Differing selection in alternative competitive environments: shade-avoidance responses and germination timing

Under competitive conditions, stem elongation in plants is thought to enhance fitness by increasing light interception. However, the onset of competition should vary with the species of competitor due to interspecific differences in timing of emergence and plant growth form. The fitness benefits of elongation may therefore depend on the timing of this plastic response. Phenotypic selection analyses and path analysis were used to evaluate selection acting on stem elongation at early and late life-history stages and the combination of germination timing and elongation in an annual plant. Velvetleaf (Abutilon theophrasti) were raised in one of three environments experienced by natural populations (cornfields; soybean fields; and disturbed, weedy sites). Due to the rapid growth rate and high density of plants in disturbed areas, selection to increase seedling-stage elongation was expected in weedy sites. Due to the wide spacing of crop plants, competition for light is initially low in cultivated fields, but intensifies as the season progresses. Selection for increased elongation at later nodes was expected in soybean fields because velvetleaf can often overtop soy and thereby increase leaf exposure. In contrast, selection against late elongation was expected in cornfields because velvetleaf are incapable of overtopping corn. Individuals that elongate would experience the carbon cost of allocating to structural tissue, but fail to experience a carbon return through increased light interception. The phenotypic selection analyses were consistent with these predictions and therefore support the role of stem elongation as an adaptation to interspecific competition. Selection also acted on the combination of germination timing and elongation. In the weedy environment, early emergence in conjunction with enhanced stem elongation conveyed the highest fitness. Reduced elongation was favored among individuals that emerged late, potentially because these individuals were unable to overtop neighbors. The results of this study demonstrate that the timing of stem elongation strongly affects competitive success. Environments that differ in the timing of competition for light select for elongation at different life-history stages, and this selection depends on the timing of emergence.     

Limits to adaptive plasticity: temperature and photoperiod influence shade-avoidance responses

In plants, the ratio of red to far-red wavelengths (R:FR) reliably indicates neighbor proximity and influences stem elongation. Enhanced elongation increases light interception and fitness under crowded conditions. However, many environmental factors vary simultaneously such that responses to R:FR may be affected by abiotic conditions or maternal environmental conditions. This study examines the effects of temperature, photoperiod, and maternal environment on stem-elongation responses to R:FR. Four populations of Abutilon theophrasti (two from disturbed, weedy areas and two from cornfields) were used in factorial common-garden experiments of temperature × R:FR × population and photoperiod × R:FR × population. Seedling growth of greenhouse- and field-derived seed was compared to evaluate maternal effects. Maternal environment did not alter seedling elongation. Higher temperatures resulted in both a twofold increase in average elongation and increased responsiveness to R:FR. Significant three-way interactions in both experiments demonstrate that population responses to R:FR differ depending on temperature and photoperiod conditions. These results indicate that elongation responses to R:FR are more variable than previously realized. The observed variability in elongation also suggests that the outcome of competitive interactions in the natural environment will depend on ambient temperature, photoperiod length, and population origin.     

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.     

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.     

Morphological canalization,integration, and plasticity in response to population density in Abutilon theophrasti: Influences of soil conditions and growth stages

Phenotypic integration and developmental canalization have been hypothesized to constrain the degree of phenotypic plasticity, but little evidence exists, probably due to the lack of studies on the relationships among the three processes, especially for plants under different environments. We conducted a field experiment by subjecting plants of Abutilon theophrasti to three densities, under infertile and fertile soil conditions, and analyzing correlations among canalization, integration, and plasticity in a variety of measured morphological traits after 50 and 70 days, to investigate the relationships among the three variables in response to density and how these responses vary with soil conditions and growth stages. Results showed trait canalization decreased and phenotypic integration and the degree of plasticity (absolute plasticity) in traits increased with density. Phenotypic integration often positively correlated with absolute plasticity, whereas correlations between trait canalization and plasticity were insignificant in most cases, with a few positive ones between canalization and absolute plasticity at low and medium densities. As plants grew, these correlations intensified in infertile soil and attenuated in fertile soil. Our findings suggested the complexity of the relationship between canalization and plasticity: Decreased canalization is more likely to facilitate active plastic responses under more favorable conditions, whereas increased level of integration should mainly be an outcome of plastic responses. Soil conditions and growth stage may affect responses of these correlations to density via modifying plant size, competition strength, and plastic responses in traits. We also predicted that decreased canalization can be advantageous or disadvantageous, and the lack of response to stress may demonstrate a stronger ability of adaptation than passive response, thus should be adaptive plasticity as active response.     

When mother knows best: A population genetic model of transgenerational versus intragenerational plasticity

Many organisms exhibit phenotypic plasticity; producing alternate phenotypes depending on the environment. Individuals can be plastic (intragenerational or direct plasticity), wherein individuals of the same genotype produce different phenotypes in response to the environments they experience. Alternatively, an individual's phenotype may be under the control of its parents, usually the mother (transgenerational or indirect plasticity), so that mother's genotype determines the phenotype produced by a given genotype of her offspring. Under what conditions does plasticity evolve to have intragenerational as opposed to transgenerational genetic control? To explore this question, we present a population genetic model for the evolution of transgenerational and intragenerational plasticity. We hypothesize that the capacity for plasticity incurs a fitness cost, which is borne either by the individual developing the plastic phenotype or by its mother. We also hypothesize that individuals are imperfect predictors of future environments and their capacity for plasticity can lead them occasionally to make a low‐fitness phenotype for a particular environment. When the cost, benefit and error parameters are equal, we show that there is no evolutionary advantage to intragenerational over transgenerational plasticity, although the rate of evolution of transgenerational plasticity is half the rate for intragenerational plasticity, as predicted by theory on indirect genetic effects. We find that transgenerational plasticity evolves when mothers are better predictors of future environments than offspring or when the fitness cost of the capacity for plasticity is more readily borne by a mother than by her developing offspring. We discuss different natural systems with either direct intragenerational plasticity or indirect transgenerational plasticity and find a pattern qualitatively in accord with the predictions of our model.     

Testing adaptive plasticity to UV: costs and benefits of stem elongation and light-induced phenolics

On exposure to ultraviolet radiation (UV), many plant species both reduce stem elongation and increase production of phenolic compounds that absorb in the UV region of the spectrum. To demonstrate that such developmental plasticity to UV is adaptive, it is necessary to show that the induced phenotype is both beneficial in inductive environments and maladaptive in non-inductive environments. We measured selection on stem elongation and phenolic content of seedlings of Impatiens capensis transplanted into ambient-UV and UV-removal treatments. We extended the range of phenotypes expressed, and thus the opportunity for selection in each UV treatment, by pretreating seedlings with either a low ratio of red:far-red wavelengths (R:FR), which induced stem elongation and reduced phenolic concentrations, or high R:FR, which had the opposite effect on these two phenotypic traits. Reduced stem length relative to biomass was advantageous for elongated plants under ambient UV, whereas increased elongation was favored in the UV-removal treatment. Selection favored an increase in the level of phenolics induced by UV in the ambient-UV treatment, but a decrease in phenolics in the absence of UV. These results are consistent with the hypotheses that reduced elongation and increased phenolic concentrations serve a UV-protective function and provide the first explicit demonstration in a wild species that plasticity of these traits to UV is adaptive. The observed cost to phenolics in the absence of UV may explain why many species plastically upregulate phenolic production when exposed to UV, rather than evolve constitutively high levels of these compounds. Finally, pretreatment with low R:FR simulating foliar shade did not exacerbate the fitness impact of UV exposure when plants had several weeks to acclimate to UV. This observation suggests that the evolution of adaptive shade avoidance responses to low R:FR in crowded stands will not be constrained by increased sensitivity to UV in elongated plants when they overtop their neighbors.     

Generalists versus specialists in fluctuating environments: a bet-hedging perspective

Bet-hedging evolves in fluctuating environments because long-term genotype success is determined by geometric (rather than arithmetic) mean fitness across generations. Diversifying bet-hedging produces different specialist offspring, whereas conservative bet-hedging produces similar generalist offspring. However, many fields, such as behavioral ecology and thermal physiology, typically consider specialist versus generalist strategies only in terms of maximizing arithmetic mean fitness benefits to individuals. Here we model how environmental variability affects optimal amounts of phenotypic variation within and among individuals to maximise genotype fitness, and we disentangle the effects of individual-level optimization and genotype-level bet-hedging by comparing long-term arithmetic versus geometric mean fitness. For traits with additive fitness effects within lifetimes (e.g. foraging-related traits), genotypes of similar generalists or diversified specialists perform equally well. However, if fitness effects are multiplicative within lifetimes (e.g. sequential survival probabilities), generalist individuals are always favored. In this case, geometric mean fitness optimization requires even more within-individual phenotypic variation than does arithmetic mean fitness, causing individuals to be more generalist than required to simply maximize their own expected fitness. In contrast to previous results in the bet-hedging literature, this generalist conservative bet-hedging effect is always favored over diversifying bet-hedging. These results link the evolution of behavioral and ecological specialization with earlier models of bet-hedging, and we apply our framework to a range of natural phenomena from habitat choice to host specificity in parasites.     

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

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

Associations between leaf developmental stability,variability, canalization,and phenotypic plasticity in Abutilon theophrasti

Developmental stability, canalization, and phenotypic plasticity are the most common sources of phenotypic variation, yet comparative studies investigating the relationships between these sources, specifically in plants, are lacking. To investigate the relationships among developmental stability or instability, developmental variability, canalization, and plasticity in plants, we conducted a field experiment with Abutilon theophrasti, by subjecting plants to three densities under infertile vs. fertile soil conditions. We measured the leaf width (leaf size) and calculated fluctuating asymmetry (FA), coefficient of variation within and among individuals (CV_intra and CV_inter), and plasticity (PI_rel) in leaf size at days 30, 50, and 70 of plant growth, to analyze the correlations among these variables in response to density and soil conditions, at each of or across all growth stages. Results showed increased density led to lower leaf FA, CV_intra, and PI_rel and higher CV_inter in fertile soil. A positive correlation between FA and PI_rel occurred in infertile soil, while correlations between CV_inter and PI_rel and between CV_inter and CV_intra were negative at high density and/or in fertile soil, with nonsignificant correlations among them in other cases. Results suggested the complexity of responses of developmental instability, variability, and canalization in leaf size, as well as their relationships, which depend on the strength of stresses. Intense aboveground competition that accelerates the decrease in leaf size (leading to lower plasticity) will be more likely to reduce developmental instability, variability, and canalization in leaf size. Increased developmental instability and intra‐ and interindividual variability should be advantageous and facilitate adaptive plasticity in less stressful conditions; thus, they are more likely to positively correlate with plasticity, whereas developmental stability and canalization with lower developmental variability should be beneficial for stabilizing plant performance in more stressful conditions, where they tend to have more negative correlations with plasticity.     

A modular concept of plant foraging behaviour: the interplay between local responses and systemic control

In this paper we examined the notion that plant foraging for resources in heterogeneous environments must involve: (1) plasticity at the level of individual modules in reaction to localized environmental signals; and (2) the potential for modification of these responses either by the signals received from connected modules that may be exposed to different conditions, or by the signals reflecting the overall resource status of the plant. A conceptual model is presented to illustrate how plant foraging behaviour is achieved through these processes acting in concert, from the signal reception through signal transduction to morphological or physiological response. Evidence to support the concept is reviewed, using selective root placement under nutritionally heterogeneous conditions and elongation responses of stems and petioles to shade as examples. We discussed how the adoption of this model can promote understanding of the ecological significance of foraging behaviour. We also identified a need to widen the experimental repertoires of both molecular physiology and ecology in order to increase our insight into both the regulation and functioning of foraging responses, and their relationship with the patterns of environmental heterogeneity under which plants have evolved.     

Plasticity of grasshopper vitellogenin production in response to diet is primarily a result of changes in fat body mass

Life history plasticity is the developmental production of different phenotypes by similar genotypes in response to different environments. Plasticity is common in early post-embryonic or adult development. Later in the developmental stage, the transition from developmentally plastic to canalized (i.e., inflexible) phases is often associated with the attainment of a threshold level of storage. Thresholds are often described simply as total body mass or cumulative consumption of food. The physiological characteristics of thresholds, such as the contributions of the growth of particular organs or the production rate of proteins, are largely unstudied. To address the physiology underlying a threshold-induced developmental transition, total vitellogenin production in response to diet quality in the lubber grasshopper was studied. For individuals that differed in age or dietary protein, somatic mass, ovarian mass, fat body mass, mass-specific vitellogenin production, vitellogenin titer, and storage protein titer were measured. Age and diet strongly affected these parameters, with ovarian mass and fat body mass contributing most to the differences. During mid vitellogenesis, females were highly plastic in response to changing food quality. Only during late vitellogenesis were females unresponsive to changes in food quality. Fat body mass was a more important component of plasticity than was mass-specific vitellogenin production. Because these two variables together make up total vitellogenin production, the greater contribution of fat body mass than mass-specific vitellogenin production suggests that growth factors may be more important than tissue stimulators in producing developmental changes in total vitellogenin production. To our knowledge, this is the first study to demonstrate that mass gain of an organ is more important to developmental plasticity than is the output of that same organ.     

Phenotypic responses of lacustrine brook charr in relation to the intensity of interspecific competition

We investigated the structure of interindividual variations in the diet of brook charr (Salvelinus fontinalis) based on stomach contents data of 3776 charr captured in 69 lakes of the Canadian Shield (Québec, Canada); 29 of these contained allopatric brook charr populations, 24 contained brook charr and creek chub (Semotilus atromaculatus) and 16 contained brook charr and white sucker (Catostomus commersoni). In any given lake, some of the charr fed almost exclusively on benthic organisms (benthic specialists, i.e., mean percent weight of benthic prey >90%), others, almost exclusively on pelagic prey (pelagic specialists, i.e., mean percent weight of benthic prey <10%), and a lesser proportion were generalist feeders (i.e. mean percent weight of benthic prey between 10 and 90%). The proportion of benthic and pelagic specialists were respectively 41.3 and 18% in allopatric brook charr populations. These proportions fit remarkably well with those based on interindividual preferences in spatial distribution, identified through radio-telemetry in another study done in two lakes of the same area. The proportion of benthic specialists was related to competition for benthic organisms with creek chub and white sucker. The effect of white sucker on brook charr diet was more pronounced than that of creek chub: the proportion of benthic specialists among brook charr decreased from 41.3% in allopatry to 19.7% in sympatry with creek chub, and to 9.9% in sympatry with white sucker. Other response variables of brook charr populations also indicate that white sucker is a stronger competitor than creek chub in this system. Because sucker and chub were introduced in these lakes during the last century, phenotypic responses of brook charr to interspecific competition appear to be rapid. Furthermore, in addition to providing a strong field support to the current hypothesis that polymorphism is promoted by arelaxation of interspecific competition, our results also indicate that phenotypic response of brook charr (i.e. the proportion of each form in a given lake) is related to the intensity of this competition.     

Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs

Plants shaded by neighbors or overhead foliage experience both a reduction in the ratio of red to far red light (R:FR), a specific cue perceived by phytochrome, and reduced photosynthetically active radiation (PAR), an essential resource. We tested the adaptive value of plasticity to crowding and to the cue and resource components of foliage shade in the annual plant Arabidopsis thaliana by exposing 36 inbred families from four natural populations to four experimental treatments: (1) high density, full sun; (2) low density, full sun; (3) low density, neutral shade; and (4) low density, low R:FR-simulated foliage shade. Genotypic selection analysis within each treatment revealed strong environmental differences in selection on plastic life-history traits. We used specific contrasts to measure plasticity to density and foliage shade, to partition responses to foliage shade into phytochrome-mediated responses to the R:FR cue and responses to PAR, and to test whether plasticity was adaptive (i.e., in the same direction as selection in each environment). Contrary to expectation, we found no evidence for adaptive plasticity to density. However, we observed both adaptive and maladaptive responses to foliage shade. In general, phytochrome-mediated plasticity to the R:FR cue of foliage shade was adaptive and counteracted maladaptive growth responses to reduced PAR. These results support the prediction that active developmental responses to environmental cues are more likely to be adaptive than are passive resource-mediated responses. Multiple regression analysis detected a few costs of adaptive plasticity and adaptive homeostasis, but such costs were infrequent and their expression depended on the environment. Thus, costs of plasticity may occasionally constrain the evolution of adaptive responses to foliage shade in Arabidopsis, but this constraint may differ among environments and is far from ubiquitous.     

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.     

Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis

In both plants and animals vein networks play an essential role in transporting nutrients. In plants veins may also provide mechanical support. The mechanism by which vein patterns are formed in a developing leaf remains largely unresolved. According to the canalization hypothesis, a signal inducing vein differentiation is transported in a polar manner and is channeled into narrow strands. Since inhibition of auxin transport affects venation patterns, auxin is likely to be part of the signal involved. However, it is not clear whether the canalization hypothesis, initially formulated over 25 years ago, is compatible with recent experimental data. In this paper we focus on three aspects of this question, and show that: (i) canalization models can account for an acropetal development of the midvein if vein formation is sink-driven; (ii) canalization models are in agreement with venation patterns resulting from inhibited auxin transport and (iii) loops and discontinuous venation patterns can be obtained assuming proper spacing of discrete auxin sources.     

The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing

Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14-h and 10-h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June-dispersed seeds in RI, but only 4% in November-dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.