Evolutionary Rescue as a Mechanism Allowing a Clonal Grass to Adapt to Novel Climates

How Does Immigration Influence Local Adaptation? A Reexamination of a Familiar Paradigm

Knowledge of the ability of plants to respond to climate change via phenotypic plasticity or genetic adaptation in ecophysiological traits and of the link of these traits to fitness is still limited. We studied the clonal grass Festuca rubra from 11 localities representing factorially crossed gradients of temperature and precipitation and cultivated them in growth chambers simulating temperature and moisture regime in the four extreme localities. We measured net photosynthetic rate, Fv /Fm , specific leaf area, osmotic potential and stomatal density and length and tested their relationship to proxies of fitness. We found strong phenotypic plasticity in photosynthetic traits and genetic differentiation in stomatal traits. The effects of temperature and moisture interacted (either as conditions of origin or growth chambers), as were effects of growth and origin. The relationships between the ecophysiological and fitness-related traits were significant but weak. Phenotypic plasticity and genetic differentiation of the species indicate the potential ability of F. rubra to adapt to novel climatic conditions. The most important challenge for the plants seems to be increasing moisture exposing plants to hypoxia. However, the plants have the potential to respond to increased moisture by changes in stomatal size and density and adjustments of osmotic potential. Changes in ecophysiological traits translate into variation in plant fitness, but the selection on the traits is relatively weak and depends on actual conditions. Despite the selection, the plants do not show strong local adaptation and local adaptation is thus likely not restricting species ability to adjust to novel conditions.

Preface: Functional biogeography in Japanese cedar

Climate change is predicted to affect plant growth, but also the allocation of biomass to aboveground and belowground plant parts. To date, studies have mostly focused on aboveground biomass, while belowground biomass and allocation patterns have received less attention. We investigated changes in biomass allocation along a controlled gradient of precipitation in an experiment with four plant species (Leymus chinensis, Stipa grandis, Artemisia frigida, and Potentilla acaulis) dominant in Inner Mongolia steppe. Results showed that aboveground biomass, belowground biomass and total biomass all increased with increasing growing season precipitation, as expected in this water-limited ecosystem. Biomass allocation patterns also changed along the precipitation gradient, but significant variation between species was apparent. Specifically, the belowground biomass: aboveground biomass ratio (i.e., B:A ratio) of S. grandis was not impacted by precipitation amount, while B:A ratios of the other three species changed in different ways along the gradient. Some of these differences in allocation strategies may be related to morphological differences, specifically, the presence of rhizomes or stolons, though no consistent patterns emerged. Isometric partitioning, i.e., constant allocation of biomass aboveground and belowground, seemed to occur for one species (S. grandis), but not for the three rhizome or stolon-forming ones. Indeed, for these species, the slope of the allometric regression between log-transformed belowground biomass and log-transformed aboveground biomass significantly differed from 1.0 and B:A ratios changed along the precipitation gradient. As changes in biomass allocation can affect ecosystem functioning and services, our results can be used as a basis for further studies into allocation patterns, especially in a context of environmental change.

By the end of this century, human-induced climate change and habitat loss may drastically reduce biodiversity, with expected effects on many amphibian lineages. One of these effects is the shift in the geographic distributions of species when tracking suitable climates. Here, we employ a macroecological approach to dynamically model geographic range shifts by coupling ecological niche models and eco-evolutionary mechanisms, aiming to assess the probability of evolutionary rescue (i.e., rapid adaptation) and dispersal under climate change. Evolutionary models estimated the probability of population persistence by adapting to changes in the temperature influenced by precipitation in the following decades, while compensating the fitness reduction and maintaining viable populations in the new climates. In addition, we evaluated emerging patterns of species richness and turnover at the assemblage level. Our approach was able to identify which amphibian populations among 7,193 species at the global scale could adapt to temperature changes or disperse into suitable regions in the future. Without evolutionary adaptation and dispersal, 47.7% of the species could go extinct until the year 2,100, whereas adding both processes will slightly decrease this extinction rate to 36.5%. Although adaptation to climate is possible for populations in about 25.7% of species, evolutionary rescue is the only possibility to avoid extinction in 4.2% of them. Dispersal will allow geographic range shifts for 49.7% of species, but only 6.5% may avoid extinction by reaching climatically suitable environments. This reconfiguration of species distributions and their persistence creates new assemblage-level patterns at the local scale. Temporal beta-diversity across the globe showed relatively low levels of species turnover, mainly due to the loss of species. Despite limitations with obtaining data, our approach provides more realistic assessments of species responses to ongoing climate changes. It shows that, although dispersal and evolutionary rescue may attenuate species losses, they are not enough to avoid a significant reduction of species’ geographic ranges in the future. Actions that guarantee a higher potential of adaptation (e.g., genetic diversity through larger population sizes) and increased connectivity for species dispersion to track suitable climates become essential, increasing the resilience of biodiversity to climate change.

This article is a Commentary on Walter et al. (2023), 239: 374–387.

Topography affects abiotic conditions which can influence the structure, function and dynamics of ecological communities. An increasing number of studies have demonstrated biological consequences of fine‐scale topographic heterogeneity but we have a limited understanding of how these effects depend on the climate context.We merged high‐resolution (1 m2) data on topography and canopy height derived from airborne lidar with ground‐based data from 15 forest plots in Puerto Rico distributed along a precipitation gradient spanningc. 800–3,500 mm/year. Ground‐based data included species composition, estimated above‐ground biomass (AGB), and two key functional traits (wood density and leaf mass per area, LMA) that reflect resource‐use strategies and a trade‐off between hydraulic safety and hydraulic efficiency. We used hierarchical Bayesian models to evaluate how the interaction between topography × climate is related to metrics of forest structure (i.e. canopy height and AGB), as well as taxonomic and functional alpha‐ and beta‐diversity.Fine‐scale topography (characterized with the topographic wetness index, TWI) significantly affected forest structure and the strength (and in some cases direction) of these effects varied across the precipitation gradient. In all plots, canopy height increased with topographic wetness but the effect was much stronger in dry compared to wet forest plots. In dry forest plots, topographically wetter microsites also had higher levels of AGB but in wet forest plots, topographically drier microsites had higher AGB.Fine‐scale topography influenced functional composition but had only weak or non‐significant effects on taxonomic and functional alpha‐ and beta‐diversity. For instance, community‐weighted wood density followed a similar pattern to AGB across plots. We also found a marginally significant association between variation of wood density and topographic heterogeneity that depended on climate context.Synthesis. The effects of fine‐scale topographic heterogeneity on tropical forest structure and composition depend on the climate context. Our study demonstrates how a stronger integration of topographic heterogeneity across precipitation gradients could improve estimates of forest structure and biomass, and may provide insight to the ways that topography might mediate species responses to drought and climate change.

Phenotypic plasticity of water-related traits reveals boundaries to the adaptive capacity of a dominant European grass species under increased drought

Will life find a way out? Evolutionary rescue and Darwinian adaptation to climate change

The importance of understanding species extinctions and its consequences for ecosystems and human life has been getting increasing public attention. Nonetheless, regardless of how pressing the current biodiversity loss is, with rare exceptions, extinctions are actually not immediate. Rather, they happen many generations after the disturbance that caused them. This means that, at any point in time after a given disturbance, there is a number of extinctions that are expected to happen. This number is the extinction debt. As long as all the extinctions triggered by the disturbance have not happened, there is a debt to be paid. This delay in extinctions can be interpreted as a window of opportunity, when conservation measures can be implemented. In this thesis, I investigated the relative importance of ecological and evolutionary processes unfolding after different disturbances scenarios, to understand how this knowledge can be used to improve conservation practices aiming at controlling extinctions. In the Introduction (chapter 1), I present the concept of extinction debts and the complicating factors behind its understanding. Namely, I start by presenting i) the theoretical basis behind the definition of extinction debts, and how each theory informed different methodologies of study, ii) the complexity of understanding and predicting eco-evolutionary dynamics, and iii) the challenges to studying extinctions under a regime of widespread and varied disturbance of natural habitats. I start the main body of the thesis (chapter 2) by summarizing the current state of empirical, theoretical, and methodological research on extinction debts. In the last 10 years, extinction debts were detected all over the globe, for a variety of ecosystems and taxonomic groups. When estimated - a rare occurrence, since quantifying debts requires often unavailable data - the sizes of these debts range from 9 to 90\% of current species richness and they have been sustained for periods ranging from 5 to 570 yr. I identified two processes whose contributions to extinction debts have been studied more often, namely 1) life-history traits that prolong individual survival, and 2) population and metapopulation dynamics that maintain populations under deteriorated conditions. Less studied are the microevolutionary dynamics happening during the payment of a debt, the delayed conjoint extinctions of interaction partners, and the extinction dynamics under different regimes of disturbances (e.g. habitat loss vs. climate change). Based on these observations, I proposed a roadmap for future research to focus on these less studies aspects. In chapters 3 and 4, I started to follow this roadmap. In chapter 3, I used a genomically-explicit, individual-based model of a plant community to study the microevolutionary processes happening after habitat loss and climate change, and potentially contributing to the settlement of a debt. I showed that population demographic recovery through trait adaptation, i.e. evolutionary rescue, is possible. In these cases, rather than directional selection, trait change involved increase in trait variation, which I interpreted as a sign of disruptive selection. Moreover, I disentangled evolutionary rescue from demographic rescue and show that the two types of rescue were equally important for community resistance, indicating that community re-assembly plays an important role in maintaining diversity following disturbance. The results demonstrated the importance of accounting for eco-evolutionary processes at the community level to understand and predict biodiversity change. Furthermore, they indicate that evolutionary rescue has a limited potential to avoid extinctions under scenarios of habitat loss and climate change. In chapter 4, I analysed the effects of habitat loss and disruption of pollination function on the extinction dynamics of plant communities. To do it, I used an individual, trait-based eco-evolutionary model (Extinction Dynamics Model, EDM) parameterized according to real-world species of calcareous grasslands. Specifically, I compared the effects of these disturbances on the magnitude of extinction debts and species extinction times, as well as how species functional traits affect species survival. I showed that the loss of habitat area generates higher number of immediate extinctions, but the loss of pollination generates higher extinction debt, as species take longer to go extinct. Moreover, reproductive traits (clonal ability, absence of selfing and insect pollination) were the traits that most influenced the occurrence of species extinction as payment of the debt. Thus, the disruption of pollination functions arose as a major factor in the creation of extinction debts. Thus, restoration policies should aim at monitoring the status of this and other ecological processes and functions in undisturbed systems, to inform its re-establishment in disturbed areas. Finally, I discuss the implications of these findings to i) the theoretical understanding of extinction debts, notably via the niche, coexistence, and metabolic theories, ii) the planning conservation measures, including communicating the very notion of extinction debts to improve understanding of the dimension of the current biodiversity crisis, and iii) future research, which must improve the understanding of the interplay between extinction cascades and extinction debts.

Questions have been raised about the ability of long‐lived organisms, such as trees, to adapt to rapid climate change, and to what extent forest management actions influence the evolutionary responses of tree species. Given the life history of trees and the time scales involved, these questions are often addressed through modeling approaches. Yet, most of these studies focus on single‐species case studies. The main objective and originality of our work is to explore the evolutionary responses of tree species to climate change using a process‐based model, in a multi‐specific context. This approach allows us to investigate the conditions necessary for evolutionary rescue in a mixed beech–fir forest. Furthermore, we explored how climate change adaptation and mitigation solutions, such as assisted gene flow and assisted migration, affect the conditions for evolutionary rescue in this forest type. To achieve these objectives, we integrated a quantitative genetic module into a process‐based forest gap model, enabling species‐specific parameters to evolve as quantitative traits under selective pressure and drift. Our results show that increased trait variability and heritability reduce the loss of forest cover following climatic warming in the short term (over a century). We also found that assisted gene flow had the expected effect of aiding species adapt to climate change. Finally, our study suggests that introducing new pre‐adapted species into the forest could improve recovery after climate change but could also hinder the evolutionary rescue of local species. We conclude that integrating evolutionary dynamics into process‐based models significantly enhances their predictive power by incorporating genetic adaptation scenarios that would otherwise be overlooked. This approach also allows us to test eco‐evolutionary hypotheses and better understand the potential consequences of adaptation measures to climate change for tree species.

Climate change, through its vast impacts on biodiversity, is one of the most-studied drivers of ecological change. Although reports of detrimental impacts of gradual global warming on the behavior and physiology of individuals, as well as on populations and communities are now common in scientific literature, much less is known about the impact of extreme climatic events (ECEs) on evolutionary processes. In this review, we provide a broad overview of the state of knowledge on ECEs in the context of evolution. We begin by discussing the drivers of evolution (i.e., mutation, selection, gene flow, and genetic drift) and how ECEs may impact them. We then discuss why rapid adaptation and evolutionary rescue in response to ECEs will be hindered in many species, due to the unpredictable nature and timing of these events. We further outline that potential changes in evolutionary processes in response to ECEs can be better understood by recognizing shifts in ecological interactions, emphasizing the connected nature of communities and ecosystems and the evolutionary consequences. We finally highlight that there is a clear gap in our knowledge of ECE impacts, particularly at the genetic level. In order to understand the relationships between climate change, ECEs, and evolutionary processes, we urgently need hypothesis-driven monitoring efforts and studies that investigate existing data through the lens of historically documented ECE events. Taken together, our review highlights that extreme climatic events associated with climate change are undermining biodiversity through diverse pathways, and that the prospects for rapid adaptation and evolutionary rescue are severely constrained by a host of ecological and genetic challenges.

Contrasting adaptive genetic consequences of stream insects under changing climate

Tidal wetlands worldwide are undergoing rapid invasions by tall‐growing clonal grasses. Prominent examples are invasions by species of the genera Spartina , Phragmites and Elymus . The responsible physiological and ecological drivers of these invasions are poorly understood. Physiological integration (PI) is a key trait of clonal plants, which enables the exchange of resources among ramets. We investigated PI in Elymus athericus , which has been rapidly spreading from high‐marsh into low‐marsh environments of European salt marshes during the last decades. We applied a nitrogen stable‐isotope approach to trace nutrient translocation between ramets in a factorial mesocosm experiment. The experiment was set up to mimic an invasion pattern commonly found in tidal wetlands, i.e. from high‐elevated and rarely flooded into low‐elevated and frequently flooded microenvironments. We tested for intraspecific variability in PI by including two genotypes of Elymus that naturally occur at different elevations within the tidal frame, a high‐marsh (HM) and a low‐marsh (LM) genotype. PI strongly increased offspring ramet aboveground and belowground biomass by 62 and 81%, respectively. Offspring ramets under drained conditions had 95% greater belowground biomass than those under flooded conditions. LM genotype offspring ramets produced 27% more aboveground biomass than HM genotypes. Offspring ramets were clearly more enriched in 15 N under flooded versus drained conditions; however, this positive effect of flooding on δ 15 N was only significant in the LM genotype. Our findings demonstrate the importance of PI for the growth of Elymus offspring ramets and thereby for the species' capacity for fast vegetative spread. We show that offspring ramets under stressful flooded conditions are more dependent on nutrient supply from parent ramets than those under drained conditions. Our data furthermore suggest a higher degree of adaptation to flooding via PI in the LM versus HM genotype. In conclusion, we highlight the importance of assessing PI and intraspecific trait variability to understand invasion processes within ecosystems.

Summary Understanding species' abilities to cope with changing climate is a key prerequisite for predicting the future fates of species and ecosystems. Despite considerable research on species responses to changing climate, we still lack understanding of the role of specific climatic factors, and their interactions, for species responses. We also lack understanding of the relative importance of plasticity vs. adaptation in determining the observed responses. As a model, we use a dominant clonal grass, Festuca rubra, originating from a natural climatic grid of 12 localities in western Norway that allows factorial combinations of temperature (mean growing season temperatures ranging from 6·5 to 10·5 °C) and precipitation (annual precipitation ranging from 600 to 2700 mm). We grew clones from all populations in four growth chambers representing the four climatic extremes in the climate grid (warm/cold × wet/dry). Genetic differentiation and direction and magnitude of plastic responses vary systematically among populations throughout the climatic grid. Growth‐related plant traits are highly plastic and their degree of plasticity depends on their origin. In contrast, the traits reflecting species' foraging strategy are not plastic but vary with the climate of origin. Levels of plasticity of growth‐related traits and genetically differentiated foraging traits thus might constrain local populations' ability to cope with novel climates. Synthesis. Shifts in temperature and precipitation, at the scale and direction expected for the region in the next century, are likely to dramatically affect plant performance. This study illustrates how the interplay between genetic differentiation and plasticity in response to both temperature and precipitation will affect the specific responses of species to climate change. Such complex responses will affect how climate‐change impacts scale up to the community and ecosystem levels. Future studies thus need to specifically consider regionally relevant climate‐change projections, and also explore the role of genetic differentiation and plasticity and how this varies within local floras. Our study also demonstrates that even widespread species with seemingly broad climatic niches may strongly differ in their population performance and plasticity. Climate‐change studies should therefore not be limited to rare and restricted species.