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.     

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.     

The consequences of phenotypic plasticity for ecological speciation

We use an individual-based numerical simulation to study the effects of phenotypic plasticity on ecological speciation. We find that adaptive plasticity evolves readily in the presence of dispersal between populations from different ecological environments. This plasticity promotes the colonization of new environments but reduces genetic divergence between them. We also find that the evolution of plasticity can either enhance or degrade the potential for divergent selection to form reproductive barriers. Of particular importance here is the timing of plasticity in relation to the timing of dispersal. If plasticity is expressed after dispersal, reproductive barriers are generally weaker because plasticity allows migrants to be better suited for their new environment. If plasticity is expressed before dispersal, reproductive barriers are either unaffected or enhanced. Among the potential reproductive barriers we considered, natural selection against migrants was the most important, primarily because it was the earliest-acting barrier. Accordingly, plasticity had a much greater effect on natural selection against migrants than on sexual selection against migrants or on natural and sexual selection against hybrids. In general, phenotypic plasticity can strongly alter the process of ecological speciation and should be considered when studying the evolution of reproductive barriers.     

The genetics of phenotypic plasticity. VII. Evolution in a spatially-structured environment

Previous models of the evolution of phenotypic plasticity have, for the most part, not considered the effects of genetic architecture and spatial structure. I examine those factors with an individual-based simulation model. With regard to genetic architecture, I considered how the presence of different types of loci would affect medium-term evolutionary outcomes. The types of loci differed in how the environment determined phenotypic expression and included loci that were insensitive to the environment (non-plastic loci), sensitive in a linear fashion, and sensitive in a quadratic fashion (both plastic loci). With regard to spatial structure, I investigated the affects of migration patterns. These simulations demonstrated that two general conditions are necessary for phenotypic plasticity to be selected. (1) The environment must have a strong influence on genotypic expression. (2) The between-generation changes in the environment must be large and predictable, in the current instance because of migration in a spatially-structured (clinal) environment. Responses to selection were not simple, however. Rarely were pure strategies — genetic specialization or phenotypic plasticity — selected for. Instead, the existence of multiple types of loci led to mixed genetic outcomes. The result of this mixed outcome were individuals with reaction norms that were less steep than the optimal reaction norm (when non-plastic and linear-plastic loci were present) or individuals with curved reaction norms when the optimal reaction norms was linear (when all three types of loci were present). A pure plasticity strategy had the highest global fitness because plastic individuals would match the optimal phenotype everywhere. The reason that the metapopulation did not achieve this global fitness optimum is that local selection is stronger than global selection. Each deme is driven to a local fitness peak based on the combined, locally additive effects of the non-plastic and plastic loci. Plasticity is only selected globally, so plasticity becomes more highly favored with high migration rates. This effect was greatest in parts of the cline where the plasticity loci were not being expressed and, thus, not locally selected upon. That is, in these demes local selection was weak or absent allowing global fitness effects to predominate.     

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.     

Habitat-specific differences in thermal plasticity in natural populations of a soil arthropod

When populations experience substantial variation in environmental conditions, they may evolve phenotypic plasticity in response to these varying selection pressures. Evolutionary theory predicts differentiation in the level of phenotypic plasticity among different habitats. We evaluated temperature-induced phenotypic responses in juvenile growth rate in natural populations of the springtail Orchesella cincta , inhabiting forest and heathland. These habitats typically co-occur but differ strongly with respect to, for example, thermal regime, relative humidity, and structure. Offspring of females from the two habitats were reared at different temperatures in climate rooms and the temperature response of juvenile growth rate and egg size was measured. We found a habitat-specific difference in plasticity of juvenile growth rate. The reaction norms of the forest populations were steeper than the reaction norms for heath populations at two replicated sampling sites. Egg weight itself was demonstrated to be a plastic trait with a higher egg weight at low temperatures, but the thermal response did not differ between habitats. We conclude that these populations have diverged due to strong local natural selection. Our results support the argument that the level of phenotypic plasticity itself can be under selection and that differentiation in reaction norms can occur even in neighbouring habitats with no barrier to gene flow.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 265–271.     

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.     

植物的表型可塑性、异速生长及其入侵能力

表型可塑性是指同一个基因型对不同环境响应产生不同表型的特性,特定性状的可塑性本身可以遗传,也可以接受选择而发生进化。植物个体的异速生长是指生物体某一特征的相对生长速率不等于第二种特征的相对生长速率的特性,该特性是由物种的遗传性决定的一种固定特征,植物往往朝着最佳的异速生长曲线进化。植物特定基因型在不同环境下,诸如生物量分配和种群几何学上的一些表型差异,既可由异速生长造成,也可由表型可塑性造成。植物本身的异速生长是一种"外观可塑性",而异速生长曲线的改变才是真正的可塑性。植物的表型可塑性、异速生长对于入侵植物的适应具有重要意义。干扰等异质性生境下表型可塑性成为物种生存扩散的有利性状,表型可塑性强的物种更有可能成为广布种。植物本身的异速生长特性或其异速生长曲线的改变都能影响其入侵能力。     

Phenotypic variability can promote the evolution of adaptive plasticity by reducing the stringency of natural selection

Adaptive phenotypic plasticity is a potent but not ubiquitous solution to environmental heterogeneity, driving interest in what factors promote and limit its evolution. Here, a novel computational model representing stochastic information flow in development is used to explore evolution from a constitutive phenotype to an adaptively plastic response. Results show that populations tend to evolve robustness to developmental stochasticity, but that this evolved robustness limits evolvability; specifically, robust genotypes have less ability to evolve adaptive plasticity when presented with a mix of both the ancestral environment and a new environment. Analytic calculations and computational experiments confirm that this constraint occurs when the initial mutational steps towards plasticity are pleiotropic, such that mutant fitnesses decline in the environment to which their parents are well‐adapted. Greater phenotypic variability improves evolvability in the model by lessening this decline as well as by improving the fitness of partial adaptations to the new environment. By making initial plastic mutations more palatable to natural selection, phenotypic variability can increase the evolvability of an innovative, plastic response without improving evolvability to simpler challenges such as a shifted optimum in a single environment. Populations that evolved robustness by negative feedback between the trait and its rate of change show a particularly strong constraining effect on the evolvability of plasticity, revealing another mechanism by which evolutionary history can limit later innovation. These results document a novel mechanism by which weakening selection could actually stimulate the evolution of a major innovation.     

Scaling up phenotypic plasticity with hierarchical population models

Individuals respond to different environments by developing different phenotypes, which is generally seen as a mechanism through which individuals can buffer adverse environmental conditions and increase their fitness. To understand the consequences of phenotypic plasticity it is necessary to study how changing a particular trait of an individual affects either its survival, growth, reproduction or a combination of these demographic vital rates (i.e. fitness components). Integrating vital rate changes due to phenotypic plasticity into models of population dynamics allows detailed study of how phenotypic changes scale up to higher levels of integration and forms an excellent tool to distinguish those plastic trait changes that really matter at the population level. A modeling approach also facilitates studying systems that are even more complex: traits and vital rates often co-vary or trade-off with other traits that may show plastic responses over environmental gradients. Here we review recent developments in the literature on population models that attempt to include phenotypic plasticity with a range of evolutionary assumptions and modeling techniques. We present in detail a model framework in which environmental impacts on population dynamics can be followed analytically through direct and indirect pathways that importantly incorporate phenotypic plasticity, trait-trait and trait-vital rate relationships. We illustrate this framework with two case studies: the population-level consequences of phenotypic responses to nutrient enrichment of plant species occurring in nutrient-poor habitats and of responses to changes in flooding regimes due to climate change. We conclude with exciting prospects for further development of this framework: selection analyses, modeling advances and the inclusion of spatial dynamics by considering dispersal traits as well.     

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.     

Assortative mating can limit the evolution of phenotypic plasticity

Phenotypic plasticity, the ability to adjust phenotype to the exposed environment, is often advantageous for organisms living in heterogeneous environments. Although the degree of plasticity appears limited in nature, many studies have reported low costs of plasticity in various species. Existing studies argue for ecological, genetic, or physiological costs or selection eliminating plasticity with high costs, but have not considered costs arising from sexual selection. Here, we show that sexual selection caused by mate choice can impede the evolution of phenotypic plasticity in a trait used for mate choice. Plasticity can remain low to moderate even in the absence of physiological or genetic costs, when individuals phenotypically adapted to contrasting environments through plasticity can mate with each other and choose mates based on phenotypic similarity. Because the non-choosy sex (i.e., males) with lower degrees of plasticity are more favored in matings by the choosy sex (i.e., females) adapted to different environments, directional selection toward higher degrees of plasticity is constrained by sexual selection. This occurs at intermediate strengths of female choosiness in the range of the parameter value we examined. Our results demonstrate that mate choice is a potential source of an indirect cost to phenotypic plasticity in a sexually selected plastic trait.     

Differentiation in phenotypic plasticity among populations of Arabis serrata Fr. & Sav. (Brassicaceae)

Studies on divergence of phenotypic plasticity in closely related species have suggested that character means and plasticity of these characters may evolve independently. Similar patterns of divergence between populations within a species have been reported although few plant species have been studied. Thus, in this paper, the patterns of differentiation between character means and phenotypic plasticity among eight populations of Arabis serrata are documented. Mean response and magnitude and pattern of phenotypic plasticity were measured and compared in plants growing under an environmental gradient of nutrients. Differences in means and coefficients of variation (CV as indicators of plasticity) among populations were compared using the Canberra metric and generating unrooted Wagner trees. Populations showed significant differences in character means in nine morphological traits. Magnitude and patterns of phenotypic plasticity showed a complex pattern of differentiation for each trait and population. Biomass traits were more plastic, in general, than characters associated with linear size. Comparisons between pairs of populations for nine morphological traits showed that in 28.6% of 252 possible cases, populations differed in means, magnitude and patterns of phenotypic plasticity. In almost 90% of the cases, populations differed in magnitude and/or pattern of plasticity. Considering all characters together, populations from similar habitats and with common life history features tended to respond in similar ways. The patterns of divergence, however, suggest that character means and character plasticities among populations are able to evolve independently.     

Maintenance of genetic variation in phenotypic plasticity: the role of environmental variation

We study genetic variation in phenotypic plasticity maintained by a balance between mutation and weak stabilizing selection. We consider linear reaction norms allowing for spatial and/or temporal variation in the environments of development and selection. We show that the overall genetic variation maintained does not depend on whether the trait is plastic or not. The genetic variances in height and slope of a linear reaction norm, and their covariance, are predicted to decrease with the variation in the environment. Non-pleiotropic loci influencing either height or slope are expected to decrease the genetic variance in slope relative to that in height. Decrease in the ratio of genetic variance in slope to genetic variance in height with increasing variation in the environment presents a test for the presence of loci that only influence the slope, and not the height. We use data on Drosophila to test the theory. In seven of eight pair-wise comparisons genetic variation in reaction norm is higher in a less variable environment than in a more variable environment, which is in accord with the model's predictions.     

The genetics of phenotypic plasticity. XII. Temporal and spatial heterogeneity

To understand empirical patterns of phenotypic plasticity, we need to explore the complexities of environmental heterogeneity and how it interacts with cue reliability. I consider both temporal and spatial variation separately and in combination, the timing of temporal variation relative to development, the timing of movement relative to selection, and two different patterns of movement: stepping‐stone and island. Among‐generation temporal heterogeneity favors plasticity, while within‐generation heterogeneity can result in cue unreliability. In general, spatial variation more strongly favors plasticity than temporal variation, and island migration more strongly favors plasticity than stepping‐stone migration. Negative correlations among environments between the time of development and selection can result in seemingly maladaptive reaction norms. The effects of higher dispersal rates depend on the life history stage when dispersal occurs and the pattern of environmental heterogeneity. Thus, patterns of environmental heterogeneity can be complex and can interact in unforeseen ways to affect cue reliability. Proper interpretation of patterns of trait plasticity requires consideration of the ecology and biology of the organism. More information on actual cue reliability and the ecological and developmental context of trait plasticity is needed.     

Maternal effects on phenotypic plasticity in larvae of the salamander <Emphasis Type="Italic">Hynobius retardatus</Emphasis>

Maternal effects are widespread and influence a variety of traits, for example, life history strategies, mate choice, and capacity to avoid predation. Therefore, maternal effects may also influence phenotypic plasticity of offspring, but few studies have addressed the relationship between maternal effects and phenotypic plasticity of offspring. We examined the relationship between a maternally influenced trait (egg size) and the phenotypic plasticity of the induction rate of the broad-headed morph in the salamander Hynobius retardatus. The relationship between egg size and the induction of the broad-headed morph was tested across experimental crowding conditions (densities of low conspecifics, high conspecifics, and high heterospecific anuran), using eggs and larvae from eight natural populations with different larval densities of conspecifics and heterospecifics. The broad-headed morph has a large mouth that enables it to consume either conspecifics or heterospecifics, and this ability gives survival advantages over the normal morph. We have determined that there is phenotypic plasticity in development, as shown by an increase in the frequency of broad-headed morph in response to an increase in the density of conspecifics and heterospecifics. This reaction norm differed between populations. We also determined that the frequency of the broad-headed morph is affected by egg size in which larger egg size resulted in expression of the broad-headed morph. Furthermore, we determined that selection acting on the propensity to develop the broad-headed morph has produced a change in egg size. Lastly, we found that an increase in egg size alters the reaction norm to favor development of the broad-headed morph. For example, an equal change in experimental density produces a greater change in the frequency of the broad-headed morph in larvae developing from large eggs than it does in larvae developing from small eggs. Population differences in plasticity might be the results of differences in egg size between populations, which is caused by the adaptive integration of the plasticity and egg size. Phenotypic plasticity can not evolve independently of maternal effects.     

Role of phenotypic plasticity and population differentiation in adaptation to novel environmental conditions

Species can adapt to new environmental conditions either through individual phenotypic plasticity, intraspecific genetic differentiation in adaptive traits, or both. Wild emmer wheat, Triticum dicoccoides, an annual grass with major distribution in Eastern Mediterranean region, is predicted to experience in the near future, as a result of global climate change, conditions more arid than in any part of the current species distribution. To understand the role of the above two means of adaptation, and the effect of population range position, we analyzed reaction norms, extent of plasticity, and phenotypic selection across two experimental environments of high and low water availability in two core and two peripheral populations of this species. We studied 12 quantitative traits, but focused primarily on the onset of reproduction and maternal investment, which are traits that are closely related to fitness and presumably involved in local adaptation in the studied species. We hypothesized that the population showing superior performance under novel environmental conditions will either be genetically differentiated in quantitative traits or exhibit higher phenotypic plasticity than the less successful populations. We found the core population K to be the most plastic in all three trait categories (phenology, reproductive traits, and fitness) and most successful among populations studied, in both experimental environments; at the same time, the core K population was clearly genetically differentiated from the two edge populations. Our results suggest that (1) two means of successful adaptation to new environmental conditions, phenotypic plasticity and adaptive genetic differentiation, are not mutually exclusive ways of achieving high adaptive ability; and (2) colonists from some core populations can be more successful in establishing beyond the current species range than colonists from the range extreme periphery with conditions seemingly closest to those in the new environment.     

Selection experiments and the study of phenotypic plasticity1

Abstract Laboratory selection experiments are powerful tools for establishing evolutionary potentials. Such experiments provide two types of information, knowledge about genetic architecture and insight into evolutionary dynamics. They can be roughly classified into two types: (1) artificial selection in which the experimenter selects on a focal trait or trait index, and (2) quasi‐natural selection in which the experimenter establishes a set of environmental conditions and then allows the population to evolve. Both approaches have been used in the study of phenotypic plasticity. Artificial selection experiments have taken various forms including: selection directly on a reaction norm, selection on a trait in multiple environments, and selection on a trait in a single environment. In the latter experiments, evolution of phenotypic plasticity is investigated as a correlated response. Quasi‐natural selection experiments have examined the effects of both spatial and temporal variation. I describe how to carry out such experiments, summarize past efforts, and suggest further avenues of research.     

Nonrandom larval dispersal can steepen marine clines

Sharp and stable clinal variation is enigmatic when found in species with high gene flow. Classical population genetic models treat gene flow as a random homogenizing force countering local adaptation across habitat discontinuities. Under this view, dispersal over large spatial scales will lower the effectiveness of adaptation by natural selection at finer spatial scales. Thus, random gene flow will create a shallow phenotypic cline across an ecotone in response to a steep selection gradient. In sedentary marine species that disperse primarily as larvae, nonrandom dispersal patterns are expected due to coastal hydrodynamics. Surprisingly sharp phenotypic and genotypic clines have been documented in marine species with high gene flow. We are interested in the extent to which nonrandom dispersal could accentuate such clines. We model a linear species range in which populations have stable and uniform densities along a selection gradient; in contrast to random dispersal, convergent advection of larvae can amplify phenotypic differentiation if coupled with a semipermeable dispersal barrier in the convergence zone. The migration load caused by directional dispersal pushes the phenotypic mean away from the local trait optimum in downstream populations, that is, near the convergence zone. A dispersal barrier is possible as a result of colliding currents if the water and larvae are mostly displaced offshore, away from suitable settlement habitat. Disjunctions in a quantitative trait were enlarged in the convergence zone by faster current flows or a more complete dispersal barrier. With advection of larvae per generation one-third as far as the average dispersal distance by diffusion, convergence on a dispersal barrier with 40% permeability generated a trait disjunction across the convergence zone of two phenotypic standard deviations. Without directional dispersal, similar clines also developed across a habitat gap, where population density was low, or across dispersal barriers with less than 1% permeability. These findings suggest that the types of hydrographic phenomena often associated with marine transition zones can strongly affect the balance between gene flow and selection and generate surprisingly steep clines given the large-scale gene flow expected from larvae.