Predicting evolutionary responses to climate change in the sea

An increasing number of short‐term experimental studies show significant effects of projected ocean warming and ocean acidification on the performance on marine organisms. Yet, it remains unclear if we can reliably predict the impact of climate change on marine populations and ecosystems, because we lack sufficient understanding of the capacity for marine organisms to adapt to rapid climate change. In this review, we emphasise why an evolutionary perspective is crucial to understanding climate change impacts in the sea and examine the approaches that may be useful for addressing this challenge. We first consider what the geological record and present‐day analogues of future climate conditions can tell us about the potential for adaptation to climate change. We also examine evidence that phenotypic plasticity may assist marine species to persist in a rapidly changing climate. We then outline the various experimental approaches that can be used to estimate evolutionary potential, focusing on molecular tools, quantitative genetics, and experimental evolution, and we describe the benefits of combining different approaches to gain a deeper understanding of evolutionary potential. Our goal is to provide a platform for future research addressing the evolutionary potential for marine organisms to cope with climate change.     

Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations

Predictions about the fate of species or populations under climate change scenarios typically neglect adaptive evolution and phenotypic plasticity, the two major mechanisms by which organisms can adapt to changing local conditions. As a consequence, we have little understanding of the scope for organisms to track changing environments by in situ adaptation. Here, we use a detailed individual-specific long-term population study of great tits (Parus major) breeding in Wytham Woods, Oxford, UK to parameterise a mechanistic model and thus directly estimate the rate of environmental change to which in situ adaptation is possible. Using the effect of changes in early spring temperature on temporal synchrony between birds and a critical food resource, we focus in particular on the contribution of phenotypic plasticity to population persistence. Despite using conservative estimates for evolutionary and reproductive potential, our results suggest little risk of population extinction under projected local temperature change; however, this conclusion relies heavily on the extent to which phenotypic plasticity tracks the changing environment. Extrapolating the model to a broad range of life histories in birds suggests that the importance of phenotypic plasticity for adjustment to projected rates of temperature change increases with slower life histories, owing to lower evolutionary potential. Understanding the determinants and constraints on phenotypic plasticity in natural populations is thus crucial for characterising the risks that rapidly changing environments pose for the persistence of such populations.     

Intraspecific variation in seedling growth responses of a relict tree species Euptelea pleiospermum to precipitation manipulation along an elevation gradient

Improving the accuracy of predictions regarding how plants respond to climate change is crucial to protecting biodiversity. However, little is known about the effects of seed source and elevation on the response of mountain plant species to reductions in precipitation. Here, we collected seeds of a tree species (Euptelea pleiospermum) from three seed sources and carried out a two-growing-season reciprocal transplant experiment with precipitation manipulation at three sites along an elevation gradient in the Shennongjia Mountains, central China. Variations in whole-plant traits, leaf traits, and root traits were investigated. We found that most plant traits of E. pleiospermum seedlings were affected by reductions in precipitation, and responses varied among different elevations and seed sources. Whole-plant traits, root biomass, and leaf traits related to photosynthesis capacity decreased under reduced precipitation treatments at mid and high elevation sites. Thus, climate change induced drought will likely have a negative influence on seedling growth at mid and high elevation regions. In addition, a home-site advantage in whole-plant traits and root traits was observed. However, the responses of leaf traits in most cases were not affected by seed source because of higher phenotypic plasticity. Our results suggested that both local adaptation and phenotypic plasticity were important in seedling growth responses to reduced precipitation. We also highlight the importance of taking intraspecific variation into account when studying the response of plants to changes in climate.

     

Phenotypic plasticity closely linked to climate at origin and resulting in increased mortality under warming and frost stress in a common grass

Phenotypic plasticity is important for species responses to global change and species coexistence. Phenotypic plasticity differs among species and traits and changes across environments. Here, we investigated phenotypic plasticity of the widespread grass Arrhenatherum elatius in response to winter warming and frost stress by comparing phenotypic plasticity of 11 geographically and environmentally distinct populations of this species to phenotypic plasticity of populations of different species originating from a single environment. The variation in phenotypic plasticity was similar for populations of a single species from different locations compared to populations of functionally and taxonomically diverse species from one environment for the studied traits (leaf biomass production and root integrity after frost) across three indices of phenotypic plasticity (RDPI, PIN, slope of reaction norm). Phenotypic plasticity was not associated with neutral genetic diversity but closely linked to the climate of the populations’ origin. Populations originating from warmer and more variable climates showed higher phenotypic plasticity. This indicates that phenotypic plasticity can itself be considered as a trait subject to local adaptation to climate. Finally, our data emphasize that high phenotypic plasticity is not per se positive for adaptation to climate change, as differences in stress responses are resulting in high phenotypic plasticity as expressed by common plasticity indices, which is likely to be related to increased mortality under stress in more plastic populations.     

Plasticity in functional traits in the context of climate change: a case study of the subalpine forb Boechera stricta (Brassicaceae)

Environmental variation often induces shifts in functional traits, yet we know little about whether plasticity will reduce extinction risks under climate change. As climate change proceeds, phenotypic plasticity could enable species with limited dispersal capacity to persist in situ, and migrating populations of other species to establish in new sites at higher elevations or latitudes. Alternatively, climate change could induce maladaptive plasticity, reducing fitness, and potentially stalling adaptation and migration. Here, we quantified plasticity in life history, foliar morphology, and ecophysiology in Boechera stricta (Brassicaceae), a perennial forb native to the Rocky Mountains. In this region, warming winters are reducing snowpack and warming springs are advancing the timing of snow melt. We hypothesized that traits that were historically advantageous in hot and dry, low‐elevation locations will be favored at higher elevation sites due to climate change. To test this hypothesis, we quantified trait variation in natural populations across an elevational gradient. We then estimated plasticity and genetic variation in common gardens at two elevations. Finally, we tested whether climatic manipulations induce plasticity, with the prediction that plants exposed to early snow removal would resemble individuals from lower elevation populations. In natural populations, foliar morphology and ecophysiology varied with elevation in the predicted directions. In the common gardens, trait plasticity was generally concordant with phenotypic clines from the natural populations. Experimental snow removal advanced flowering phenology by 7 days, which is similar in magnitude to flowering time shifts over 2–3 decades of climate change. Therefore, snow manipulations in this system can be used to predict eco‐evolutionary responses to global change. Snow removal also altered foliar morphology, but in unexpected ways. Extensive plasticity could buffer against immediate fitness declines due to changing climates.     

Diapause and bet-hedging strategies in insects: a meta-analysis of reaction norm shapes

Many organisms escape from lethal climatological conditions by entering a resistant resting stage called diapause, which needs to be optimally timed with seasonal change. As climate change exerts selection pressure on phenology, the evolution of mean diapause timing, but also of phenotypic plasticity and bet-hedging strategies is expected. The potential of the latter strategy as a means of coping with environmental unpredictability has received little attention in the climate change literature. Populations should be adapted to spatial variation in local conditions; contemporary patterns of phenological strategies across a geographic range may hence provide information about their evolvability. We thus extracted 458 diapause reaction norms from 60 studies. First, we correlated mean diapause timing with mean winter onset. Then we partitioned the reaction norm variance into a temporal component (phenotypic plasticity) and among-offspring variance (diversified bet-hedging) and correlated this variance composition with variability of winter onset. Mean diapause timing correlated reasonably well with mean winter onset, except for populations at high latitudes, which apparently failed to track early onsets. Variance among offspring was, however, limited and correlated only weakly with environmental variability, indicating little scope for bet-hedging. The apparent lack of phenological bet-hedging strategies may pose a risk in a less predictable climate, but we also highlight the need for more data on alternative strategies.     

Phenotypic plasticity and longevity in plants and animals: cause and effect?

Immobile plants and immobile modular animals outlive unitary animals. This paper discusses competing but not necessarily mutually exclusive theories to explain this extreme longevity, especially from the perspective of phenotypic plasticity. Stem cell immortality, vascular autonomy, and epicormic branching are some important features of the phenotypic plasticity of plants that contribute to their longevity. Monocarpy versus polycarpy can also influence the kind of senescent processes experienced by plants. How density-dependent phenomena affecting the establishment of juveniles in these immobile organisms can influence the evolution of senescence, and consequently longevity, is reviewed and discussed. Whether climate change scenarios will favour long-lived or short-lived organisms, with their attendant levels of plasticity, is also presented.     

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.     

异质生境中水生植物表型可塑性的研究进展

水生植物是一类以草本植物为主、与水紧密相关的生态类群, 大多数具有克隆性。面对水环境的变化, 水生植物在形态、行为和生理上表现出多样化的表型可塑性, 对异质生境具有很强的适应能力。表型可塑性研究已在陆生植物的多个类群展开, 然而目前对异质生境下水生植物的生态适应对策, 尤其是表型可塑性的研究尚重视不够。本文在阐明克隆植物表型可塑性主要实现方式及其关系、水生环境异质性及其特点的基础上, 重点从形态可塑性、觅食行为、克隆整合、克隆分工和风险分摊等5个方面讨论了水生植物如何通过表型可塑性适应异质性水生环境。在今后的水生植物表型可塑性研究中, 建议着重探讨以下问题: (1)表型可塑性的变化规律及机理; (2)克隆整合对群落和生态系统的影响; (3)克隆整合与克隆片段化的权衡; (4)不同克隆构型的表型可塑性及其内在机制; (5)表型可塑性的适应性进化; (6)水生植物与其他类群/营养级物种的关系; (7)水生生态系统对全球变化的响应。     

Epigenetic regulation of adaptive responses of forest tree species to the environment

Epigenetic variation is likely to contribute to the phenotypic plasticity and adaptative capacity of plant species, and may be especially important for long‐lived organisms with complex life cycles, including forest trees. Diverse environmental stresses and hybridization/polyploidization events can create reversible heritable epigenetic marks that can be transmitted to subsequent generations as a form of molecular “memory”. Epigenetic changes might also contribute to the ability of plants to colonize or persist in variable environments. In this review, we provide an overview of recent data on epigenetic mechanisms involved in developmental processes and responses to environmental cues in plant, with a focus on forest tree species. We consider the possible role of forest tree epigenetics as a new source of adaptive traits in plant breeding, biotechnology, and ecosystem conservation under rapid climate change.     

Phenological plasticity will not help all species adapt to climate change

Concerns are rising about the capacity of species to adapt quickly enough to climate change. In long‐lived organisms such as trees, genetic adaptation is slow, and how much phenotypic plasticity can help them cope with climate change remains largely unknown. Here, we assess whether, where and when phenological plasticity is and will be adaptive in three major European tree species. We use a process‐based species distribution model, parameterized with extensive ecological data, and manipulate plasticity to suppress phenological variations due to interannual, geographical and trend climate variability, under current and projected climatic conditions. We show that phenological plasticity is not always adaptive and mostly affects fitness at the margins of the species' distribution and climatic niche. Under current climatic conditions, phenological plasticity constrains the northern range limit of oak and beech and the southern range limit of pine. Under future climatic conditions, phenological plasticity becomes strongly adaptive towards the trailing edges of beech and oak, but severely constrains the range and niche of pine. Our results call for caution when interpreting geographical variation in trait means as adaptive, and strongly point towards species distribution models explicitly taking phenotypic plasticity into account when forecasting species distribution under climate change scenarios.     

克隆植物的表型可塑性与等级选择

表型可塑性是指生物个体生长发育过程中遭受不同环境条件作用时产生不同表型的能力。进化的发生有赖于自然选择对种群遗传可变性产生的效力以及各基因型的表型可塑性。有足够的证据说明表型可塑性的可遗传性,它实际上是进化改变的一个成分。一般通过优化模型、数量遗传模型和配子模型来研究表型可塑性的进化。植物的构型是相对固定的,并未完全抑制表型可塑性。克隆植物因其双构件性而具有更广泛的、具有重要生态适应意义的表型可塑性。构件性使克隆植物具有以分株为基本单位的等级结构,从而使克隆植物的表型选择也具有等级性。构件等级一般包含基株、克隆片段或分株系统以及分株3个典型水平。目前认为克隆植物的自然选择有两种模式,分别以等级选择模型和基因型选择模型表征。等级选择模型认为:不同的等级水平同时也是表型选择水平,环境对各水平具有作用,各水平之间也有相互作用,多重表型选择水平的净效应最终通过繁殖水平——分株传递到随后的世代中。基因型选择模型指出:克隆生长引起分株的遗传变异,并通过基株内分株间以及基株间的非随机交配引起种子库等位基因频率的改变,产生微进化。这两种选择模式均突出强调了分株水平在自然选择过程中的变异性以及在进化中的重要性,强调了克隆生长和种子繁殖对基株适合度的贡献。基因型选择模型包含等级选择模型的观点,是对等级选择模型的重要补充。克隆植物的表型可塑性表现在3个典型等级层次上,由于各层次对自然选择压力具有不同的反应,其表型变异程度一般表现出“分株层次>分株片段层次>基株层次”的等级性反应模式。很多证据表明,在构件有机体中构件具有最大的表型可塑性,植物的表型可塑性实际上是构件而非整个遗传个体的反应。这说明克隆植物的等级反应模式可能具有普适性。如果该反应模式同时还是构件等级中不同“个体”适应性可塑性反应的模式,那么可以预测:1)在克隆植物中,分株层次受到的自然选择强度也最大,并首先发生适应性可塑性变化,最终引起克隆植物微进化;2)由于较弱的有性繁殖能力,克隆植物在进化过程中的保守性可能大于非克隆植物。克隆植物等级反应模式的普适性亟待验证。     

Plant responses to simulated warming and drought: a comparative study of functional plasticity between congeneric mid and high elevation species

Aims Effects of climate change, especially changes in temperatures and precipitation patterns, are particularly pronounced in alpine regions. In response, plants may exhibit phenotypic plasticity in key functional traits allowing short-term adjustment to novel conditions. However, little is known about the degree of phenotypic plasticity of high elevation species relative to mid elevation congeners.Methods We transplanted 14 herbaceous perennial species from high elevation into two common gardens (1050 and 2000 m.a.s.l.) in the Swiss Alps, and we examined plastic responses in key functional traits to changes in temperature and soil water availability. This design was replicated with 14 congeneric species from mid elevation to assess if the degree of phenotypic plasticity differs between mid and high elevation species. Survival was assessed across two growing seasons, while aboveground biomass and specific leaf area (SLA) were measured after the first growing season, and biomass allocation to belowground and reproductive structures after the second. Moreover, a phenotypic plasticity index was calculated for the functional traits to compare the degree of plasticity between mid and high elevation species.Important findings Aboveground biomass was higher in mid elevation species relative to high elevation congeners in all treatments, yet decreased for both with elevation and drought. Similarly, SLA decreased with elevation and drought. Root mass fraction (RMF) was generally higher in high elevation species, and decreased with drought at the lower site. Drought increased the allocation to reproductive structures, especially when plants were grown at their elevation of origin. Interestingly, no difference was found in the degree of phenotypic plasticity averaged across mid and high elevation species for any of the studied functional traits. These results indicate that phenotypic plasticity in the focal traits did not depend on the elevation of origin of the species. Plasticity was not related to environmental heterogeneity, nor constrained by selective pressures at high elevation. However, both species groups showed a remarkable capacity for short-term acclimation to a prospective climate through rapid adjustments in key functional traits.     

Historical comparisons show evolutionary changes in drought responses in European plant species after two decades of climate change

Plants must continuously respond to environmental changes, and a timely question is whether and how populations respond to ongoing global warming and increased drought frequencies and intensities. Plants can either respond through migration or through phenotypic plasticity or their populations can adapt evolutionarily, which encompasses the evolution of trait means and of trait plasticity. One way to detect such evolutionary changes within plant populations is through historical comparisons where plants grown from seeds collected in the past (“ancestors”) are compared to freshly collected seeds from the same populations (“descendants”) in common garden experiments. We used 21- to 26-year-old seeds stored in seed banks for two multi-species experiments that investigated changes in phenotypic traits and their plasticity conferring drought tolerance in early life stages of European plant species. In the first experiment, we used seedlings of four Mediterranean species, ceased watering and recorded their day of mortality. In the second experiment, we studied phenotypic responses to drought in juvenile plants of nine species originating from temperate regions in Europe. In one of four species in the first experiment, descendants survived significantly longer without watering and were smaller than their ancestors. In the second experiment, descendant plants were generally taller under well-watered conditions but smaller under drought than their ancestors, thus showing stronger plasticity. Our historical comparisons suggest that some populations have likely evolved through changes in trait means and plasticity in ways consistent with adaptation to increased drought. Using seed bank material for historical comparisons has several weaknesses, such as unknown sampling protocols or invisible fractions. However, we show how accurately sampled and stored seed bank collections can be used similar to the resurrection approach for investigating rapid evolutionary processes in early life stages of plants under climate change.     

Hormone signaling and phenotypic plasticity in nematode development and evolution

Phenotypic plasticity refers to the ability of an organism to adopt different phenotypes depending on environmental conditions. In animals and plants, the progression of juvenile development and the formation of dormant stages are often associated with phenotypic plasticity, indicating the importance of phenotypic plasticity for life-history theory. Phenotypic plasticity has long been emphasized as?a crucial principle in ecology and as facilitator of phenotypic evolution. In nematodes, several examples of phenotypic plasticity have been studied at the genetic and developmental level. In addition, the influence of different environmental factors has been investigated under laboratory conditions. These studies have provided detailed insight into the molecular basis of phenotypic plasticity and its?ecological and evolutionary implications. Here, we review recent studies on the formation of dauer larvae in Caenorhabditis elegans, the evolution of nematode parasitism and the generation of a novel feeding trait in Pristionchus pacificus. These examples reveal a conserved and co-opted role of an endocrine signaling module involving the steroid hormone dafachronic acid. We will discuss how hormone signaling might facilitate life-history and morphological evolution.     

Phenology research for natural resource management in the United States

Natural resource professionals in the United States recognize that climate-induced changes in phenology can substantially affect resource management. This is reflected in national climate change response plans recently released by major resource agencies. However, managers on-the-ground are often unclear about how to use phenological information to inform their management practices. Until recently, this was at least partially due to the lack of broad-based, standardized phenology data collection across taxa and geographic regions. Such efforts are now underway, albeit in very early stages. Nonetheless, a major hurdle still exists: phenology-linked climate change research has focused more on describing broad ecological changes rather than making direct connections to local to regional management concerns. To help researchers better design relevant research for use in conservation and management decision-making processes, we describe phenology-related research topics that facilitate “actionable” science. Examples include research on evolution and phenotypic plasticity related to vulnerability, the demographic consequences of trophic mismatch, the role of invasive species, and building robust ecological forecast models. Such efforts will increase phenology literacy among on-the-ground resource managers and provide information relevant for short- and long-term decision-making, particularly as related to climate response planning and implementing climate-informed monitoring in the context of adaptive management. In sum, we argue that phenological information is a crucial component of the resource management toolbox that facilitates identification and evaluation of strategies that will reduce the vulnerability of natural systems to climate change. Management-savvy researchers can play an important role in reaching this goal.     

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes

Climate warming affects plant physiology through genetic adaptation and phenotypic plasticity, but little is known about how these mechanisms influence ecosystem processes. We used three elevation gradients and a reciprocal transplant experiment to show that temperature causes genetic change in the sedge Eriophorum vaginatum. We demonstrate that plants originating from warmer climate produce fewer secondary compounds, grow faster and accelerate carbon dioxide (CO₂) release to the atmosphere. However, warmer climate also caused plasticity in E. vaginatum, inhibiting nitrogen metabolism, photosynthesis and growth and slowing CO₂ release into the atmosphere. Genetic differentiation and plasticity in E. vaginatum thus had opposing effects on CO₂ fluxes, suggesting that warming over many generations may buffer, or reverse, the short‐term influence of this species over carbon cycle processes. Our findings demonstrate the capacity for plant evolution to impact ecosystem processes, and reveal a further mechanism through which plants will shape ecosystem responses to climate change.     

Intraspecific variation in thermal acclimation and tolerance between populations of the winter ant,Prenolepis imparis

Thermal phenotypic plasticity, otherwise known as acclimation, plays an essential role in how organisms respond to short‐term temperature changes. Plasticity buffers the impact of harmful temperature changes; therefore, understanding variation in plasticity in natural populations is crucial for understanding how species will respond to the changing climate. However, very few studies have examined patterns of phenotypic plasticity among populations, especially among ant populations. Considering that this intraspecies variation can provide insight into adaptive variation in populations, the goal of this study was to quantify the short‐term acclimation ability and thermal tolerance of several populations of the winter ant, Prenolepis imparis. We tested for correlations between thermal plasticity and thermal tolerance, elevation, and body size. We characterized the thermal environment both above and below ground for several populations distributed across different elevations within California, USA. In addition, we measured the short‐term acclimation ability and thermal tolerance of those populations. To measure thermal tolerance, we used chill‐coma recovery time (CCRT) and knockdown time as indicators of cold and heat tolerance, respectively. Short‐term phenotypic plasticity was assessed by calculating acclimation capacity using CCRT and knockdown time after exposure to both high and low temperatures. We found that several populations displayed different chill‐coma recovery times and a few displayed different heat knockdown times, and that the acclimation capacities of cold and heat tolerance differed among most populations. The high‐elevation populations displayed increased tolerance to the cold (faster CCRT) and greater plasticity. For high‐temperature tolerance, we found heat tolerance was not associated with altitude; instead, greater tolerance to the heat was correlated with increased plasticity at higher temperatures. These current findings provide insight into thermal adaptation and factors that contribute to phenotypic diversity by revealing physiological variance among populations.     

Plastic responses in the metabolome and functional traits of maize plants to temperature variations

Environmentally inducible phenotypic plasticity is a major player in plant responses to climate change. However, metabolic responses and their role in determining the phenotypic plasticity of plants that are subjected to temperature variations remain poorly understood. The metabolomic profiles and metabolite levels in the leaves of three maize inbred lines grown in different temperature conditions were examined with a nuclear magnetic resonance metabolomic technique. The relationship of functional traits to metabolome profiles and the metabolic mechanism underlying temperature variations were then explored. A comparative analysis showed that during heat and cold stress, maize plants shared common plastic responses in biomass accumulation, carbon, nitrogen, sugars, some amino acids and compatible solutes. We also found that the plastic response of maize plants to heat stress was different from that under cold stress, mainly involving biomass allocation, shikimate and its aromatic amino acid derivatives, and other non‐polar metabolites. The plastic responsiveness of functional traits of maize lines to temperature variations was low, while the metabolic responsiveness in plasticity was high, indicating that functional and metabolic plasticity may play different roles in maize plant adaptation to temperature variations. A linear regression analysis revealed that the maize lines could adapt to growth temperature variations through the interrelation of plastic responses in the metabolomes and functional traits, such as biomass allocation and the status of carbon and nitrogen. We provide valuable insight into the plastic response strategy of maize plants to temperature variations that will permit the optimisation of crop cultivation in an increasingly variable environment.