-elevation populations and in normal versus drought years to test the potential for up-slope migration and phenotypic selection to alter the distribution of key life history traits in montane environments. We find that lower-elevation populations tend to outperform local populations, confirming the potential for up-slope migration. Although selection generally favored some local montane traits, including larger flowers and larger stem size at flowering, drought conditions tended to select for earlier flowering typical of lower-elevation genotypes. Taken together, this suggests that monkeyflower lineages moving upward in elevation could experience selection for novel trait combinations, particularly under warmer and drier conditions that are predicted to occur with continued climate change.

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.

Causes of maladaptation.

Evolutionary biologists tend to approach the study of the natural world within a framework of adaptation, inspired perhaps by the power of natural selection to produce fitness advantages that drive population persistence and biological diversity. In contrast, evolution has rarely been studied through the lens of adaptation's complement, maladaptation. This contrast is surprising because maladaptation is a prevalent feature of evolution: population trait values are rarely distributed optimally; local populations often have lower fitness than imported ones; populations decline; and local and global extinctions are common. Yet we lack a general framework for understanding maladaptation; for instance in terms of distribution, severity, and dynamics. Similar uncertainties apply to the causes of maladaptation. We suggest that incorporating maladaptation-based perspectives into evolutionary biology would facilitate better understanding of the natural world. Approaches within a maladaptation framework might be especially profitable in applied evolution contexts - where reductions in fitness are common. Toward advancing a more balanced study of evolution, here we present a conceptual framework describing causes of maladaptation. As the introductory article for a Special Feature on maladaptation, we also summarize the studies in this Issue, highlighting the causes of maladaptation in each study. We hope that our framework and the papers in this Special Issue will help catalyze the study of maladaptation in applied evolution, supporting greater understanding of evolutionary dynamics in our rapidly changing world.

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.