Maintenance of genetic variation in phenotypic plasticity: the role of environmental variation

We study genetic variation in phenotypic plasticity maintained by a balance between mutation and weak stabilizing selection. We consider linear reaction norms allowing for spatial and/or temporal variation in the environments of development and selection. We show that the overall genetic variation maintained does not depend on whether the trait is plastic or not. The genetic variances in height and slope of a linear reaction norm, and their covariance, are predicted to decrease with the variation in the environment. Non-pleiotropic loci influencing either height or slope are expected to decrease the genetic variance in slope relative to that in height. Decrease in the ratio of genetic variance in slope to genetic variance in height with increasing variation in the environment presents a test for the presence of loci that only influence the slope, and not the height. We use data on Drosophila to test the theory. In seven of eight pair-wise comparisons genetic variation in reaction norm is higher in a less variable environment than in a more variable environment, which is in accord with the model's predictions.     

Temporal environmental variation and phenotypic plasticity: a mechanism underlying priority effects

Understanding the role of history in the formation of communities has been a major challenge in community ecology. Here, we explore the role of phenotypic plasticity and its associated trait‐mediated indirect interactions as a mechanism behind priority effects. Using organisms with inducible defenses as a model system, we examine how aquatic communities initially containing different predator environments are affected at the individual and community level by the colonization of a second predator. Snails and tadpoles were established in four different caged‐predator environments (no predator, fish, crayfish or water bugs). These four communities were then crossed with three predator colonization treatments (no colonization, early colonization, or late colonization) using lethal water bugs as the predator. The snails responded to the caged predator environments with predator‐specific behavioral and morphological defenses. In the colonization treatments, snails possessing the wrong phenotype attempted to induce phenotypic changes to defend themselves against the new risk. However, snails initially induced by a different predator environment often suffered high predation rates. Hence, temporal variation in predation risk not only challenged the snail prey to try to track this environmental variation through time by adjusting their defensive phenotypes, but also caused trait‐mediated interactions between snails and the colonizing predator. For tadpoles within these communities, there was little evidence that the morphological responses of snails indirectly effected tadpole predation rates by colonizing water bugs. Unexpectedly, predation rates on tadpoles by colonizing water bugs were generally higher in the three caged‐predator treatments, suggesting that water bugs elevated their foraging activity in response to potentially competing predators. In summary, we demonstrate an important priority effect in which the initial occurrence of one species of predator can facilitate predation by a second predator that colonizes at a later date (i.e. a TMII) suggesting that phenotypic plasticity can be an important driver behind priority effects (i.e. historical exposure to predators).     

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.     

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.     

Chaoborus predation and the function of phenotypic variation in Daphnia

To investigate the role of helmet formation in defense against predation, laboratory experiments were used to analyze the effects of morphological changes in Daphnia on susceptibility to Chaoborus predation. Behavioral observations of Chaoborus preying on helmeted and non-helmeted Daphnia suggest pre-contact advantages for helmeted prey but post-contact advantages for non-helmeted prey. Helmeted Daphnia are better at evading capture by Chaoborus but may also be more easily handled by the predator. Swimming behavior of the prey, which is influenced by the presence of a tailspine, may affect Chaoborus strike distance. These results re-emphasize the potential hydromechanical importance of body shape changes in defense against predation.     

Combining genetic variation and phenotypic plasticity in tradeoff modelling

Tradeoffs lead to antagonistic relationships between phenotypic traits and are thought to be determined both genetically and environmentally. We present here an allocation model that distinguishes between the genetic and environmental components of variation in resource allocation. In this model we introduced plasticity of resource allocation which was considered to be an adaptive response to environmental variations. The results show that resource allocation plasticity is a key parameter for the existence of environmental (i.e. inter environments and intra genotype) correlations and is therefore necessary to detect environment-induced tradeoffs. We also investigated the impact of the resource allocation plasticity and other factors on genetic (i.e. inter genotypes) correlations. Our results show that resource allocation plasticity induces a masking effect of tradeoffs when studying genetic correlations and increases the masking effect of resource variation by making apparent correlations positive when negative correlations are expected. In addition, by simulating different sources of resource acquisition variation, we demonstrated that resource variation might have different effects on correlations according to the experimental design and the studied biological material. Further development of this model may be used to investigate the theoretical implications of tradeoffs in evolutionary biology and to improve design and interpretation of experimental studies.     

Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments

Adaptive phenotypic plasticity and adaptive genetic differentiation enable plant lineages to maximize their fitness in response to environmental heterogeneity. The spatial scale of environmental variation relative to the average dispersal distance of a species determines whether selection will favor plasticity, local adaptation, or an intermediate strategy. Habitats where the spatial scale of environmental variation is less than the dispersal distance of a species are fine grained and should favor the expression of adaptive plasticity, while coarse-grained habitats, where environmental variation occurs on spatial scales greater than dispersal, should favor adaptive genetic differentiation. However, there is relatively little information available characterizing the link between the spatial scale of environmental variation and patterns of selection on plasticity measured in the field. I examined patterns of spatial environmental variation within a serpentine mosaic grassland and selection on an annual plant (Erodium cicutarium) within that landscape. Results indicate that serpentine soil patches are a significantly finer-grained habitat than non-serpentine patches. Additionally, selection generally favored increased plasticity on serpentine soils and diminished plasticity on non-serpentine soils. This is the first empirical example of differential selection for phenotypic plasticity in the field as a result of strong differences in the grain of environmental heterogeneity within habitats.     

Estimating the variation,autocorrelation, and environmental sensitivity of phenotypic selection

Despite considerable interest in temporal and spatial variation of phenotypic selection, very few methods allow quantifying this variation while correctly accounting for the error variance of each individual estimate. Furthermore, the available methods do not estimate the autocorrelation of phenotypic selection, which is a major determinant of eco‐evolutionary dynamics in changing environments. We introduce a new method for measuring variable phenotypic selection using random regression. We rely on model selection to assess the support for stabilizing selection, and for a moving optimum that may include a trend plus (possibly autocorrelated) fluctuations. The environmental sensitivity of selection also can be estimated by including an environmental covariate. After testing our method on extensive simulations, we apply it to breeding time in a great tit population in the Netherlands. Our analysis finds support for an optimum that is well predicted by spring temperature, and occurs about 33 days before a peak in food biomass, consistent with what is known from the biology of this species. We also detect autocorrelated fluctuations in the optimum, beyond those caused by temperature and the food peak. Because our approach directly estimates parameters that appear in theoretical models, it should be particularly useful for predicting eco‐evolutionary responses to environmental change.     

Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure

Thermal performance curves (TPCs) describe the effects of temperature on biological rate processes. Here, we use examples from our work on common killifish (Fundulus heteroclitus) to illustrate some important conceptual issues relating to TPCs in the context of using these curves to predict the responses of organisms to climate change. Phenotypic plasticity has the capacity to alter the shape and position of the TPCs for acute exposures, but these changes can be obscured when rate processes are measured only following chronic exposures. For example, the acute TPC for mitochondrial respiration in killifish is exponential in shape, but this shape changes with acclimation. If respiration rate is measured only at the acclimation temperature, the TPC is linear, concealing the underlying mechanistic complexity at an acute time scale. These issues are particularly problematic when attempting to use TPCs to predict the responses of organisms to temperature change in natural environments. Many TPCs are generated using laboratory exposures to constant temperatures, but temperature fluctuates in the natural environment, and the mechanisms influencing performance at acute and chronic time scales, and the responses of the performance traits at these time scales may be quite different. Unfortunately, our current understanding of the mechanisms underlying the responses of organisms to temperature change is incomplete, particularly with respect to integrating from processes occurring at the level of single proteins up to whole-organism functions across different time scales, which is a challenge for the development of strongly grounded mechanistic models of responses to global climate change.     

The other side of phenotypic plasticity: a developmental system that generates an invariant phenotype despite environmental variation

Understanding how the environment impacts development is of central interest in developmental and evolutionary biology. On the one hand, we would like to understand how the environment induces phenotypic changes (the study of phenotypic plasticity). On the other hand, we may ask how a development system maintains a stable and precise phenotypic output despite the presence of environmental variation. We study such developmental robustness to environmental variation using vulval cell fate patterning in the nematode Caenorhabditis elegans as a study system. Here we review both mechanistic and evolutionary aspects of these studies, focusing on recently obtained experimental results. First, we present evidence indicating that vulval formation is under stabilizing selection. Second, we discusss quantitative data on the precision and variability in the output of the vulval developmental system in different environments and different genetic backgrounds. Third, we illustrate how environmental and genetic variation modulate the cellular and molecular processes underlying the formation of the vulva. Fourth, we discuss the evolutionary significance of environmental sensitivity of this developmental system.     

Patterns of phenotypic and genetic variation for the plasticity of diapause incidence

Phenotypic plasticity describes an organism's ability to produce multiple phenotypes in direct response to its environmental conditions. Over the past 15 years empiricists have found that this plasticity frequently exhibits geographic variation and often possesses a significant heritable genetic basis. However, few studies have examined both of these aspects of plasticity simultaneously. Here, we examined both the geographic and genetic variations of the plasticity for diapause incidence (the proportion of eggs that enter an arrested state of development capable of surviving over the winter) relative to temperatures and photoperiods associated with long and short season environments across six populations of the striped ground cricket, Allonemobius socius, using a half-sibling split brood quantitative genetic design. We found that plasticity, as measured by the slope of the reaction norm, was greater in the southern-low altitude region (where populations are bivoltine) relative to the southern-high and northern-low altitude regions (where populations are univoltine). However, the heritability of plasticity was only significantly different from zero in univoltine populations that experienced "intermediate" natal season lengths. These patterns suggest that selection may favor the plasticity of diapause incidence in bivoltine regions, but act against plasticity in regions in which populations are univoltine. Furthermore, our data suggest that under "intermediate" natal season length conditions, the interplay between local adaptation and gene flow may keep the plasticity of diapause incidence low (but still significant) while maintaining its genetic variation. As such, this study not only provides a novel observation into the geographic variation of phenotypic plasticity, but also provides much needed groundwork for tests of its adaptive significance.     

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.     

Environmental change, phenotypic plasticity, and genetic compensation

When a species encounters novel environmental conditions, some phenotypic characters may develop differently than in the ancestral environment. Most environmental perturbations of development are likely to reduce fitness, and thus selection would usually be expected to favor genetic changes that restore the ancestral phenotype. I propose the term "genetic compensation" to refer to this form of adaptive evolution. Genetic compensation is a subset of genetic accommodation and the reverse of genetic assimilation. When genetic compensation has occurred along a spatial environmental gradient, the mean trait values of populations in different environments may be more similar in the field than when representatives of the same populations are raised in a common environment (i.e., countergradient variation). If compensation is complete, genetic divergence between populations may be cryptic, that is, not detectable in the field. Here I apply the concept of genetic compensation to three examples involving carotenoid-based sexual coloration and then use these and other examples to discuss the concept in a broader context. I show that genetic compensation may lead to a cryptic form of reproductive isolation between populations evolving in different environments, may explain some puzzling cases in which heritable traits exposed to strong directional selection fail to show the expected evolutionary response, and may complicate efforts to monitor populations for signs of environmental deterioration.     

Clinal life-history variation in the river-sculpin,Cottus hangiongensis: an example of phenotypic plasticity

An amphidromous sculpin,Cottus hangiongensis, distributed freely in a natural river system, exhibited clinal differences in population density, sex ratio, age composition and life-history. In a second river, in which the distribution was restricted to a narrow area in the lower reaches by a notched weir, the species was characterized by high population density and a similar population structure in two different habitats. Little life-history variation was evident. Field observations suggested that clinal life-history variations inC. hangiongensis were not genotypic, but environmentally-induced, phenotypic responses. Rearing experiments demonstrated that the maturity of one-year old males was delayed under low density conditions, and that no relationship existed between the timing of maturity and the sex ratio. This suggests that phenotypic life-history variation inC. hangiongensis is induced primarily in response to population density. Such phenotypic plasticity in life-histories of individualC. hangiongensis populations may be an adaptation for exploitation of broad and heterogenous river habitats.     

Inter-population variation and phenotypic plasticity in kairomone use by a poly-specialist spider-eating predator

Journal of Ethology - Previous research on Cyrba algerina (Araneae, Salticidae) has shown this jumping spider expresses predatory specialisation with respect to spiders as prey as well as...     

Role of phenotypic plasticity and population differentiation in adaptation to novel environmental conditions

Species can adapt to new environmental conditions either through individual phenotypic plasticity, intraspecific genetic differentiation in adaptive traits, or both. Wild emmer wheat, Triticum dicoccoides, an annual grass with major distribution in Eastern Mediterranean region, is predicted to experience in the near future, as a result of global climate change, conditions more arid than in any part of the current species distribution. To understand the role of the above two means of adaptation, and the effect of population range position, we analyzed reaction norms, extent of plasticity, and phenotypic selection across two experimental environments of high and low water availability in two core and two peripheral populations of this species. We studied 12 quantitative traits, but focused primarily on the onset of reproduction and maternal investment, which are traits that are closely related to fitness and presumably involved in local adaptation in the studied species. We hypothesized that the population showing superior performance under novel environmental conditions will either be genetically differentiated in quantitative traits or exhibit higher phenotypic plasticity than the less successful populations. We found the core population K to be the most plastic in all three trait categories (phenology, reproductive traits, and fitness) and most successful among populations studied, in both experimental environments; at the same time, the core K population was clearly genetically differentiated from the two edge populations. Our results suggest that (1) two means of successful adaptation to new environmental conditions, phenotypic plasticity and adaptive genetic differentiation, are not mutually exclusive ways of achieving high adaptive ability; and (2) colonists from some core populations can be more successful in establishing beyond the current species range than colonists from the range extreme periphery with conditions seemingly closest to those in the new environment.     

Empirical patterns of environmental variation favor adaptive transgenerational plasticity

Effects of parental environment on offspring traits have been well known for decades. Interest in this transgenerational form of phenotypic plasticity has recently surged due to advances in our understanding of its mechanistic basis. Theoretical research has simultaneously advanced by predicting the environmental conditions that should favor the adaptive evolution of transgenerational plasticity. Yet whether such conditions actually exist in nature remains largely unexplored. Here, using long‐term climate data, we modeled optimal levels of transgenerational plasticity for an organism with a one‐year life cycle at a spatial resolution of 4 km² across the continental United States. Both annual temperature and precipitation levels were often autocorrelated, but the strength and direction of these autocorrelations varied considerably even among nearby sites. When present, such environmental autocorrelations render offspring environments statistically predictable based on the parental environment, a key condition for the adaptive evolution of transgenerational plasticity. Results of our optimality models were consistent with this prediction: High levels of transgenerational plasticity were favored at sites with strong environmental autocorrelations, and little‐to‐no transgenerational plasticity was favored at sites with weak or nonexistent autocorrelations. These results are among the first to show that natural patterns of environmental variation favor the evolution of adaptive transgenerational plasticity. Furthermore, these findings suggest that transgenerational plasticity is likely variable in nature, depending on site‐specific patterns of environmental variation.