ADAPTATION TO FINE-GRAINED ENVIRONMENTAL VARIATION: AN ANALYSIS OF WITHIN-INDIVIDUAL LEAF VARIATION IN AN ANNUAL PLANT

Recent studies of evolution in heterogeneous environments have concentrated on the role of coarse-grained environmental variation. Here I explore the potential for a modular organism to adapt to fine-grained environmental variation through within-individual variation among modules. I describe the pattern of variation among leaves of single individuals and report results of initial analyses of genetic variation for within-individual variability in leaf traits and of genetic correlations that could influence the rate of further evolution of within-individual variation of these traits. Plants from 24 paternal half-sib families were raised in growth chambers, and five traits were measured for two leaves produced by each plant. Four of the five traits differed significantly between sampling times. Genetic analyses revealed significant additive genetic variation for within-individual variation in several traits. Estimates of family mean correlations between traits expressed at different times suggest few relationships that would be expected to impede response to selection for changes in the pattern of within-individual variation in leaf traits. These results support the possibility that within-individual variation could evolve as an adaptive response to fine-grained environmental variation and suggest a need for further investigation to improve understanding of evolution in heterogeneous environments.     

Does phenotypic plasticity initiate developmental bias?

The generation of variation is paramount for the action of natural selection. Although biologists are now moving beyond the idea that random mutation provides the sole source of variation for adaptive evolution, we still assume that variation occurs randomly. In this review, we discuss an alternative view for how phenotypic plasticity, which has become well accepted as a source of phenotypic variation within evolutionary biology, can generate nonrandom variation. Although phenotypic plasticity is often defined as a property of a genotype, we argue that it needs to be considered more explicitly as a property of developmental systems involving more than the genotype. We provide examples of where plasticity could be initiating developmental bias, either through direct active responses to similar stimuli across populations or as the result of programmed variation within developmental systems. Such biased variation can echo past adaptations that reflect the evolutionary history of a lineage but can also serve to initiate evolution when environments change. Such adaptive programs can remain latent for millions of years and allow development to harbor an array of complex adaptations that can initiate new bouts of evolution. Specifically, we address how ideas such as the flexible stem hypothesis and cryptic genetic variation overlap, how modularity among traits can direct the outcomes of plasticity, and how the structure of developmental signaling pathways is limited to a few outcomes. We highlight key questions throughout and conclude by providing suggestions for future research that can address how plasticity initiates and harbors developmental bias.     

Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly

Polyphenisms—the expression of discrete phenotypic morphs in response to environmental variation—are examples of phenotypic plasticity that may potentially be adaptive in the face of predictable environmental heterogeneity. In the butterfly Bicyclus anynana, we examine the hormonal regulation of phenotypic plasticity that involves divergent developmental trajectories into distinct adult morphs for a suite of traits as an adaptation to contrasting seasonal environments. This polyphenism is induced by temperature during development and mediated by ecdysteroid hormones. We reared larvae at separate temperatures spanning the natural range of seasonal environments and measured reaction norms for ecdysteroids, juvenile hormones (JHs) and adult fitness traits. Timing of peak ecdysteroid, but not JH titres, showed a binary response to the linear temperature gradient. Several adult traits (e.g. relative abdomen mass) responded in a similar, dimorphic manner, while others (e.g. wing pattern) showed a linear response. This study demonstrates that hormone dynamics can translate a linear environmental gradient into a discrete signal and, thus, that polyphenic differences between adult morphs can already be programmed at the stage of hormone signalling during development. The range of phenotypic responses observed within the suite of traits indicates both shared regulation and independent, trait-specific sensitivity to the hormone signal.     

Mechanisms driving plant functional trait variation in a tropical forest

Plant functional trait variation in tropical forests results from taxonomic differences in phylogeny and associated genetic differences, as well as, phenotypic plastic responses to the environment. Accounting for the underlying mechanisms driving plant functional trait variation is important for understanding the potential rate of change of ecosystems since trait acclimation via phenotypic plasticity is very fast compared to shifts in community composition and genetic adaptation. We here applied a statistical technique to decompose the relative roles of phenotypic plasticity, genetic adaptation, and phylogenetic constraints. We examined typically obtained plant functional traits, such as wood density, plant height, specific leaf area, leaf area, leaf thickness, leaf dry mass content, leaf nitrogen content, and leaf phosphorus content. We assumed that genetic differences in plant functional traits between species and genotypes increase with environmental heterogeneity and geographic distance, whereas trait variation due to plastic acclimation to the local environment is independent of spatial distance between sampling sites. Results suggest that most of the observed trait variation could not be explained by the measured environmental variables, thus indicating a limited potential to predict individual plant traits from commonly assessed parameters. However, we found a difference in the response of plant functional traits, such that leaf traits varied in response to canopy‐light regime and nutrient availability, whereas wood traits were related to topoedaphic factors and water availability. Our analysis furthermore revealed differences in the functional response of coexisting neotropical tree species, which suggests that endemic species with conservative ecological strategies might be especially prone to competitive exclusion under projected climate change.     

Variation in phenotypic plasticity and selection patterns in blue tit breeding time: between- and within-population comparisons

1.?Phenotypic plasticity, the response of individual phenotypes to their environment, can allow organisms to cope with spatio-temporal variation in environmental conditions. Recent studies have shown that variation exists among individuals in their capacity to adjust their traits to environmental changes and that this individual plasticity can be under strong selection. Yet, little is known on the extent and ultimate causes of variation between populations and individuals in plasticity patterns. 2.?In passerines, timing of breeding is a key life-history trait strongly related to fitness and is known to vary with the environment, but few studies have investigated the within-species variation in individual plasticity. 3.?Here, we studied between- and within-population variation in breeding time, phenotypic plasticity and selection patterns for this trait in four Mediterranean populations of blue tits (Cyanistes caeruleus) breeding in habitats varying in structure and quality. 4.?Although there was no significant warming over the course of the study, we found evidence for earlier onset of breeding in warmer years in all populations, with reduced plasticity in the less predictable environment. In two of four populations, there was significant inter-individual variation in plasticity for laying date. Interestingly, selection for earlier laying date was significant only in populations where there was no inter-individual differences in plasticity. 5.?Our results show that generalization of plasticity patterns among populations of the same species might be challenging even at a small spatial scale and that the amount of within-individual variation in phenotypic plasticity may be linked to selective pressures acting on these phenotypic traits.     

Phenotypic plasticity closely linked to climate at origin and resulting in increased mortality under warming and frost stress in a common grass

Phenotypic plasticity is important for species responses to global change and species coexistence. Phenotypic plasticity differs among species and traits and changes across environments. Here, we investigated phenotypic plasticity of the widespread grass Arrhenatherum elatius in response to winter warming and frost stress by comparing phenotypic plasticity of 11 geographically and environmentally distinct populations of this species to phenotypic plasticity of populations of different species originating from a single environment. The variation in phenotypic plasticity was similar for populations of a single species from different locations compared to populations of functionally and taxonomically diverse species from one environment for the studied traits (leaf biomass production and root integrity after frost) across three indices of phenotypic plasticity (RDPI, PIN, slope of reaction norm). Phenotypic plasticity was not associated with neutral genetic diversity but closely linked to the climate of the populations’ origin. Populations originating from warmer and more variable climates showed higher phenotypic plasticity. This indicates that phenotypic plasticity can itself be considered as a trait subject to local adaptation to climate. Finally, our data emphasize that high phenotypic plasticity is not per se positive for adaptation to climate change, as differences in stress responses are resulting in high phenotypic plasticity as expressed by common plasticity indices, which is likely to be related to increased mortality under stress in more plastic populations.     

Multivariate selection shapes environment-dependent variation in the clonal morphology of a red seaweed

Within-individual strategies of variation (e.g., phenotypic plasticity) are particularly relevant to modular organisms, in which ramets of the same genetic individual may encounter diverse environments imposing diverse patterns of selection. Hence, measuring selection in heterogeneous environments is essential to understanding whether environment-dependent phenotypic change enhances the fitness of modular individuals. In sublittoral marine habitats, competition for light and space among modular taxa generates extreme patchiness in resource availability. Little is known, however, of the potential for plasticity within individuals to arise from spatially-variable selection in such systems. We tested whether plasticity enhances genet-level fitness in Asparagopsis armata, a clonal seaweed in which correlated traits mediate morphological responses to variation in light. Using the capacity for rapid, clonal growth to measure fitness, we identified aspects of ramet morphology targeted by selection in two contrasting light environments and compared patterns of selection across environments. We found that directional selection on single traits, coupled with linear and nonlinear selection on multi-trait interactions, shape ramet morphology within environments and favor different phenotypes in each. Evidence of environment-dependent, multivariate selection on correlated traits is novel for any marine modular organism and demonstrates that seaweeds, such as A. armata, may potentially adapt to environmental heterogeneity via plasticity in clonal morphology.     

Biosystematic Studies on Adenophora potaninii Korsh. Complex (Campanulaceae). Ⅰ. Phenotypic Plasticity

Phenotypic plasticity is the environmental modification of genotypic expression and an important means by which individual plants respond to environmental heterogeneity. The study of phenotypic plasticity in the genus Adenophora, which is very complicated taxo nomically because of great morphological variation, proves to be helpful in both investigating the phenotypic variation so as to evaluate potential taxonomic value of their characters and providing important sources of information on the variation, adaptation and evolution of the genus. Twenty-three populations representing all the six species in Adenophora potaninii complex were transplanted into the garden. Of them six populations were selected for study ing their performance in the field and in the garden, in addition to cultivation experiment under different treatments. The results show that there exists considerable developmental plasticity in some leaf, floral and capsule characters. In particular, the leaf shape and length of calyx lobe display significant developmental variation with the maximum being three times as great as the minimum, which is noteworthy because they were previously considered as diagnostic. The characters of root, caudex, stem and inflorescence are found to be very plastic, especially the root diameter, the number of stems, stem height and inflorescence length with great environmental plasticity. In addition, the populations from different habi tats show distinct amounts of plasticity. On the contrary, the characters of leaf, floral, cap sule and seed are less influenced by environments. It seems that the considerable variation in the characters of leaf is attributed mainly to genetic differences. Finally, the phenotypic plasticity of morphological characters of A. potaninii complex and its taxonomic significanceis discussed.     

泡沙参复合体（桔梗科）的物种生物学研究：Ⅰ表型的可塑性

表型可塑性是生物变异中由环境引起的一种变异,是植物适应的一种重要方式。对沙参属这样一个形态上复杂多变、分类上很难处理的类群,研究其表型可塑性不仅为探讨性状变异、判断其系统学意义及选择可靠的分类性状提供了有益的资料,而且有助于揭示沙参属植物变异、适应和进化的机制。本文从泡沙参复合体中选择了6个居群,利用播种和移栽试验,通过对不同个体和居群在一致条件下的表现及野外和移栽后的对比,对根、茎、叶、花和果等形态性状的表型可塑性进行了初步的观测分析。结果表明,一些叶片、花部和果实性状具有较大的发育可塑性,尤其是叶形、花萼裂片不仅发育变化大,而且随发育过程定向变化。环境可塑性较大的性状主要是根、茎、花序分枝等性状,而叶片、花部、果实和种子性状的环境饰变能力都较小。最后,对泡沙参复合体形态性状的变异从发育可塑性和环境可塑性的角度进行了讨论。     

Geometric morphometrics and leaf phenotypic plasticity: assessing fluctuating asymmetry and allometry in European white oaks (Quercus)

Because plants are unable to move away from unfavourable habitats and environmental perturbations, leaf phenotypic plasticity facilitates light absorption and gas exchange. Oaks (Quercus spp.) are particularly known for their adaptability and plastic phenotypes, and leaf allometry and developmental instability may represent important mechanisms for their adaptation to environments and evolution. Because of its important role in the adaptation of plant populations to different environments, allometry can be involved in diversifying selection. Developmental instability is related to environmental perturbations and stresses by producing random deviations in structures characterized by bilateral symmetry, such as oak leaves. In addition, developmental instability can also arise from genetic bottlenecks or as a result of hybridization. The splitting of symmetric and asymmetric components of variation and their separate analysis allows the variability in leaf shape traits to be summarized, reducing the variation produced by developmental instability. The geometric morphometric approach is a useful method for the study of leaf asymmetry and allometric patterns. This method provides an important tool for the visualization of shape attributes that characterize species with highly variable leaf phenotypic patterns. In this study, leaf shape and size variability of three white oak species was investigated by means of a two‐dimensional landmark‐based method providing improved knowledge of variance partitioning, species discrimination, fluctuating asymmetry and allometric patterns of variation resulting from the different analyses. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 335–348.     

MODELING PHENOTYPIC PLASTICITY IN GROWTH TRAJECTORIES: A STATISTICAL FRAMEWORK

Phenotypic plasticity, that is multiple phenotypes produced by a single genotype in response to environmental change, has been thought to play an important role in evolution and speciation. Historically, knowledge about phenotypic plasticity has resulted from the analysis of static traits measured at a single time point. New insight into the adaptive nature of plasticity can be gained by an understanding of how organisms alter their developmental processes in a range of environments. Recent advances in statistical modeling of functional data and developmental genetics allow us to construct a dynamic framework of plastic response in developmental form and pattern. Under this framework, development, genetics, and evolution can be synthesized through statistical bridges to better address how evolution results from phenotypic variation in the process of development via genetic alterations.     

Testing the adaptive plasticity of Iris pumila leaf traits to natural light conditions using phenotypic selection analysis

A multivariate selection analysis has been used to test the adaptiveness of several Iris pumila leaf traits that display plasticity to natural light conditions. Siblings of a synthetic population comprising 31 families of two populations from contrasting light habitats were grown at an open dune site and in the understory of a Pinus nigra stand in order to score variation in phenotypic expression of six leaf traits: number of senescent leaves, number of live leaves, leaf length, leaf width, leaf angle, and specific leaf area. The ambient light conditions affected the values of all traits studied except for specific leaf area. In accordance to ecophysiological expectations for an adaptive response to light, both leaf length and width were significantly greater while the angle between sequential leaves was significantly smaller in the woodland understory than at the exposed dune site. The relationship between leaf traits and vegetative fitness (total leaf area) differed across light habitats as predicted by functional hypotheses. The standardized linear selection gradient (β′) for leaf length and width were positive in sign in both environments, but their magnitude for leaf length was higher in the shade than under full sunlight. Since plasticity of leaf length in the woodland shade has been recognized as adaptive, fitness cost of producing plastic change in leaf length was assessed. In both of the available methods used, the two-step and the multivariate regression procedures, a rather high negative association between the fitness value and the plasticity of leaf length was obtained, indicating a cost of plasticity. The selection gradient for leaf angle was weak and significant only in the woodland understory. Genetic correlations between trait expressions in contrasting light environments were negative in sign and low in magnitude, implying a significant genetic variation for plasticity in these leaf traits. Furthermore, leaf length and leaf width were found to be genetically positively coupled, which indicates that there is a potential for these two traits to evolve toward their optimal phenotypic values even faster than would be expected if they were genetically independent.     

Phenotypic variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system

Secondary sexual characters have been hypothesized to demonstrate increased phenotypic variation between and within individuals as compared to ordinary morphological traits. We tested whether this was the case by studying phenotypic variation, expressed as the coefficient of variation (CV), and developmental instability, measured as fluctuating asymmetry (FA), in ornamental and non-ornamental traits of 70 bird species with feather ornamentation while controlling for similarity among species due to common descent. Secondary sexual characters differed from ordinary morphological traits by showing large phenotypic CV and FA. This difference can be explained by the different mode of selection operating on each kind of trait: a history of intense directional (ornaments) and stabilizing selection (non-ornaments). Phenotypic variation is reduced in the sex with more intense sexual selection (males), but does not differ among species with different mating systems. The strength of stabilizing selection arising from natural selection is associated with decreased CV (wing CV is smaller than tarsus or tail CVs). We found evidence of FA being reduced in ornamental feathers strongly affected by aerodynamics (tail feathers) compared to other ornaments, but only in females. In conclusion, CV and FA were not related, suggesting mat phenotypic plasticity and developmental instability are independent components of phenotypic variation.     

Environmental Heterogeneity and Population Differentiation in Plasticity to Drought in <Emphasis Type="Italic">Convolvulus Chilensis</Emphasis> (Convolvulaceae)

Plant populations may show differentiation in phenotypic plasticity, and theory predicts that greater levels of environmental heterogeneity should select for higher magnitudes of phenotypic plasticity. We evaluated phenotypic responses to reduced soil moisture in plants of Convolvulus chilensis grown in a greenhouse from seeds collected in three natural populations that differ in environmental heterogeneity (precipitation regime). Among several morphological and ecophysiological traits evaluated, only four traits showed differentiation among populations in plasticity to soil moisture: leaf area, leaf shape, leaf area ratio (LAR), and foliar trichome density. In all of these traits plasticity to drought was greatest in plants from the population with the highest interannual variation in precipitation. We further tested the adaptive nature of these plastic responses by evaluating the relationship between phenotypic traits and total biomass, as a proxy for plant fitness, in the low water environment. Foliar trichome density appears to be the only trait that shows adaptive patterns of plasticity to drought. Plants from populations showing plasticity had higher trichome density when growing in soils with reduced moisture, and foliar trichome density was positively associated with total biomass. Co-ordinating editor: F. Stuefer     

PLASTICITY VERSUS ENVIRONMENTAL CANALIZATION: POPULATION DIFFERENCES IN THERMAL RESPONSES ALONG A LATITUDINAL GRADIENT IN DROSOPHILA SERRATA

The phenotypic plasticity of traits, defined as the ability of a genotype to express different phenotypic values of the trait across a range of environments, can vary between habitats depending on levels of temporal and spatial heterogeneity. Other traits can be insensitive to environmental perturbations and show environmental canalization. We tested levels of phenotypic plasticity in diverse Drosophila serrata populations along a latitudinal cline ranging from a temperate, variable climate to a tropical, stable climate by measuring developmental rate and size-related traits at three temperatures (16°C, 22°C, and 28°C). We then compared the slopes of the thermal reaction norms among populations. The 16–22°C part of the reaction norms for developmental rate was flatter (more canalized) for the temperate populations than for the tropical populations. However, slopes for the reaction norms of the two morphological traits (wing size, wing:thorax ratio), were steeper (more plastic) in the temperate versus the tropical populations over the entire thermal range. The different latitudinal patterns in plasticity for developmental rate and the morphological traits may reflect contrasting selection pressures along the tropical–temperate thermal gradient.     

Selective processes in development: implications for the costs and benefits of phenotypic plasticity

Adaptive phenotypic plasticity, the ability of a genotype to develop a phenotype appropriate to the local environment, allows organisms to cope with environmental variation and has implications for predicting how organisms will respond to rapid, human-induced environmental change. This review focuses on the importance of developmental selection, broadly defined as a developmental process that involves the sampling of a range of phenotypes and feedback from the environment reinforcing high-performing phenotypes. I hypothesize that understanding the degree to which developmental selection underlies plasticity is key to predicting the costs, benefits, and consequences of plasticity. First, I review examples that illustrate that elements of developmental selection are common across the development of many different traits, from physiology and immunity to circulation and behavior. Second, I argue that developmental selection, relative to a fixed strategy or determinate (switch) mechanisms of plasticity, increases the probability that an individual will develop a phenotype best matched to the local environment. However, the exploration and environmental feedback associated with developmental selection is costly in terms of time, energy, and predation risk, resulting in major changes in life history such as increased duration of development and greater investment in individual offspring. Third, I discuss implications of developmental selection as a mechanism of plasticity, from predicting adaptive responses to novel environments to understanding conditions under which genetic assimilation may fuel diversification. Finally, I outline exciting areas of future research, in particular exploring costs of selective processes in the development of traits outside of behavior and modeling developmental selection and evolution in novel environments.     

Plasticity to wind is modular and genetically variable in Arabidopsis thaliana

Thigmomorphogenesis, the characteristic phenotypic changes by which plants react to mechanical stress, is a widespread and probably adaptive type of phenotypic plasticity. However, little is known about its genetic basis and population variation. Here, we examine genetic variation for thigmomorphogenesis within and among natural populations of the model system Arabidopsis thaliana. Offspring from 17 field-collected European populations was subjected to three levels of mechanical stress exerted by wind. Overall, plants were remarkably tolerant to mechanical stress. Even high wind speed did not significantly alter the correlation structure among phenotypic traits. However, wind significantly affected plant growth and phenology, and there was genetic variation for some aspects of plasticity to wind among A. thaliana populations. Our most interesting finding was that phenotypic traits were organized into three distinct and to a large degree statistically independent covariance modules associated with plant size, phenology, and growth form, respectively. These phenotypic modules differed in their responsiveness to wind, in the degree of genetic variability for plasticity, and in the extent to which plasticity affected fitness. It is likely, therefore, that thigmomorphogenesis in this species evolves quasi-independently in different phenotypic modules.     

Quantitative genetic and translocation experiments reveal genotype‐by‐environment effects on juvenile life‐history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha)

Understanding the genetic architecture of phenotypic plasticity is required to assess how populations might respond to heterogeneous or changing environments. Although several studies have examined population‐level patterns in environmental heterogeneity and plasticity, few studies have examined individual‐level variation in plasticity. Here, we use the North Carolina II breeding design and translocation experiments between two populations of Chinook salmon to detail the genetic architecture and plasticity of offspring survival and growth. We followed the survival of 50 800 offspring through the larval stage and used parentage analysis to examine survival and growth through freshwater rearing. In one population, we found that additive genetic, nonadditive genetic and maternal effects explained 25%, 34% and 55% of the variance in larvae survival, respectively. In the second population, these effects explained 0%, 24% and 61% of the variance in larvae survival. In contrast, fry survival was regulated primarily by additive genetic effects, which indicates a shift from maternal to genetic effects as development proceeds. Fry growth also showed strong additive genetic effects. Translocations between populations revealed that offspring survival and growth varied between environments, the degree of which differed among families. These results indicate genetic differences among individuals in their degree of plasticity and consequently their ability to respond to environmental variation.     

Low genetic diversity contrasts with high phenotypic variability in heptaploid Spartina densiflora populations invading the Pacific coast of North America

Species can respond to environmental pressures through genetic and epigenetic changes and through phenotypic plasticity, but few studies have evaluated the relationships between genetic differentiation and phenotypic plasticity of plant species along changing environmental conditions throughout wide latitudinal ranges. We studied inter‐ and intrapopulation genetic diversity (using simple sequence repeats and chloroplast DNA sequencing) and inter‐ and intrapopulation phenotypic variability of 33 plant traits (using field and common‐garden measurements) for five populations of the invasive cordgrass Spartina densiflora Brongn. along the Pacific coast of North America from San Francisco Bay to Vancouver Island. Studied populations showed very low genetic diversity, high levels of phenotypic variability when growing in contrasted environments and high intrapopulation phenotypic variability for many plant traits. This intrapopulation phenotypic variability was especially high, irrespective of environmental conditions, for those traits showing also high phenotypic plasticity. Within‐population variation represented 84% of the total genetic variation coinciding with certain individual plants keeping consistent responses for three plant traits (chlorophyll b and carotenoid contents, and dead shoot biomass) in the field and in common‐garden conditions. These populations have most likely undergone genetic bottleneck since their introduction from South America; multiple introductions are unknown but possible as the population from Vancouver Island was the most recent and one of the most genetically diverse. S. densiflora appears as a species that would not be very affected itself by climate change and sea‐level rise as it can disperse, establish, and acclimate to contrasted environments along wide latitudinal ranges.