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 as a developing trait: exploring the implications

Individual differences in plasticity have been classically framed as genotype-by-environment interactions, with different genotypes showing different reaction norms in response to environmental conditions. However, research has shown that early experience can be a critical factor in shaping an individual's plasticity to later environmental factors. In other words, plasticity itself can be investigated as a developing trait that reflects the combined action of an individual's genes and previous interactions with the environment. In this paper I explore some implications of the idea that the early environment modulates long-term plasticity, with an emphasis on plasticity in behavioral traits. I begin by focusing on the mechanisms that mediate plasticity at the proximate level, and discussing the possibility that some traits may work as generalized mediators of plasticity by affecting the sensitivity of multiple phenol types across developmental contexts. I then tackle the complex problem of the evolution of reaction norms for plasticity. Next, I consider a number of potential implications for research on parental effects and phenotypic matching, and conclude by discussing how plasticity may become a target of evolutionary conflict between parents and offspring. In total, I aim to show how the idea of plasticity as a developing trait offers a rich source of questions and insights that may inform future research in this area.     

Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes

Phenotypic plasticity itself evolves, as does any other quantitative trait. A very different question is whether phenotypic plasticity causes evolution or is a major evolutionary mechanism. Existing models of the evolution of phenotypic plasticity cover many of the proposals in the literature about the role of phenotypic plasticity in evolution. I will extend existing models to cover adaptation to a novel environment, the appearance of ecotypes and possible covariation between phenotypic plasticity and mean trait value of ecotypes. Genetic assimilation does not sufficiently explain details of observed patterns. Phenotypic plasticity as a major mechanism for evolution--such as, invading new niches, speciation or macroevolution--has, at present, neither empirical nor model support.     

The genetics of phenotypic plasticity. XV. Genetic assimilation,the Baldwin effect,and evolutionary rescue

We used an individual‐based simulation model to examine the role of phenotypic plasticity on persistence and adaptation to two patterns of environmental variation, a single, abrupt step change and continual, linear change. Our model tested the assumptions and predictions of the theory of genetic assimilation, explored the evolutionary dynamics of the Baldwin effect, and provided expectations for the evolutionary response to climate change. We found that genetic assimilation as originally postulated is not likely to occur because the replacement of plasticity by fixed genetic effects takes much longer than the environment is likely to remain stable. On the other hand, trait plasticity as an enhancement to continual evolutionary change may be an important evolutionary mechanism as long as plasticity has little or no costs. Whether or not plasticity helps or hinders evolutionary rescue following a step change in the environment depends on whether plasticity is costly. For linear environmental change, noncostly plasticity always decreases extinction rates, while costly plasticity can create a fitness drag and increase the chance of extinction. Thus, with changing climates plasticity can enhance adaptation and prevent extinction under some conditions, but not others.     

When mother knows best: A population genetic model of transgenerational versus intragenerational plasticity

Many organisms exhibit phenotypic plasticity; producing alternate phenotypes depending on the environment. Individuals can be plastic (intragenerational or direct plasticity), wherein individuals of the same genotype produce different phenotypes in response to the environments they experience. Alternatively, an individual's phenotype may be under the control of its parents, usually the mother (transgenerational or indirect plasticity), so that mother's genotype determines the phenotype produced by a given genotype of her offspring. Under what conditions does plasticity evolve to have intragenerational as opposed to transgenerational genetic control? To explore this question, we present a population genetic model for the evolution of transgenerational and intragenerational plasticity. We hypothesize that the capacity for plasticity incurs a fitness cost, which is borne either by the individual developing the plastic phenotype or by its mother. We also hypothesize that individuals are imperfect predictors of future environments and their capacity for plasticity can lead them occasionally to make a low‐fitness phenotype for a particular environment. When the cost, benefit and error parameters are equal, we show that there is no evolutionary advantage to intragenerational over transgenerational plasticity, although the rate of evolution of transgenerational plasticity is half the rate for intragenerational plasticity, as predicted by theory on indirect genetic effects. We find that transgenerational plasticity evolves when mothers are better predictors of future environments than offspring or when the fitness cost of the capacity for plasticity is more readily borne by a mother than by her developing offspring. We discuss different natural systems with either direct intragenerational plasticity or indirect transgenerational plasticity and find a pattern qualitatively in accord with the predictions of our model.     

Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles

Costs of phenotypic plasticity are important for the evolution of plasticity because they prevent organisms from shaping themselves at will to match heterogeneous environments. These costs occur when plastic genotypes have relatively low fitness regardless of the trait value expressed. We report two experiments in which we measured selection on predator-induced plasticity in the behaviour and external morphology of frog tadpoles (Rana temporaria). We assessed costs under stressful and benign conditions, measured fitness as larval growth rate or competitive ability and focused analysis on aggregate measures of whole-organism plasticity. There was little convincing evidence for a cost of phenotypic plasticity in our experiments, and costs of canalization were nearly as frequent as costs of plasticity. Neither the magnitude of the cost nor the variation around the estimate (detectability) was sensitive to environmental stress.     

The relationships between physical capacity and biomechanical plasticity in old adults during level and incline walking

Old compared to young adults exhibit increased hip and decreased ankle mechanical output during walking – a phenomenon known as biomechanical plasticity. Previous comparison studies suggest that low compared to high capacity old adults exhibit larger magnitudes of this plasticity, however the precise relationship between capacity and plasticity magnitude remains unclear. The purpose of this study was to quantify the relationships between physical capacity and biomechanical plasticity magnitude during level and incline walking. Data were collected for 32 old adults walking over level and inclined (+10°) surfaces at self-selected, comfortable speeds. Physical capacity was measured using the Short-Form Health Survey Physical Component (SF-36 PC) and biomechanical plasticity was quantified by ratios of hip extensor to ankle plantarfexor peak torques, angular impulses, peak positive powers, and positive work (larger ratios indicate larger magnitudes of plasticity). SF-36 PC scores correlated positively with all four biomechanical plasticity ratios during level walking and three of the four ratios during incline walking. Some of the biomechanical plasticity ratios correlated positively with comfortable walking speeds and stride frequencies, indicating better walking performance with larger magnitudes of plasticity. Additionally, all four biomechanical plasticity ratios were larger during incline compared to level walking, suggesting the need for larger magnitudes of plasticity during the more difficult task. These results indicate that larger magnitudes of biomechanical plasticity afford functional benefits such as increased level and incline walking performance for old adults. Increased walking performance has the potential to increase quality of life in the growing population of old adults.     

Exploring ecological significance of tree crown plasticity through three-dimensional modelling

BACKGROUND AND AIMS: Morphogenetic plasticity may be as important as physiological plasticity in determining plant adaptability to changing environmental conditions. This study examines the importance of crown plasticity of trees in stands. METHODS: A three-dimensional forest simulator is used to explore the impact of crown shape plasticity on tree growth. Crown deformation is mediated through the local response to light and overall allometric constraints governing tree dimensions. By altering shape response parameters of Hevea brasiliensis the impact of increased or decreased plasticity is explored in a variety of competitive environments defined by various combinations of tree density and relative frequency of different strategies. The possible interactions between plasticity and growth rate and plasticity and below-ground competition are also explored. KEY RESULTS: Crown plasticity confers competitive superiority in all cases studied. Interactions with other processes may downplay or enhance this competitive advantage. CONCLUSIONS: Simulation results strongly suggest that crown plasticity does have a significant impact on tree performance in nature and that commonly observed crown shape deformation response of trees is of adaptive value.     

The genetics of phenotypic plasticity. XIII. Interactions with developmental instability

In a heterogeneous environment, natural selection on a trait can lead to a variety of outcomes, including phenotypic plasticity and bet‐hedging through developmental instability. These outcomes depend on the magnitude and pattern of that heterogeneity and the spatial and temporal distribution of individuals. However, we do not know if and how those two outcomes might interact with each other. I examined the joint evolution of plasticity and instability through the use of an individual‐based simulation in which each could be genetically independent or pleiotropically linked. When plasticity and instability were determined by different loci, the only effect on the evolution of plasticity was the elimination of plasticity as a bet‐hedging strategy. In contrast, the effects on the evolution of instability were more substantial. If conditions were such that the population was likely to evolve to the optimal reaction norm, then instability was disfavored. Instability was favored only when the lack of a reliable environmental cue disfavored plasticity. When plasticity and instability were determined by the same loci, instability acted as a strong limitation on the evolution of plasticity. Under some conditions, selection for instability resulted in maladaptive plasticity. Therefore, before testing any models of plasticity or instability evolution, or interpreting empirical patterns, it is important to know the ecological, life history, developmental, and genetic contexts of trait phenotypic plasticity and developmental instability.     

Proteomics in the study of hippocampal plasticity

Synaptic plasticity is the dynamic regulation of the strength of synaptic communication between nerve cells. It is central to neuronal development as well as experience-dependent remodeling of the adult nervous system as occurs during memory formation. Aberrant forms of synaptic plasticity also accompany a variety of neurological and psychiatric diseases, and unraveling the biological basis of synaptic plasticity has been a major goal in neurobiology research. The biochemical and structural mechanisms underlying different forms of synaptic plasticity are complex, involving multiple signaling cascades, reconfigurations of structural proteins and the trafficking of synaptic proteins. As such, proteomics should be a valuable tool in dissecting the molecular events underlying normal and disease-related forms of plasticity. In fact, progress in this area has been disappointingly slow. We discuss the particular challenges associated with proteomic interrogation of synaptic plasticity processes and outline ways in which we believe proteomics may advance the field over the next few years. We pay particular attention to technical advances being made in small sample proteomics and the advent of proteomic imaging in studying brain plasticity.     

Constraints on the evolution of adaptive phenotypic plasticity in plants

The high potential fitness benefit of phenotypic plasticity tempts us to expect phenotypic plasticity as a frequent adaptation to environmental heterogeneity. Examples of proven adaptive plasticity in plants, however, are scarce and most plastic responses actually may be 'passive' rather than adaptive. This suggests that frequently requirements for the evolution of adaptive plasticity are not met or that such evolution is impeded by constraints. Here we outline requirements and potential constraints for the evolution of adaptive phenotypic plasticity, identify open questions, and propose new research approaches. Important open questions concern the genetic background of plasticity, genetic variation in plasticity, selection for plasticity in natural habitats, and the nature and occurrence of costs and limits of plasticity. Especially promising tools to address these questions are selection gradient analysis, meta-analysis of studies on genotype-by-environment interactions, QTL analysis, cDNA-microarray scanning and quantitative PCR to quantify gene expression, and two-dimensional gel electrophoresis to quantify protein expression. Studying plasticity along the pathway from gene expression to the phenotype and its relationship with fitness will help us to better understand why adaptive plasticity is not more universal, and to more realistically predict the evolution of plastic responses to environmental change.     

POPULATION DIFFERENTIATION FOR PHENOTYPIC PLASTICITY IN THE STELLARIA LONGIPES COMPLEX

Population differentiation for phenotypic plasticity of 12 morphological and reproductive traits was investigated in five populations of the Stellaria longipes complex including a population of the sand dune endemic S. arenicola. Population differentiation was detected for the mean (genotypic) value, amount of plasticity, and pattern of plasticity of traits. Average amount of plasticity was not related to degree of isozyme variability in the populations. Differentiation for pattern of plasticity was much more common than for amount. The direction and extent of divergence among populations was dependent on which of the three trait aspects was under consideration (mean, amount of plasticity, pattern of plasticity) and did not reflect their similarity as revealed by enzyme electrophoretic data. It was concluded that trait means, amounts of plasticity, and patterns of plasticity are independent of one another during evolutionary divergence and may be influenced by mosaic selection.     

Homeostatic plasticity in the CNS: synaptic and intrinsic forms

The study of experience-dependent plasticity has been dominated by questions of how Hebbian plasticity mechanisms act during learning and development. This is unsurprising as Hebbian plasticity constitutes the most fully developed and influential model of how information is stored in neural circuits and how neural circuitry can develop without extensive genetic instructions. Yet Hebbian plasticity may not be sufficient for understanding either learning or development: the dramatic changes in synapse number and strength that can be produced by this kind of plasticity tend to threaten the stability of neural circuits. Recent work has suggested that, in addition to Hebbian plasticity, homeostatic regulatory mechanisms are active in a variety of preparations. These mechanisms alter both the synaptic connections between neurons and the intrinsic electrical properties of individual neurons, in such a way as to maintain some constancy in neuronal properties despite the changes wrought by Hebbian mechanisms. Here we review the evidence for homeostatic plasticity in the central nervous system, with special emphasis on results from cortical preparations.     

Neuroplasticity in respiratory motor control.

Although recent evidence demonstrates considerable neuroplasticity in the respiratory control system, a comprehensive conceptual framework is lacking. Our goals in this review are to define plasticity (and related neural properties) as it pertains to respiratory control and to discuss potential sites, mechanisms, and known categories of respiratory plasticity. Respiratory plasticity is defined as a persistent change in the neural control system based on prior experience. Plasticity may involve structural and/or functional alterations (most commonly both) and can arise from multiple cellular/synaptic mechanisms at different sites in the respiratory control system. Respiratory neuroplasticity is critically dependent on the establishment of necessary preconditions, the stimulus paradigm, the balance between opposing modulatory systems, age, gender, and genetics. Respiratory plasticity can be induced by hypoxia, hypercapnia, exercise, injury, stress, and pharmacological interventions or conditioning and occurs during development as well as in adults. Developmental plasticity is induced by experiences (e.g., altered respiratory gases) during sensitive developmental periods, thereby altering mature respiratory control. The same experience later in life has little or no effect. In adults, neuromodulation plays a prominent role in several forms of respiratory plasticity. For example, serotonergic modulation is thought to initiate and/or maintain respiratory plasticity following intermittent hypoxia, repeated hypercapnic exercise, spinal sensory denervation, spinal cord injury, and at least some conditioned reflexes. Considerable work is necessary before we fully appreciate the biological significance of respiratory plasticity, its underlying cellular/molecular and network mechanisms, and the potential to harness respiratory plasticity as a therapeutic tool.     

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity''s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.     

Costs and limits of phenotypic plasticity

The costs and limits of phenotypic plasticity are thought to have important ecological and evolutionary consequences, yet they are not as well understood as the benefits of plasticity. At least nine ideas exist regarding how plasticity may be costly or limited, but these have rarely been discussed together. The most commonly discussed cost is that of maintaining the sensory and regulatory machinery needed for plasticity, which may require energy and material expenses. A frequently considered limit to the benefit of plasticity is that the environmental cues guiding plastic development can be unreliable. Such costs and limits have recently been included in theoretical models and, perhaps more importantly, relevant empirical studies now have emerged. Despite the current interest in costs and limits of plasticity, several lines of reasoning suggest that they might be difficult to demonstrate.     

Hyaluronan-based extracellular matrix under conditions of homeostatic plasticity

Neuronal networks are balanced by mechanisms of homeostatic plasticity, which adjusts synaptic strength via molecular and morphological changes in the pre- and post-synapse. Here, we wondered whether the hyaluronic acid-based extracellular matrix (ECM) of the brain is involved in mechanisms of homeostatic plasticity. We hypothesized that the ECM, being rich in chondroitin sulfate proteoglycans such as brevican, which are suggested to stabilize synapses by their inhibitory effect on structural plasticity, must be remodelled to allow for structural and molecular changes during conditions of homeostatic plasticity. We found a high abundance of cleaved brevican fragments throughout the hippocampus and cortex and in neuronal cultures, with the strongest labelling in perineuronal nets on parvalbumin-positive interneurons. Using an antibody specific for a brevican fragment cleaved by the matrix metalloprotease ADAMTS4, we identified the enzyme as the main brevican-processing protease. Interestingly, we found ADAMTS4 largely associated with synapses. After inducing homeostatic plasticity in neuronal cell cultures by prolonged network inactivation, we found increased brevican processing at inhibitory as well as excitatory synapses, which is in line with the ADAMTS4 subcellular localization. Thus, the ECM is remodelled in conditions of homeostatic plasticity, which may liberate synapses to allow for a higher degree of structural plasticity.     

Neuronal cytoskeleton in synaptic plasticity and regeneration

During development, dynamic changes in the axonal growth cone and dendrite are necessary for exploratory movements underlying initial axo‐dendritic contact and ultimately the formation of a functional synapse. In the adult central nervous system, an impressive degree of plasticity is retained through morphological and molecular rearrangements in the pre‐ and post‐synaptic compartments that underlie the strengthening or weakening of synaptic pathways. Plasticity is regulated by the interplay of permissive and inhibitory extracellular cues, which signal through receptors at the synapse to regulate the closure of critical periods of developmental plasticity as well as by acute changes in plasticity in response to experience and activity in the adult. The molecular underpinnings of synaptic plasticity are actively studied and it is clear that the cytoskeleton is a key substrate for many cues that affect plasticity. Many of the cues that restrict synaptic plasticity exhibit residual activity in the injured adult CNS and restrict regenerative growth by targeting the cytoskeleton. Here, we review some of the latest insights into how cytoskeletal remodeling affects neuronal plasticity and discuss how the cytoskeleton is being targeted in an effort to promote plasticity and repair following traumatic injury in the central nervous system.     

Glial cells in synaptic plasticity.

Plasticity of synaptic transmission is believed to be the cellular basis for learning and memory, and depends upon different pre- and post-synaptic neuronal mechanisms. Recently, however, an increasing number of studies have implicated a third element in plasticity; the perisynaptic glial cell. Originally glial cells were thought to be important for metabolic maintenance and support of the nervous system. However, work in the past decade has clearly demonstrated active involvement of glia in stability and overall nervous system function as well as synaptic plasticity. Through specific modulation of glial cell function, a wide variety of roles for glia in synaptic plasticity have been uncovered. Furthermore, interesting circumstantial evidence suggests a glial involvement in multiple other types of plasticity. We will discuss recent advances in neuron-glial interactions that take place during synaptic plasticity and explore different plasticity phenomena in which glial cells may be involved.     

Costs and limits of phenotypic plasticity: Tests with predator-induced morphology and life history in a freshwater snail

Potential constraints on the evolution of phenotypic plasticity were tested using data from a previous study on predator-induced morphology and life history in the freshwater snail Physa heterostropha. The benefit of plasticity can be reduced if facultative development is associated with energetic costs, developmental instability, or an impaired developmental range. I examined plasticity in two traits for 29 families of P. heterostropha to see if it was associated with growth rate or fecundity, within-family phenotypic variance, or the potential to produce extreme phenotypes. Support was found for only one of the potential constraints. There was a strong negative selection gradient for growth rate associated with plasticity in shell shape (β = ?0.3, P < 0.0001). This result was attributed to a genetic correlation between morphological plasticity and an antipredator behavior that restricts feeding. Thus, reduced growth associated with morphological plasticity may have had unmeasured fitness benefits. The growth reduction, therefore, is equivocal as a cost of plasticity. Using different fitness components (e.g., survival, fecundity, growth) to seek constraints on plasticity will yield different results in selection gradient analyses. Procedural and conceptual issues related to tests for costs and limits of plasticity are discussed, such as whether constraints on plasticity will be evolutionarily ephemeral and difficult to detect in nature.