Ecological and evolutionary responses of an arctic plant to variation in microclimate and soil

The arctic and alpine regions are predicted to experience some of the highest rates of climate change, and the arctic vegetation is expected to be especially sensitive to such changes. Understanding the ecological and evolutionary responses of arctic plant species to changes in climate is therefore a key objective. Geothermal areas, where natural temperature gradients occur over small spatial scales, and without many of the confounding environmental factors present in latitudinal and other gradient studies, provide a natural experimental setting in which to examine the response of arctic–alpine plants to increasing temperatures. To test the ecological and evolutionary response of the circumpolar alpine bistort Persicaria vivipara to temperature, we collected plant material and soil from areas with low, intermediate and high soil temperatures and grew them at three different temperatures in a three-factorial growth chamber experiment. At higher experimental soil temperatures, sprouting was earlier and plants had more leaves. Sprouting was earlier in soil originating from intermediate temperature and plants had more leaves when grown in soil originating from low temperatures. We did not find evidence of local adaptation or genetic variation in reaction norms among plants originating from areas with low, intermediate and high soil temperature. Our findings suggest that the alpine bistort has a strong plastic response to warming, but that differences in soil temperature have not resulted in genetic differentiation. The lack of an observed evolutionary response may, for example, be due to the absence of temperature-mediated selection on P. vivipara, the low rate of sexual recombination, or high levels of gene flow balancing differences in selection. When placed within the context of other studies, we conclude that arctic–alpine plant species often show strong plastic responses to spring warming, while evidence of evolutionary responses varies among species.     

Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia

Rapid climate change will impose strong directional selection pressures on natural plant populations. Climate-linked genetic variation in natural populations indicates that an evolutionary response is possible. We investigated such a response by comparing individuals subjected to elevated drought and warming treatments with individuals establishing in an unmanipulated climate within the same population. We report that reduction in seedling establishment in response to climate manipulations is nonrandom and results from the selection pressure imposed by artificially warmed and droughted conditions. When compared against control samples, high single-locus genetic divergence occurred in drought and warming treatment samples, with genetic differentiation up to 37 times higher than background (mean neutral locus) genetic differentiation. These loci violate assumptions of selective neutrality, indicating the signature of natural selection by drought. Our results demonstrate that rapid evolution in response to climate change may be widespread in natural populations, based on genetic variation already present within the population.     

Rapid genetic divergence in response to 15 years of simulated climate change

Genetic diversity may play an important role in allowing individual species to resist climate change, by permitting evolutionary responses. Our understanding of the potential for such responses to climate change remains limited, and very few experimental tests have been carried out within intact ecosystems. Here, we use amplified fragment length polymorphism (AFLP) data to assess genetic divergence and test for signatures of evolutionary change driven by long‐term simulated climate change applied to natural grassland at Buxton Climate Change Impacts Laboratory (BCCIL). Experimental climate treatments were applied to grassland plots for 15 years using a replicated and spatially blocked design and included warming, drought and precipitation treatments. We detected significant genetic differentiation between climate change treatments and control plots in two coexisting perennial plant study species (Festuca ovina and Plantago lanceolata). Outlier analyses revealed a consistent signature of selection associated with experimental climate treatments at individual AFLP loci in P. lanceolata, but not in F. ovina. Average background differentiation at putatively neutral AFLP loci was close to zero, and genomewide genetic structure was associated neither with species abundance changes (demography) nor with plant community‐level responses to long‐term climate treatments. Our results demonstrate genetic divergence in response to a suite of climatic environments in reproductively mature populations of two perennial plant species and are consistent with an evolutionary response to climatic selection in P. lanceolata. These genetic changes have occurred in parallel with impacts on plant community structure and may have contributed to the persistence of individual species through 15 years of simulated climate change at BCCIL.     

Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

The genomic footprint of climate adaptation in Chironomus riparius

The gradual heterogeneity of climatic factors poses varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift and adaptation, to nonclinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool‐Seq data and population genetic modelling. Common‐garden experiments revealed significantly different population growth rates at test temperatures corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an F_ST outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total, we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.     

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.     

Running to stand still: adaptation and the response of plants to rapid climate change

Climate is a potent selective force in natural populations, yet the importance of adaptation in the response of plant species to past climate change has been questioned. As many species are unlikely to migrate fast enough to track the rapidly changing climate of the future, adaptation must play an increasingly important role in their response. In this paper we review recent work that has documented climate‐related genetic diversity within populations or on the microgeographical scale. We then describe studies that have looked at the potential evolutionary responses of plant populations to future climate change. We argue that in fragmented landscapes, rapid climate change has the potential to overwhelm the capacity for adaptation in many plant populations and dramatically alter their genetic composition. The consequences are likely to include unpredictable changes in the presence and abundance of species within communities and a reduction in their ability to resist and recover from further environmental perturbations, such as pest and disease outbreaks and extreme climatic events. Overall, a range‐wide increase in extinction risk is likely to result. We call for further research into understanding the causes and consequences of the maintenance and loss of climate‐related genetic diversity within populations.     

Long day plants and the response to global warming: rapid evolutionary change in day length sensitivity is possible in wild beet

Day length is a key factor in flowering induction in many plant species in a seasonal environment with flowering induction usually happening at shorter day lengths in lower latitudes. Now, the climate changes systematically at a considerable speed due to global warming. As a consequence, earlier flowering will be selected for in long day plants by favouring a lower threshold for day length sensitivity, on the condition of available genetic variability. Here, we show that there is considerable genetic variation for day length sensitivity in our study species, the seabeet Beta vulgaris subsp. maritima. In the northernmost natural populations without vernalization requirement, in southwest France, the necessary day length for flowering induction could be reduced by artificial selection in <10 generations from >13 h to <11 h, the latter value corresponding to populations in the Beta-species complex from Northern Africa and the eastern part of the Mediterranean tested under the same conditions. A quantitative genetic analysis provided evidence of a gradual change without detectable major genes. Additional experiments were carried out to separate the response to photoperiod from age and energy effects. A certain effect of energy availability has been found, whereas age effects could be excluded. These results indicate a considerable potential for evolutionary change in adjusting flowering time in a changing climate.     

Climate change and evolution: disentangling environmental and genetic responses

Rapid climate change is likely to impose strong selection pressures on traits important for fitness, and therefore, microevolution in response to climate-mediated selection is potentially an important mechanism mitigating negative consequences of climate change. We reviewed the empirical evidence for recent microevolutionary responses to climate change in longitudinal studies emphasizing the following three perspectives emerging from the published data. First, although signatures of climate change are clearly visible in many ecological processes, similar examples of microevolutionary responses in literature are in fact very rare. Second, the quality of evidence for microevolutionary responses to climate change is far from satisfactory as the documented responses are often - if not typically - based on nongenetic data. We reinforce the view that it is as important to make the distinction between genetic (evolutionary) and phenotypic (includes a nongenetic, plastic component) responses clear, as it is to understand the relative roles of plasticity and genetics in adaptation to climate change. Third, in order to illustrate the difficulties and their potential ubiquity in detection of microevolution in response to natural selection, we reviewed the quantitative genetic studies on microevolutionary responses to natural selection in the context of long-term studies of vertebrates. The available evidence points to the overall conclusion that many responses perceived as adaptations to changing environmental conditions could be environmentally induced plastic responses rather than microevolutionary adaptations. Hence, clear-cut evidence indicating a significant role for evolutionary adaptation to ongoing climate warming is conspicuously scarce.     

Rapid,nonparallel genomic evolution of Brassica rapa (field mustard) under experimental drought

While we know that climate change can potentially cause rapid phenotypic evolution, our understanding of the genetic basis and degree of genetic parallelism of rapid evolutionary responses to climate change is limited. In this study, we combined the resurrection approach with an evolve-and-resequence design to examine genome-wide evolutionary changes following drought. We exposed genetically similar replicate populations of the annual plant Brassica rapa derived from a field population in southern California to four generations of experimental drought or watered conditions in a greenhouse. Genome-wide sequencing of ancestral and descendant population pools identified hundreds of SNPs that showed evidence of rapidly evolving in response to drought. Several of these were in stress response genes, and two were identified in a prior study of drought response in this species. However, almost all genetic changes were unique among experimental populations, indicating that the evolutionary changes were largely nonparallel, despite the fact that genetically similar replicates of the same founder population had experienced controlled and consistent selection regimes. This nonparallelism of evolution at the genetic level is potentially because of polygenetic adaptation allowing for multiple different genetic routes to similar phenotypic outcomes. Our findings help to elucidate the relationship between rapid phenotypic and genomic evolution and shed light on the degree of parallelism and predictability of genomic evolution to environmental change.     

Spatio‐temporal variation in fitness responses to contrasting environments in Arabidopsis thaliana

The evolutionary response of organisms to global climate change is expected to be strongly conditioned by preexisting standing genetic variation. In addition, natural selection imposed by global climate change on fitness‐related traits can be heterogeneous over time. We estimated selection of life‐history traits of an entire genetic lineage of the plant Arabidopsis thaliana occurring in north‐western Iberian Peninsula that were transplanted over multiple years into two environmentally contrasting field sites in southern Spain, as southern environments are expected to move progressively northwards with climate change in the Iberian Peninsula. The results indicated that natural selection on flowering time prevailed over that on recruitment. Selection favored early flowering in six of eight experiments and late flowering in the other two. Such heterogeneity of selection for flowering time might be a powerful mechanism for maintaining genetic diversity in the long run. We also found that north‐western A. thaliana accessions from warmer environments exhibited higher fitness and higher phenotypic plasticity for flowering time in southern experimental facilities. Overall, our transplant experiments suggested that north‐western Iberian A. thaliana has the means to cope with increasingly warmer environments in the region as predicted by trends in global climate change models.     

Eco‐genomic analysis of the poleward range expansion of the wasp spider Argiope bruennichi shows rapid adaptation and genomic admixture

Poleward range expansions are commonly attributed to global change, but could alternatively be driven by rapid evolutionary adaptation. A well‐documented example of a range expansion during the past decades is provided by the European wasp spider Argiope bruennichi. Using ecological niche modeling, thermal tolerance experiments and a genome‐wide analysis of gene expression divergence, we show that invasive populations have adapted to novel climatic conditions in the course of their expansion. Their climatic niche shift is mirrored in an increased cold tolerance and a population‐specific and functionally differentiated gene expression response. We generated an Argiope reference genome sequence and used population genome resequencing to assess genomic changes associated with the new climatic adaptations. We find clear genetic differentiation and a significant admixture with alleles from East Asian populations in the invasive Northern European populations. Population genetic modeling suggests that at least some of these introgressing alleles have contributed to the new adaptations during the expansion. Our results thus confirm the notion that range expansions are not a simple consequence of climate change, but are accompanied by fast genetic changes and adaptations that may be fuelled through admixture between long separated lineages.     

Eco‐evolution on the edge during climate change

We urgently need to predict species responses to climate change to minimize future biodiversity loss and ensure we do not waste limited resources on ineffective conservation strategies. Currently, most predictions of species responses to climate change ignore the potential for evolution. However, evolution can alter species ecological responses, and different aspects of evolution and ecology can interact to produce complex eco‐evolutionary dynamics under climate change. Here we review how evolution could alter ecological responses to climate change on species warm and cool range margins, where evolution could be especially important. We discuss different aspects of evolution in isolation, and then synthesize results to consider how multiple evolutionary processes might interact and affect conservation strategies. On species cool range margins, the evolution of dispersal could increase range expansion rates and allow species to adapt to novel conditions in their new range. However, low genetic variation and genetic drift in small range‐front populations could also slow or halt range expansions. Together, these eco‐evolutionary effects could cause a three‐step, stop‐and‐go expansion pattern for many species. On warm range margins, isolation among populations could maintain high genetic variation that facilitates evolution to novel climates and allows species to persist longer than expected without evolution. This ‘evolutionary extinction debt’ could then prevent other species from shifting their ranges. However, as climate change increases isolation among populations, increasing dispersal mortality could select for decreased dispersal and cause rapid range contractions. Some of these eco‐evolutionary dynamics could explain why many species are not responding to climate change as predicted. We conclude by suggesting that resurveying historical studies that measured trait frequencies, the strength of selection, or heritabilities could be an efficient way to increase our eco‐evolutionary knowledge in climate change biology.     

Evolutionary potential of a widespread clonal grass under changing climate

Adaptive responses are probably the most effective long‐term responses of populations to climate change, but they require sufficient evolutionary potential upon which selection can act. This requires high genetic variance for the traits under selection and low antagonizing genetic covariances between the different traits. Evolutionary potential estimates are still scarce for long‐lived, clonal plants, although these species are predicted to dominate the landscape with climate change. We studied the evolutionary potential of a perennial grass, Festuca rubra, in western Norway, in two controlled environments corresponding to extreme environments in natural populations: cold–dry and warm–wet, the latter being consistent with the climatic predictions for the country. We estimated genetic variances, covariances, selection gradients and response to selection for a wide range of growth, resource acquisition and physiological traits, and compared their estimates between the environments. We showed that the evolutionary potential of F. rubra is high in both environments, and genetic covariances define one main direction along which selection can act with relatively few constraints to selection. The observed response to selection at present is not sufficient to produce genotypes adapted to the predicted climate change under a simple, space for time substitution model. However, the current populations contain genotypes which are pre‐adapted to the new climate, especially for growth and resource acquisition traits. Overall, these results suggest that the present populations of the long‐lived clonal plant may have sufficient evolutionary potential to withstand long‐term climate changes through adaptive responses.     

Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change

Poleward range expansions are widespread responses to recent climate change and are crucial for the future persistence of many species. However, evolutionary change in traits such as colonization history and habitat preference may also be necessary to track environmental change across a fragmented landscape. Understanding the likelihood and speed of such adaptive change is important in determining the rate of species extinction with ongoing climate change. We conducted an amplified fragment length polymorphism (AFLP)‐based genome scan across the recently expanded UK range of the Brown Argus butterfly, Aricia agestis, and used outlier‐based (DFDIST and BayeScan) and association‐based (Isolation‐By‐Adaptation) statistical approaches to identify signatures of evolutionary change associated with range expansion and habitat use. We present evidence for (i) limited effects of range expansion on population genetic structure and (ii) strong signatures of selection at approximately 5% AFLP loci associated with both the poleward range expansion of A. agestis and differences in habitat use across long‐established and recently colonized sites. Patterns of allele frequency variation at these candidate loci suggest that adaptation to new habitats at the range margin has involved selection on genetic variation in habitat use found across the long‐established part of the range. Our results suggest that evolutionary change is likely to affect species’ responses to climate change and that genetic variation in ecological traits across species’ distributions should be maximized to facilitate range shifts across a fragmented landscape, particularly in species that show strong associations with particular habitats.     

Increases in the evolutionary potential of upper thermal limits under warmer temperatures in two rainforest Drosophila species

Tropical and subtropical species represent the majority of biodiversity. These species are predicted to lack the capacity to evolve higher thermal limits in response to selection imposed by climatic change. However, these assessments have relied on indirect estimates of adaptive capacity, using conditions that do not reflect environmental changes projected under climate change. Using a paternal half‐sib full‐sib breeding design, we estimated the additive genetic variance and narrow‐sense heritability for adult upper thermal limits in two rainforest‐restricted species of Drosophila reared under two thermal regimes, reflecting increases in seasonal temperature projected for the Wet Tropics of Australia and under standard laboratory conditions (constant 25°C). Estimates of additive genetic variation and narrow‐sense heritability for adult heat tolerance were significantly different from zero in both species under projected summer, but not winter or constant, thermal regimes. In contrast, significant broad‐sense genetic variation was apparent in all thermal regimes for egg‐to‐adult viability. Environment‐dependent changes in the expression of genetic variation for adult upper thermal limits suggest that predicting adaptive responses to climate change will be difficult. Estimating adaptive capacity under conditions that do not reflect future environmental conditions may provide limited insight into evolutionary responses to climate change.     

High fitness costs of climate change‐induced camouflage mismatch

Anthropogenic climate change has created myriad stressors that threaten to cause local extinctions if wild populations fail to adapt to novel conditions. We studied individual and population‐level fitness costs of a climate change‐induced stressor: camouflage mismatch in seasonally colour molting species confronting decreasing snow cover duration. Based on field measurements of radiocollared snowshoe hares, we found strong selection on coat colour molt phenology, such that animals mismatched with the colour of their background experienced weekly survival decreases up to 7%. In the absence of adaptive response, we show that these mortality costs would result in strong population‐level declines by the end of the century. However, natural selection acting on wide individual variation in molt phenology might enable evolutionary adaptation to camouflage mismatch. We conclude that evolutionary rescue will be critical for hares and other colour molting species to keep up with climate change.     

Linking genotype to phenotype in a changing ocean: inferring the genomic architecture of a blue mussel stress response with genome‐wide association

A key component to understanding the evolutionary response to a changing climate is linking underlying genetic variation to phenotypic variation in stress response. Here, we use a genome‐wide association approach (GWAS) to understand the genetic architecture of calcification rates under simulated climate stress. We take advantage of the genomic gradient across the blue mussel hybrid zone (Mytilus edulis and Mytilus trossulus) in the Gulf of Maine (GOM) to link genetic variation with variance in calcification rates in response to simulated climate change. Falling calcium carbonate saturation states are predicted to negatively impact many marine organisms that build calcium carbonate shells – like blue mussels. We sampled wild mussels and measured net calcification phenotypes after exposing mussels to a ‘climate change’ common garden, where we raised temperature by 3°C, decreased pH by 0.2 units and limited food supply by filtering out planktonic particles >5 μm, compared to ambient GOM conditions in the summer. This climate change exposure greatly increased phenotypic variation in net calcification rates compared to ambient conditions. We then used regression models to link the phenotypic variation with over 170 000 single nucleotide polymorphism loci (SNPs) generated by genotype by sequencing to identify genomic locations associated with calcification phenotype, and estimate heritability and architecture of the trait. We identified at least one of potentially 2–10 genomic regions responsible for 30% of the phenotypic variation in calcification rates that are potential targets of natural selection by climate change. Our simulations suggest a power of 13.7% with our study's average effective sample size of 118 individuals and rare alleles, but a power of >90% when effective sample size is 900.     

Adaptive genetic diversity of trees for forest conservation in a future climate: a case study on Norway spruce in Austria

Genetic resources of forest trees are considered as a key factor for the persistence of forest ecosystems because the ability of tree species to survive under changing climate depends strongly on their intraspecific variation in climate response. Therefore, utilizing available genetic variation in climate response and planting alternative provenances suitable for future climatic conditions is considered as an important adaptation measure for forestry. On the other hand, the distribution of adaptive genetic diversity of many tree species is still unknown and the predicted shift of ecological zones and species’ distribution may threaten forest genetic resources that are important for adaptation. Here, we use Norway spruce in Austria as a case study to demonstrate the genetic variation in climate response and to analyse the existing network of genetic conservation units for its effectiveness to safeguard the hotspots of adaptive and neutral genetic diversity of this species. An analysis of the climate response of 480 provenances, clustered into 9 groups of climatically similar provenances, revealed high variation among provenance groups. The most productive and promising provenance clusters for future climates originate from three regions that today depict the warmest and driest areas of the natural spruce distribution in Austria. Gap analysis of the Austrian genetic conservation units in the EUFGIS Portal suggests adequate coverage of the genetic hotspots in southern parts of Austria, but not in eastern and northern Austria. Therefore conservation measures and sustainable utilization of the valuable genetic resources in these regions need to be expanded to cover their high adaptive genetic variation and local adaptation to a warmer climate. The study shows that current conservation efforts need to be evaluated for their effectiveness to protect genetic resources that are important for the survival of trees in a future climate.