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.     

GENETIC CONSTRAINTS ON ADAPTATION TO A CHANGING ENVIRONMENT

Genetic correlations between traits can constrain responses to natural selection. To what extent such correlations limit adaptation depends on patterns of directional selection. I derive the expected rate of adaptation (or evolvability) under randomly changing selection gradients. When directional selection gradients have an arbitrary covariance matrix, the average rate of adaptation depends on genetic correlations between traits, contrary to the isotropic case investigated in previous studies. Adaptation may be faster on average with more genetic correlation between traits, if these traits are selected to change jointly more often than the average pair of traits. However, natural selection maximizes the long‐term fitness of a population, not necessarily its rate of adaptation. I therefore derive the average lag load caused by deviations of the mean phenotype from an optimum, under several forms of environmental changes typically experienced by natural populations, both stochastic and deterministic. Simple formulas are produced for how the G matrix affects long‐term fitness in these contexts, and I discuss how their parameters can be estimated empirically.     

Epigenetic population differentiation in field‐ and common garden‐grown Scabiosa columbaria plants

Populations often differ in phenotype and these differences can be caused by adaptation by natural selection, random neutral processes, and environmental responses. The most straightforward way to divide mechanisms that influence phenotypic variation is heritable variation and environmental‐induced variation (e.g., plasticity). While genetic variation is responsible for most heritable phenotypic variation, part of this is also caused by nongenetic inheritance. Epigenetic processes may be one of the underlying mechanisms of plasticity and nongenetic inheritance and can therefore possibly contribute to heritable differences through drift and selection. Epigenetic variation may be influenced directly by the environment, and part of this variation can be transmitted to next generations. Field screenings combined with common garden experiments will add valuable insights into epigenetic differentiation, epigenetic memory and can help to reveal part of the relative importance of epigenetics in explaining trait variation. We explored both genetic and epigenetic diversity, structure and differentiation in the field and a common garden for five British and five French Scabiosa columbaria populations. Genetic and epigenetic variation was subsequently correlated with trait variation. Populations showed significant epigenetic differentiation between populations and countries in the field, but also when grown in a common garden. By comparing the epigenetic variation between field and common garden‐grown plants, we showed that a considerable part of the epigenetic memory differed from the field‐grown plants and was presumably environmentally induced. The memory component can consist of heritable variation in methylation that is not sensitive to environments and possibly genetically based, or environmentally induced variation that is heritable, or a combination of both. Additionally, random epimutations might be responsible for some differences as well. By comparing epigenetic variation in both the field and common environment, our study provides useful insight into the environmental and genetic components of epigenetic variation.     

EVOLUTION AND EXTINCTION IN A CHANGING ENVIRONMENT: A QUANTITATIVE-GENETIC ANALYSIS

Because of the ubiquity of genetic variation for quantitative traits, virtually all populations have some capacity to respond evolutionarily to selective challenges. However, natural selection imposes demographic costs on a population, and if these costs are sufficiently large, the likelihood of extinction will be high. We consider how the mean time to extinction depends on selective pressures (rate and stochasticity of environmental change, and strength of selection), population parameters (carrying capacity, and reproductive capacity), and genetics (rate of polygenic mutation). We assume that in a randomly mating, finite population subject to density-dependent population growth, individual fitness is determined by a single quantitative-genetic character under Gaussian stabilizing selection with the optimum phenotype exhibiting directional change, or random fluctuations, or both. The quantitative trait is determined by a finite number of freely recombining, mutationally equivalent, additive loci. The dynamics of evolution and extinction are investigated, assuming that the population is initially under mutation-selection-drift balance. Under this model, in a directionally changing environment, the mean phenotype lags behind the optimum, but on the average evolves parallel to it. The magnitude of the lag determines the vulnerability to extinction. In finite populations, stochastic variation in the genetic variance can be quite pronounced, and bottlenecks in the genetic variance temporarily can impair the population's adaptive capacity enough to cause extinction when it would otherwise be unlikely in an effectively infinite population. We find that maximum sustainable rates of evolution or, equivalently, critical rates of environmental change, may be considerably less than 10% of a phenotypic standard deviation per generation.     

Evolution of phenotypic plasticity and environmental tolerance of a labile quantitative character in a fluctuating environment

Quantitative genetic models of evolution of phenotypic plasticity are used to derive environmental tolerance curves for a population in a changing environment, providing a theoretical foundation for integrating physiological and community ecology with evolutionary genetics of plasticity and norms of reaction. Plasticity is modelled for a labile quantitative character undergoing continuous reversible development and selection in a fluctuating environment. If there is no cost of plasticity, a labile character evolves expected plasticity equalling the slope of the optimal phenotype as a function of the environment. This contrasts with previous theory for plasticity influenced by the environment at a critical stage of early development determining a constant adult phenotype on which selection acts, for which the expected plasticity is reduced by the environmental predictability over the discrete time lag between development and selection. With a cost of plasticity in a labile character, the expected plasticity depends on the cost and on the environmental variance and predictability averaged over the continuous developmental time lag. Environmental tolerance curves derived from this model confirm traditional assumptions in physiological ecology and provide new insights. Tolerance curve width increases with larger environmental variance, but can only evolve within a limited range. The strength of the trade‐off between tolerance curve height and width depends on the cost of plasticity. Asymmetric tolerance curves caused by male sterility at high temperature are illustrated. A simple condition is given for a large transient increase in plasticity and tolerance curve width following a sudden change in average environment.     

Adaptive divergence in plasticity in natural populations of Impatiens capensis and its consequences for performance in novel habitats

We tested for adaptive differentiation between two natural populations of Impatiens capensis from sites known to differ in selection on plasticity to density. We also determined the degree to which plasticity to density within a site was correlated with plastic responses of experimental immigrants to foreign sites. Inbred lines, derived from natural populations in an open-canopy site and a woodland site, were planted reciprocally in both original sites at naturally occurring high densities and at low density. The density manipulation represents environmental variation typically experienced within the site of a given population, and the transplant manipulation represents environmental differences between sites of different populations. Internode elongation, meristem allocation, leaf length, flowering date, and total lifetime fitness were measured. Genotypes originating in the open site, where selection favored plasticity of first internode length and flowering time (Donohue et al. 2000a), were more plastic in those characters than genotypes originating from the woodland site, where plasticity was maladaptive. Therefore, these two populations appear to have responded to divergent selection on plasticity. Plasticity to density strongly resembled plasticity to site differences for many characters, suggesting that similar environmental factors elicit plasticity both to density and to overhead canopy. Thus, plasticity that evolved in response to density variation within a site influenced phenotypic expression in the foreign site. Plastic responses to site caused immigrants from foreign populations to resemble native genotypes more closely. In particular, immigrants from the open site converged toward the selectively favored early-flowering phenotype of native genotypes in the woodland site, thereby reducing potential fitness differences between foreign and native genotypes. However, because genotypes from the woods population were less plastic than genotypes from the sun population, phenotypic differences between populations were greatest in the open site at low density. Therefore, population differences in plasticity can cause genotypes from foreign populations to be more strongly selected against in some environments than in others. However, genetic constraints and limits to plasticity prevented complete convergence of immigrants to the native phenotype in any environment.     

Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis

We investigated the conditions under which plastic responses to density are adaptive in natural populations of Impatiens capensis and determined whether plasticity has evolved differently in different selective environments. Previous studies showed that a population that evolved in a sunny site exhibited greater plasticity in response to density than did a population that evolved in a woodland site. Using replicate inbred lines in a reciprocal transplant that included a density manipulation, we asked whether such population differentiation was consistent with the hypothesis of adaptive divergence. We hypothesized that plasticity would be more strongly favored in the sunny site than in the woodland site; consequently, we predicted that selection would be more strongly density dependent in the sunny site, favoring the phenotype that was expressed at each density. Selection on internode length and flowering date was consistent with the hypothesis of adaptive divergence in plasticity. Few costs or benefits of plasticity were detected independently from the expressed phenotype, so plasticity was selected primarily through selection on the phenotype. Correlations between phenotypes and their plasticity varied with the environment and would cause indirect selection on plasticity to be environment dependent. We showed that an appropriate plastic response even to a rare environment can greatly increase genotypic fitness when that environment is favorable. Selection on the measured characters contributed to local adaptation and fully accounted for fitness differences between populations in all treatments except the woodland site at natural density.     

Plasticity versus canalization: population differences in the timing of shade-avoidance responses

The reliability of environmental cues and costs of a fixed phenotype are two factors determining whether selection favors phenotypic plasticity or environmental specialization. This study examines the relationship between these two factors and the evolution of plant competitive strategies (plastic vs. fixed morphologies). In natural plant populations, shifts in light quality associated with foliar shade reliably indicate the presence of neighbors. These cues mediate plastic stem-elongation responses that often increase competitive ability and access to light. Using experimental light treatments (full sun, neutral shade, and foliar shade), genetic differences among populations of Abutilon theophrasti (velvetleaf) in average elongation and plasticity to foliar-shade cues were examined. Six populations, two from each of three site types (fields in continuous corn cultivation, fields undergoing corn-soy rotation, and weedy sites), were exposed to the light treatments at two stages in their life history. At the seedling stage, populations derived from cornfield sites exhibited higher, average elongation than populations from either rotating corn-soy fields or weedy areas. Because seedling elongation may delay shading of velvetleaf by corn, population differences may reflect adaptive responses to directional selection imposed by competitive conditions. However, the effects of simulated foliar shade on elongation were three times as great as the average population differences, and these comparatively higher levels of elongation were associated with an allocation cost. These results are consistent with the hypothesis that phenotypic plasticity may limit the evolution of specialists; reliable environmental cues enable individuals to facultatively adopt highly elongated, costly phenotypes in crowded patches while avoiding the costs of that phenotype in less crowded microsites. At later life-history stages, populations experiencing competition with corn exhibited lower plasticity to light quality than populations derived from weedy areas. Elongation at later nodes is maladaptive in cornfields because velvetleaf is ultimately incapable of overtopping corn; individuals that elongate therefore experience the cost of allocating to stems but fail to improve leaf exposure. The decreased responsiveness of cornfield populations to light quality is consistent with theoretical predictions in which reduced plasticity is favored when environmental cues fail to mediate an adaptive response.     

The fitness costs of developmental canalization and plasticity

Organisms are capable of an astonishing repertoire of phenotypic responses to the environment, and these often define important adaptive solutions to heterogeneous and unpredictable conditions. The terms ‘phenotypic plasticity’ and ‘canalization’ indicate whether environmental variation has a large or small effect on the phenotype. The evolution of canalization and plasticity is influenced by optimizing selection‐targeting traits within environments, but inherent fitness costs of plasticity may also be important. We present a meta‐analysis of 27 studies (of 16 species of plant and 7 animals) that have measured selection on the degree of plasticity independent of the characters expressed within environments. Costs of plasticity and canalization were equally frequent and usually mild; large costs were observed only in studies with low sample size. We tested the importance of several covariates, but only the degree of environmental stress was marginally positively related to the cost of plasticity. These findings suggest that costs of plasticity are often weak, and may influence phenotypic evolution only under stressful conditions.     

Strategies in functional poly(ester amide) syntheses to study human coronary artery smooth muscle cell interactions

The design of new generation cardiovascular biomaterials focuses on biomimetic properties that are capable of eliciting specific cellular responses and directing new tissue formation. Synthetic poly(ester amide)s (PEAs) containing α-amino acid residues have the potential to elicit favorable cellular responses. Furthermore, they are biodegradable owing to the incorporation of naturally occurring amino acids. In this study, a family of PEAs was synthesized from selected α-amino acids using both solution and interfacial polymerization approaches to optimize their properties for vascular tissue engineering applications. By careful selection of the monomers and the polymerization approach, high-molecular-weight PEAs with low glass-transition temperatures were obtained. Human coronary artery smooth muscle cells (HCASMCs) cultured directly on bare PEA films attached and spread well up to 7 days of culture. Moreover, cell viability was significantly enhanced on all nonfunctional PEAs compared with tissue culture polystyrene controls. The trifluoroacetic acid salt of the lysine-containing functional PEAs was found to retard cell growth but still supported cell viability up to 5 days of culture. Immunostaining of HCASMCs revealed strong vinculin expression, suggesting that the HCASMCs initiated cellular processes for focal adhesion contacts with all PEA surfaces. Conversely, smooth muscle α-actin expression was not abundant on the PEA surfaces, suggesting a proliferative smooth muscle cell phenotype. Altogether, our results indicate that these PEAs are promising materials for vascular tissue engineering scaffolds.     

Environmental variation partitioned into separate heritable components

Trait variation is normally separated into genetic and environmental components, yet genetic factors also control the expression of environmental variation, encompassing plasticity across environmental gradients and within‐environment responses. We defined four components of environmental variation: plasticity across environments, variability in plasticity, variation within environments, and differences in within‐environment variation across environments. We assessed these components for cold tolerance across five rearing temperatures using the Drosophila melanogaster Genetic Reference Panel (DGRP). The four components were found to be heritable, and genetically correlated to different extents. By whole genome single marker regression, we detected multiple candidate genes controlling the four components and showed limited overlap in genes affecting them. Using the binary UAS‐GAL4 system, we functionally validated the effects of a subset of candidate genes affecting each of the four components of environmental variation and also confirmed the genetic and phenotypic correlations obtained from the DGRP in distinct genetic backgrounds. We delineate selection targets associated with environmental variation and the constraints acting upon them, providing a framework for evolutionary and applied studies on environmental sensitivity. Based on our results we suggest that the traditional quantitative genetic view of environmental variation and genotype‐by‐environment interactions needs revisiting.     

CONTRASTING PATTERNS OF PHENOTYPIC PLASTICITY IN REPRODUCTIVE TRAITS IN TWO GREAT TIT (PARUS MAJOR) POPULATIONS

Phenotypic plasticity is an important mechanism via which populations can respond to changing environmental conditions, but we know very little about how natural populations vary with respect to plasticity. Here we use random‐regression animal models to understand the multivariate phenotypic and genetic patterns of plasticity variation in two key life‐history traits, laying date and clutch size, using data from long‐term studies of great tits in The Netherlands (Hoge Veluwe [HV]) and UK (Wytham Woods [WW]). We show that, while population‐level responses of laying date and clutch size to temperature were similar in the two populations, between‐individual variation in plasticity differed markedly. Both populations showed significant variation in phenotypic plasticity (IxE) for laying date, but IxE was significantly higher in HV than in WW. There were no significant genotype‐by‐environment interactions (GxE) for laying date, yet differences in GxE were marginally nonsignificant between HV and WW. For clutch size, we only found significant IxE and GxE in WW but no significant difference between populations. From a multivariate perspective, plasticity in laying date was not correlated with plasticity in clutch size in either population. Our results suggest that generalizations about the form and cause of any response to changing environmental conditions across populations may be difficult.     

Population responses to anthropogenic disturbance: lessons from three‐spined sticklebacks Gasterosteus aculeatus in eutrophic habitats

Human‐induced environmental changes differ from most natural changes in which they happen at a faster rate and require quicker responses from populations. The first response of populations is usually phenotypically plastic alterations of morphology, physiology and behaviour. This plasticity can be favourable and move the population closer to an adaptive peak in the altered environment and, hence, maintain a viable population, or be maladaptive and move the population further from the peak and increase the risk of extinction. The radiation of the three‐spined stickleback Gasterosteus aculeatus from the ocean to different freshwater habitats has provided much information on adaptation to new environmental conditions. Currently, human‐induced eutrophication is changing the breeding areas of these fish, which creates a model system for investigation of responses to rapid environmental disturbance. Results show that a primary reaction is plastic alterations of behaviour, with some adjustments being adaptive while others are not. At the same time, the strength of sexual selection on several traits is relaxed, which could increase the relative importance of survival selection. Whether this will restore population viability depends on the amount of standing genetic variation in the right direction. Human disturbances can be dramatic and resolution of the limit of flexibility and the possibility of genetic adaptation should be important targets of future research.     

When three traits make a line: evolution of phenotypic plasticity and genetic assimilation through linear reaction norms in stochastic environments

Genetic assimilation emerges from selection on phenotypic plasticity. Yet, commonly used quantitative genetics models of linear reaction norms considering intercept and slope as traits do not mimic the full process of genetic assimilation. We argue that intercept–slope reaction norm models are insufficient representations of genetic effects on linear reaction norms and that considering reaction norm intercept as a trait is unfortunate because the definition of this trait relates to a specific environmental value (zero) and confounds genetic effects on reaction norm elevation with genetic effects on environmental perception. Instead, we suggest a model with three traits representing genetic effects that, respectively, (i) are independent of the environment, (ii) alter the sensitivity of the phenotype to the environment and (iii) determine how the organism perceives the environment. The model predicts that, given sufficient additive genetic variation in environmental perception, the environmental value at which reaction norms tend to cross will respond rapidly to selection after an abrupt environmental change, and eventually becomes equal to the new mean environment. This readjustment of the zone of canalization becomes completed without changes in genetic correlations, genetic drift or imposing any fitness costs of maintaining plasticity. The asymptotic evolutionary outcome of this three‐trait linear reaction norm generally entails a lower degree of phenotypic plasticity than the two‐trait model, and maximum expected fitness does not occur at the mean trait values in the population.     

Genetic architecture of survival and fitness-related traits in two populations of Atlantic salmon

The additive genetic effects of traits can be used to predict evolutionary trajectories, such as responses to selection. Non-additive genetic and maternal environmental effects can also change evolutionary trajectories and influence phenotypes, but these effects have received less attention by researchers. We partitioned the phenotypic variance of survival and fitness-related traits into additive genetic, non-additive genetic and maternal environmental effects using a full-factorial breeding design within two allopatric populations of Atlantic salmon (Salmo salar). Maternal environmental effects were large at early life stages, but decreased during development, with non-additive genetic effects being most significant at later juvenile stages (alevin and fry). Non-additive genetic effects were also, on average, larger than additive genetic effects. The populations, generally, did not differ in the trait values or inferred genetic architecture of the traits. Any differences between the populations for trait values could be explained by maternal environmental effects. We discuss whether the similarities in architectures of these populations is the result of natural selection across a common juvenile environment.     

Rapid evolution and behavioral plasticity following introduction to an environment with reduced predation risk

Adaptive behavioral plasticity can play a beneficial role when a population becomes established in a novel environment if environmental cues allow the expression of appropriate behavior. Further, plasticity itself can evolve over time in a new environment causing changes in the way or degree to which animals respond to environmental cues. Colonization events provide an opportunity to investigate such relationships between behavioral plasticity and adaptation to new environments. Here, we investigated the evolution of behavior and behavioral plasticity during colonization of a new environment, by testing if female mate‐choice behavior diverged in Trinidadian guppies 2–3 years (~6–9 generations) after being introduced to four locations with reduced predation risk. We collected wild‐caught fish from the source and introduced populations, and we reared out second‐generation females in the laboratory with and without predator cues to examine their plastic responses to a bright and dull male. We found introduced females were less responsive to males when reared without predator cues, but both introduced and source females were similarly responsive when reared with predator cues. Thus, the parallel evolution of behavior across multiple populations in the low‐predation environment was only observed in the treatment mimicking the introduction environment. Such results are consistent with theory predicting that the evolution of plasticity is a by‐product of differential selection across environments.     

Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation

Adaptation to a sudden extreme change in environment, beyond the usual range of background environmental fluctuations, is analysed using a quantitative genetic model of phenotypic plasticity. Generations are discrete, with time lag τ between a critical period for environmental influence on individual development and natural selection on adult phenotypes. The optimum phenotype, and genotypic norms of reaction, are linear functions of the environment. Reaction norm elevation and slope (plasticity) vary among genotypes. Initially, in the average background environment, the character is canalized with minimum genetic and phenotypic variance, and no correlation between reaction norm elevation and slope. The optimal plasticity is proportional to the predictability of environmental fluctuations over time lag τ. During the first generation in the new environment the mean fitness suddenly drops and the mean phenotype jumps towards the new optimum phenotype by plasticity. Subsequent adaptation occurs in two phases. Rapid evolution of increased plasticity allows the mean phenotype to closely approach the new optimum. The new phenotype then undergoes slow genetic assimilation, with reduction in plasticity compensated by genetic evolution of reaction norm elevation in the original environment.     

Density dependence and population differentiation of genetic architecture in Impatiens capensis in natural environments

We identified environment-dependent constraints on the evolution of plasticity to density under natural conditions in two natural populations of Impatiens capensis. We also examined the expression of population divergence in genetic variance-covariance matrices in these natural environments. Inbred lines, originally collected from a sunny site with high seedling densities and a woodland site with low seedling densities, were planted in both original sites at natural high densities and at low density. Morphological and life-history characters were measured. More genetic variation for plastic responses to density was expressed in the sun site than in the woodland site, so the evolutionary potential of plasticity was greater in the sun site. Strong genetic correlations between the same character expressed at different densities and correlations among different characters could constrain the evolution of plasticity in both sites. Genetically based trade-offs in meristem allocation to vegetative growth and reproduction were apparent only in the high-resource environment with no overhead canopy and no intraspecific competition. Therefore, genetic constraints on the evolution of plasticity depended on the site and density in which plants were grown, and correlated responses to selection on plastic characters are also expected to differ between sites and densities. Population differentiation in genetic variance-covariance matrices was detected, but matrix structural differences, as opposed to proportional differences, were detected between populations only in the sun site at natural high density. Thus, population divergence in genetic architecture can occur rapidly and on a fine spatial scale, but the expression of such divergence may depend on the environment.     

Reaction norms of Arabidopsis. I. Plasticity of characters and correlations across water,nutrient and light gradients

The univariate and multivariate study of variation for phenotypic plasticity is central to providing a clear understanding of hypotheses about the genetic control and evolution of reaction norms in natural populations. Arabidopsis thaliana is an ideal organism for the study of Genotype × Environment interactions (i.e., genetic variation for plasticity), because of the ease with which it can be grown in large numbers and due to the amount of information already available on its genetics, physiology and developmental biology. In this paper, we report on the plasticity, genetic variation and G × E interactions of four populations of A. thaliana in response to three environmental gradients (water, light and nutrients), each characterized by four levels of the controlled parameter. We measured nine traits and obtained their reaction norms. Path analysis was used to study the plasticity of character correlations. We found a tendency for A. thaliana reaction norms to be linear (either flat, i.e. no plasticity, or with a significant slope), in accordance with previous studies. We detected substantial amounts of genetic variation for plasticity in the light and nutrient gradients, but not in the water gradient. Dramatic restructuring of character correlations was induced by changes in environmental conditions, although some paths tended to be stable irrespective of the environment, thereby suggesting some degree of canalization.