Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles

Costs of phenotypic plasticity are important for the evolution of plasticity because they prevent organisms from shaping themselves at will to match heterogeneous environments. These costs occur when plastic genotypes have relatively low fitness regardless of the trait value expressed. We report two experiments in which we measured selection on predator-induced plasticity in the behaviour and external morphology of frog tadpoles (Rana temporaria). We assessed costs under stressful and benign conditions, measured fitness as larval growth rate or competitive ability and focused analysis on aggregate measures of whole-organism plasticity. There was little convincing evidence for a cost of phenotypic plasticity in our experiments, and costs of canalization were nearly as frequent as costs of plasticity. Neither the magnitude of the cost nor the variation around the estimate (detectability) was sensitive to environmental stress.     

Promising directions in plant phenotypic plasticity

A research agenda for the next phase of plasticity studies calls for contributions from a diverse group of biologists, working both independently and collaboratively, to pursue four promising directions: examining dynamic, anatomical/architectural, and cross-generational plasticity along with simpler growth traits; carefully assessing the adaptive significance of those plasticity patterns; investigating the intricate transduction pathways that lead from environmental signal to phenotypic response; and considering the rich environmental context of natural systems. Progress in these areas will allow us to address broad and timely questions regarding the ecological and evolutionary significance of plasticity and the nature of phenotypic determination.     

The shape of things to come: linking developmental plasticity to post‐metamorphic morphology in anurans

Development consists of growth and differentiation, which can be partially decoupled and can be affected by environmental factors to different extents. In amphibians, variation in the larval environment influences development and causes changes in post‐metamorphic shape. We examined post‐metamorphic consequences, both morphological and locomotory, of alterations in growth and development. We reared tadpoles of two phylogenetically and ecologically distant frog species (the red‐eyed treefrog Agalychnis callidryas and the African clawed frog Xenopus laevis) under different temperatures with ad libitum food supply and under different food levels at a constant temperature. Low temperature and low food levels both resulted in similarly extended larval periods. However, low temperature yielded relatively long‐legged frogs with a lower degree of ossification than warm temperature, whereas low food yielded relatively short‐legged frogs with a higher degree of ossification than high food levels. Such allometric differences had no effect on locomotor performance of juveniles. Our results provide a basis for understanding the relationship between growth, differentiation and post‐metamorphic shape in anurans and help explain many of the discrepancies reported in previous studies.     

Brain plasticity over the metamorphic boundary: carry-over effect of larval environment on froglet brain development

Brain development shows high plasticity in response to environmental heterogeneity. However, it is unknown how environmental variation during development may affect brain architecture across life history switch points in species with complex life cycles. Previously, we showed that predation and competition affect brain development in common frog (Rana temporaria) tadpoles. Here, we studied whether larval environment had carry-over effects in brains of metamorphs. Tadpoles grown at high density had large optic tecta at metamorphosis, whereas tadpoles grown under predation risk had small diencephala. We found that larval density had a carry-over effect on froglet optic tectum size, whereas the effect of larval predation risk had vanished by metamorphosis. We discuss the possibility that the observed changes may be adaptive, reflecting the needs of an organism in given environmental and developmental contexts.     

The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics

We model the evolution of reaction norms focusing on three aspects: frequency-dependent selection arising from resource competition, maintenance and production costs of phenotypic plasticity, and three characteristics of environmental heterogeneity (frequency of environments, their intrinsic carrying capacity and the sensitivity to phenotypic maladaptation in these environments). We show that (i) reaction norms evolve so as to trade adaptation for acquiring resources against cost avoidance; (ii) maintenance costs cause reaction norms to better adapt to frequent rather than to infrequent environments, whereas production costs do not; and (iii) evolved reaction norms confer better adaptation to environments with low rather than with high intrinsic carrying capacity. The two previous findings contradict earlier theoretical results and originate from two previously unexplored features that are included in our model. First, production costs of phenotypic plasticity are only incurred when a given phenotype is actually produced. Therefore, they are proportional to the frequency of environments, and these frequencies thus affect the selection pressure to avoid costs just as much as the selection pressure to improve adaptation. This prevents the frequency of environments from affecting the evolving reaction norm. Secondly, our model describes the evolution of plasticity for a phenotype determining an individual's capability to acquire resources, and thus its realized carrying capacity. When individuals are distributed randomly across environments, they cannot avoid experiencing environments with intrinsically low carrying capacity. As selection pressures arising from the need to improve adaptation are stronger under such extreme conditions than under mild ones, better adaptation to environments with low rather than with high intrinsic carrying capacity results.     

Life-history evolution in spatially heterogeneous environments,with and without phenotypic plasticity

Summary The formulation of Kawecki and Stearns (1993) adapted for sexual populations is used to characterize lifehistory evolution in spatially heterogeneous environments comprising a number of distinct habitats. Three types of evolutionary outcome/optimal strategy are distinguished, appertaining to populations with phenotypic plasticity, populations without it (here called aplastic) and to populations that are reproductively isolated. In general plastic and isolated optima differ, but do not differ if none of the habitats provide source or sink populations. Plastic, aplastic and isolated optima are calculated and compared in three numerical examples representing trade-offs involving reproductive effort, egg size and defence. Locating the aplastic optimum involves numerical construction of a fitness landscape showing how allelic fitness depends on aplastic strategy and on the relative frequencies of the habitats. In all three examples the aplastic optimum lies between or almost between the plastic optima. In two cases the aplastic optimum switches abruptly between the plastic optima as the relative frequencies of the habitats change, and in the third case the switch is gradual. The abruptness or otherwise of the switch depends on the position and structure of the valleys in the fitness landscape and this in turn depends on how sharply the fitness peaks are differentiated.     

The effect of phenotypic plasticity on evolution in multipeaked fitness landscapes

When facing the challenge of developing an individual that best fits its environment, nature demonstrates an interesting combination of two fundamentally different adaptive mechanisms: genetic evolution and phenotypic plasticity. Following numerous computational models, it has become the accepted wisdom that lifetime acclimation (e.g. via learning) smooths the fitness landscape and consequently accelerates evolution. However, analytical studies, focusing on the effect of phenotypic plasticity on evolution in simple unimodal landscapes, have often found that learning hinders the evolutionary process rather than accelerating it. Here, we provide a general framework for studying the effect of plasticity on evolution in multipeaked landscapes and introduce a rigorous mathematical analysis of these dynamics. We show that the convergence rate of the evolutionary process in a given arbitrary one-dimensional fitness landscape is dominated by the largest descent (drawdown) in the landscape and provide numerical evidence to support an analogous dominance also in multidimensional landscapes. We consider several schemes of phenotypic plasticity and examine their effect on the landscape drawdown, identifying the conditions under which phenotypic plasticity is advantageous. The lack of such a drawdown in unimodal landscapes vs. its dominance in multipeaked landscapes accounts for the seemingly contradictory findings of previous studies.     

Evolutionary reduction of developmental plasticity in desert spadefoot toads

Organisms vary their rates of growth and development in response to environmental inputs. Such developmental plasticity may be adaptive and positively correlate with environmental heterogeneity. However, the evolution of developmental plasticity among closely related taxa is not well understood. To determine the evolutionary pattern of plasticity, we compared plasticity in time to and size at metamorphosis in response to water desiccation in tadpoles among spadefoot species that differ in breeding pond and larval period durations. Like most tadpoles, spadefoot tadpoles possess the remarkable ability to accelerate development in response to pond drying to avoid desiccation. Here, we hypothesize that desert spadefoot tadpoles have evolved reduced plasticity to avoid desiccation in ephemeral desert pools compared to their nondesert relatives that breed in long-duration ponds. We recorded time to and size at metamorphosis following experimental manipulation of water levels and found that desert-adapted species had much less plasticity in larval period and size at metamorphosis than nondesert species, which retain the hypothetical ancestral state of plasticity. Furthermore, we observed a correlation between degree of plasticity and fat body content that may provide mechanistic insights into the evolution of developmental plasticity in amphibians.     

Predation- and competition-mediated brain plasticity in Rana temporaria tadpoles

An increasing number of studies have demonstrated phenotypic plasticity in brain size and architecture in response to environmental variation. However, our knowledge on how brain architecture is affected by commonplace ecological interactions is rudimentary. For example, while intraspecific competition and risk of predation are known to induce adaptive plastic modifications in morphology and behaviour in a wide variety of organisms, their effects on brain development have not been studied. We studied experimentally the influence of density and predation risk on brain development in common frog (Rana temporaria) tadpoles. Tadpoles grown at low density and under predation risk developed smaller brains than tadpoles at the other treatment combinations. Further, at high densities, tadpoles developed larger optic tecta and smaller medulla oblongata than those grown at low densities. These results demonstrate that ecological interactions - like intraspecific competition and predation risk - can have strong effects on brain development in lower vertebrates.     

How stress selects for reversible phenotypic plasticity

Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays. The selective advantage of genotypes that are able to produce adaptive reversible plastic phenotypes is calculated by using the concept of environmental tolerance. Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non-induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions.     

Effects of inbreeding on phenotypic plasticity in cultivated Phlox

Summary Inbreeding is known to increase developmental instability in outbreeding plants, and it has been argued that phenotypic plasticity in response to environmental variation might be similarly affected. To investigate whether phenotypic plasticity is altered by inbreeding, an outcrossed group and three successive generations of inbred cultivated Phlox drummondii were grown in six different treatments (Control, Low Water, Low Nutrient, Early and Late Leaf Removal, and Small Pots). Twelve plant characters were measured to determine the effects of the treatments and inbreeding. For those characters where inbreeding level by treatment interaction was indicated, the amounts and patterns of plasticity were examined to determine the source of the interaction. Despite substantial evidence for inbreeding depression of plant vigor and fecundity, there was no indication of an increase in the amount of phenotypic plasticity with progressive inbreeding. There was also no evidence that inbreeding systematically disrupts the pattern of plastic response to the environment.     

Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi

1. The exotic cladoceran Daphnia lumholtzi has recently invaded freshwater systems throughout the United States. Daphnia lumholtzi possesses extravagant head spines that are longer than those found on any other North American Daphnia. These spines are effective at reducing predation from many of the predators that are native to newly invaded habitats; however, they are plastic both in nature and in laboratory cultures. The purpose of this experiment was to better understand what environmental cues induce and maintain these effective predator‐deterrent spines. We conducted life‐table experiments on individual D. lumholtzi grown in water conditioned with an invertebrate insect predator, Chaoborus punctipennis, and water conditioned with a vertebrate fish predator, Lepomis macrochirus. 2. Daphnia lumholtzi exhibited morphological plasticity in response to kairomones released by both predators. However, direct exposure to predator kairomones during postembryonic development did not induce long spines in D. lumholtzi. In contrast, neonates produced from individuals exposed to Lepomis kairomones had significantly longer head and tail spines than neonates produced from control and Chaoborus individuals. These results suggest that there may be a maternal, or pre‐embryonic, effect of kairomone exposure on spine development in D. lumholtzi. 3. Independent of these morphological shifts, D. lumholtzi also exhibited plasticity in life history characteristics in response to predator kairomones. For example, D. lumholtzi exhibited delayed reproduction in response to Chaoborus kairomones, and significantly more individuals produced resting eggs, or ephippia, in the presence of Lepomis kairomones.     

Constraints on the evolution of adaptive phenotypic plasticity in plants

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

The genetics of phenotypic plasticity I. Heritability

Methods for estimating the genetic component of phenotypic plasticity are presented. In the general case of clonal replicates or full-sibs raised in several environments, the heritability of plasticity can be measured as the ratio of the genotype-environment interaction variance to the total phenotypic variance. In the special case of only two environments plasticity also can be measured as the difference among environments in genotype or family means. In that case, the heritability of plasticity can be measured as either a ratio of variance components or as the slope of a parent-offspring regression. The general measure suffers because no least-square standard errors have been developed, although they can be calculated by maximum-likelihood or bootstrapping techniques. For the other two methods least-square standard errors can be calculated but require very large experiments for statistical significance to be achieved. The heritability measures are compared using data on plasticity of thorax size in response to temperature in Drosophila melanogaster. The heritability estimates are all in close agreement. Models of the evolution of phenotypic plasticity have treated it as a trait in its own right and as a cross-environment genetic correlation. Although the first approach is the one used here, neither one is preferred.     

Correlated response in plasticity to selection for early flowering in Arabidopsis thaliana

Phenotypic plasticity is an important strategy for coping with changing environments. However, environmental change usually results in strong directional selection, and little is known empirically about how this affects plasticity. If genes affecting a trait value also affect its plasticity, selection on the trait should influence plasticity. Synthetic outbred populations of Arabidopsis thaliana were selected for earlier flowering under simulated spring- and winter-annual conditions to investigate the correlated response of flowering time plasticity and its effect on family-by-environment variance (Vg×e) within each selected line. We found that selection affected plasticity in an environmentally dependent manner: under simulated spring-annual conditions, selection increased the magnitude of plastic response but decreased Vg×e; selection under simulated winter-annual conditions reduced the magnitude of plastic response but did not alter Vg×e significantly. As selection may constrain future response to environmental change, the environment for crop breeding and ex situ conservation programmes should be carefully chosen. Models of species persistence under environmental change should also consider the interaction between selection and plasticity.     

A modular concept of phenotypic plasticity in plants

Based on empirical evidence from the literature we propose that, in nature, phenotypic plasticity in plants is usually expressed at a subindividual level. While reaction norms (i.e. the type and the degree of plant responses to environmental variation) are a property of genotypes, they are expressed at the level of modular subunits in most plants. We thus contend that phenotypic plasticity is not a whole-plant response, but a property of individual meristems, leaves, branches and roots, triggered by local environmental conditions. Communication and behavioural integration of interconnected modules can change the local responses in different ways: it may enhance or diminish local plastic effects, thereby increasing or decreasing the differences between integrated modules exposed to different conditions. Modular integration can also induce qualitatively different responses, which are not expressed if all modules experience the same conditions. We propose that the response of a plant to its environment is the sum of all modular responses to their local conditions plus all interaction effects that are due to integration. The local response rules to environmental variation, and the modular interaction rules may be seen as evolving traits targeted by natural selection. Following this notion, whole-plant reaction norms are an integrative by-product of modular plasticity, which has far-reaching methodological, ecological and evolutionary implications.