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The evolutionary consequences of ecological interactions mediated through phenotypic plasticity.

Phenotypic plasticity describes the capacity of a genotype to exhibit a range of phenotypes in response to variation in the environment. Environmental variation encompasses both abiotic and biotic components of the environment, including interactions among organisms. The strength and outcome of many ecological interactions, ranging from antagonism to mutualism, are mediated through the phenotypically plastic responses of one or more players in the interaction. Herein, three broadly defined, non-mutually exclusive, evolutionary consequences of ecological interactions mediated through phenotypic plasticity are discussed. (1) The predictable plastic response of one partner can favor behaviors, physiological responses, and life history traits of an interacting partner that manipulate, circumvent, or ameliorate the response of that partner. (2) Phenotypic plasticity can generate substantial spatial and temporal variation within and among populations. Such phenotypic variation can depend on the density and identity of interacting players in an ecological community, and can ultimately affect the evolutionary outcome of ecological interactions. (3) Phenotypic plasticity affects the strength and direction of natural selection. Ecological interactions mediated through phenotypic plasticity are ubiquitous in nature, and the potential evolutionary consequences of these interactions illustrate the complexity inherent in understanding evolution in a community context.

Adaptation, Physiological↗

Ecological consequences of phenotypic plasticity.

Phenotypic plasticity is widespread in nature, and often involves ecologically relevant behavioral, physiological, morphological and life-historical traits. As a result, plasticity alters numerous interactions between organisms and their abiotic and biotic environments. Although much work on plasticity has focused on its patterns of expression and evolution, researchers are increasingly interested in understanding how plasticity can affect ecological patterns and processes at various levels. Here, we highlight an expanding body of work that examines how plasticity can affect all levels of ecological organization through effects on demographic parameters, direct and indirect species interactions, such as competition, predation, and coexistence, and ultimately carbon and nutrient cycles.

Journal Article↗

Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity.

Adaptive phenotypic plasticity in chemical defense is thought to play a major role in plant-herbivore interactions. We investigated genetic variation for inducibility of defensive traits in wild radish plants and asked if the evolution of induction is constrained by costs of phenotypic plasticity. In a greenhouse experiment using paternal half-sibling families, we show additive genetic variation for plasticity in glucosinolate concentration. Genetic variation for glucosinolates was not detected in undamaged plants, but was significant following herbivory by a specialist herbivore, Pieris rapae. On average, damaged plants had 55% higher concentrations of glucosinolates compared to controls. In addition, we found significant narrow-sense heritabilities for leaf size, trichome number, flowering phenology, and lifetime fruit production. In a second experiment, we found evidence of genetic variation in induced plant resistance to P. rapae. Although overall there was little evidence for genetic correlations between the defensive and life-history traits we measured, we show that more plastic families had lower fitness than less plastic families in the absence of herbivory (i.e., evidence for genetic costs of plasticity). Thus, there is genetic variation for induction of defense in wild radish, and the evolution of inducibility may be constrained by costs of plasticity.

Animals↗

Shade tolerance, photoinhibition sensitivity and phenotypic plasticity of Ilex aquifolium in continental Mediterranean sites.

Shade tolerance, plastic phenotypic response to light and sensitivity to photoinhibition were studied in holly (Ilex aquifolium L.) seedlings transported from the field to a greenhouse and in adult trees in the field. All plants were growing in, or originated from, continental Mediterranean sites in central Spain. Seedlings tolerated moderate but not deep shade. Mortality was high and growth reduced in 1% sunlight. Survival was maximal in 12% sunlight and minimal in full sunlight, although the relative growth rate of the seedlings surviving in high light was similar to that of plants in moderate shade. Maximum photochemical efficiency at predawn was significantly lower in sun plants than in shade plants in the field, revealing chronic photoinhibition that was most pronounced in winter. Plasticity in response to available light varied according to the variable studied, being low for photosynthetic capacity and stomatal conductance, and high for specific leaf area, root:shoot ratio and leaf area ratio, particularly in seedlings. Differences in water relations and hydraulic features between sun and shade plants in the field were marginal. High water potential at the turgor loss point of field-grown plants suggested that holly is sensitive to drought during both the seedling and the adult stage. Low relative growth rates in both high and low light with low physiological plasticity in response to light indicate the existence of a stress-tolerance mechanism. We conclude that holly is a facultative understory plant in areas of oceanic and relatively mild climate, but an obligate understory plant in dry continental areas such as the study site. The impact of abandonment of traditional management practices and climate change on these Mediterranean populations is discussed.

Chlorophyll↗

An investigation into the role of phenotypic plasticity in evolution.

Phenotypic plasticity can modify evolutionary pathways and accelerate the course of evolution. This was brought out in a quantitative model by Hinton & Nowlan (1987, Complex Systems 1, 497-502). The present work confirms and extends their results. We consider a population of genetically haploid individuals of fixed size. Genotypes are represented by one-dimensional arrays (strings) of genes. Each gene can be in one of three allelic states, designated 1, 0 and X. 1 and 0 stand for fixed states, that is for states with predetermined effects on the phenotype. X stands for a plastic state: the phenotypic effect of an X can be equivalent to that of a 1 or a 0, the actual choice being realized by a process of random coin-tossing. Our model, in contrast to that of Hinton and Nowlan, assumes a relatively smooth dependence of fitness on distance from a pre-assigned target genotype. From the fitness values, the number of individuals reaching reproductive maturity is determined. Reproduction involves random mating and a single recombinational event, with one of the two progeny genotypes becoming, in turn, a possible parental genotype for the next generation. We find that it is because of the special assumptions in the Hinton and Nowlan model that phenotypic plasticity invariably accelerates evolution. The relationship is not as straightforward with realistic fitness schemes. Instead, the general result is that plasticity, up to a certain optimal level, slows down the rate of evolutionary change but improves the level of adaptation finally reached.

Adaptation, Physiological↗

Artificial selection on phenotypically plastic traits.

Many phenotypes respond physiologically or developmentally to continuously distributed environmental variables such as temperature and nutritional quality. Information about phenotypic plasticity can be used to improve the efficiency of artificial selection. Here we show that the quantitative genetic theory for 'infinite-dimensional' traits such as reaction norms provides a natural framework to accomplish this goal. It is expected to improve selection responses by making more efficient use of information about environmental effects than do conventional methods. The approach is illustrated by deriving an index for mass selection of a phenotypically plastic trait. We suggest that the same approach could be extended directly to more general and efficient breeding schemes, such as those based on general best linear unbiased prediction. Methods for estimating genetic covariance functions are reviewed.

Animals↗

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.

Adaptation, Physiological↗

Predator-induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.

Animals↗

How stress selects for reversible phenotypic plasticity.

Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays. The selective advantage of genotypes that are able to produce adaptive reversible plastic phenotypes is calculated by using the concept of environmental tolerance. Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non-induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions.

Computer Simulation↗

A regulatory network analysis of phenotypic plasticity in yeast.

Models for the evolution of phenotypic plasticity suggest when and why plasticity might evolve. However, relatively little is known about the genetic basis of plasticity. Molecular studies have recently demonstrated that gene networks can provide a powerful way to infer phenotype from genotype. Information on the structure of the yeast gene regulatory network was combined with data on variation in gene expression in yeast across multiple environments in order to explore the genetic basis of phenotypic plasticity. The phenotypic plasticity of a gene was positively correlated with the number of transcription factors regulating that gene and was significantly lower for transcription factors than for downstream, nonregulatory genes. Plasticity of a gene was also affected by the local substructure of the network in which it was found and by the gene's function. These results illustrate how network analyses can be used to understand the complex genetic architecture of quantitative traits.

Gene Expression Regulation, Fungal↗

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.

Adaptation, Physiological↗

Phenotypic plasticity opposes species invasions by altering fitness surface.

Understanding species invasion is a central problem in ecology because invasions of exotic species severely impact ecosystems, and because invasions underlie fundamental ecological processes. However, the influence on invasions of phenotypic plasticity, a key component of many species interactions, is unknown. We present a model in which phenotypic plasticity of a resident species increases its ability to oppose invaders, and plasticity of an invader increases its ability to displace residents. Whereas these effects are expected due to increased fitness associated with phenotypic plasticity, the model additionally reveals a new and unforeseen mechanism by which plasticity affects invasions: phenotypic plasticity increases the steepness of the fitness surface, thereby making invasion more difficult, even by phenotypically plastic invaders. Our results should apply to phenotypically plastic responses to any fluctuating environmental factors including predation risk, and to other factors that affect the fitness surface such as the generalism of predators. We extend the results to competition, and argue that phenotypic plasticity's effect on the fitness surface will destabilize coexistence at local scales, but stabilize coexistence at regional scales. Our study emphasizes the need to incorporate variable interaction strengths due to phenotypic plasticity into invasion biology and ecological theory on competition and coexistence in fragmented landscapes.

Adaptation, Physiological↗

Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis.

Environmentally induced phenotypic plasticity allows developing organisms to respond adaptively to changes in their habitat. Desert amphibians have evolved traits which allow successful development in unpredictable environments. Tadpoles of these species can accelerate metamorphosis as their pond dries, thus escaping mortality in the larval habitat. This developmental response can be replicated in the laboratory, which allows elucidation of the underlying physiological mechanisms. Here I demonstrate a link between a classical neurohormonal stress pathway (involving corticotropin-releasing hormone, CRH) and the developmental response to habitat desiccation. Injections of CRH-like peptides accelerated metamorphosis in western spadefoot toad tadpoles. Conversely, treatment with two CRH antagonists, the CRH receptor antagonist alpha-helical CRH(9-41) and anti-CRH serum, attenuated the developmental acceleration induced by habitat desiccation. Tadpoles subjected to habitat desiccation exhibited elevated hypothalamic CRH content at the time when they responded developmentally to the declining water level. CRH injections elevated whole-body thyroxine, triiodothyronine, and corticosterone content, the primary hormonal regulators of metamorphosis. In contrast, alpha-helical CRH(9-41) reduced thyroid activity. These results support a central role for CRH as a neurohormonal transducer of environmental stimuli into the endocrine response which modulates the rate of metamorphosis. Because in mammals, increased fetal/placental CRH production may initiate parturition, and CRH has been implicated in precipitating preterm birth arising from fetal stress, this neurohormonal pathway may represent a phylogenetically ancient developmental regulatory system that allows the organism to escape an unfavorable larval/fetal habitat.

Animals↗

Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations.

Adaptive phenotypic plasticity in the form of capacity to accelerate development as a response to pond drying risk is known from many amphibian species. However, very little is known about factors that might constrain the evolution of this type of plasticity, and few studies have explored to what degree plasticity might be constrained by trade-offs dictated by adaptation to different environmental conditions. We compared the ability of southern and northern Scandinavian common frog (Rana temporaria) larvae originating from 10 different populations to accelerate their development in response to simulated pond drying risk and the resulting costs in metamorphic size in a factorial laboratory experiment. We found that (i) northern larvae developed faster than the southern larvae in all treatments, (ii) a capacity to accelerate the response was present in all five southern and all five northern populations tested, but that the magnitude of the response was much larger (and less variable) in the southern than in the northern populations, and that (iii) significant plasticity costs in metamorphic size were present in the southern populations, the plastic genotypes having smaller metamorphic size in the absence of desiccation risk, but no evidence for plasticity costs was found in the northern populations. We suggest that the weaker response to pond drying risk in the northern populations is due to stronger selection on large metamorphic size as compared with southern populations. In other words, seasonal time constraints that have selected the northern larvae to be fast growing and developing, may also constrain their innate ability for adaptive phenotypic plasticity.

Adaptation, Physiological↗

Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution?

The claim that phenotypic plasticity speeds up evolution towards a target phenotype is a recent incarnation of the Baldwin effect. To differentiate this theory from earlier interpretations of Baldwin's ideas, we name it the Baldwin expediting effect. Models that demonstrate this effect assume an extreme fitness scenario which bestows high fitness upon a single optimal phenotype and treats all other phenotypes as equal. In two modeling frameworks, we demonstrate that the effects of plasticity on the rate of evolution are highly dependent on the fitness function and population starting conditions. We argue that phenotypic plasticity does not universally facilitate evolution. Furthermore, in cases where the Baldwin expediting effect occurs, it is not necessarily correlated with increased fitness and therefore is not sufficient to explain the evolutionary success of plasticity.

Biological Evolution↗

Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations.

Phenotypic plasticity provides means for adapting to environmental unpredictability. In terms of accelerated development in the face of pond-drying risk, phenotypic plasticity has been demonstrated in many amphibian species, but two issues of evolutionary interest remain unexplored. First, the heritable basis of plastic responses is poorly established. Second, it is not known whether interpopulational differences in capacity to respond to pond-drying risk exist, although such differences, when matched with differences in desiccation risk would provide strong evidence for local adaptation. We investigated sources of within- and among-population variation in plastic responses to simulated pond-drying risk (three desiccation treatments) in two Rana temporaria populations originating from contrasting environments: (1) high desiccation risk with weak seasonal time constraint (southern population); and (2) low desiccation risk with severe seasonal time constraint (northern population). The larvae originating from the environment with high desiccation risk responded adaptively to the fast decreasing water treatment by accelerating their development and metamorphosing earlier, but this was not the case in the larvae originating from the environment with low desiccation risk. In both populations, metamorphic size was smaller in the high-desiccation-risk treatment, but the effect was larger in the southern population. Significant additive genetic variation in development rate was found in the northern and was nearly significant in the southern population, but there was no evidence for genetic variation in plasticity for development rates in either of the populations. No genetic variation for plasticity was found either in size at metamorphosis or growth rate. All metamorphic traits were heritable, and additive genetic variances were generally somewhat higher in the southern population, although significantly so in only one trait. Dominance variances were also significant in three of four traits, but the populations did not differ. Maternal effects in metamorphic traits were generally weak in both populations. Within-environment phenotypic correlations between larval period and metamorphic size were positive and genetic correlations negative in both populations. These results suggest that adaptive phenotypic plasticity is not a species-specific fixed trait, but evolution of interpopulational differences in plastic responses are possible, although heritability of plasticity appears to be low. The lack of adaptive response to desiccation risk in northern larvae is consistent with the interpretation that selection imposed by shorter growing season has favored rapid development in north (approximately 8% faster development in north as compared to south) or a minimum metamorphic size at the expense of phenotypic plasticity.

Adaptation, Physiological↗

The consequences of phenotypic plasticity in cyclically varying environments: a genetic algorithm study.

By "phenotypic plasticity" we refer to the capacity of a genotype to exhibit different phenotypes, whether in the same or in different environments. We have previously demonstrated that phenotypic plasticity can improve the degree of adaptation achieved via natural selection (Behera & Nanjundiah, 1995). That result was obtained from a genetic algorithm model of haploid genotypes (idealized as one-dimensional strings of genes) evolving in a fixed environment. Here, the dynamics of evolution is examined under conditions of a cyclically varying environment. We find that the rate of evolution, as well as the extent of adaptation (as measured by mean population fitness) is lowered because of environmental cycling. The decrease in adaptation caused by a varying environment can, however, be partly or wholly compensated by an increase in the degree of plasticity that a genotype is capable of. Also, the reduction of population fitness caused by a variable environment can be partially offset by decreasing the total number of genetic loci. We conjecture that an increase in genome size may have been among the factors responsible for the evolution of phenotypic plasticity.

Adaptation, Physiological↗

The role of phenotypic plasticity in driving genetic evolution.

Models of population divergence and speciation are often based on the assumption that differences between populations are due to genetic factors, and that phenotypic change is due to natural selection. It is equally plausible that some of the differences among populations are due to phenotypic plasticity. We use the metaphor of the adaptive landscape to review the role of phenotypic plasticity in driving genetic evolution. Moderate levels of phenotypic plasticity are optimal in permitting population survival in a new environment and in bringing populations into the realm of attraction of an adaptive peak. High levels of plasticity may increase the probability of population persistence but reduce the likelihood of genetic change, because the plastic response itself places the population close to a peak. Moderate levels of plasticity arise whenever multiple traits, some of which are plastic and others not, form a composite trait involved in the adaptive response. For example, altered behaviours may drive selection on morphology and physiology. Because there is likely to be a considerable element of chance in which behaviours become established, behavioural change followed by morphological and physiological evolution may be a potent force in driving evolution in novel directions. We assess the role of phenotypic plasticity in stimulating evolution by considering two examples from birds: (i) the evolution of red and yellow plumage coloration due to carotenoid consumption; and (ii) the evolution of foraging behaviours on islands. Phenotypic plasticity is widespread in nature and may speed up, slow down, or have little effect on evolutionary change. Moderate levels of plasticity may often facilitate genetic evolution but careful analyses of individual cases are needed to ascertain whether plasticity has been essential or merely incidental to population differentiation.

Adaptation, Biological↗