Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation

Adaptation to a sudden extreme change in environment, beyond the usual range of background environmental fluctuations, is analysed using a quantitative genetic model of phenotypic plasticity. Generations are discrete, with time lag τ between a critical period for environmental influence on individual development and natural selection on adult phenotypes. The optimum phenotype, and genotypic norms of reaction, are linear functions of the environment. Reaction norm elevation and slope (plasticity) vary among genotypes. Initially, in the average background environment, the character is canalized with minimum genetic and phenotypic variance, and no correlation between reaction norm elevation and slope. The optimal plasticity is proportional to the predictability of environmental fluctuations over time lag τ. During the first generation in the new environment the mean fitness suddenly drops and the mean phenotype jumps towards the new optimum phenotype by plasticity. Subsequent adaptation occurs in two phases. Rapid evolution of increased plasticity allows the mean phenotype to closely approach the new optimum. The new phenotype then undergoes slow genetic assimilation, with reduction in plasticity compensated by genetic evolution of reaction norm elevation in the original environment.     

The combined effects of temporal autocorrelation and the costs of plasticity on the evolution of plasticity

Adaptive phenotypic plasticity is an important source of intraspecific variation, and for many plastic traits, the costs or factors limiting plasticity seem cryptic. However, there are several different factors that may constrain the evolution of plasticity, but few models have considered costs and limiting factors simultaneously. Here we use a simulation model to investigate how the optimal level of plasticity in a population depends on a fixed maintenance fitness cost for plasticity or an incremental fitness cost for producing a plastic response in combination with environmental unpredictability (environmental fluctuation speed) limiting plasticity. Our model identifies two mechanisms that act, almost separately, to constrain the evolution of plasticity: (i) the fitness cost of plasticity scaled by the nonplastic environmental tolerance, and (ii) the environmental fluctuation speed scaled by the rate of phenotypic change. That is, the evolution of plasticity is constrained by the high cost of plasticity in combination with high tolerance for environmental variation, or fast environmental changes in combination with slow plastic response. Qualitatively similar results are found when maintenance and incremental fitness costs of plasticity are incorporated, although a larger degree of plasticity is selected for with an incremental cost. Our model highlights that it is important to consider direct fitness costs and phenotypic limitations in relation to nonplastic environmental tolerance and environmental fluctuations, respectively, to understand what constrains the evolution of phenotypic plasticity.     

GENOTYPE-ENVIRONMENT INTERACTION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY

Studies of spatial variation in the environment have primarily focused on how genetic variation can be maintained. Many one-locus genetic models have addressed this issue, but, for several reasons, these models are not directly applicable to quantitative (polygenic) traits. One reason is that for continuously varying characters, the evolution of the mean phenotype expressed in different environments (the norm of reaction) is also of interest. Our quantitative genetic models describe the evolution of phenotypic response to the environment, also known as phenotypic plasticity (Gause, 1947), and illustrate how the norm of reaction (Schmalhausen, 1949) can be shaped by selection. These models utilize the statistical relationship which exists between genotype-environment interaction and genetic correlation to describe evolution of the mean phenotype under soft and hard selection in coarse-grained environments. Just as genetic correlations among characters within a single environment can constrain the response to simultaneous selection, so can a genetic correlation between states of a character which are expressed in two environments. Unless the genetic correlation across environments is ± 1, polygenic variation is exhausted, or there is a cost to plasticity, panmictic populations under a bivariate fitness function will eventually attain the optimum mean phenotype for a given character in each environment. However, very high positive or negative correlations can substantially slow the rate of evolution and may produce temporary maladaptation in one environment before the optimum joint phenotype is finally attained. Evolutionary trajectories under hard and soft selection can differ: in hard selection, the environments with the highest initial mean fitness contribute most individuals to the mating pool. In both hard and soft selection, evolution toward the optimum in a rare environment is much slower than it is in a common one. A subdivided population model reveals that migration restriction can facilitate local adaptation. However, unless there is no migration or one of the special cases discussed for panmictic populations holds, no geographical variation in the norm of reaction will be maintained at equilibrium. Implications of these results for the interpretation of spatial patterns of phenotypic variation in natural populations are discussed.     

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.     

A history of phenotypic plasticity accelerates adaptation to a new environment

Can a history of phenotypic plasticity increase the rate of adaptation to a new environment? Theory suggests it can be through two different mechanisms. Phenotypically plastic organisms can adapt rapidly to new environments through genetic assimilation, or the fluctuating environments that result in phenotypic plasticity can produce evolvable genetic architectures. In this article, I studied a model of a gene regulatory network that determined a phenotypic character in one population selected for phenotypic plasticity and a second population in a constant environment. A history of phenotypic plasticity increased the rate of adaptation in a new environment, but the amount of this increase was dependent on the strength of selection in the original environment. Phenotypic variance in the original environment predicted the adaptive capacity of the trait within, but not between, plastic and nonplastic populations. These results have implications for invasive species and ecological studies of rapid adaptation.     

The genetics of phenotypic plasticity. X. Variation versus uncertainty

Despite the apparent advantages of adaptive plasticity, it is not common. We examined the effects of variation and uncertainty on selection for plasticity using an individual-based computer simulation model. In the model, the environment consisted of a linear gradient of 50 demes with dispersal occurring either before or after selection. Individuals consisted of multiple loci whose phenotypic expression either are affected (plastic) or are not affected (nonplastic) by the environment. Typically, evolution occurred first as genetic differentiation, which was then replaced by the evolution of adaptive plasticity, opposite to the evolutionary trend that is often assumed. Increasing dispersal rates selected for plasticity, if selection occurred before dispersal. If selection occurred after dispersal, the highest plasticity was at intermediate dispersal rates. Temporal variation in the environment occurring after development, but before selection, favored the evolution of plasticity. With dispersal before selection, such temporal variation resulted in hyperplasticity, with a reaction norm much steeper than the optimum. This effect was enhanced with negative temporal autocorrelation and can be interpreted as representing a form of bet hedging. As the number of nonplastic loci increased, plasticity was disfavored due to an increase in the uncertainty of the genomic environment. This effect was reversed with temporal variation. Thus, variation and uncertainty affect whether or not plasticity is favored with different sources of variation-arising from the amount and timing of dispersal, from temporal variation, and even from the genetic architecture underlying the phenotype-having contrasting, interacting, and at times unexpected effects.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.     

Phenotypic plasticity and population viability: the importance of environmental predictability

Phenotypic plasticity plays a key role in modulating how environmental variation influences population dynamics, but we have only rudimentary understanding of how plasticity interacts with the magnitude and predictability of environmental variation to affect population dynamics and persistence. We developed a stochastic individual-based model, in which phenotypes could respond to a temporally fluctuating environmental cue and fitness depended on the match between the phenotype and a randomly fluctuating trait optimum, to assess the absolute fitness and population dynamic consequences of plasticity under different levels of environmental stochasticity and cue reliability. When cue and optimum were tightly correlated, plasticity buffered absolute fitness from environmental variability, and population size remained high and relatively invariant. In contrast, when this correlation weakened and environmental variability was high, strong plasticity reduced population size, and populations with excessively strong plasticity had substantially greater extinction probability. Given that environments might become more variable and unpredictable in the future owing to anthropogenic influences, reaction norms that evolved under historic selective regimes could imperil populations in novel or changing environmental contexts. We suggest that demographic models (e.g. population viability analyses) would benefit from a more explicit consideration of how phenotypic plasticity influences population responses to environmental change.     

Environmental and genetic cues in the evolution of phenotypic polymorphism

Phenotypic polymorphism is a consequence of developmental plasticity, in which the trajectories of developing organisms diverge under the influence of cues. Environmental and genetic phenotype determination are the two main categories of polymorphic development. Even though both may evolve as a response to varied environments, they are traditionally regarded as fundamentally distinct phenomena. They can however be joined into a single framework that emphasizes the parallel roles of environmental and genetic cues in phenotype determination. First, from the point of view of immediate causation, it is common that phenotypic variants can be induced either by environmental or by allelic variation, and this is referred to as gene-environment interchangeability. Second, from the point of view of adaptation, genetic cues in the form of allelic variation at polymorphic loci can play similar roles as environmental cues in providing information to the developmental system about coming selective conditions. Both types of cues can help a developing organism to fit its phenotype to selective circumstances. This perspective of information in environmental and genetic cues can produce testable hypotheses about phenotype determination, and can thus increase our understanding of the evolution of phenotypic polymorphism.     

Avoiding extinction under nonlinear environmental change: models of evolutionary rescue with plasticity

Rapid environmental changes are putting numerous species at risk of extinction. For migration-limited species, persistence depends on either phenotypic plasticity or evolutionary adaptation (evolutionary rescue). Current theory on evolutionary rescue typically assumes linear environmental change. Yet accelerating environmental change may pose a bigger threat. Here, we present a model of a species encountering an environment with accelerating or decelerating change, to which it can adapt through evolution or phenotypic plasticity (within-generational or transgenerational). We show that unless either form of plasticity is sufficiently strong or adaptive genetic variation is sufficiently plentiful, accelerating or decelerating environmental change increases extinction risk compared to linear environmental change for the same mean rate of environmental change.     

THE EVOLUTIONARY GENETICS OF AN ADAPTIVE MATERNAL EFFECT: EGG SIZE PLASTICITY IN A SEED BEETLE

In many organisms, a female's environment provides a reliable indicator of the environmental conditions that her progeny will encounter. In such cases, maternal effects may evolve as mechanisms for transgenerational phenotypic plasticity whereby, in response to a predictive environmental cue, a mother can change the type of eggs that she makes or can program a developmental switch in her offspring, which produces offspring prepared for the environmental conditions predicted by the cue. One potentially common mechanism by which females manipulate the phenotype of their progeny is egg size plasticity, in which females vary egg size in response to environmental cues. We describe an experiment in which we quantify genetic variation in egg size and egg size plasticity in a seed beetle, Stator limbatus, and measure the genetic constraints on the evolution of egg size plasticity, quantified as the genetic correlation between the size of eggs laid across host plants. We found that genetic variation is present within populations for the size of eggs laid on seeds of two host plants (Acacia greggii and Cercidium floridum; h² ranged between 0.217 and 0.908), and that the heritability of egg size differed between populations and hosts (higher on A. greggii than on C. floridum). We also found that the evolution of egg size plasticity (the maternal effect) is in part constrained by a high genetic correlation across host plants (r_G > 0.6). However, the cross-environment genetic correlation is less than 1.0, which indicates that the size of eggs laid on these two hosts can diverge in response to natural selection and that egg size plasticity is thus capable of evolving in response to natural selection.     

Trade‐offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases. In this study, we used a combination of statistical genetics, experimental evolution and common garden experiments to investigate the evolutionary potential for thermal adaptation in the potato late blight pathogen, Phytophthora infestans, and infer its likely response to changing temperatures. We found a trade‐off associated with thermal adaptation to heterogeneous environments in P. infestans, with the degree of the trade‐off peaking approximately at the pathogen's optimum growth temperature. A genetic trade‐off in thermal adaptation was also evidenced by the negative association between a strain's growth rate and its thermal range for growth, and warm climates selecting for a low pathogen growth rate. We also found a mirror effect of phenotypic plasticity and genetic adaptation on growth rate. At below the optimum, phenotypic plasticity enhances pathogen's growth rate but nature selects for slower growing genotypes when temperature increases. At above the optimum, phenotypic plasticity reduces pathogen's growth rate but natural selection favours for faster growing genotypes when temperature increases further. We conclude from these findings that the growth rate of P. infestans will only be marginally affected by global warming.     

Evolution of phenotypic fluctuation under host-parasite interactions

Robustness and plasticity are essential features that allow biological systems to cope with complex and variable environments. In a constant environment, robustness, i.e., insensitivity of phenotypes, is expected to increase, whereas plasticity, i.e., the changeability of phenotypes, tends to diminish. Under a variable environment, existence of plasticity will be relevant. The robustness and plasticity, on the other hand, are related to phenotypic variances. As phenotypic variances decrease with the increase in robustness to perturbations, they are expected to decrease through the evolution. However, in nature, phenotypic fluctuation is preserved to a certain degree. One possible cause for this is environmental variation, where one of the most important “environmental” factors will be inter-species interactions. As a first step toward investigating phenotypic fluctuation in response to an inter-species interaction, we present the study of a simple two-species system that comprises hosts and parasites. Hosts are expected to evolve to achieve a phenotype that optimizes fitness. Then, the robustness of the corresponding phenotype will be increased by reducing phenotypic fluctuations. Conversely, plasticity tends to evolve to avoid certain phenotypes that are attacked by parasites. By using a dynamic model of gene expression for the host, we investigate the evolution of the genotype-phenotype map and of phenotypic variances. If the host–parasite interaction is weak, the fittest phenotype of the host evolves to reduce phenotypic variances. In contrast, if there exists a sufficient degree of interaction, the phenotypic variances of hosts increase to escape parasite attacks. For the latter case, we found two strategies: if the noise in the stochastic gene expression is below a certain threshold, the phenotypic variance increases via genetic diversification, whereas above this threshold, it is increased mediated by noise-induced phenotypic fluctuation. We examine how the increase in the phenotypic variances caused by parasite interactions influences the growth rate of a single host, and observed a trade-off between the two. Our results help elucidate the roles played by noise and genetic mutations in the evolution of phenotypic fluctuation and robustness in response to host–parasite interactions.     

Phenotypic plasticity as a component of evolutionary change

Phenotypic plasticity has often been assumed to buffer the effects of natural selection and thus act as a constraint on evolutionary change. It has become increasingly clear, however, that phenotypic plasticity actually represents a fundamental component of evolutionary change. Where genetic variation for plasticity exists, a population with a different mean plasticity can evolve. Recent attention has been focused on the conditions necessary for the evolution of phenotypic plasticity, i.e. those under which a generalist strategy, as opposed to a range of genetically differentiated specialists, will be favoured. It is also now clear that genotypes that perform best in one environment usually perform less well than other genotypes in a different environment; hence, their greater response is not an adaptation to environmental variation. A response to environmental variation is only adaptive if it represents a mechanism by which relative fitness is maintained in the face of environmental variation. Adaptive plasticity may thus involve both physiological homeostasis and morphological response.     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.     

The timescale of environmental fluctuations determines the competitive advantages of phenotypic plasticity and rapid evolution

Organisms can respond to fluctuating environments by phenotypic plasticity and rapid evolution, both occurring on similar timescales to the environmental fluctuations. Because each adaptation mechanism has been independently studied, the effects of different adaptation mechanisms on ecological dynamics are not well understood. Here, using mathematical modeling, we compared the advantages of phenotypic plasticity and rapid evolution under conditions where the environment fluctuated between two states on various timescales. The results indicate that the advantages of phenotypic plasticity under environmental fluctuations on different timescales depend on the cost and the speed of plasticity. Both the speed of plastic adaptation and the cost of plasticity affect competition results, while the quantitative effects of them vary depending on the timescales. When the environment fluctuates on short timescales, the two populations with evolution and plasticity coexist, although the population with evolution is dominant. On moderate timescales, the two populations also coexist; however, the population with plasticity becomes dominant. On long timescales, whether the population with phenotypic plasticity or evolution is more advantageous depended on the cost of plasticity. Moreover, our results indicate that the mechanisms resulting in the dominance of the plastic population over the population with evolution are different depending on the timescales of environmental fluctuations. Therefore, the timescales of environmental fluctuations deserve more attention if we are to better understand the detailed competition results underlying phenotypic variation.     

Gene regulation,quantitative genetics and the evolution of reaction norms

Summary The ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.     

Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail

Temporal and spatial patterns of phenotypic variation have traditionally been thought to reflect genetic differentiation produced by natural selection. Recently, however, there has been growing interest in how natural selection may shape the genetics of phenotypic plasticity to produce patterns of geographic variation and phenotypic evolution. Because the covariance between genetic and environmental influences can modulate the expression of phenotypic variation, a complete understanding of geographic variation requires determining whether these influences covary in the same (cogradient variation) or in opposing (countergradient variation) directions. We focus on marine snails from rocky intertidal shores as an ideal system to explore how genetic and plastic influences contribute to geographic and historical patterns of phenotypic variation. Phenotypic plasticity in response to predator cues, wave action, and water temperature appear to exert a strong influence on small and large-scale morphological variation in marine snails. In particular, plasticity in snail shell thickness: (i) may contribute to phenotypic evolution, (ii) appears to have evolved across small and large spatial scales, and (iii) may be driven by life history trade-offs tied to architectural constraints imposed by the shell. The plasticity exhibited by these snails represents an important adaptive strategy to the pronounced heterogeneity of the intertidal zone and undoubtedly has played a key role in their evolution.