The genetics of phenotypic plasticity. XI. Joint evolution of plasticity and dispersal rate

In a spatially heterogeneous environment, the rate at which individuals move among habitats affects whether selection favors phenotypic plasticity or genetic differentiation, with high dispersal rates favoring trait plasticity. Until now, in theoretical explorations of plasticity evolution, dispersal rate has been treated as a fixed, albeit probabilistic, characteristic of a population, raising the question of what happens when the propensity to disperse and trait plasticity are allowed to evolve jointly. We examined the effects of their joint evolution 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 loci whose phenotypic expression either are affected by the environment (plastic) or are not affected (nonplastic), plus a locus determining the propensity to disperse. When dispersal rate and trait plasticity evolve jointly, the system tends to dichotomous outcomes of either high trait plasticity and high dispersal, or low trait plasticity and low dispersal. The outcome strongly depended on starting conditions, with high trait plasticity and dispersal favored when the system started at high values for either trait plasticity or dispersal rate (or both). Adding a cost of plasticity tended to drive the system to genetic differentiation, although this effect also depended on initial conditions. Genetic linkage between trait plasticity loci and dispersal loci further enhanced this strong dichotomy in evolutionary outcomes. All of these effects depended on organismal life history pattern, and in particular whether selection occurred before or after dispersal. These results can explain why adaptive trait plasticity is less common than might be expected.     

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.     

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.     

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.     

DEVELOPMENTAL INSTABILITY IS GENETICALLY CORRELATED WITH PHENOTYPIC PLASTICITY,CONSTRAINING HERITABILITY,AND FITNESS

Although adaptive plasticity would seem always to be favored by selection, it occurs less often than expected. This lack of ubiquity suggests that there must be trade‐offs, costs, or limitations associated with plasticity. Yet, few costs have been found. We explore one type of limitation, a correlation between plasticity and developmental instability, and use quantitative genetic theory to show why one should expect a genetic correlation. We test that hypothesis using the Landsberg erecta × Cape Verde Islands recombinant inbred lines (RILs) of Arabidopsis thaliana. RILs were grown at four different nitrogen (N) supply levels that span the range of N availabilities previously documented in North American field populations. We found a significant multivariate relationship between the cross‐environment trait plasticity and the within‐environment, within‐RIL developmental instability across 13 traits. This genetic covariation between plasticity and developmental instability has two costs. First, theory predicts diminished fitness for highly plastic lines under stabilizing selection, because their developmental instability and variance around the optimum phenotype will be greater compared to nonplastic genotypes. Second, empirically the most plastic traits exhibited heritabilities reduced by 57% on average compared to nonplastic traits. This demonstration of potential costs in inclusive fitness and heritability provoke a rethinking of the evolutionary role of plasticity.     

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Phenotypic plasticity allows organisms to alter their phenotype in direct response to changes in the environment. Despite growing recognition of plasticity's role in ecology and evolution, few studies have probed plasticity's molecular bases—especially using natural populations. We investigated the genetic basis of phenotypic plasticity in natural populations of spadefoot toads (Spea multiplicata). Spea tadpoles normally develop into an “omnivore” morph that is favored in long‐lasting, low‐density ponds. However, if tadpoles consume freshwater shrimp or other tadpoles, they can alternatively develop (via plasticity) into a “carnivore” morph that is favored in ephemeral, high‐density ponds. By combining natural variation in pond ecology and morph production with population genetic approaches, we identified candidate loci associated with each morph (carnivores vs. omnivores) and loci associated with adaptive phenotypic plasticity (adaptive vs. maladaptive morph choice). Our candidate morph loci mapped to two genes, whereas our candidate plasticity loci mapped to 14 genes. In both cases, the identified genes tended to have functions related to their putative role in spadefoot tadpole biology. Our results thereby form the basis for future studies into the molecular mechanisms that mediate plasticity in spadefoots. More generally, these results illustrate how diverse loci might mediate adaptive plasticity.     

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.     

Genetic evolution,plasticity, and bet‐hedging as adaptive responses to temporally autocorrelated fluctuating selection: A quantitative genetic model

Adaptive responses to autocorrelated environmental fluctuations through evolution in mean reaction norm elevation and slope and an independent component of the phenotypic variance are analyzed using a quantitative genetic model. Analytic approximations expressing the mutual dependencies between all three response modes are derived and solved for the joint evolutionary outcome. Both genetic evolution in reaction norm elevation and plasticity are favored by slow temporal fluctuations, with plasticity, in the absence of microenvironmental variability, being the dominant evolutionary outcome for reasonable parameter values. For fast fluctuations, tracking of the optimal phenotype through genetic evolution and plasticity is limited. If residual fluctuations in the optimal phenotype are large and stabilizing selection is strong, selection then acts to increase the phenotypic variance (bet‐hedging adaptive). Otherwise, canalizing selection occurs. If the phenotypic variance increases with plasticity through the effect of microenvironmental variability, this shifts the joint evolutionary balance away from plasticity in favor of genetic evolution. If microenvironmental deviations experienced by each individual at the time of development and selection are correlated, however, more plasticity evolves. The adaptive significance of evolutionary fluctuations in plasticity and the phenotypic variance, transient evolution, and the validity of the analytic approximations are investigated using simulations.     

Niche construction through germination cueing: life-history responses to timing of germination in Arabidopsis thaliana

Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life-history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life-history traits, and whether germination timing influenced the expression of genetic variation for life-history traits. Adult life-history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life-history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life-history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life-history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life-history traits and the genetic variation of these traits.     

GENERALISTS,SPECIALISTS, AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN SYMPATRIC POPULATIONS OF DISTINCT SPECIES

The evolution of phenotypic plasticity is studied in a model with two reproductively isolated “species” in a coarse-grained environment, consisting of two types of habitats. A quantitative genetic model for selection was constructed, in which habitats differ in the optimal value for a focal trait, and with random dispersal among habitats. The main interest was to study the effects of different selection regimes. Three cases were investigated: (1) without any limits to plasticity; (2) without genetic variation for plasticity; and (3) with a fitness cost for phenotypically plastic reactions. In almost all cases a generalist strategy to exploit both habitats emerged. Without any limits to plasticity, optimal adaptive reactions evolved. Without any genetic variation for plasticity, a compromise strategy with an intermediate, fixed phenotype evolved, whereas in the presence of costs a plastic compromise between the demands of the habitats and the costs associated with plasticity was found. Specialization and phenotypic differentiation was only found when selection within habitats was severe and optimal phenotypes for different habitats were widely different. Under soft selection (local regulation of population numbers in each habitat) the specialists coexisted; under hard selection (global regulation of population numbers) one specialist outcompeted the other. The prevalent evolutionary outcome of compromises rather than specialization implies that costs or constraints are not necessarily detectable as local adaptation in transplantation or translocation experiments.     

Foraging environment determines the genetic architecture and evolutionary potential of trophic morphology in cichlid fishes

Phenotypic plasticity allows organisms to change their phenotype in response to shifts in the environment. While a central topic in current discussions of evolutionary potential, a comprehensive understanding of the genetic underpinnings of plasticity is lacking in systems undergoing adaptive diversification. Here, we investigate the genetic basis of phenotypic plasticity in a textbook adaptive radiation, Lake Malawi cichlid fishes. Specifically, we crossed two divergent species to generate an F₃ hybrid mapping population. At early juvenile stages, hybrid families were split and reared in alternate foraging environments that mimicked benthic/scraping or limnetic/sucking modes of feeding. These alternate treatments produced a variation in morphology that was broadly similar to the major axis of divergence among Malawi cichlids, providing support for the flexible stem theory of adaptive radiation. Next, we found that the genetic architecture of several morphological traits was highly sensitive to the environment. In particular, of 22 significant quantitative trait loci (QTL), only one was shared between the environments. In addition, we identified QTL acting across environments with alternate alleles being differentially sensitive to the environment. Thus, our data suggest that while plasticity is largely determined by loci specific to a given environment, it may also be influenced by loci operating across environments. Finally, our mapping data provide evidence for the evolution of plasticity via genetic assimilation at an important regulatory locus, ptch1. In all, our data address long‐standing discussions about the genetic basis and evolution of plasticity. They also underscore the importance of the environment in affecting developmental outcomes, genetic architectures, morphological diversity and evolutionary potential.     

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 Evolution of Plasticity and Nonplastic Spatial and Temporal Adaptations in the Presence of Imperfect Environmental Cues

A model for the evolution of plasticity is considered in which the phenotype, undergoing stabilizing selection, is modeled as a linear function of an environmental cue correlated with the phenotypic optimum, with the coefficients z(0) and z(1) evolving according to standard quantitative genetic theory. In contrast to previous theoretical models, as the rate of migration between demes or the rate of cyclic fluctuations in the optimum increases, the amount of plasticity z&d1;1 at equilibrium is shown to increase gradually, in part accounting for the effect of reduced nonplastic adaptation and reaching a maximum equal to the squared correlation between the environmental cue and the phenotypic optimum. Given that information available to the organism is limited, this bias of the expressed phenotype toward the global optimum is still optimal, however, in a certain decision-theoretic sense. When genetic variation in the plastic component of the trait is small so that spatial or temporal differentiation in plasticity is small, the effect of plasticity on nonplastic adaptation is to reduce the effects of variation in the phenotypic optimum by a factor 1-z&d1;1 only. Information acquisition costs and joint evolution of sensory systems are discussed.     

The evolution of plastic recombination

Empirical data suggest that recombination rates may change in response to stress. To study the evolution of plastic recombination, we develop a modifier model using the same theoretical framework used to study conventional (nonplastic) modifiers, thus allowing direct comparison. We examine the evolution of plastic recombination in both haploid and diploid systems. In haploids, a plastic modifier spreads by forming associations with selectively favored alleles. Relative to nonplastic effects, selection on the plastic effects of a modifier is both much stronger and less sensitive to the specifics of the selection regime (e.g., epistasis). In contrast, the evolution of plastic recombination in diploids is much more restricted. Selection on plasticity requires the ability to detect DNA damage or cis-trans effects as may occur through maternal effects on fitness.     

Riverscape genomics of a threatened fish across a hydroclimatically heterogeneous river basin

Understanding how natural selection generates and maintains adaptive genetic diversity in heterogeneous environments is key to predicting the evolutionary response of populations to rapid environmental change. Detecting selection in complex spatial environments remains challenging, especially for threatened species where the effects of strong genetic drift may overwhelm signatures of selection. We carried out a basinwide riverscape genomic analysis in the threatened southern pygmy perch (Nannoperca australis), an ecological specialist with low dispersal potential. High‐resolution environmental data and 5162 high‐quality filtered SNPs were used to clarify spatial population structure and to assess footprints of selection associated with a steep hydroclimatic gradient and with human disturbance across the naturally and anthropogenically fragmented Murray–Darling Basin (Australia). Our approach included F_ST outlier tests to define neutral loci, and a combination of spatially explicit genotype–environment association analyses to identify candidate adaptive loci while controlling for the effects of landscape structure and shared population history. We found low levels of genetic diversity and strong neutral population structure consistent with expectations based on spatial stream hierarchy and life history. In contrast, variables related to precipitation and temperature appeared as the most important environmental surrogates for putatively adaptive genetic variation at both regional and local scales. Human disturbance also influenced the variation in candidate loci for adaptation, but only at a local scale. Our study contributes to understanding of adaptive evolution along naturally and anthropogenically fragmented ecosystems. It also offers a tangible example of the potential contributions of landscape genomics for informing in situ and ex situ conservation management of biodiversity.     

Progress and prospects in mapping recent selection in the genome

One of the central goals of evolutionary biology is to understand the genetic basis of adaptive evolution. The availability of nearly complete genome sequences from a variety of organisms has facilitated the collection of data on naturally occurring genetic variation on the scale of hundreds of loci to whole genomes. Such data have changed the focus of molecular population genetics from making inferences about adaptive evolution at single loci to identifying which loci, out of hundreds to thousands, have been recent targets of natural selection. A major challenge in this effort is distinguishing the effects of selection from those of the demographic history of populations. Here we review some current progress and remaining challenges in the field.     

Direct and indirect selection on flowering time,water‐use efficiency (WUE, δ13C), and WUE plasticity to drought in Arabidopsis thaliana

Flowering time and water-use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time, WUE, and WUE plasticity to drought in Arabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) Is WUE plasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions of A. thaliana grown in well-watered and season-ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment. WUE and flowering time were consistently positively genetically correlated. WUE was correlated with WUE plasticity, but the direction changed between treatments. Selection generally favored early flowering and low WUE, with drought favoring earlier flowering significantly more than well-watered conditions. Selection for lower WUE was marginally stronger under drought. There were no net fitness costs of WUE plasticity. WUE plasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation between WUE and flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions of A. thaliana. WUE plasticity may be favored over completely fixed development in environments with periodic drought.     

Selection and sex‐biased dispersal in a coastal shark: the influence of philopatry on adaptive variation

Sex‐biased dispersal is expected to homogenize nuclear genetic variation relative to variation in genetic material inherited through the philopatric sex. When site fidelity occurs across a heterogeneous environment, local selective regimes may alter this pattern. We assessed spatial patterns of variation in nuclear‐encoded, single nucleotide polymorphisms (SNPs) and sequences of the mitochondrial control region in bonnethead sharks (Sphyrna tiburo), a species thought to exhibit female philopatry, collected from summer habitats used for gestation. Geographic patterns of mtDNA haplotypes and putatively neutral SNPs confirmed female philopatry and male‐mediated gene flow along the northeastern coast of the Gulf of Mexico. A total of 30 outlier SNP loci were identified; alleles at over half of these loci exhibited signatures of latitude‐associated selection. Our results indicate that in species with sex‐biased dispersal, philopatry can facilitate sorting of locally adaptive variation, with the dispersing sex facilitating movement of potentially adaptive variation among locations and environments.     

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.