Evaluating the fitness consequences of plasticity in tolerance to pesticides

In a rapidly changing world, phenotypic plasticity may be a critical mechanism allowing populations to rapidly acclimate when faced with novel anthropogenic stressors. Theory predicts that if exposure to anthropogenic stress is heterogeneous, plasticity should be maintained as it allows organisms to avoid unnecessary expression of costly traits (i.e., phenotypic costs) when stressors are absent. Conversely, if exposure to stressors becomes constant, costs or limits of plasticity may lead to evolutionary trait canalization (i.e., genetic assimilation). While these concepts are well‐established in theory, few studies have examined whether these factors explain patterns of plasticity in natural populations facing anthropogenic stress. Using wild populations of wood frogs that vary in plasticity in tolerance to pesticides, the goal of this study was to evaluate the environmental conditions under which plasticity is expected to be advantageous or detrimental. We found that when pesticides were absent, more plastic populations exhibited lower pesticide tolerance and were more fit than less plastic populations, likely avoiding the cost of expressing high tolerance when it was not necessary. Contrary to our predictions, when pesticides were present, more plastic populations were as fit as less plastic populations, showing no signs of costs or limits of plasticity. Amidst unprecedented global change, understanding the factors shaping the evolution of plasticity will become increasingly important.     

The evolution of tolerance to damage in Gentianella campestris: natural selection and the quantitative genetics of tolerance

In the framework of phenotypic plasticity, tolerance to browsing can be operationally defined as a norm of reaction comparing plant performance in undamaged and damaged conditions. Genetic variation in tolerance is then indicated by heterogeneity in the slopes of norms of reaction from a population. We investigated field gentian (Gentianella campestris) tolerance to damage in the framework of phenotypic plasticity using a sample of maternal lines from natural populations grown under common garden conditions and randomly split into either a control or an artificial clipping treatment. We found a diversity of tolerance norms of reaction at both the population and family level: the impacts of clipping ranged from poor tolerance (negative slope) to overcompensation (positive slope). We detected heterogeneity in tolerance norms of reaction in four populations. Similarly, we found a variety of plastic architectural responses to clipping and genetic variation in these responses in several populations. Overall, we found that the most tolerant populations were late flowering and also exhibit the greatest plastic increases in node (meristem) production in response to damage. We studied damage-imposed natural selection on plasticity in plant architecture in 10 of the sampled populations. In general, there was strong positive direct selection on final number of nodes for both control and clipped plants. However, the total selection on nodes (direct + indirect selection) within each treatment category depended heavily on the frequency of damage and cross-treatment genetic correlations in node production. In some cases, strong correlated responses to selection across the damage treatment led to total selection against nodes in the more rare environment. This could ultimately lead to the evolution of maladaptive phenotypes in one or both of the treatment categories. These results suggest that tolerance and a variety of architectural responses to damage may evolve by both direct and indirect responses to natural selection. While the present study demonstrates the potential importance of cross-treatment genetic correlations in directing the evolution of tolerance traits, such as branch or node production, we did not find any strong evidence of genetic trade-offs in candidate tolerance traits between undamaged and damaged conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Potential local adaptation in populations of invasive reed canary grass (Phalaris arundinacea) across an urbanization gradient

Urban stressors represent strong selective gradients that can elicit evolutionary change, especially in non‐native species that may harbor substantial within‐population variability. To test whether urban stressors drive phenotypic differentiation and influence local adaptation, we compared stress responses of populations of a ubiquitous invader, reed canary grass (Phalaris arundinacea). Specifically, we quantified responses to salt, copper, and zinc additions by reed canary grass collected from four populations spanning an urbanization gradient (natural, rural, moderate urban, and intense urban). We measured ten phenotypic traits and trait plasticities, because reed canary grass is known to be highly plastic and because plasticity may enhance invasion success. We tested the following hypotheses: (a) Source populations vary systematically in their stress response, with the intense urban population least sensitive and the natural population most sensitive, and (b) plastic responses are adaptive under stressful conditions. We found clear trait variation among populations, with the greatest divergence in traits and trait plasticities between the natural and intense urban populations. The intense urban population showed stress tolerator characteristics for resource acquisition traits including leaf dry matter content and specific root length. Trait plasticity varied among populations for over half the traits measured, highlighting that plasticity differences were as common as trait differences. Plasticity in root mass ratio and specific root length were adaptive in some contexts, suggesting that natural selection by anthropogenic stressors may have contributed to root trait differences. Reed canary grass populations in highly urbanized wetlands may therefore be evolving enhanced tolerance to urban stressors, suggesting a mechanism by which invasive species may proliferate across urban wetland systems generally.     

Gene regulation,quantitative genetics and the evolution of reaction norms

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

Old wine in new bottles: reaction norms in salmonid fishes

Genetic variability in reaction norms reflects differences in the ability of individuals, populations and ultimately species to respond to environmental change. By increasing our understanding of how genotype × environment interactions influence evolution, studies of genetic variation in phenotypic plasticity serve to refine our capacity to predict how populations will respond to natural and anthropogenic environmental variability, including climate change. Given the extraordinary variability in morphology, behaviour and life history in salmonids, one might anticipate the research milieu on reaction norms in these fishes to be empirically rich and intellectually engaging. Here, I undertake a review of genetic variability in continuous and discontinuous (threshold) norms of reaction in salmonid fishes, as determined primarily (but not exclusively) by common-garden experiments. Although in its infancy from a numerical publication perspective, there is taxonomically broad evidence of genetic differentiation in continuous, threshold and bivariate reaction norms among individuals, families and populations (including inter-population hybrids and backcrosses) for traits as divergent as embryonic development, age and size at maturity, and gene expression. There is compelling inferential evidence that plasticity is heritable and that population differences in reaction norms can reflect adaptive responses, by natural selection, to local environments. As a stimulus for future work, a series of 20 research questions are identified that focus on reaction-norm variability, selection, costs and constraints, demographic and conservation consequences, and genetic markers and correlates of phenotypic plasticity.     

The ubiquity of phenotypic plasticity in plants: a synthesis

Adaptation to heterogeneous environments can occur via phenotypic plasticity, but how often this occurs is unknown. Reciprocal transplant studies provide a rich dataset to address this issue in plant populations because they allow for a determination of the prevalence of plastic versus canalized responses. From 31 reciprocal transplant studies, we quantified the frequency of five possible evolutionary patterns: (1) canalized response–no differentiation: no plasticity, the mean phenotypes of the populations are not different; (2) canalized response–population differentiation: no plasticity, the mean phenotypes of the populations are different; (3) perfect adaptive plasticity: plastic responses with similar reaction norms between populations; (4) adaptive plasticity: plastic responses with parallel, but not congruent reaction norms between populations; and (5) nonadaptive plasticity: plastic responses with differences in the slope of the reaction norms. The analysis included 362 records: 50.8% life‐history traits, 43.6% morphological traits, and 5.5% physiological traits. Across all traits, 52% of the trait records were not plastic, and either showed no difference in means across sites (17%) or differed among sites (83%). Among the 48% of trait records that showed some sort of plasticity, 49.4% showed perfect adaptive plasticity, 19.5% adaptive plasticity, and 31% nonadaptive plasticity. These results suggest that canalized responses are more common than adaptive plasticity as an evolutionary response to environmental heterogeneity.     

Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes

We argue that phenotypic plasticity should be broadly construed to encompass a diversity of phenomena spanning several hierarchical levels of organization. Despite seemingly disparate outcomes among different groups of organisms (e.g., the opening/closing of stomata in leaves, adjustments of allocation to growth/reproduction, or the production of different castes in social insects), there are underlying shared processes that initiate these responses. At the most fundamental level, all plastic responses originate at the level of individual cells, which receive and process signals from their environment. The broad variations in physiology, morphology, behavior, etc., that can be produced by a single genotype, can be accounted for by processes regulating gene expression in response to environmental variation. Although evolution of adaptive plasticity may not be possible for some types of environmental signals, in many cases selection has molded responses to environmental variation that generate precise and repeatable patterns of gene expression. We highlight the example of responses of plants to variation in light quality and quantity, mediated via the phytochrome genes. Responses to changes in light at particular stages of plants' life cycles (e.g., seed germination, competition, reproduction) are controlled by different members of this gene family. The mechanistic details of the cell and molecular biology of phytochrome gene action (e.g., their effects on expression of other genes) is outlined. Plasticity of cells and organisms to internal and external environmental signals is pervasive, and represents not just an outcome of evolutionary processes, but also a potentially important molder of them. Phenotypes originally initiated via a plastic response, can be fixed through genetic assimilation as alternate regulatory pathways are shut off. Evolution of mechanisms of plasticity and canalization can both reduce genetic variation, as well as shield it. When the organism encounters novel environmental conditions, this shielded variation may be expressed, revealing hidden reaction norms that represent the raw material for subsequent evolution.     

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

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

Phenotypic plasticity: Eco-Devo and evolution

Phenotypic plasticity refers to the ability of an organism to alter its physiology/morphology/behavior in response to changes in environmental conditions. Although encompassing various phenomena spanning multi-ple levels of organization, most plastic responses seem to take place by altering gene expression and eventually altering ontogenetic trajectory in response to environmental variation. Epigenetic modifications provide a plausi-ble link between the environment and alterations in gene expression, and the alterations in phenotype based on environmentally induced epigenetic modifications can be inherited transgenerationally. Even closely related species and populations with different genotypes may exhibit differences in the patterns and the extents of plastic responses, indicating the wide existence of plasticity genes which are independent of trait means and directly respond to environmental stimuli by triggering phenotypic changes. The ability of plasticity is not only able to affect the adaptive evolution of species significantly, but is also an outcome of evolutionary processes. Therefore, phenotypic plasticity is a potentially important molder of adaptation and evolution.     

Constraints on the evolution of adaptive phenotypic plasticity in plants

The high potential fitness benefit of phenotypic plasticity tempts us to expect phenotypic plasticity as a frequent adaptation to environmental heterogeneity. Examples of proven adaptive plasticity in plants, however, are scarce and most plastic responses actually may be 'passive' rather than adaptive. This suggests that frequently requirements for the evolution of adaptive plasticity are not met or that such evolution is impeded by constraints. Here we outline requirements and potential constraints for the evolution of adaptive phenotypic plasticity, identify open questions, and propose new research approaches. Important open questions concern the genetic background of plasticity, genetic variation in plasticity, selection for plasticity in natural habitats, and the nature and occurrence of costs and limits of plasticity. Especially promising tools to address these questions are selection gradient analysis, meta-analysis of studies on genotype-by-environment interactions, QTL analysis, cDNA-microarray scanning and quantitative PCR to quantify gene expression, and two-dimensional gel electrophoresis to quantify protein expression. Studying plasticity along the pathway from gene expression to the phenotype and its relationship with fitness will help us to better understand why adaptive plasticity is not more universal, and to more realistically predict the evolution of plastic responses to environmental change.     

Geographic variation in plasticity in Eristalis arbustorum

To study the evolution of phenotypic plasticity in the field, six populations of the hoverfly Eristalis arbustorum were sampled along two parallel North-South transects over a maximum daily temperature gradient. Three populations were sampled per transect. Egg batches were collected and the offspring were reared in a split family set up over three different pupal temperature regimes in the laboratory to produce population reaction norms of colour pattern, pupal development time, wing length and thorax length. Wing length and colour pattern were corrected for body size. All four characters showed plasticity in response to rearing temperature and significant differences in height, slope and shape of the reaction norms were found. Only male colour pattern showed variation in reaction norms along the North-South gradient. Most other characters showed variation in reaction norms from West to East. The two populations lying in the middle of the transects were frequendy different from the others. Within the populations, significant genotype-environment interactions were frequently found for wing length and colour pattern, indicating that genetic variation for plasticity was present. The results suggest that the populations may have evolved plastic responses to suit local environmental conditions.     

On the fate of seasonally plastic traits in a rainforest butterfly under relaxed selection

Many organisms display phenotypic plasticity as adaptation to seasonal environmental fluctuations. Often, such seasonal responses entails plasticity of a whole suite of morphological and life‐history traits that together contribute to the adaptive phenotypes in the alternative environments. While phenotypic plasticity in general is a well‐studied phenomenon, little is known about the evolutionary fate of plastic responses if natural selection on plasticity is relaxed. Here, we study whether the presumed ancestral seasonal plasticity of the rainforest butterfly Bicyclus sanaos (Fabricius, 1793) is still retained despite the fact that this species inhabits an environmentally stable habitat. Being exposed to an atypical range of temperatures in the laboratory revealed hidden reaction norms for several traits, including wing pattern. In contrast, reproductive body allocation has lost the plastic response. In the savannah butterfly, B. anynana (Butler, 1879), these traits show strong developmental plasticity as an adaptation to the contrasting environments of its seasonal habitat and they are coordinated via a common developmental hormonal system. Our results for B. sanaos indicate that such integration of plastic traits – as a result of past selection on expressing a coordinated environmental response – can be broken when the optimal reaction norms for those traits diverge in a new environment.     

Evolution of environmental cues for phenotypic plasticity

Phenotypically plastic characters may respond to multiple variables in their environment, but the evolutionary consequences of this phenomenon have rarely been addressed theoretically. We model the evolution of linear reaction norms in response to several correlated environmental variables, in a population undergoing stationary environmental fluctuations. At evolutionary equilibrium, the linear combination of environmental variables that acts as a developmental cue for the plastic trait is the multivariate best linear predictor of changes in the optimum. However, the reaction norm with respect to any single environmental variable may exhibit nonintuitive patterns. Apparently maladaptive, or hyperadaptive plasticity can evolve with respect to single environmental variables, and costs of plasticity may increase, rather than reduce, plasticity in response to some variables. We also find conditions for the evolution of an indirect environmental indicator that affects expression of a plastic phenotype, despite not influencing natural selection on it.     

Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback

Phenotypic plasticity is predicted to facilitate individual survival and/or evolve in response to novel environments. Plasticity that facilitates survival should both permit colonization and act as a buffer against further evolution, with contemporary and derived forms predicted to be similarly plastic for a suite of traits. On the other hand, given the importance of plasticity in maintaining internal homeostasis, derived populations that encounter greater environmental heterogeneity should evolve greater plasticity. We tested the evolutionary significance of phenotypic plasticity in coastal British Columbian postglacial populations of threespine stickleback (Gasterosteus aculeatus) that evolved under greater seasonal extremes in temperature after invading freshwater lakes from the sea. Two ancestral (contemporary marine) and two derived (contemporary freshwater) populations of stickleback were raised near their thermal tolerance extremes, 7 and 22 °C. Gene expression plasticity was estimated for more than 14 000 genes. Over five thousand genes were similarly plastic in marine and freshwater stickleback, but freshwater populations exhibited significantly more genes with plastic expression than marine populations. Furthermore, several of the loci shown to exhibit gene expression plasticity have been previously implicated in the adaptive evolution of freshwater populations, including a gene involved in mitochondrial regulation (PPARAa). Collectively, these data provide molecular evidence that highlights the importance of plasticity in colonization and adaptation to new environments.     

植物表型可塑性研究进展

表型可塑性已成为生态进化发育生物学的核心概念,很大程度上由于植物可塑性研究的主要贡献,但人们仍远未完全了解表型可塑性的原因和结果。从整体角度理出表型可塑性研究发展的基本脉络,介绍研究内容、途径和简史,聚焦于几个主要方面的研究进展及发展方向。现代可塑性研究的兴盛始于关于可塑性的进化学重要性的一篇综述,从现象的描述、对其遗传基础和可塑性本身进化的讨论,发展到探索其背后的发育机制、植物生长与适应策略、生态学影响等。未来可塑性研究应在重新理解和评价表型可塑性及其适应性的基础上,更关注自然条件下环境因子和可塑响应的复杂性。表型可塑性的生态-进化学意义仍将是未来研究的重点。     

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.