The evolutionary ecology of individual phenotypic plasticity in wild populations

The ability of individual organisms to alter morphological and life-history traits in response to the conditions they experience is an example of phenotypic plasticity which is fundamental to any population's ability to deal with short-term environmental change. We currently know little about the prevalence, and evolutionary and ecological causes and consequences of variation in life history plasticity in the wild. Here we outline an analytical framework, utilizing the reaction norm concept and random regression statistical models, to assess the between-individual variation in life history plasticity that may underlie population level responses to the environment at both phenotypic and genetic levels. We discuss applications of this framework to date in wild vertebrate populations, and illustrate how natural selection and ecological constraint may alter a population's response to the environment through their effects at the individual level. Finally, we present future directions and challenges for research into individual plasticity.     

Rethinking phenotypic plasticity and its consequences for individuals,populations and species

Much research has been devoted to identify the conditions under which selection favours flexible individuals or genotypes that are able to modify their growth, development and behaviour in response to environmental cues, to unravel the mechanisms of plasticity and to explore its influence on patterns of diversity among individuals, populations and species. The consequences of developmental plasticity and phenotypic flexibility for the performance and ecological success of populations and species have attracted a comparatively limited but currently growing interest. Here, I re-emphasize that an increased understanding of the roles of plasticity in these contexts requires a ‘whole organism'' (rather than ‘single trait'') approach, taking into consideration that organisms are integrated complex phenotypes. I further argue that plasticity and genetic polymorphism should be analysed and discussed within a common framework. I summarize predictions from theory on how phenotypic variation stemming from developmental plasticity and phenotypic flexibility may affect different aspects of population-level performance. I argue that it is important to distinguish between effects associated with greater interindividual phenotypic variation resulting from plasticity, and effects mediated by variation among individuals in the capacity to express plasticity and flexibility as such. Finally, I claim that rigorous testing of predictions requires methods that allow for quantifying and comparing whole organism plasticity, as well as the ability to experimentally manipulate the level of and capacity for developmental plasticity and phenotypic flexibility independent of genetic variation.     

Comparing the consequences of natural selection,adaptive phenotypic plasticity,and matching habitat choice for phenotype–environment matching,population genetic structure,and reproductive isolation in meta‐populations

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.     

Epigenetics in natural animal populations

Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally‐mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.     

Adaptive maternal behavioral plasticity and developmental programming mitigate the transgenerational effects of temperature in dung beetles

Phenotypic plasticity allows organisms to cope with rapid environmental change. Yet exactly when during ontogeny plastic responses are elicited, whether plastic responses produced in one generation influence phenotypic variation and fitness in subsequent generations, and the role of plasticity in shaping population divergences, remains overall poorly understood. Here, we use the dung beetle Onthophagus taurus to assess plastic responses to temperature at several life stages bridging three generations and compare these responses across three recently diverged populations. We find that beetles reared at hotter temperatures grow less than those reared at mild temperatures, and that this attenuated growth has transgenerational consequences by reducing offspring size and survival in subsequent generations. However, we also find evidence that plasticity may mitigate these consequences in two ways: 1) mothers modify the temperature of their offspring's developmental environment via behavioral plasticity and 2) in one population, offspring exhibit accelerated growth when exposed to hot temperatures during very early development (‘developmental programming’). Lastly, our study reveals that offspring responses to temperature diverged among populations in fewer than 100 generations, possibly in response to range‐specific changes in climatic or social conditions.     

Naturally occurring variation in tadpole morphology and performance linked to predator regime

Divergent natural selection drives a considerable amount of the phenotypic and genetic variation observed in natural populations. For example, variation in the predator community can generate conflicting selection on behavioral, life‐history, morphological, and performance traits. Differences in predator regime can subsequently increase phenotypic and genetic variations in the population and result in the evolution of reproductive barriers (ecological speciation) or phenotypic plasticity. We evaluated morphology and swimming performance in field collected Bronze Frog larvae (Lithobates clamitans) in ponds dominated by predatory fish and those dominated by invertebrate predators. Based on previous experimental findings, we hypothesized that tadpoles from fish‐dominated ponds would have small bodies, long tails, and large tail muscles and that these features would facilitate fast‐start speed. We also expected to see increased tail fin depth (i.e., the tail‐lure morphology) in tadpoles from invertebrate‐dominated ponds. Our results support our expectations with respect to morphology in affecting swimming performance of tadpoles in fish‐dominated ponds. Furthermore, it is likely that divergent natural selection is playing a role in the diversification on morphology and locomotor performance in this system.     

Epigenetic correlates of plant phenotypic plasticity: DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees

Phenotypic plasticity is central to the persistence of populations and a key element in the evolution of species and ecological interactions, but its mechanistic basis is poorly understood. This article examines the hypothesis that epigenetic variation caused by changes in DNA methylation are related to phenotypic plasticity in a heterophyllous tree producing two contrasting leaf types. The relationship between mammalian browsing and the production of prickly leaves was studied in a population of Ilex aquifolium (Aquifoliaceae). DNA methylation profiles of contiguous prickly and nonprickly leaves on heterophyllous branchlets were compared using a methylation‐sensitive amplified polymorphism (MSAP) method. Browsing and the production of prickly leaves were correlated across trees. Within heterophyllous branchlets, pairs of contiguous prickly and nonprickly leaves differed in genome‐wide DNA methylation. The mean per‐marker probability of methylation declined significantly from nonprickly to prickly leaves. Methylation differences between leaf types did not occur randomly across the genome, but affected predominantly certain specific markers. The results of this study, although correlative in nature, support the emerging three‐way link between herbivory, phenotypic plasticity and epigenetic changes in plants, and also contribute to the crystallization of the consensus that epigenetic variation can complement genetic variation as a source of phenotypic variation in natural plant populations. © 2012 The Linnean Society of London     

Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis>

Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes’ responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant populations.     

Developmental thermal plasticity among Drosophila melanogaster populations

Many biotic and abiotic variables influence the dispersal and distribution of organisms. Temperature has a major role in determining these patterns because it changes daily, seasonally and spatially, and these fluctuations have a significant impact on an organism's behaviour and fitness. Most ecologically relevant phenotypes that are adaptive are also complex and thus they are influenced by many underlying loci that interact with the environment. In this study, we quantified the degree of thermal phenotypic plasticity within and among populations by measuring chill‐coma recovery times of lines reared from egg to adult at two different environmental temperatures. We used sixty genotypes from six natural populations of Drosophila melanogaster sampled along a latitudinal gradient in South America. We found significant variation in thermal plasticity both within and among populations. All populations exhibit a cold acclimation response, with flies reared at lower temperatures having increased resistance to cold. We tested a series of environmental parameters against the variation in population mean thermal plasticity and discovered the mean thermal plasticity was significantly correlated with altitude of origin of the population. Pairing our data with previous experiments on viability fitness assays in the same populations in fixed and variable environments suggests an adaptive role of this thermal plasticity in variable laboratory environments. Altogether, these data demonstrate abundant variation in adaptive thermal plasticity within and among populations.     

The biology hidden inside residual within‐individual phenotypic variation

Phenotypes vary hierarchically among taxa and populations, among genotypes within populations, among individuals within genotypes, and also within individuals for repeatedly expressed, labile phenotypic traits. This hierarchy produces some fundamental challenges to clearly defining biological phenomena and constructing a consistent explanatory framework. We use a heuristic statistical model to explore two consequences of this hierarchy. First, although the variation existing among individuals within populations has long been of interest to evolutionary biologists, within‐individual variation has been much less emphasized. Within‐individual variance occurs when labile phenotypes (behaviour, physiology, and sometimes morphology) exhibit phenotypic plasticity or deviate from a norm‐of‐reaction within the same individual. A statistical partitioning of phenotypic variance leads us to explore an array of ideas about residual within‐individual variation. We use this approach to draw attention to additional processes that may influence within‐individual phenotypic variance, including interactions among environmental factors, ecological effects on the fitness consequences of plasticity, and various types of adaptive variance. Second, our framework for investigating variation in phenotypic variance reveals that interactions between levels of the hierarchy form the preconditions for the evolution of all types of plasticity, and we extend this idea to the residual level within individuals, where both adaptive plasticity in residuals and canalization‐like processes (stability) can evolve. With the statistical tools now available to examine heterogeneous residual variance, an array of novel questions linking phenotype to environment can be usefully addressed.     

Phenotypic Integration and the Plasticity of Integration in an Amphicarpic Annual

In annual plants, including amphicarpic annuals, variation in light availability can evoke phenotypic plasticity in multiple traits. We examined plasticity to light availability of vegetative and reproductive performance traits in Amphicarpaea bracteata (Fabaceae) by developing and evaluating three path-analysis models using data from a greenhouse study. To assess whether light availability altered the phenotypic integration of these performance traits, we examined the models' fit to data collected within a high- or a low-light treatment. We also examined whether a single model or alternate models were required to fit data from the two contrasting light treatments. Using our path-analysis approach, we also made comparisons among three population types: shade- and sun-native populations of the widespread variety A. bracteata var. bracteata and sun-native populations of the variety A. bracteata var. comosa. Although each type of population was somewhat distinctive in patterns of integration and in the plasticity of integration, patterns did not correspond to contrasting ecological affinity, i.e., shade- and sun-native population types or to genetic relatedness of the two varieties. Counter to the prediction that selection regimes involving variation in one or more environmental factor favor intermediate levels of integration, phenotypic integration in A. bracteata was very flexible, with plasticity occurring in a trait-by-trait manner. In particular, there was an inverse relationship between aerial and subterranean reproductive modes in low but not high light. Previous studies of amphicarpic annuals have not observed this type of environment-specific life history trade-off.     

Population size and identity influence the reaction norm of the rare,endemic plant Cochlearia bavarica across a gradient of environmental stress

Habitat degradation and loss can result in population decline and genetic erosion, limiting the ability of organisms to cope with environmental change, whether this is through evolutionary genetic response (requiring genetic variation) or through phenotypic plasticity (i.e., the ability of a given genotype to express a variable phenotype across environments). Here we address the question whether plants from small populations are less plastic or more susceptible to environmental stress than plants from large populations. We collected seed families from small (<100) versus large natural populations (>1,000 flowering plants) of the rare, endemic plant Cochlearia bavarica (Brassicaceae). We exposed the seedlings to a range of environments, created by manipulating water supply and light intensity in a 2 x 2 factorial design in the greenhouse. We monitored plant growth and survival for 300 days. Significant effects of offspring environment on offspring characters demonstrated that there is phenotypic plasticity in the responses to environmental stress in this species. Significant effects of population size group, but mainly of population identity within the population size groups, and of maternal plant identity within populations indicated variation due to genetic (plus potentially maternal) variation for offspring traits. The environment x maternal plant identity interaction was rarely significant, providing little evidence for genetically- (plus potentially maternally-) based variation in plasticity within populations. However, significant environment x population-size-group and environment x population-identity interactions suggested that populations differed in the amount of plasticity, the mean amount being smaller in small populations than in large populations. Whereas on day 210 the differences between small and large populations were largest in the environment in which plants grew biggest (i.e., under benign conditions), on day 270 the difference was largest in stressful environments. These results show that population size and population identity can affect growth and survival differently across environmental stress gradients. Moreover, these effects can themselves be modified by time-dependent variation in the interaction between plants and their environment.     

Neutral markers, ecologically relevant traits, and the structure of genetic variation in Daphnia

Zooplankton, Daphnia in particular, are increasingly used as model organisms to investigate general evolutionary biological questions. I here discuss some recent insights into the patterns and processes determining genetic diversity within and genetic differentiation among natural populations of cyclically parthenogenetic Daphnia. I focus on three aspects: (1) the interplay of phenotypic plasticity and genetic polymorphism in explaining variability in ecologically relevant traits, (2) the patterns of genetic variation revealed by neutral markers and ecologically relevant traits, and (3) the evolutionary ecological importance of hybridization events in Daphnia. The need for studies on the evolutionary ecology of sexual reproduction and dispersal via ephippial eggs in Daphnia is stressed.     

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.     

Linking genes to communities and ecosystems: Daphnia as an ecogenomic model

How do genetic variation and evolutionary change in critical species affect the composition and functioning of populations, communities and ecosystems? Illuminating the links in the causal chain from genes up to ecosystems is a particularly exciting prospect now that the feedbacks between ecological and evolutionary changes are known to be bidirectional. Yet to fully explore phenomena that span multiple levels of the biological hierarchy requires model organisms and systems that feature a comprehensive triad of strong ecological interactions in nature, experimental tractability in diverse contexts and accessibility to modern genomic tools. The water flea Daphnia satisfies these criteria, and genomic approaches capitalizing on the pivotal role Daphnia plays in the functioning of pelagic freshwater food webs will enable investigations of eco-evolutionary dynamics in unprecedented detail. Because its ecology is profoundly influenced by both genetic polymorphism and phenotypic plasticity, Daphnia represents a model system with tremendous potential for developing a mechanistic understanding of the relationship between traits at the genetic, organismal and population levels, and consequences for community and ecosystem dynamics. Here, we highlight the combination of traits and ecological interactions that make Daphnia a definitive model system, focusing on the additional power and capabilities enabled by recent molecular and genomic advances.     

Reaction norms of Arabidopsis (Brassicaceae). III. Response to nutrients in 26 populations from a worldwide collection

The study of phenotypic plasticity, the ability of a given genotype to express different phenotypes as environments change, is becoming a central focus of ecological genetics and evolutionary theory. To help address the most pressing questions about plasticity (its genetic control, ecological relevance, and macroevolutionary consequences) we advocate the use of Arabidopsis thaliana (and eventually other related species of the same genus) as a model system. In this study we present experimental data concerning: (a) the extent of reaction norm variation to two levels of nutrients in a worldwide collection of 26 A. thaliana populations; and (b) the existence of multivariate associations among key phenotypic characters, and their reaction to changes in the environment. We found significant among-population genetic variation for eight of the nine traits measured, as well as plasticity in four traits. Five traits showed significant differences in genetic variation between the two environments. The multivariate association of the nine traits defines four major groups of covarying characters, each of which may be plastic or not, depending on the particular population. The use of populations that can be easily obtained by any researcher, because they are part of a worldwide collection, implies that it will be easy to build on our results during future investigations of phenotypic plasticity in this species.     

Geographic variation in animal colour polymorphisms and its role in speciation

Polymorphic species, in which multiple variants coexist within a population, are often used as model systems in evolutionary biology. Recent research has been dominated by the hypothesis that polymorphism can be a precursor to speciation. To date, the majority of research regarding polymorphism and speciation has focused on whether polymorphism is maintained within a population or whether morphs within populations may diverge to form separate species (sympatric speciation); however, the geographical context of speciation in polymorphic systems is likely to be both diverse and complex. In this review, we draw attention to the geographic variation in morph composition and frequencies that characterises many, if not most polymorphic species. Recent theoretical and empirical developments suggest that such variation in the number, type and frequency of morphs present among populations can increase the probability of speciation. Thus, the geographical context of a polymorphism requires a greater research focus. Here, we review the prevalence, causes and evolutionary consequences of geographic variation in polymorphism in colour‐polymorphic animal species. The prevalence and nature of geographic variation in polymorphism suggests that polymorphism may be a precursor to and facilitate speciation more commonly than appreciated previously. We argue that a better understanding of the processes generating geographic variation in polymorphism is vital to understanding how polymorphism can promote speciation.     

Comparing indigenous and introduced populations of Melaleuca quinquenervia (Cav.) Blake: response of seedlings to water and pH levels

Melaleuca quinquenervia is a wetland tree species indigenous to eastern Australia. It was separately introduced to east and west Florida as an ornamental, but has since become invasive, dominating several habitat types. We tested the predictions that (1) Australian populations would exhibit more genetic variation than Florida populations, due to founder effect, and (2) high phenotypic plasticity would be found in all populations, due to the wide range of habitats occupied. We compared the phenotypic plasticity and familial variation among three Australian populations, two east Florida, and two west Florida populations in a greenhouse experiment. We grew seedlings collected from different maternal trees in each population under two water levels and three pH levels, reflecting the natural range of water levels and soil pH in Florida and Australian Melaleuca stands. We measured leaf size and shape, growth rate and above-ground biomass of seedlings and determined the components of phenotypic variance (familial, environmental, and their interaction) using univariate and multivariate analysis of variance. All traits showed significant among-population and among-family variation, as well as significant phenotypic plasticity, in response to both water level and pH level changes. Sensitivity to pH was particularly high, presumably because plants were grown under pHs ranging from 4.7 to 7.4, and because pH can influence nutrient availability. Familial variation contains genetic variation, but it may also be confounded with maternal environmental effects. Comparing Australian to Floridian Melaleuca, amounts of familial variation and phenotypic plasticity varied by trait. Overall, Australian Melaleuca had more among-population variation than Floridian Melaleuca, presumably reflecting the wider latitudinal range and longer time for evolutionary change in Australia, but had similar amounts of among-family variation, within any one population. If maternal effects are strong, among-population differences may merely reflect greater environmental differences among Australian sites than Florida sites. Australian Melaleuca had less phenotypic plasticity, possibly due to founder effects in Florida or to subsequent adaptive evolution of phenotypic plasticity in Floridian populations. Floridian Melaleuca shows little loss of familial variation, compared to indigenous Australian populations, and that, in combination with its high phenotypic plasticity, should allow it to continue to colonize new areas successfully.     

Phenotypic plasticity in insects: the effects of substrate color on the coloration of two ground-hopper species

SUMMARY The question of how phenotypic variation is maintained within populations has long been a central issue in evolutionary biology. Most of these studies focused on the maintenance of genetic variability, but the phenotype of organisms may also be influenced by environmental cues experienced during ontogeny. Color polymorphism has received particular attention in evolutionary studies as it has strong fitness consequences. However, if body coloration is influenced by the environment, any conclusions on evolutionary consequences of fitness trade-offs can be misleading. Here we present data from a laboratory experiment on the influence of substrate color on three aspects of the coloration of two ground-hopper species, Tetrix subulata and Tetrix ceperoi . We reared hatchlings either on dark or on light substrates, using a split-brood design. Although the type of pronotal pattern changed mainly in response to nymphal development, the basic color was strongly influenced by the substrate color. In both species, black and dark olive color morphs were found more frequently on the dark substrate, whereas the gray color morph dominated on the light substrate. These findings have considerable implications for our understanding of color morph evolution as they show that color polymorphism may not only be maintained by natural selection acting on discrete color morphs, but also by phenotypic plasticity, which enables organisms to adjust to the environmental conditions experienced during ontogeny. This facultative morphology is opposing to the prevailing view of color morph adaptation, which assumes a purely genetic determination and co-evolution of discrete color morphs with life history traits.     

Intraspecific variation in thermal acclimation and tolerance between populations of the winter ant,Prenolepis imparis

Thermal phenotypic plasticity, otherwise known as acclimation, plays an essential role in how organisms respond to short‐term temperature changes. Plasticity buffers the impact of harmful temperature changes; therefore, understanding variation in plasticity in natural populations is crucial for understanding how species will respond to the changing climate. However, very few studies have examined patterns of phenotypic plasticity among populations, especially among ant populations. Considering that this intraspecies variation can provide insight into adaptive variation in populations, the goal of this study was to quantify the short‐term acclimation ability and thermal tolerance of several populations of the winter ant, Prenolepis imparis. We tested for correlations between thermal plasticity and thermal tolerance, elevation, and body size. We characterized the thermal environment both above and below ground for several populations distributed across different elevations within California, USA. In addition, we measured the short‐term acclimation ability and thermal tolerance of those populations. To measure thermal tolerance, we used chill‐coma recovery time (CCRT) and knockdown time as indicators of cold and heat tolerance, respectively. Short‐term phenotypic plasticity was assessed by calculating acclimation capacity using CCRT and knockdown time after exposure to both high and low temperatures. We found that several populations displayed different chill‐coma recovery times and a few displayed different heat knockdown times, and that the acclimation capacities of cold and heat tolerance differed among most populations. The high‐elevation populations displayed increased tolerance to the cold (faster CCRT) and greater plasticity. For high‐temperature tolerance, we found heat tolerance was not associated with altitude; instead, greater tolerance to the heat was correlated with increased plasticity at higher temperatures. These current findings provide insight into thermal adaptation and factors that contribute to phenotypic diversity by revealing physiological variance among populations.