THE GENETICS OF PHENOTYPIC PLASTICITY. VIII. THE COST OF PLASTICITY IN DAPHNIA PULEX

In a heterogeneous world, the optimal strategy for an individual is to continually change its phenotype to match the optimal type. However, in the real world, organisms do not behave in this fashion. One potential reason why is that phenotypic plasticity is costly. We measured production and maintenance costs of plasticity in the freshwater crustacean Daphnia pulex (Cladocera: Crustacea) in response to the presence of chemical signals from a predator, the insect Chaoborus americanus. We looked at three changes in juvenile body size and shape: body length, body depth, and tailspine length. Fitness costs were measured as changes in adult growth and fecundity, and summarized as the intrinsic rate of increase (r) for individuals reared in the presence or absence of Chaoborus extract. The cost of plasticity was measured as a multiple regression of mean clone fitness against trait and trait plasticity. We found scant evidence for either production or maintenance costs of plasticity. We also failed to find direct costs of these juvenile structures, which is surprising, as others have found such costs. We attribute the lack of measurable direct or plasticity costs to a decrease in metabolic rates in the presence of the Chaoborus extract. This decrease in metabolic rate may have compensated for any cost increases. We call for more extensive measures of the costs of plasticity, especially under natural conditions, and the incorporation of costs into evolutionary models.     

The role of phenotypic plasticity in driving genetic evolution

Models of population divergence and speciation are often based on the assumption that differences between populations are due to genetic factors, and that phenotypic change is due to natural selection. It is equally plausible that some of the differences among populations are due to phenotypic plasticity. We use the metaphor of the adaptive landscape to review the role of phenotypic plasticity in driving genetic evolution. Moderate levels of phenotypic plasticity are optimal in permitting population survival in a new environment and in bringing populations into the realm of attraction of an adaptive peak. High levels of plasticity may increase the probability of population persistence but reduce the likelihood of genetic change, because the plastic response itself places the population close to a peak. Moderate levels of plasticity arise whenever multiple traits, some of which are plastic and others not, form a composite trait involved in the adaptive response. For example, altered behaviours may drive selection on morphology and physiology. Because there is likely to be a considerable element of chance in which behaviours become established, behavioural change followed by morphological and physiological evolution may be a potent force in driving evolution in novel directions. We assess the role of phenotypic plasticity in stimulating evolution by considering two examples from birds: (i) the evolution of red and yellow plumage coloration due to carotenoid consumption; and (ii) the evolution of foraging behaviours on islands. Phenotypic plasticity is widespread in nature and may speed up, slow down, or have little effect on evolutionary change. Moderate levels of plasticity may often facilitate genetic evolution but careful analyses of individual cases are needed to ascertain whether plasticity has been essential or merely incidental to population differentiation.     

Optimal reproductive allocation in annuals and an informational constraint on plasticity

In this computational study, we examined optimal reproductive allocation schedules in annual plants whose season lengths vary in predictability. We discuss relationships among season-length predictability, the form of the optimal allocation schedule, the degree of plasticity reflected in the optimal reaction norm, and the competitive consequences of plasticity and bet-hedging. We used an evolutionary algorithm to search the allocation-schedule space for optima, given different distributions of season length. The resulting schedules maximize geometric-mean fecundity under their selecting distributions. We then examined the relative fitness of these schedules in simulated competition among reaction norms optimized for different degrees of season-length predictability. Gradedness of optimal schedules decreases with increasing season-length predictability, and reaction norms comprising highly graded schedules reflect lesser plasticity than norms comprising schedules that are less graded. In simulations, competitively successful genotypes were those that reflected plasticity appropriate to the season-length predictability. Informational constraints in the form of low season-length predictability select for low plasticity and high bet-hedging in allocation. Because an environmental cue must mediate the relationship between environment and fitness, plasticity in reproductive allocation ought to be understood not as a direct response to the selective environment, but rather to cues that are correlated with relevant environmental parameters.     

Genetic correlation between temperature-induced plasticity of life-history traits in a soil arthropod

Temperature is considered one of the most important mediators of phenotypic plasticity in ectotherms. However, the costs and benefits shaping the evolution of different thermal responses are poorly elucidated. One of the possible constraints to phenotypic plasticity is its intrinsic genetic cost, such as genetic linkage or pleiotropy. Genetic coupling of the thermal response curves for different life history traits may significantly affect the evolution of thermal sensitivity in thermally fluctuating environments. We used the collembolan Orchesella cincta to study if there is genetic variation in temperature-induced phenotypic plasticity in life history traits, and if the degree of temperature-induced plasticity is correlated across traits. Egg development rate, juvenile growth rate and egg size of 19 inbred isofemale lines were measured at two temperatures. Our results show that temperature was a highly significant factor for all three traits. Egg development rate and juvenile growth rate increased with increasing temperature, while egg size decreased. Line by temperature interaction was significant for all traits tested; indicating that genetic variation for temperature-induced plasticity existed. The degree of plasticity was significantly positively correlated between egg development rate and growth rate, but plasticity in egg size was not correlated to the other two plasticity traits. The findings suggest that the thermal plasticities of egg development rate and growth rate are partly under the control of the same genes or genetic regions. Hence, evolution of the thermal plasticity of traits cannot be understood in isolation of the response of other traits. If traits have similar and additive effects on fitness, genetic coupling between these traits may well facilitate the evolution of optimal phenotypes. However, for this we need to know the selective forces under field conditions.     

Within-individual plasticity explains age-related decrease in stress response in a short-lived bird

A crucial problem for every organism is how to allocate energy between competing life-history components. The optimal allocation decision is often state-dependent and mediated by hormones. Here, we investigated how age, a major state variable affects individuals'' hormonal response to a standardized stressor: a trait that may reflect allocation between self-maintenance and reproduction. We caught free-living house sparrows and measured their hormonal (corticosterone) response to capture stress in consecutive years. Using a long-term ringing dataset, we determined the age of the birds, and we partitioned the variation into within- and among-individual age components to investigate the effects of plasticity versus selection or gene flow, respectively, on the stress response. We found large among-individual variation in the birds'' hormone profiles, but overall, birds responded less strongly to capture stress as they grew older. These results suggest that stress responsiveness is a plastic trait that may vary within individuals in an adaptive manner, and natural selection may act on the reaction norms producing optimal phenotypic response in the actual environment and life-history stage.     

植物的表型可塑性、异速生长及其入侵能力

表型可塑性是指同一个基因型对不同环境响应产生不同表型的特性,特定性状的可塑性本身可以遗传,也可以接受选择而发生进化。植物个体的异速生长是指生物体某一特征的相对生长速率不等于第二种特征的相对生长速率的特性,该特性是由物种的遗传性决定的一种固定特征,植物往往朝着最佳的异速生长曲线进化。植物特定基因型在不同环境下,诸如生物量分配和种群几何学上的一些表型差异,既可由异速生长造成,也可由表型可塑性造成。植物本身的异速生长是一种"外观可塑性",而异速生长曲线的改变才是真正的可塑性。植物的表型可塑性、异速生长对于入侵植物的适应具有重要意义。干扰等异质性生境下表型可塑性成为物种生存扩散的有利性状,表型可塑性强的物种更有可能成为广布种。植物本身的异速生长特性或其异速生长曲线的改变都能影响其入侵能力。     

Evolution of environmental cues for phenotypic plasticity

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

The alignment between phenotypic plasticity,the major axis of genetic variation and the response to selection

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.     

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

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

Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses

Phenotypic plasticity is a key factor for the success of organisms in heterogeneous environments. Although many forms of phenotypic plasticity can be induced and retracted repeatedly, few extant models have analyzed conditions for the evolution of reversible plasticity. We present a general model of reversible plasticity to examine how plastic shifts in the mode and breadth of environmental tolerance functions (that determine relative fitness) depend on time lags in response to environmental change, the pattern of individual exposure to inducing and noninducing environments, and the quality of available information about the environment. We couched the model in terms of prey-induced responses to variable predation regimes. With longer response lags relative to the rate of environmental change, the modes of tolerance functions in both the presence or absence of predators converge on a generalist strategy that lies intermediate between the optimal functions for the two environments in the absence of response lags. Incomplete information about the level of predation risk in inducing environments causes prey to have broader tolerance functions even at the cost of reduced maximal fitness. We give a detailed analysis of how these factors and interactions among them select for joint patterns of mode and breadth plasticity.     

Evolutionary Analyses of Morphological and Physiological Plasticity in Thermally Variable Environments

SYNOPSIS. Morphological and physiological plasticity is oftenthought to represent an adaptive response to variable environments.However, determining whether a given pattern of plasticity isin fact adaptive is analytically challenging, as is evaluatingthe degree of and limits to adaptive plasticity. Here we describea general methodological framework for studying the evolutionof plastic responses. This framework synthesizes recent analyticaladvances from both evolutionary ecology and functional biology,and it does so by integrating field experiments, functionaland physiological analyses, environmental data, and geneticstudies of plasticity. We argue that studies of plasticity inresponse to the thermal environment may be particularly valuablein understanding the role of environmental variation in theevolution of plasticity: not only can thermally-relevant traitsoften be mechanistically and physiologically linked to the thermalenvironment, but also the variability and predictability ofthe thermal environment itself can be quantified on ecologicallyrelevant time scales. We illustrate this approach by reviewinga case study of seasonal plasticity in the extent of wing melanizationin Western White Butterflies (Pontia occidentalis). This reviewdemonstrates that 1) wing melanin plasticity is heritable, 2)plasticity does increase fitness in nature, but the effect variesbetween seasons and between years, 3) selection on existingvariation in the magnitude of plasticity favors increased plasticityin one melanin trait that affects thermoregulation, but 4) themarked unpredictability of short-term (within-season) weatherpatterns substantially limits the capacity of plasticity tomatch optimal wing phenotypes to the weather conditions actuallyexperienced. We complement the above case study with a casualreview of selected aspects of thermal acclimation responses.The magnitude of thermal acclimation ("flexibility") is demonstrablymodest rather than fully compensatory. The magnitude of geneticvariation (crucial to evolutionary responses to selection) inthermal acclimation responses has been investigated in onlya few species to date. In conclusion, we suggest that an understandingof selection and evolution of thermal acclimation will be enhancedby experimental examinations of mechanistic links between traitsand environments, of the physiological bases and functionalconsequences of acclimation, of patterns of environmental variabilityand predictability, of the fitness consequences of acclimationin nature, and of potential genetic constraints.     

Pre- and postsynaptically expressed spike-timing-dependent plasticity contribute differentially to neuronal learning

A plethora of experimental studies have shown that long-term synaptic plasticity can be expressed pre- or postsynaptically depending on a range of factors such as developmental stage, synapse type, and activity patterns. The functional consequences of this diversity are not clear, although it is understood that whereas postsynaptic expression of plasticity predominantly affects synaptic response amplitude, presynaptic expression alters both synaptic response amplitude and short-term dynamics. In most models of neuronal learning, long-term synaptic plasticity is implemented as changes in connective weights. The consideration of long-term plasticity as a fixed change in amplitude corresponds more closely to post- than to presynaptic expression, which means theoretical outcomes based on this choice of implementation may have a postsynaptic bias. To explore the functional implications of the diversity of expression of long-term synaptic plasticity, we adapted a model of long-term plasticity, more specifically spike-timing-dependent plasticity (STDP), such that it was expressed either independently pre- or postsynaptically, or in a mixture of both ways. We compared pair-based standard STDP models and a biologically tuned triplet STDP model, and investigated the outcomes in a minimal setting, using two different learning schemes: in the first, inputs were triggered at different latencies, and in the second a subset of inputs were temporally correlated. We found that presynaptic changes adjusted the speed of learning, while postsynaptic expression was more efficient at regulating spike timing and frequency. When combining both expression loci, postsynaptic changes amplified the response range, while presynaptic plasticity allowed control over postsynaptic firing rates, potentially providing a form of activity homeostasis. Our findings highlight how the seemingly innocuous choice of implementing synaptic plasticity by single weight modification may unwittingly introduce a postsynaptic bias in modelling outcomes. We conclude that pre- and postsynaptically expressed plasticity are not interchangeable, but enable complimentary functions.     

Effects of resource level and habitat type on behavioral and morphological plasticity in Eurasian perch

Spatial and temporal heterogeneity in the environment is a common feature affecting many natural populations. For example, both the resource levels and optimal habitat choices of individuals likely change over time. One way for organisms to cope with environmental variation is to display adaptive plasticity in traits such as behavior and morphology. Since trait plasticity is hypothesized to be a prerequisite for character divergence, studies of mechanisms behind such plasticity are warranted. In this study, we looked at the interaction of two potentially important environmental variables on behavioral and morphological plasticity in Eurasian perch (Perca fluviatilis L.). More specifically, the plastic responses in activity and morphology of perch exposed to different resource levels and simulated habitat types were studied in an aquarium experiment. The resource level experienced had a large influence on plasticity in both activity and morphology. Behavioral adaptations have been thought to mediate morphological transitions, and we suggest that the morphological response to the resource level was mediated by differences in activity and growth rates. The habitat type also affected morphological plasticity but to a lesser extent, and there was no effect on activity from habitat type. Based on these results, we suggest that it is essential to include several environmental factors acting in concert when studying mechanisms behind trait plasticity. We also propose that variation in resource levels might play a key role in fostering trait plasticity in at least fish populations, while other environmental variables such as divergent habitat complexities and prey types might be less influential. Dynamics in resource levels and optimal habitat choices might thus be important factors influencing character divergence in natural populations.     

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.     

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity''s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.     

Simulated herbivory does not constrain phenotypic plasticity to shade through ontogeny in a relict tree

Ecological limits to phenotypic plasticity (PP), induced by simultaneous biotic and abiotic factors, can prevent organisms from exhibiting optimal plasticity, and in turn lead to decreased fitness. Herbivory is an important biotic stressor and may limit plant functional responses to challenging environmental conditions such as shading. In this study we investigated whether plant functional responses and PP to shade are constrained by herbivory, and whether such constraints are due to direct effects based on resource limitation by considering ontogeny. We used as a model system the relict tree Prunus lusitanica and implemented an indoor experiment to quantify the response of saplings of different ages to shade and herbivory. We measured five functional traits and quantitatively calculated PP. Results showed that herbivory did not constrain functional responses or PP to shade except for shoot:root ratio (SR), which, despite showing a high PP in damaged saplings, decreased under shade instead of increasing. Damaged saplings of older age did not exhibit reduced constraints on functional responses to shade and generally presented a lower PP than damaged saplings of younger age. Our findings suggest that herbivory‐mediated constraints on plant plasticity to shade may not be as widespread as previously thought. Nonetheless, the negative effect of herbivory on SR plastic expression to shade could be detrimental for plant fitness. Finally, our results suggest a secondary role of direct effects (resource‐based) on P. lusitanica plasticity limitation. Further studies should quantify plant resources in order to gain a better understanding of this seldom‐explored subject.     

Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations

Adaptive phenotypic plasticity in the form of capacity to accelerate development as a response to pond drying risk is known from many amphibian species. However, very little is known about factors that might constrain the evolution of this type of plasticity, and few studies have explored to what degree plasticity might be constrained by trade-offs dictated by adaptation to different environmental conditions. We compared the ability of southern and northern Scandinavian common frog (Rana temporaria) larvae originating from 10 different populations to accelerate their development in response to simulated pond drying risk and the resulting costs in metamorphic size in a factorial laboratory experiment. We found that (i) northern larvae developed faster than the southern larvae in all treatments, (ii) a capacity to accelerate the response was present in all five southern and all five northern populations tested, but that the magnitude of the response was much larger (and less variable) in the southern than in the northern populations, and that (iii) significant plasticity costs in metamorphic size were present in the southern populations, the plastic genotypes having smaller metamorphic size in the absence of desiccation risk, but no evidence for plasticity costs was found in the northern populations. We suggest that the weaker response to pond drying risk in the northern populations is due to stronger selection on large metamorphic size as compared with southern populations. In other words, seasonal time constraints that have selected the northern larvae to be fast growing and developing, may also constrain their innate ability for adaptive phenotypic plasticity.     

Rapid evolution of thermal plasticity in mountain lake Daphnia populations

Populations at risk of extinction due to climate change may be rescued by adaptive evolution or plasticity. Selective agents, such as introduced predators, may enhance or constrain plastic or adaptive responses to temperature. We tested responses of Daphnia to temperature by collecting populations from lakes across an elevational gradient in the presence and absence of fish predators (long‐term selection). We subsequently grew these populations at two elevations in field mesocosms over two years (short‐term selection), followed by a common‐garden experiment at two temperatures in the lab to measure life‐history traits. Both long‐term and short‐term selection affected traits, suggesting that genetic variation of plasticity within populations enabled individuals to rapidly evolve plasticity in response to high temperature. We found that short‐term selection by high temperature increased plasticity for growth rate in all populations. Fecundity was higher in populations from fishless lakes and body size showed greater plasticity in populations from warm lakes (long‐term selection). Neither body size nor fecundity were affected by short‐term thermal selection. These results demonstrate that plasticity is an important component of the life‐history response of Daphnia, and that genetic variation within populations enabled rapid evolution of plasticity in response to selection by temperature.     

The evolutionary ecology of individual phenotypic plasticity in wild populations

The ability of individual organisms to alter morphological and life-history traits in response to the conditions they experience is an example of phenotypic plasticity which is fundamental to any population's ability to deal with short-term environmental change. We currently know little about the prevalence, and evolutionary and ecological causes and consequences of variation in life history plasticity in the wild. Here we outline an analytical framework, utilizing the reaction norm concept and random regression statistical models, to assess the between-individual variation in life history plasticity that may underlie population level responses to the environment at both phenotypic and genetic levels. We discuss applications of this framework to date in wild vertebrate populations, and illustrate how natural selection and ecological constraint may alter a population's response to the environment through their effects at the individual level. Finally, we present future directions and challenges for research into individual plasticity.     

Metapopulation structure favors plasticity over local adaptation

We describe a model for the evolutionary consequences of plasticity in an environmentally heterogeneous metapopulation in which specialists for each of two alternative environments and one plastic type are initially present. The model is similar to that proposed by Moran (1992) but extends her work to two sites. We show that with migration between sites the plastic type is favored over local specialists across a broad range of parameter space. The plastic type may dominate or be fixed even in an environmentally uniform site, and even if the plasticity has imperfect accuracy or bears some cost such that a local specialist has higher fitness in that site, as long as there is some migration between sites with different distributions of environmental states. These results suggest that differences among taxa in dispersal and hence realized migration rates may play a heretofore unrecognized role in their patterns of adaptive population differentiation. Migration relaxes the thresholds for both environmental heterogeneity and accuracy of plastic response above which plasticity is favored. Furthermore, small changes in response accuracy can dramatically and abruptly alter the evolutionary outcome in the metapopulation. A fitness cost to plasticity will substantially reduce the range of conditions in which the plastic type will prevail only if the cost is both large and global rather than environment specific.