Plant adaptation to climate change—Where are we?

Climate change poses critical challenges for population persistence in natural communities, for agriculture and environmental sustainability, and for food security. In this review, we discuss recent progress in climatic adaptation in plants. We evaluate whether climate change exerts novel selection and disrupts local adaptation, whether gene flow can facilitate adaptive responses to climate change, and whether adaptive phenotypic plasticity could sustain populations in the short term. Furthermore, we discuss how climate change influences species interactions. Through a more in‐depth understanding of these eco‐evolutionary dynamics, we will increase our capacity to predict the adaptive potential of plants under climate change. In addition, we review studies that dissect the genetic basis of plant adaptation to climate change. Finally, we highlight key research gaps, ranging from validating gene function to elucidating molecular mechanisms, expanding research systems from model species to other natural species, testing the fitness consequences of alleles in natural environments, and designing multifactorial studies that more closely reflect the complex and interactive effects of multiple climate change factors. By leveraging interdisciplinary tools (e.g., cutting‐edge omics toolkits, novel ecological strategies, newly developed genome editing technology), researchers can more accurately predict the probability that species can persist through this rapid and intense period of environmental change, as well as cultivate crops to withstand climate change, and conserve biodiversity in natural systems.     

Is sexual selection beneficial during adaptation to environmental change?

The role of sexual selection in adaptation is disputed. A balance between sexual and viability selection can be achieved in stable environments, but environmental perturbations could change the costs and benefits arising from sexual selection and influence the rate of adaptation. Here we synthesise theoretical and empirical work on the role of sexual selection in adaptation to changed conditions. Contrasting results have been gained, but the majority of studies suggest that sexual selection has no significant effect or a negative effect on the rate of adaptation. However, once sexually selected traits start to evolve, sexual selection can accelerate adaptation. The role of sexual selection in extinction appears to be minor, but the results could be skewed.     

Vivipary in Polygonum viviparum: an adaptation to cold climate?

Populations of Polygonurn viviparurn were investigated in the Swiss Alps at 14 sites, ranging from 450 m to 2530 m above sea level. The average length of stems and the mean number of reproductive organs (flowers + bulbils) decreased significantly with increasing altitude. On average, the ratio of flowers to bulbils per inflorescence also declined so that at high altitudes, bulbil production was more pronounced. Increased allocation to vegetative reproduction is discussed as an adaptation to cold climate. It is suggested that enhanced vegetative reproduction might be controlled by incornplete floral induction in high altitudes. In addition variability within and between populations was investigated by isozyme electrophoresis and the examination of bulbil colours. A considerable amount of variability was found in alpine populations. The demonstrated genetic variability showed that in P. viviparum it is likely that minor sexual reproduction is maintained even under alpine conditions. This is reflected in different enzyme phenotypes and different bulbil colours.     

Is subarctic forest advance able to keep pace with climate change?

Recent climate warming and scenarios for further warming have led to expectations of rapid movement of ecological boundaries. Here we focus on the circumarctic forest–tundra ecotone (FTE), which represents an important bioclimatic zone with feedbacks from forest advance and corresponding tundra disappearance (up to 50% loss predicted this century) driving widespread ecological and climatic changes. We address FTE advance and climate history relations over the 20th century, using FTE response data from 151 sites across the circumarctic area and site‐specific climate data. Specifically, we investigate spatial uniformity of FTE advance, statistical associations with 20th century climate trends, and whether advance rates match climate change velocities (CCVs). Study sites diverged into four regions (Eastern Canada; Central and Western Canada and Alaska; Siberia; and Western Eurasia) based on their climate history, although all were characterized by similar qualitative patterns of behaviour (with about half of the sites showing advancing behaviour). The main associations between climate trend variables and behaviour indicate the importance of precipitation rather than temperature for both qualitative and quantitative behaviours, and the importance of non‐growing season as well as growing season months. Poleward latitudinal advance rates differed significantly among regions, being smallest in Eastern Canada (~10 m/year) and largest in Western Eurasia (~100 m/year). These rates were 1–2 orders of magnitude smaller than expected if vegetation distribution remained in equilibrium with climate. The many biotic and abiotic factors influencing FTE behaviour make poleward advance rates matching predicted 21st century CCVs (~10³–10⁴ m/year) unlikely. The lack of empirical evidence for swift forest relocation and the discrepancy between CCV and FTE response contradict equilibrium model‐based assumptions and warrant caution when assessing global‐change‐related biotic and abiotic implications, including land–atmosphere feedbacks and carbon sequestration.     

Is the life cycle of high arctic aphids adapted to climate change?

The high arctic aphid Acyrthosiphon svalbardicum Heikinheimo is endemic to Svalbard and has developed a shortened life cycle to cope with harsh environmental conditions prevailing in this archipelago. Previous studies in the 1990s showed that contrarily to Sitobion calvulum, a species which is also restricted to Svalbard and displays a two-generation life cycle, A. svalbardicum can produce a third generation that, on average, should complete its development and reproduction once every 28 years. Because temperature has risen substantially in Svalbard during the past 10 –15 years and is predicted to rise further, budget requirements for this extra-generation should be met more and more frequently and the impact of the resulting demographic increase should be easily measurable in field populations of A. svalbardicum. Here, we tested this hypothesis by performing a series of experiments designed to study population dynamics and morph production of A. svalbardicum. Surprisingly, the three-generation life cycle was not detected either in field populations surveyed for two consecutive years or in controlled conditions where temperature was manipulated. Although we cannot reject the possibility that A. svalbardicum populations may develop a three-generation life cycle under certain circumstances, this strategy seems very rare and not adaptive as it would have been selected in the recent years of warming observed in Svalbard.     

Can climate change lead to gap formation?

Consider a situation where spatial heterogeneity leads to a cline, a gradual transition in dominance of two competing species. We first prove, in the context of a simplified competition–diffusion model, that there exists a stationary solution showing that the two species coexist in a transition zone. What happens then if, owing to climate change, the environmental profile moves with constant speed in space? We show here that, when the speed with which the environmental condition shifts exceeds the Fisher invasion speed of the advancing species, an expanding gap will form. We raise the question of whether such a phenomenon has been or can be observed.     

Is there evidence for a shift in fish growth and recruitment success linked to climate change?

This study investigated whether a putative shift in climate regime in the North Atlantic in the 1990s coincided with changes in the growth and recruitment of roach Rutilus rutilus in the north-east of England. The relationships between R. rutilus growth and recruitment and the environment were significantly different before and after the putative shift in climate regime. Water temperature, river discharge, growth, recruitment success and the Gulf Stream Index co-varied until the late 1990s, indicating a gradual progression between periods of warm-and-dry and cold-and-wet summers. Since the late 1990s, there has been an increased prevalence of warm-and-wet summers, and recruitment success has oscillated between extremes on an almost annual basis. The north wall (northern boundary) of the Gulf Stream has been undergoing a displacement south since the late 1990s, and the speed and amplitude of the change appears to support the hypothesis that there was a regime shift in the climate of the North Atlantic Ocean. It is possible that a continued displacement south of the north wall of the Gulf Stream will lead to further increases in river discharge, reductions in water temperature and reduced fish growth and recruitment success in the long term.     

Plant–microbiome interactions and their impacts on plant adaptation to climate change

Plants have co-evolved with a wide range of microbial communities over hundreds of millions of years, this has drastically influenced their adaptation to biotic and abiotic stress. The rapid development of multi-omics approaches has greatly improved our understanding of the diversity, composition, and functions of plant microbiomes, but how global climate change affects the assembly of plant microbiomes and their roles in regulating host plant adaptation to changing environmental conditions is not fully known. In this review, we summarize recent advancements in the community assembly of plant microbiomes, and their responses to climate change factors such as elevated CO₂ levels, warming, and drought. We further delineate the research trends and hotspots in plant–microbiome interactions in the context of climate change, and summarize the key mechanisms by which plant microbiomes influence plant adaptation to the changing climate. We propose that future research is urgently needed to unravel the impact of key plant genes and signal molecules modulated by climate change on microbial communities, to elucidate the evolutionary response of plant–microbe interactions at the community level, and to engineer synthetic microbial communities to mitigate the effects of climate change on plant fitness.     

Opinion: Is gene mapping in wild populations useful for understanding and predicting adaptation to global change?

Changing environmental conditions will inevitably alter selection pressures. Over the long term, populations have to adapt to these altered conditions by evolutionary change to avoid extinction. Quantifying the ‘evolutionary potential’ of populations to predict whether they will be able to adapt fast enough to forecasted changes is crucial to fully assess the threat for biodiversity posed by climate change. Technological advances in sequencing and high‐throughput genotyping have now made genomic studies possible in a wide range of species. Such studies, in theory, allow an unprecedented understanding of the genomics of ecologically relevant traits and thereby a detailed assessment of the population's evolutionary potential. Aimed at a wider audience than only evolutionary geneticists, this paper gives an overview of how gene‐mapping studies have contributed to our understanding and prediction of evolutionary adaptations to climate change, identifies potential reasons why their contribution to understanding adaptation to climate change may remain limited, and highlights approaches to study and predict climate change adaptation that may be more promising, at least in the medium term.     

Is the siesta an adaptation to disease?

Why does the practice of the siesta vary across human cultures? One explanation is that it is a form of energy conservation in environments with high temperatures and/or agricultural labor. Disease palliation and prevention represents another area where the siesta might be beneficial. A preliminary study used the Human Relations Area Files (HRAF) to examine the characteristics associated with siesta occurrence. Siestas were not statistically associated with high temperatures or agricultural labor (p>.05). They were, however, statistically associated with the occurrence of malaria (p<.05) and marginally associated with parasitic and chronic infectious disease. Preliminary results suggest that siestas could be adaptive in environments with chronic infectious disease.     

Is immunity to malaria really short-lived?

Protection against Plasmodium falciparum malaria is usually considered to be the cumulative product of repeated exposure to parasites, and thus a function of age, in endemic areas. The recent outbreak of malaria in the central highlands of Madagascar gave Philippe Deloron and Claire Chougnet the opportunity to compare the incidence of malaria in children and young adults exposed to malaria for the first time, with that in older adults who spent their childhood in the study area before malaria control was introduced. Protection, as well as immune responses to two major P. falciparum antigens, was not related to age. Individuals older than 40 years were more protected than were younger adults. This increased protection was probably due to immunological memory.     

Reducing uncertainty in species＇ responses to climate change

According to the fifth assessment report of the Intergovernmental Panel on Climate Change, wanning of the climate system is unequivocal, and since the 1950s, many of the observed changes are unprecedented over decades to millennia. In the Northern Hemisphere, 1983- 2012 was likely the wannest 30-year period of the last 1,400 years （IPCC 2013）. Although some evidence for ecological change associated with recent warming is available from all biomes, general assessments of species＇ responses to climate change remain associated with great uncertainty （Parmesan, 2006; Post et al., 2009b）.     

Is long-lived foliage in Picea mariana an adaptation to nutrient-poor conditions?

Summary This study evaluated the contribution of different ages of foliage to the nutrient and carbon balance of black spruce (Picea mariana (Mill.) B.S.P.) from a nutrient-poor peatland in Alberta. Seasonal patterns of foliar nitrogen and phosphorus concentration and content were examined in six needle cohorts up to 10 years old. Trees were treated to simulate excess nutrient deficiency (removal of all one-year-old foliage), nutrient excess (fertilized with 250, 50, 100 kg ha^–1 NPK split application in June and July), or left as controls. Gas exchange (net assimilation-Na, stomatal conductance-g_s, mesophyll conductance-g_m, water-use efficiency-WUE, dark respiration-RS) was measured on six different needle cohorts in several control trees in 1989 and 1990. Nitrogen and phosphorus concentration decreased with needle age. Foliar nutrient concentration fell from April to June and then was stable until September except for the fertilized trees where it increased. There was no evidence of greater than normal retranslocation of nutrients from older needles for defoliated trees or greater than normal nutrient loading in older needles of fertilized trees. NA, g_s, g_m, WUE, and RS were similar for all needles up to six or eight years old, these older needles having NA of 65% of current needles and similar RS. The results do not support to conclusion that older needles of black spruce are retained as an adaptation to nutrient stress. It does not appear that older needles serve as a nutrient storage site in conditions of excess nutrient availability or a greater than normal nutrient source during times of excess nutrient deficiency. It appears that the maintenance of long-livedfoliage in black spruce does not provide for greater flexibility in tree nutrient allocation. Their contribution to the carbon balance of the tree seems to be sufficient to explain their retention.     

How is adaptation to climate change reflected in current practice of forest management and conservation? A case study from Germany

Climate change is expected to challenge forest management and nature conservation in forests. Besides forest species, strategies and references for management and conservation will be affected. In this paper, we qualitatively analysed whether forest conservation and management practice have already adapted to the impacts of climate change and to what extent those practices reflect the adaptation strategies dealt with in international peer-reviewed literature. To this end, we conducted thirteen in-depth interviews with forest practitioners (forest officers/forest district officers) in four regions in Germany. The interview regions were selected to represent the variation in tree species composition, forest ownership regimes and vulnerability to climate change. Although interviewees claimed to take climate change and adaptation strategies into account, in practice such strategies have as yet only occasionally been implemented. Our results suggest that strategies for adapting forest management to climate change are just in the early stages of development or supplement existing strategies relating to general risk reduction or nature-orientated forest management. The extent to which climate change adaptation strategies have influenced overall management varies. This variation and the lack of specific strategies also reflect the existing uncertainties about future changes in climate and about the capacity of forest ecosystems to adapt. We conclude that, in the face of climate change, forest management will have a major influence on future biodiversity composition of forest ecosystems. Hence, a framework for conservation in forests providing recommendations which also take into account the consequences of climate change needs to be developed.     

Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate?

Summary. The cytology of leaf cells from five different high-alpine plants was studied and compared with structures in chloroplasts from the typical high-alpine plant Ranunculus glacialis previously described as having frequent envelope plus stroma protrusions. The plants under investigation ranged from subalpine/alpine Geum montanum through alpine Geum reptans, Poa alpina var. vivipara, and Oxyria digyna to nival Cerastium uniflorum and R. glacialis. The general leaf structure (by light microscopy) and leaf mesophyll cell ultrastructure (by transmission electron microscopy [TEM]) did not show any specialized structures unique to these mountain species. However, chloroplast protrusion formation could be found in G. reptans and, to a greater extent, in O. digyna. The other species exhibited only a low percentage of such chloroplast structural changes. Occurrence of protrusions in samples of G. montanum and O. digyna growing in a mild climate at about 50 m above sea level was drastically reduced. Serial TEM sections of O. digyna cells showed that the protrusions can appear as rather broad and long appendices of plastids, often forming pocketlike structures where mitochondria and microbodies are in close vicinity to the plastid and to each other. It is suggested that some high-alpine plants may form such protrusions to facilitate fast exchange of molecules between cytoplasm and plastid as an adaptation to the short, often unfavorable vegetation period in the Alps, while other species may have developed different types of adaptation that are not expressed in ultrastructural changes of the plastids. Correspondence and reprints: Institute of Botany, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria.     

Is there a single biochemical adaptation to anhydrobiosis?

Even though water is required for the maintenance of biologicalintegrity, numerous organisms are capable of surviving lossof virtually all their cellular water and existing in a stateknown as anhydrobiosis. Over the past three decades we and othershave established that disaccharides such as trehalose and sucroseare almost certainly involved in stabilizing the dry cells.We discuss here some of the evidence behind the mechanism ofthis stabilization. Until the past few years this mechanismhas been sufficiently appealing that a consensus has been developingthat acquisition of these sugars in the cytoplasm may be bothnecessary and sufficient for anhydrobiosis. We show here thatthere are other routes to achieve the effects conferred by thesugars and that other adaptations are almost certainly required,at least in environmental conditions that are less than optimal.Under optimal storage conditions, the presence of the sugarsalone may be sufficient to stabilize even mammalian cells inthe dry state, findings that are already finding use in humanclinical medicine.