Ecological limits to plant phenotypic plasticity

Phenotypic plasticity is considered the major means by which plants cope with environmental heterogeneity. Although ubiquitous in nature, actual phenotypic plasticity is far from being maximal. This has been explained by the existence of internal limits to its expression. However, phenotypic plasticity takes place within an ecological context and plants are generally exposed to multifactor environments and to simultaneous interactions with many species. These external, ecological factors may limit phenotypic plasticity or curtail its adaptive value, but seldom have they been considered because limits to plasticity have typically addressed factors internal to the plant. We show that plastic responses to abiotic factors are reduced under situations of conservative resource use in stressful and unpredictable habitats, and that extreme levels in a given abiotic factor can negatively influence plastic responses to another factor. We illustrate how herbivory may limit plant phenotypic plasticity because damaged plants can only rarely attain the optimal phenotype in the challenging environment. Finally, it is examined how phenotypic changes involved in trait-mediated interactions can entail costs for the plant in further interactions with other species in the community. Ecological limits to plasticity must be included in any realistic approach to understand the evolution of plasticity in complex environments and to predict plant responses to global change.     

Costs of inducible defence along a resource gradient

In addition to having constitutive defence traits, many organisms also respond to predation by phenotypic plasticity. In order for plasticity to be adaptive, induced defences should incur a benefit to the organism in, for example, decreased risk of predation. However, the production of defence traits may include costs in fitness components such as growth, time to reproduction, or fecundity. To test the hypothesis that the expression of phenotypic plasticity incurs costs, we performed a common garden experiment with a freshwater snail, Radix balthica, a species known to change morphology in the presence of molluscivorous fish. We measured a number of predator-induced morphological and behavioural defence traits in snails that we reared in the presence or absence of chemical cues from fish. Further, we quantified the costs of plasticity in fitness characters related to fecundity and growth. Since plastic responses may be inhibited under limited resource conditions, we reared snails in different densities and thereby levels of competition. Snails exposed to predator cues grew rounder and thicker shells, traits confirmed to be adaptive in environments with fish. Defence traits were consistently expressed independent of density, suggesting strong selection from predatory molluscivorous fish. However, the expression of defence traits resulted in reduced growth rate and fecundity, particularly with limited resources. Our results suggest full defence in predator related traits regardless of resource availability, and costs of defence consequently paid in traits related to fitness.     

Phenotypic plasticity facilitates initial colonization of a novel environment

Phenotypic plasticity can allow organisms to respond to environmental changes by producing better matching phenotypes without any genetic change. Because of this, plasticity is predicted to be a major mechanism by which a population can survive the initial stage of colonizing a novel environment. We tested this prediction by challenging wild Drosophila melanogaster with increasingly extreme larval environments and then examining expression of alcohol dehydrogenase (ADH) and its relationship to larval survival in the first generation of encountering a novel environment. We found that most families responded in the adaptive direction of increased ADH activity in higher alcohol environments and families with higher plasticity were also more likely to survive in the highest alcohol environment. Thus, plasticity of ADH activity was positively selected in the most extreme environment and was a key trait influencing fitness. Furthermore, there was significant heritability of ADH plasticity that can allow plasticity to evolve in subsequent generations after initial colonization. The adaptive value of plasticity, however, was only evident in the most extreme environment and had little impact on fitness in less extreme environments. The results provide one of the first direct tests of the adaptive role of phenotypic plasticity in colonizing a novel environment.     

Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis

Plants possess a remarkable capacity to alter their phenotype in response to the highly heterogeneous light conditions they commonly encounter in natural environments. In the present study with the weedy annual plant Sinapis arvensis, we (a) tested for the adaptive value of phenotypic plasticity in morphological and life history traits in response to low light and (b) explored possible fitness costs of plasticity. Replicates of 31 half-sib families were grown individually in the greenhouse under full light and under low light (40% of ambient) imposed by neutral shade cloth. Low light resulted in a large increase in hypocotyl length and specific leaf area (SLA), a reduction in juvenile biomass and a delayed onset of flowering. Phenotypic selection analysis within each light environment revealed that selection favoured large SLA under low light, but not under high light, suggesting that the observed increase in SLA was adaptive. In contrast, plasticity in the other traits measured was maladaptive (i.e. in the opposite direction to that favoured by selection in the low light environment). We detected significant additive genetic variance in plasticity in most phenotypic traits and in fitness (number of seeds). Using genotypic selection gradient analysis, we found that families with high plasticity in SLA had a lower fitness than families with low plasticity, when the effect of SLA on fitness was statistically kept constant. This indicates that plasticity in SLA incurred a direct fitness cost. However, a cost of plasticity was only expressed under low light, but not under high light. Thus, models on the evolution of phenotypic plasticity will need to incorporate plasticity costs that vary in magnitude depending on environmental conditions.     

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.     

Plasticity of physiology in Lobelia: testing for adaptation and constraint

Phenotypic plasticity is thought to be a major mechanism allowing sessile organisms such as plants to adapt to environmental heterogeneity. However, the adaptive value of many common plastic responses has not been tested by linking these responses to fitness. Even when plasticity is adaptive, costs of plasticity, such as the energy necessary to maintain regulatory pathways for plastic responses, may constrain its evolution. We used a greenhouse experiment to test whether plastic physiological responses to soil water availability (wet vs. dry conditions) were adaptive and/or costly in the congeneric wildflowers Lobelia cardinalis and L. siphilitica. Eight physiological traits related to carbon and water uptake were measured. Specific leaf area (SLA), photosynthetic rate (A), stomatal conductance (gs), and photosynthetic capacity (Amax) responded plastically to soil water availability in L. cardinalis. Plasticity in Amax was maladaptive, plasticity in A and g(s) was adaptive, and plasticity in SLA was adaptively neutral. The nature of adaptive plasticity in L. cardinalis, however, differed from previous studies. Lobelia cardinalis plants with more conservative water use, characterized by lower g(s), did not have higher fitness under drought conditions. Instead, well-watered L. cardinalis that had higher g(s) had higher fitness. Only Amax responded plastically to drought in L. siphilitica, and this response was adaptively neutral. We detected no costs of plasticity for any physiological trait in either L. cardinalis or L. siphilitica, suggesting that the evolution of plasticity in these traits would not be constrained by costs. Physiological responses to drought in plants are presumed to be adaptive, but our data suggest that much of this plasticity can be adaptively neutral or maladaptive.     

Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants

Phenotypic plasticity may play a key role in the adaptation of organisms to changing environmental conditions. A special case of plasticity is represented by heterophylly, the ability of semi-aquatic plants to produce different types of leaves below and above water. Submerged leaves are thin and lack both a cuticle and stomata, whereas aerial leaves are thicker, cutinized and bear stomata. The striking variability in the submerged, floating and aerial leaves of heterophyllous aquatics has historically been considered a paradigmatic example of adaptive phenotypic plasticity. An extensive body of developmental and physiological research reveals that heterophylly is quite often mediated by similar environmental cues across diverse taxa, which may imply a common underlying mechanism. Patterns of plasticity in response to environmental cues in the laboratory are consistent with the hypothesis of individual adaptation to heterogeneous environments, and the distribution of this trait among phylogenetically related aquatic angiosperms suggests either convergent or parallel evolution in their descent from terrestrial ancestors. Yet, critical evaluations of the ecological and evolutionary significance of this trait are scarce. In this essay, we discuss the patterns of plasticity revealed by experimental manipulative studies of heterophylly in the context of the general problem of adaptive phenotypic plasticity, and suggest avenues for future research that are needed in assessing the ecological and evolutionary significance of this trait.     

Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments

Adaptive plasticity is expected to be important when the grain of environmental variation is encompassed in offspring dispersal distance. We investigated patterns of local adaptation, selection and plasticity in an association of plant morphology with fine-scale habitat shifts from oak canopy understory to adjacent grassland habitat in Claytonia perfoliata. Populations from beneath the canopy of oak trees were >90 % broad leaved and large seeded, while plants from adjacent grassland habitat were >90 % linear-leaved and small seeded. In a 2-year study, we used reciprocal transplants and phenotypic selection analysis to investigate local adaptation, selection, plasticity and maternal effects in this trait-environment association. Transgenerational effects were studied by planting offspring of inbred maternal families grown in both environments across the same environments in the second year. Reciprocal transplants revealed local adaptation to habitat type: broad-leaved forms had higher fitness in oak understory and linear-leaved plants had higher fitness in open grassland habitat. Phenotypic selection analyses indicated selection for narrower leaves and lower SLA in open habitat, and selection for broad leaves and intermediate values of SLA in understory. Both plant morphs exhibited plastic responses in traits in the same direction as selection on traits (narrower leaves and lower SLA in open habitat) suggesting that plasticity is adaptive. We detected an adaptive transgenerational effect in which maternal environment influenced offspring fitness; offspring of grassland-reared plants had higher fitness than understory-reared plants when grown in grassland. We did not detect costs of plasticity, but did find a positive association between leaf shape plasticity and fitness in linear-leaved plants in grassland habitat. Together, these findings indicate that fixed differences in trait values corresponding to selection across habitat contribute to local adaptation, but that plasticity and maternal environmental effects may be favored through promotion of survival across heterogeneous environments.     

Toward a population genetic framework of developmental evolution: the costs,limits, and consequences of phenotypic plasticity

Adaptive phenotypic plasticity allows organisms to cope with environmental variability, and yet, despite its adaptive significance, phenotypic plasticity is neither ubiquitous nor infinite. In this review, we merge developmental and population genetic perspectives to explore costs and limits on the evolution of plasticity. Specifically, we focus on the role of modularity in developmental genetic networks as a mechanism underlying phenotypic plasticity, and apply to it lessons learned from population genetic theory on the interplay between relaxed selection and mutation accumulation. We argue that the environmental specificity of gene expression and the associated reduction in pleiotropic constraints drive a fundamental tradeoff between the range of plasticity that can be accommodated and mutation accumulation in alternative developmental networks. This tradeoff has broad implications for understanding the origin and maintenance of plasticity and may contribute to a better understanding of the role of plasticity in the origin, diversification, and loss of phenotypic diversity.     

Adaptive plasticity in response to light and nutrient availability in the clonal plant Duchesnea indica

克隆植物蛇莓对光照强度和养分条件的适应性可塑性 表型可塑性可帮助植物缓冲环境压力并使其表型与当地环境相匹配,但目前仅少数性状的可塑性被广泛认为是适应性的。为充分理解可塑性的适应性意义,仍需进一步研究更多的植物功能性状及其环境因子。本研究将匍匐茎克隆植物蛇莓(Duchesnea indica)的21个基因型种植于不同的光照和养分条件下,并利用选择梯度分析检测了形态和生理可塑性对光照强度和养分有效性变化的适应性值。在遮荫条件下,蛇莓适合度(果实数、分株数和生物量)降低,节间缩短变细,成熟叶叶绿素含量降低,但叶柄长度、比叶面积、老叶叶绿素含量均增加。在低养分条件下,植株叶柄缩短,叶面积缩小变厚,叶绿素含量降低,但果实数量和根冠比增加。选择梯度分析表明,叶柄长度和老叶叶绿素含量对光照变化的可塑性是适应性的,老叶和成熟叶叶绿素含量对养分变化的可塑性也是适应性的。因此,不同性状的可塑性适应值取决于特定的生态背景。该研究的发现有助于理解克隆植物表型可塑性响应环境变化的适应性意义。     

Plastic inducible morphologies are not always adaptive: The importance of time delays in a stochastic environment

Summary We present a mathematical model for predicting the expected fitness of phenotypically plastic organisms experiencing a variable environment. We assume that individuals experience two discrete environments probabilistically in time (as a Markov process) and that there are two different phenotypic states, each yielding the highest fitness in one of the two environments. We compare the expected fitness of a phenotypically fixed individual to that of an individual whose phenotype is induced to produce the better phenotype in each environment with a time lag between experiencing a new environment and realization of the new phenotype. Such time lags are common in organisms where phenotypically plastic, inducible traits have been documented. We find that although plasticity is generally adaptive when time lags are short (relative to the time scale of environmental variability), plasticity can be disadvantageous for longer lag times. Asymmetries in environmental change probabilities and/or the relative fitnesses of each phenotype strongly influence whether plasticity is favoured. In contrast to other models, our model does not require costs for plasticity to be disadvantageous; costs affect the results quantitatively, not qualitatively.     

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.     

Testing the grain-size model for the evolution of phenotypic plasticity

Phenotypic plasticity is the ability of a genotype to modify its phenotypic characteristics in response to different environments. Theory predicts that adaptive plasticity should primarily evolve in organisms that experience heterogeneous environments. An organism's dispersal rate is a key component in these models, because the degree of dispersal partly determines the extent of environmental heterogeneity. Here, I provide the first large-scale test of the theoretical prediction that phenotypic plasticity evolves in association with dispersal rate using meta-analysis of data from 258 experiments from the literature on plasticity in marine invertebrates. In line with predictions, phenotypic plasticity is generally greater in species with higher dispersal rates, suggesting that dispersal and environmental heterogeneity are important selective agents for evolution of plasticity in marine habitats.     

Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses

Phenotypic plasticity is a key factor for the success of organisms in heterogeneous environments. Although many forms of phenotypic plasticity can be induced and retracted repeatedly, few extant models have analyzed conditions for the evolution of reversible plasticity. We present a general model of reversible plasticity to examine how plastic shifts in the mode and breadth of environmental tolerance functions (that determine relative fitness) depend on time lags in response to environmental change, the pattern of individual exposure to inducing and noninducing environments, and the quality of available information about the environment. We couched the model in terms of prey-induced responses to variable predation regimes. With longer response lags relative to the rate of environmental change, the modes of tolerance functions in both the presence or absence of predators converge on a generalist strategy that lies intermediate between the optimal functions for the two environments in the absence of response lags. Incomplete information about the level of predation risk in inducing environments causes prey to have broader tolerance functions even at the cost of reduced maximal fitness. We give a detailed analysis of how these factors and interactions among them select for joint patterns of mode and breadth plasticity.     

植物表型可塑性研究进展

表型可塑性已成为生态进化发育生物学的核心概念,很大程度上由于植物可塑性研究的主要贡献,但人们仍远未完全了解表型可塑性的原因和结果。从整体角度理出表型可塑性研究发展的基本脉络,介绍研究内容、途径和简史,聚焦于几个主要方面的研究进展及发展方向。现代可塑性研究的兴盛始于关于可塑性的进化学重要性的一篇综述,从现象的描述、对其遗传基础和可塑性本身进化的讨论,发展到探索其背后的发育机制、植物生长与适应策略、生态学影响等。未来可塑性研究应在重新理解和评价表型可塑性及其适应性的基础上,更关注自然条件下环境因子和可塑响应的复杂性。表型可塑性的生态-进化学意义仍将是未来研究的重点。     

CHARACTERIZING SELECTION ON PHENOTYPIC PLASTICITY IN RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY

Adaptive genetic differentiation and adaptive phenotypic plasticity can increase the fitness of plant lineages in heterogeneous environments. We examine the relative importance of genetic differentiation and plasticity in determining the fitness of the annual plant, Erodium cicutarium, in a serpentine grassland in California. Previous work demonstrated that the serpentine sites within this mosaic display stronger dispersal‐scale heterogeneity than nonserpentine sites. We conducted a reciprocal transplant experiment among six sites to characterize selection on plasticity expressed by 180 full‐sibling families in response to natural environmental heterogeneity across these sites. Multivariate axes of environmental variation were constructed using a principal components analysis of soil chemistry data collected at every experimental block. Simple linear regressions were used to characterize the intercept, and slope (linear and curvilinear) of reaction norms for each full‐sibling family in response to each axis of environmental variation. Multiple linear regression analyses revealed significant selection on trait means and slopes of reaction norms. Multivariate analyses of variance demonstrated genetic differentiation between serpentine and nonserpentine lineages in the expression of plasticity in response to three of the five axes of environmental variation considered. In all but one case, serpentine genotypes expressed a stronger adaptive plastic response than nonserpentine genotypes.     

The fitness costs of developmental canalization and plasticity

Organisms are capable of an astonishing repertoire of phenotypic responses to the environment, and these often define important adaptive solutions to heterogeneous and unpredictable conditions. The terms ‘phenotypic plasticity’ and ‘canalization’ indicate whether environmental variation has a large or small effect on the phenotype. The evolution of canalization and plasticity is influenced by optimizing selection‐targeting traits within environments, but inherent fitness costs of plasticity may also be important. We present a meta‐analysis of 27 studies (of 16 species of plant and 7 animals) that have measured selection on the degree of plasticity independent of the characters expressed within environments. Costs of plasticity and canalization were equally frequent and usually mild; large costs were observed only in studies with low sample size. We tested the importance of several covariates, but only the degree of environmental stress was marginally positively related to the cost of plasticity. These findings suggest that costs of plasticity are often weak, and may influence phenotypic evolution only under stressful conditions.     

Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments

Adaptive phenotypic plasticity and adaptive genetic differentiation enable plant lineages to maximize their fitness in response to environmental heterogeneity. The spatial scale of environmental variation relative to the average dispersal distance of a species determines whether selection will favor plasticity, local adaptation, or an intermediate strategy. Habitats where the spatial scale of environmental variation is less than the dispersal distance of a species are fine grained and should favor the expression of adaptive plasticity, while coarse-grained habitats, where environmental variation occurs on spatial scales greater than dispersal, should favor adaptive genetic differentiation. However, there is relatively little information available characterizing the link between the spatial scale of environmental variation and patterns of selection on plasticity measured in the field. I examined patterns of spatial environmental variation within a serpentine mosaic grassland and selection on an annual plant (Erodium cicutarium) within that landscape. Results indicate that serpentine soil patches are a significantly finer-grained habitat than non-serpentine patches. Additionally, selection generally favored increased plasticity on serpentine soils and diminished plasticity on non-serpentine soils. This is the first empirical example of differential selection for phenotypic plasticity in the field as a result of strong differences in the grain of environmental heterogeneity within habitats.