Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis

Plants possess a remarkable capacity to alter their phenotype in response to the highly heterogeneous light conditions they commonly encounter in natural environments. In the present study with the weedy annual plant Sinapis arvensis, we (a) tested for the adaptive value of phenotypic plasticity in morphological and life history traits in response to low light and (b) explored possible fitness costs of plasticity. Replicates of 31 half-sib families were grown individually in the greenhouse under full light and under low light (40% of ambient) imposed by neutral shade cloth. Low light resulted in a large increase in hypocotyl length and specific leaf area (SLA), a reduction in juvenile biomass and a delayed onset of flowering. Phenotypic selection analysis within each light environment revealed that selection favoured large SLA under low light, but not under high light, suggesting that the observed increase in SLA was adaptive. In contrast, plasticity in the other traits measured was maladaptive (i.e. in the opposite direction to that favoured by selection in the low light environment). We detected significant additive genetic variance in plasticity in most phenotypic traits and in fitness (number of seeds). Using genotypic selection gradient analysis, we found that families with high plasticity in SLA had a lower fitness than families with low plasticity, when the effect of SLA on fitness was statistically kept constant. This indicates that plasticity in SLA incurred a direct fitness cost. However, a cost of plasticity was only expressed under low light, but not under high light. Thus, models on the evolution of phenotypic plasticity will need to incorporate plasticity costs that vary in magnitude depending on environmental conditions.     

DEVELOPMENTAL INSTABILITY IS GENETICALLY CORRELATED WITH PHENOTYPIC PLASTICITY,CONSTRAINING HERITABILITY,AND FITNESS

Although adaptive plasticity would seem always to be favored by selection, it occurs less often than expected. This lack of ubiquity suggests that there must be trade‐offs, costs, or limitations associated with plasticity. Yet, few costs have been found. We explore one type of limitation, a correlation between plasticity and developmental instability, and use quantitative genetic theory to show why one should expect a genetic correlation. We test that hypothesis using the Landsberg erecta × Cape Verde Islands recombinant inbred lines (RILs) of Arabidopsis thaliana. RILs were grown at four different nitrogen (N) supply levels that span the range of N availabilities previously documented in North American field populations. We found a significant multivariate relationship between the cross‐environment trait plasticity and the within‐environment, within‐RIL developmental instability across 13 traits. This genetic covariation between plasticity and developmental instability has two costs. First, theory predicts diminished fitness for highly plastic lines under stabilizing selection, because their developmental instability and variance around the optimum phenotype will be greater compared to nonplastic genotypes. Second, empirically the most plastic traits exhibited heritabilities reduced by 57% on average compared to nonplastic traits. This demonstration of potential costs in inclusive fitness and heritability provoke a rethinking of the evolutionary role of plasticity.     

Costs and limits of phenotypic plasticity: Tests with predator-induced morphology and life history in a freshwater snail

Potential constraints on the evolution of phenotypic plasticity were tested using data from a previous study on predator-induced morphology and life history in the freshwater snail Physa heterostropha. The benefit of plasticity can be reduced if facultative development is associated with energetic costs, developmental instability, or an impaired developmental range. I examined plasticity in two traits for 29 families of P. heterostropha to see if it was associated with growth rate or fecundity, within-family phenotypic variance, or the potential to produce extreme phenotypes. Support was found for only one of the potential constraints. There was a strong negative selection gradient for growth rate associated with plasticity in shell shape (β = ?0.3, P < 0.0001). This result was attributed to a genetic correlation between morphological plasticity and an antipredator behavior that restricts feeding. Thus, reduced growth associated with morphological plasticity may have had unmeasured fitness benefits. The growth reduction, therefore, is equivocal as a cost of plasticity. Using different fitness components (e.g., survival, fecundity, growth) to seek constraints on plasticity will yield different results in selection gradient analyses. Procedural and conceptual issues related to tests for costs and limits of plasticity are discussed, such as whether constraints on plasticity will be evolutionarily ephemeral and difficult to detect in nature.     

Adaptive explanations for sensitive windows in development

Development in many organisms appears to show evidence of sensitive windows—periods or stages in ontogeny in which individual experience has a particularly strong influence on the phenotype (compared to other periods or stages). Despite great interest in sensitive windows from both fundamental and applied perspectives, the functional (adaptive) reasons why they have evolved are unclear. Here we outline a conceptual framework for understanding when natural selection should favour changes in plasticity across development. Our approach builds on previous theory on the evolution of phenotypic plasticity, which relates individual and population differences in plasticity to two factors: the degree of uncertainty about the environmental conditions and the extent to which experiences during development (‘cues’) provide information about those conditions. We argue that systematic variation in these two factors often occurs within the lifetime of a single individual, which will select for developmental changes in plasticity. Of central importance is how informational properties of the environment interact with the life history of the organism. Phenotypes may be more or less sensitive to environmental cues at different points in development because of systematic changes in (i) the frequency of cues, (ii) the informativeness of cues, (iii) the fitness benefits of information and/or (iv) the constraints on plasticity. In relatively stable environments, a sensible null expectation is that plasticity will gradually decline with age as the developing individual gathers information. We review recent models on the evolution of developmental changes in plasticity and explain how they fit into our conceptual framework. Our aim is to encourage an adaptive perspective on sensitive windows in development.     

Phenotypic plasticity as a component of evolutionary change

Phenotypic plasticity has often been assumed to buffer the effects of natural selection and thus act as a constraint on evolutionary change. It has become increasingly clear, however, that phenotypic plasticity actually represents a fundamental component of evolutionary change. Where genetic variation for plasticity exists, a population with a different mean plasticity can evolve. Recent attention has been focused on the conditions necessary for the evolution of phenotypic plasticity, i.e. those under which a generalist strategy, as opposed to a range of genetically differentiated specialists, will be favoured. It is also now clear that genotypes that perform best in one environment usually perform less well than other genotypes in a different environment; hence, their greater response is not an adaptation to environmental variation. A response to environmental variation is only adaptive if it represents a mechanism by which relative fitness is maintained in the face of environmental variation. Adaptive plasticity may thus involve both physiological homeostasis and morphological response.     

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.     

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

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

Symmetric competition as a general model for single-species adaptive dynamics

Adaptive dynamics is a widely used framework for modeling long-term evolution of continuous phenotypes. It is based on invasion fitness functions, which determine selection gradients and the canonical equation of adaptive dynamics. Even though the derivation of the adaptive dynamics from a given invasion fitness function is general and model-independent, the derivation of the invasion fitness function itself requires specification of an underlying ecological model. Therefore, evolutionary insights gained from adaptive dynamics models are generally model-dependent. Logistic models for symmetric, frequency-dependent competition are widely used in this context. Such models have the property that the selection gradients derived from them are gradients of scalar functions, which reflects a certain gradient property of the corresponding invasion fitness function. We show that any adaptive dynamics model that is based on an invasion fitness functions with this gradient property can be transformed into a generalized symmetric competition model. This provides a precise delineation of the generality of results derived from competition models. Roughly speaking, to understand the adaptive dynamics of the class of models satisfying a certain gradient condition, one only needs a complete understanding of the adaptive dynamics of symmetric, frequency-dependent competition. We show how this result can be applied to number of basic issues in evolutionary theory.     

Genetic variation and plasticity of Plantago coronopus under saline conditions

Phenotypic plasticity may allow organisms to cope with variation in the environmental conditions they encounter in their natural habitats. Salt adaptation appears to be an excellent example of such a plastic response. Many plant species accumulate organic solutes in response to saline conditions. Comparative and molecular studies suggest that this is an adaptation to osmotic stress. However, evidence relating the physiological responses to fitness parameters is rare and requires assessing the potential costs and benefits of plasticity. We studied the response of thirty families derived from plants collected in three populations of Plantago coronopus in a greenhouse experiment under saline and non-saline conditions. We indeed found a positive selection gradient for the sorbitol percentage under saline conditions: plant families with a higher proportion of sorbitol produced more spikes. No effects of sorbitol on fitness parameters were found under non-saline conditions.Populations also differed genetically in leaf number, spike number, sorbitol concentration and percentages of different soluble sugars. Salt treatment led to a reduction of vegetative biomass and spike production but increased leaf dry matter percentage and leaf thickness. Both under saline and non-saline conditions there was a negative trade-off between vegetative growth and reproduction. Families with a high plasticity in leaf thickness had a lower total spike length under non-saline conditions. This would imply that natural selection under predominantly non-saline conditions would lead to a decrease in the ability to change leaf morphology in response to exposure to salt. All other tests revealed no indication for any costs of plasticity to saline conditions.     

GENOTYPE-ENVIRONMENT INTERACTION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY

Studies of spatial variation in the environment have primarily focused on how genetic variation can be maintained. Many one-locus genetic models have addressed this issue, but, for several reasons, these models are not directly applicable to quantitative (polygenic) traits. One reason is that for continuously varying characters, the evolution of the mean phenotype expressed in different environments (the norm of reaction) is also of interest. Our quantitative genetic models describe the evolution of phenotypic response to the environment, also known as phenotypic plasticity (Gause, 1947), and illustrate how the norm of reaction (Schmalhausen, 1949) can be shaped by selection. These models utilize the statistical relationship which exists between genotype-environment interaction and genetic correlation to describe evolution of the mean phenotype under soft and hard selection in coarse-grained environments. Just as genetic correlations among characters within a single environment can constrain the response to simultaneous selection, so can a genetic correlation between states of a character which are expressed in two environments. Unless the genetic correlation across environments is ± 1, polygenic variation is exhausted, or there is a cost to plasticity, panmictic populations under a bivariate fitness function will eventually attain the optimum mean phenotype for a given character in each environment. However, very high positive or negative correlations can substantially slow the rate of evolution and may produce temporary maladaptation in one environment before the optimum joint phenotype is finally attained. Evolutionary trajectories under hard and soft selection can differ: in hard selection, the environments with the highest initial mean fitness contribute most individuals to the mating pool. In both hard and soft selection, evolution toward the optimum in a rare environment is much slower than it is in a common one. A subdivided population model reveals that migration restriction can facilitate local adaptation. However, unless there is no migration or one of the special cases discussed for panmictic populations holds, no geographical variation in the norm of reaction will be maintained at equilibrium. Implications of these results for the interpretation of spatial patterns of phenotypic variation in natural populations are discussed.     

Seasonal variation in basal and plastic cold tolerance: Adaptation is influenced by both long‐ and short‐term phenotypic plasticity

Understanding how thermal selection affects phenotypic distributions across different time scales will allow us to predict the effect of climate change on the fitness of ectotherms. We tested how seasonal temperature variation affects basal levels of cold tolerance and two types of phenotypic plasticity in Drosophila melanogaster. Developmental acclimation occurs as developmental stages of an organism are exposed to seasonal changes in temperature and its effect is irreversible, while reversible short‐term acclimation occurs daily in response to diurnal changes in temperature. We collected wild flies from a temperate population across seasons and measured two cold tolerance metrics (chill‐coma recovery and cold stress survival) and their responses to developmental and short‐term acclimation. Chill‐coma recovery responded to seasonal shifts in temperature, and phenotypic plasticity following both short‐term and developmental acclimation improved cold tolerance. This improvement indicated that both types of plasticity are adaptive, and that plasticity can compensate for genetic variation in basal cold tolerance during warmer parts of the season when flies tend to be less cold tolerant. We also observed a significantly stronger trade‐off between basal cold tolerance and short‐term acclimation during warmer months. For the longer‐term developmental acclimation, a trade‐off persisted regardless of season. A relationship between the two types of plasticity may provide additional insight into why some measures of thermal tolerance are more sensitive to seasonal variation than others.     

Developmental plasticity and the origin of novel forms: unveiling cryptic genetic variation via "use and disuse"

Natural selection eliminates phenotypic variation from populations, generation after generation-an observation that haunted Darwin. So, how does new phenotypic variation arise, and is it always random with respect to fitness? Repeated behavioral responses to a novel environment-particularly those that are learned-are typically advantageous. If those behaviors yield more extreme or novel morphological variants via developmental plasticity, then previously cryptic genetic variation may be exposed to natural selection. Significantly, because the mean phenotypic effect of "use and disuse" is also typically favorable, previously cryptic genetic variation can be transformed into phenotypic variation that is both visible to selection and biased in an adaptive direction. Therefore, use-induced developmental plasticity in a very real sense "creates" new phenotypic variation that is nonrandom with respect to fitness, in contrast to the random phenotypic effects of mutation, recombination, and "direct effects" of environment (stress, nutrition). I offer here (a) a brief review of the immense literature on the effects of "use and disuse" on morphology, (b) a simple yet general model illustrating how cryptic genetic variation may be exposed to selection by developmentally plastic responses that alter trait performance in response to "use and disuse," and (c) a more detailed model of a positive feedback loop between learning (handed behavior) and morphological plasticity (use-induced morphological asymmetry) that may rapidly generate novel phenotypic variation and facilitate the evolution of conspicuous morphological asymmetries. Evidence from several sources suggests that handed behaviors played an important role both in the origin of novel forms (asymmetries) and in their subsequent evolution.     

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.     

Habitat change and the scale of habitat selection: shifting gradients used by coexisting Arctic rodents

The conservation and understanding of biodiversity requires development and testing of models that illustrate how climate change and other anthropogenic effects alter habitat and its selection at different spatial scales. Models of fitness along a habitat gradient illustrate the connection between fine‐scale variation in fitness and the selection of habitat as discontinuous patches in the landscape. According to these models, climate change can increase fitness values of static habitats, shift the fitness value of habitat patches along underlying gradients of habitat quality, or alter both fitness and habitat quality. It should be possible to differentiate amongst these scenarios by associating differences in the abundance and distribution of species with metrics of habitat that document the gradient while controlling for changes in density at larger scales of analysis. Comparisons of habitat selection by two species of lemmings, over an interval of 15 years, are consistent with the theory. The pattern of habitat selection at the scale of wet versus dry tundra habitats changed through time. The change in habitat selection was reflected by different, but nevertheless density‐dependent, patterns of association with the structure and composition of habitat. Abundant collared lemmings abandoned stations where altered habitat characteristics caused a shift to new locations along the wet‐to‐dry gradient. The confirmation of scale‐dependent theory provides new insights into how one might begin to forecast future habitat selection under different scenarios of climate and habitat change.     

Quantifying the causal pathways contributing to natural selection

The consequences of natural selection can be understood from a purely statistical perspective. In contrast, an explicitly causal approach is required to understand why trait values covary with fitness. In particular, key evolutionary constructs, such as sexual selection, fecundity selection, and so on, are best understood as selection via particular fitness components. To formalize and operationalize these concepts, we must disentangle the various causal pathways contributing to selection. Such decompositions are currently only known for linear models, where they are sometimes referred to as “Wright's rules.” Here, we provide a general framework, based on path analysis, for partitioning selection among its contributing causal pathways. We show how the extended selection gradient—which represents selection arising from a trait's causal effects on fitness—can be decomposed into path-specific selection gradients, which correspond to distinct causal mechanisms of selection. This framework allows for nonlinear effects and nonadditive interactions among variables, which may be estimated using standard statistical methods (e.g., generalized linear [mixed] models or generalized additive models). We thus provide a generalization of Wright's path rules that accommodates the nonlinear and nonadditive mechanisms by which natural selection commonly arises.     

The genetics of phenotypic plasticity. V. Evolution of reaction norm shape

We present a general quantitative genetic model for the evolution of reaction norms. This model goes beyond previous models by simultaneously permitting any shaped reaction norm and allowing for the imposition of genetic constraints. Earlier models are shown to be special cases of our general model; we discuss in detail models involving just two macroenvironments, linear reaction norms, and quadratic reaction norms. The model predicts that, for the case of a temporally varying environment, a population will converge on (1) the genotype with the maximum mean geometric fitness over all environments, (2) a linear reaction norm whose slope is proportional to the covariance between the environment of development and the environment of selection, and (3) a linear reaction norm even if nonlinear reaction norms are possible. An examination of experimental studies finds some limited support for these predictions. We discuss the limitations of our model and the need for more realistic gametic models and additional data on the genetic and developmental bases of plasticity.     

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.     

Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.     

Habitat selection and the value of information in heterogenous landscapes

Despite the wide usage of the term information in evolutionary ecology, there is no general treatise between fitness (i.e. density‐dependent population growth) and selection of the environment sensu lato. Here we 1) initiate the building of a quantitative framework with which to examine the relationship between information use in spatially heterogeneous landscapes and density‐dependent population growth, and 2) illustrate its utility by applying the framework to an existing model of breeding habitat selection. We begin by linking information, as a process of narrowing choice, to population growth/fitness. Second, we define a measure of a population's penalty of ignorance based on the Kullback–Leibler index that combines the contributions of resource selection (i.e. biased use of breeding sites) and density‐dependent depletion. Third, we quantify the extent to which environmental heterogeneity (i.e. mean and variance within a landscape) constrains sustainable population growth of unbiased agents. We call this the heterogeneity‐based fitness deficit, and combine this with population simulations to quantify the independent contribution of information‐use strategies to the total population growth rate. We further capitalize on this example to highlight the interactive effects of information between ecological scales when fear affects individual fitness through phenotypic plasticity. Informed breeding habitat selection moderates the demographic cost of fear commensurate with density‐dependent information use. Thus, future work should attempt to differentiate between phenotypic plasticity (i.e. acute fear) and demographic responses (i.e. chronic changes in population size). We conclude with a broader discussion of information in alternative contexts, and explore some evolutionary considerations for information use. We note how competition among individuals may constrain the information state among individuals, and the implications of this constraint under environmental change.