How to balance the offspring quality–quantity tradeoff when environmental cues are unreliable

Maternal effects on offspring size can have a strong effect on fitness, as larger offspring often survive better under harsh environmental conditions. Selection should hence favour mothers that find an optimal solution to the offspring size versus number tradeoff. If environmental conditions are variable, there will not be a single optimal offspring size, as predicted in a constant environment, but plastic responses can be favoured. To be able to adjust offspring size in an adaptive manner, mothers have to use environmental cues to predict offspring environmental conditions. Cues can be unreliable, however, particularly in species where individuals occupy different niches at different life stages. Here we model the evolution of plasticity of offspring size when the environmental cues mothers use to predict the conditions experienced by their offspring are not perfectly reliable. Our results show that plastic strategies are likely to be superior to fixed strategies in a stochastically varying environment when the environmental cues are at least moderately reliable, with the threshold depending on plasticity costs and the difference of resources available to mothers. Plasticity is more likely to occur if resource availability is not too different between environments. For any given scenario, plasticity in offspring size is favoured if offspring survival varies greatly between environmental states. Whenever plastic strategies are optimal, the occurring switches performed by mothers between small and large offspring are predicted to be substantial, as small adjustments are unlikely to reap fitness benefits great enough to overcome the costs of plasticity.     

Rapid evolution and behavioral plasticity following introduction to an environment with reduced predation risk

Adaptive behavioral plasticity can play a beneficial role when a population becomes established in a novel environment if environmental cues allow the expression of appropriate behavior. Further, plasticity itself can evolve over time in a new environment causing changes in the way or degree to which animals respond to environmental cues. Colonization events provide an opportunity to investigate such relationships between behavioral plasticity and adaptation to new environments. Here, we investigated the evolution of behavior and behavioral plasticity during colonization of a new environment, by testing if female mate‐choice behavior diverged in Trinidadian guppies 2–3 years (~6–9 generations) after being introduced to four locations with reduced predation risk. We collected wild‐caught fish from the source and introduced populations, and we reared out second‐generation females in the laboratory with and without predator cues to examine their plastic responses to a bright and dull male. We found introduced females were less responsive to males when reared without predator cues, but both introduced and source females were similarly responsive when reared with predator cues. Thus, the parallel evolution of behavior across multiple populations in the low‐predation environment was only observed in the treatment mimicking the introduction environment. Such results are consistent with theory predicting that the evolution of plasticity is a by‐product of differential selection across environments.     

The genetics of phenotypic plasticity. XI. Joint evolution of plasticity and dispersal rate

In a spatially heterogeneous environment, the rate at which individuals move among habitats affects whether selection favors phenotypic plasticity or genetic differentiation, with high dispersal rates favoring trait plasticity. Until now, in theoretical explorations of plasticity evolution, dispersal rate has been treated as a fixed, albeit probabilistic, characteristic of a population, raising the question of what happens when the propensity to disperse and trait plasticity are allowed to evolve jointly. We examined the effects of their joint evolution on selection for plasticity using an individual-based computer simulation model. In the model, the environment consisted of a linear gradient of 50 demes with dispersal occurring either before or after selection. Individuals consisted of loci whose phenotypic expression either are affected by the environment (plastic) or are not affected (nonplastic), plus a locus determining the propensity to disperse. When dispersal rate and trait plasticity evolve jointly, the system tends to dichotomous outcomes of either high trait plasticity and high dispersal, or low trait plasticity and low dispersal. The outcome strongly depended on starting conditions, with high trait plasticity and dispersal favored when the system started at high values for either trait plasticity or dispersal rate (or both). Adding a cost of plasticity tended to drive the system to genetic differentiation, although this effect also depended on initial conditions. Genetic linkage between trait plasticity loci and dispersal loci further enhanced this strong dichotomy in evolutionary outcomes. All of these effects depended on organismal life history pattern, and in particular whether selection occurred before or after dispersal. These results can explain why adaptive trait plasticity is less common than might be expected.     

Shedding light on the evolution of plasticity in natural populations

Plasticity allows for changes in phenotype in response to environmental cues, often facilitating local adaptation to seasonal environments. Phenotypic plasticity alone, however, may not always be sufficient to ensure adaptation to new localities. In particular, changing cues associated with shifting seasonal regimes may no longer induce appropriate phenotypic responses in new environments ( Nicotra et al. 2010 ). Plastic responses must thus evolve to avoid being maladaptive. To date, the extent to which plastic responses can change and the genetic mechanisms by which this can happen have remained elusive. In this issue of Molecular Ecology, Blackman et al. (2011a) harness natural variation in flowering time among populations of the wild sunflower, Helianthus annuus, to demonstrate that plasticity has indeed evolved in this species. Remarkably, they are able to detect changes in gene expression that are associated with both a loss of plasticity and a reversal of the plastic response. These changes occur in two separate, but integrated, regulatory pathways controlling the transition to flowering, suggesting that complex regulatory networks that incorporate multiple environmental and developmental cues may facilitate the evolution of plastic responses. This study leverages knowledge from plant genetic models to provide a surprising level of insight into the evolution of an adaptive trait in a non‐model species. Through discoveries of the roles of gene duplication and network modularity in the evolution of plastic responses, the study raises questions about the degree to which species‐specific network architectures may act as a constraint to the potential of adaptation.     

Phylogenetic patterns of trait and trait plasticity evolution: Insights from amphibian embryos

Environmental variation favors the evolution of phenotypic plasticity. For many species, we understand the costs and benefits of different phenotypes, but we lack a broad understanding of how plastic traits evolve across large clades. Using identical experiments conducted across North America, we examined prey responses to predator cues. We quantified five life‐history traits and the magnitude of their plasticity for 23 amphibian species/populations (spanning three families and five genera) when exposed to no cues, crushed‐egg cues, and predatory crayfish cues. Embryonic responses varied considerably among species and phylogenetic signal was common among the traits, whereas phylogenetic signal was rare for trait plasticities. Among trait‐evolution models, the Ornstein–Uhlenbeck (OU) model provided the best fit or was essentially tied with Brownian motion. Using the best fitting model, evolutionary rates for plasticities were higher than traits for three life‐history traits and lower for two. These data suggest that the evolution of life‐history traits in amphibian embryos is more constrained by a species’ position in the phylogeny than is the evolution of life history plasticities. The fact that an OU model of trait evolution was often a good fit to patterns of trait variation may indicate adaptive optima for traits and their plasticities.     

Developmental noise and ecological opportunity across space can release constraints on the evolution of plasticity

Phenotypic plasticity is a potentially definitive solution to environment heterogeneity, driving biologists to understand why it is not ubiquitous in nature. While costs and constraints may limit the success of plasticity, we are still far from a complete theory of when these limitations actually proscribe adaptive plasticity. Here I use a simple model of plasticity incorporating developmental noise to explore the competitive and evolutionary relationships of specialist and generalist genotypes spreading across a heterogeneous landscape. Results show that plasticity can arise in the context of specialism, preadapting genotypes to later evolve toward plastic generalism. Developmental noise helps a mutant with imperfect plasticity successfully compete against its ancestor, providing an evolutionary path by which subsequent mutations can refine plasticity toward its optimum. These results address how the complex selection pressures across a heterogeneous environment can help evolution find paths around constraints arising from developmental mechanisms.     

Stress relief may promote the evolution of greater phenotypic plasticity in exotic invasive species: a hypothesis

Invasion ecologists have often found that exotic invaders evolve to be more plastic than conspecific populations from their native range. However, an open question is why some exotic invaders can even evolve to be more plastic given that there may be costs to being plastic. Investigation into the benefits and costs of plasticity suggests that stress may constrain the expression of plasticity (thereby reducing the benefits of plasticity) and exacerbate the costs of plasticity (although this possibility might not be generally applicable). Therefore, evolution of adaptive plasticity is more likely to be constrained in stressful environments. Upon introduction to a new range, exotic species may experience more favorable growth conditions (e.g., because of release from natural enemies). Therefore, we hypothesize that any factors mitigating stress in the introduced range may promote exotic invaders to evolve increased adaptive plasticity by reducing the costs and increasing the benefits of plasticity. Empirical evidence is largely consistent with this hypothesis. This hypothesis contributes to our understanding of why invasive species are often found to be more competitive in a subset of environments. Tests of this hypothesis may not only help us understand what caused increased plasticity in some exotic invaders, but could also tell us if costs (unless very small) are more likely to inhibit the evolution of adaptive plasticity in stressful environments in general.     

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.     

Prospecting and dispersal: their eco-evolutionary dynamics and implications for population patterns

Dispersal is not a blind process, and evidence is accumulating that individual dispersal strategies are informed in most, if not all, organisms. The acquisition and use of information are traits that may evolve across space and time as a function of the balance between costs and benefits of informed dispersal. If information is available, individuals can potentially use it in making better decisions, thereby increasing their fitness. However, prospecting for and using information probably entail costs that may constrain the evolution of informed dispersal, potentially with population-level consequences. By using individual-based, spatially explicit simulations, we detected clear coevolutionary dynamics between prospecting and dispersal movement strategies that differed in sign and magnitude depending on their respective costs. More specifically, we found that informed dispersal strategies evolve when the costs of information acquisition during prospecting are low but only if there are mortality costs associated with dispersal movements. That is, selection favours informed dispersal strategies when the acquisition and use processes themselves were not too expensive. When non-informed dispersal strategies evolve, they do so jointly with the evolution of long dispersal distance because this maximizes the sampling area. In some cases, selection produces dispersal rules different from those that would be ‘optimal’ (i.e. the best possible population performance—in our context quantitatively measured as population density and patch occupancy—among all possible individual movement rules) for the population. That is, on the one hand, informed dispersal strategies led to population performance below its highest possible level. On the other hand, un- and poorly informed individuals nearly optimized population performance, both in terms of density and patch occupancy.     

Modular phenotypic plasticity: divergent responses of barnacle penis and feeding leg form to variation in density and wave-exposure

Traits can evolve both in response to direct selection and in response to indirect selection on other linked traits. Although the evolutionary significance of coupled traits (e.g., through shared components of developmental pathways, or through competition for shared developmental resources) is now well accepted, we know comparatively little about how developmental coupling may restrict the independent responses of two or more phenotypically plastic traits in response to conflicting environmental cues. Such studies are important because coupled development, if present, could act as an important limit to the evolution of functionally independent plasticity in multiple traits. I tested whether developmental coupling can restrict the direction of plastic responses by studying how penis form and leg form--both highly plastic traits of barnacles--varied in response to differences in conspecific density and water velocity. Penis length and leg length in Balanus glandula varied in parallel with variation in wave-exposure but varied in opposite directions with variation in conspecific density. This study represents one of the rare tests of developmental coupling between multiple (demonstrably adaptive) plastic traits: Barnacle legs and penises appear to exhibit modular development that can respond concurrently--yet in independent directions--to conflicting environmental cues.     

Plasticity of physiology in Lobelia: testing for adaptation and constraint

Phenotypic plasticity is thought to be a major mechanism allowing sessile organisms such as plants to adapt to environmental heterogeneity. However, the adaptive value of many common plastic responses has not been tested by linking these responses to fitness. Even when plasticity is adaptive, costs of plasticity, such as the energy necessary to maintain regulatory pathways for plastic responses, may constrain its evolution. We used a greenhouse experiment to test whether plastic physiological responses to soil water availability (wet vs. dry conditions) were adaptive and/or costly in the congeneric wildflowers Lobelia cardinalis and L. siphilitica. Eight physiological traits related to carbon and water uptake were measured. Specific leaf area (SLA), photosynthetic rate (A), stomatal conductance (gs), and photosynthetic capacity (Amax) responded plastically to soil water availability in L. cardinalis. Plasticity in Amax was maladaptive, plasticity in A and g(s) was adaptive, and plasticity in SLA was adaptively neutral. The nature of adaptive plasticity in L. cardinalis, however, differed from previous studies. Lobelia cardinalis plants with more conservative water use, characterized by lower g(s), did not have higher fitness under drought conditions. Instead, well-watered L. cardinalis that had higher g(s) had higher fitness. Only Amax responded plastically to drought in L. siphilitica, and this response was adaptively neutral. We detected no costs of plasticity for any physiological trait in either L. cardinalis or L. siphilitica, suggesting that the evolution of plasticity in these traits would not be constrained by costs. Physiological responses to drought in plants are presumed to be adaptive, but our data suggest that much of this plasticity can be adaptively neutral or maladaptive.     

Plasticity predicts evolution in a marine alga

Under global change, populations have four possible responses: ‘migrate, acclimate, adapt or die’ (Gienapp et al. 2008 Climate change and evolution: disentangling environmental and genetic response. Mol. Ecol. 17, 167–178. (doi:10.1111/j.1365-294X.2007.03413.x)). The challenge is to predict how much migration, acclimatization or adaptation populations are capable of. We have previously shown that populations from more variable environments are more plastic (Schaum et al. 2013 Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nature 3, 298–230. (doi:10.1038/nclimate1774)), and here we use experimental evolution with a marine microbe to learn that plastic responses predict the extent of adaptation in the face of elevated partial pressure of CO₂ (pCO₂). Specifically, plastic populations evolve more, and plastic responses in traits other than growth can predict changes in growth in a marine microbe. The relationship between plasticity and evolution is strongest when populations evolve in fluctuating environments, which favour the evolution and maintenance of plasticity. Strikingly, plasticity predicts the extent, but not direction of phenotypic evolution. The plastic response to elevated pCO₂ in green algae is to increase cell division rates, but the evolutionary response here is to decrease cell division rates over 400 generations until cells are dividing at the same rate their ancestors did in ambient CO₂. Slow-growing cells have higher mitochondrial potential and withstand further environmental change better than faster growing cells. Based on this, we hypothesize that slow growth is adaptive under CO₂ enrichment when associated with the production of higher quality daughter cells.     

Plasticity versus canalization: population differences in the timing of shade-avoidance responses

The reliability of environmental cues and costs of a fixed phenotype are two factors determining whether selection favors phenotypic plasticity or environmental specialization. This study examines the relationship between these two factors and the evolution of plant competitive strategies (plastic vs. fixed morphologies). In natural plant populations, shifts in light quality associated with foliar shade reliably indicate the presence of neighbors. These cues mediate plastic stem-elongation responses that often increase competitive ability and access to light. Using experimental light treatments (full sun, neutral shade, and foliar shade), genetic differences among populations of Abutilon theophrasti (velvetleaf) in average elongation and plasticity to foliar-shade cues were examined. Six populations, two from each of three site types (fields in continuous corn cultivation, fields undergoing corn-soy rotation, and weedy sites), were exposed to the light treatments at two stages in their life history. At the seedling stage, populations derived from cornfield sites exhibited higher, average elongation than populations from either rotating corn-soy fields or weedy areas. Because seedling elongation may delay shading of velvetleaf by corn, population differences may reflect adaptive responses to directional selection imposed by competitive conditions. However, the effects of simulated foliar shade on elongation were three times as great as the average population differences, and these comparatively higher levels of elongation were associated with an allocation cost. These results are consistent with the hypothesis that phenotypic plasticity may limit the evolution of specialists; reliable environmental cues enable individuals to facultatively adopt highly elongated, costly phenotypes in crowded patches while avoiding the costs of that phenotype in less crowded microsites. At later life-history stages, populations experiencing competition with corn exhibited lower plasticity to light quality than populations derived from weedy areas. Elongation at later nodes is maladaptive in cornfields because velvetleaf is ultimately incapable of overtopping corn; individuals that elongate therefore experience the cost of allocating to stems but fail to improve leaf exposure. The decreased responsiveness of cornfield populations to light quality is consistent with theoretical predictions in which reduced plasticity is favored when environmental cues fail to mediate an adaptive response.     

Geographic variation and thermal plasticity shape salamander metabolic rates under current and future climates

Predicted changes in global temperature are expected to increase extinction risk for ectotherms, primarily through increased metabolic rates. Higher metabolic rates generate increased maintenance energy costs which are a major component of energy budgets. Organisms often employ plastic or evolutionary (e.g., local adaptation) mechanisms to optimize metabolic rate with respect to their environment. We examined relationships between temperature and standard metabolic rate across four populations of a widespread amphibian species to determine if populations vary in metabolic response and if their metabolic rates are plastic to seasonal thermal cues. Populations from warmer climates lowered metabolic rates when acclimating to summer temperatures as compared to spring temperatures. This may act as an energy saving mechanism during the warmest time of the year. No such plasticity was evident in populations from cooler climates. Both juvenile and adult salamanders exhibited metabolic plasticity. Although some populations responded to historic climate thermal cues, no populations showed plastic metabolic rate responses to future climate temperatures, indicating there are constraints on plastic responses. We postulate that impacts of warming will likely impact the energy budgets of salamanders, potentially affecting key demographic rates, such as individual growth and investment in reproduction.     

A predictive model of avian natal dispersal distance provides prior information for investigating response to landscape change

1. Informative Bayesian priors can improve the precision of estimates in ecological studies or estimate parameters for which little or no information is available. While Bayesian analyses are becoming more popular in ecology, the use of strongly informative priors remains rare, perhaps because examples of informative priors are not readily available in the published literature. 2. Dispersal distance is an important ecological parameter, but is difficult to measure and estimates are scarce. General models that provide informative prior estimates of dispersal distances will therefore be valuable. 3. Using a world-wide data set on birds, we develop a predictive model of median natal dispersal distance that includes body mass, wingspan, sex and feeding guild. This model predicts median dispersal distance well when using the fitted data and an independent test data set, explaining up to 53% of the variation. 4. Using this model, we predict a priori estimates of median dispersal distance for 57 woodland-dependent bird species in northern Victoria, Australia. These estimates are then used to investigate the relationship between dispersal ability and vulnerability to landscape-scale changes in habitat cover and fragmentation. 5. We find evidence that woodland bird species with poor predicted dispersal ability are more vulnerable to habitat fragmentation than those species with longer predicted dispersal distances, thus improving the understanding of this important phenomenon. 6. The value of constructing informative priors from existing information is also demonstrated. When used as informative priors for four example species, predicted dispersal distances reduced the 95% credible intervals of posterior estimates of dispersal distance by 8-19%. Further, should we have wished to collect information on avian dispersal distances and relate it to species' responses to habitat loss and fragmentation, data from 221 individuals across 57 species would have been required to obtain estimates with the same precision as those provided by the general model.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

Phenotypic variability can promote the evolution of adaptive plasticity by reducing the stringency of natural selection

Adaptive phenotypic plasticity is a potent but not ubiquitous solution to environmental heterogeneity, driving interest in what factors promote and limit its evolution. Here, a novel computational model representing stochastic information flow in development is used to explore evolution from a constitutive phenotype to an adaptively plastic response. Results show that populations tend to evolve robustness to developmental stochasticity, but that this evolved robustness limits evolvability; specifically, robust genotypes have less ability to evolve adaptive plasticity when presented with a mix of both the ancestral environment and a new environment. Analytic calculations and computational experiments confirm that this constraint occurs when the initial mutational steps towards plasticity are pleiotropic, such that mutant fitnesses decline in the environment to which their parents are well‐adapted. Greater phenotypic variability improves evolvability in the model by lessening this decline as well as by improving the fitness of partial adaptations to the new environment. By making initial plastic mutations more palatable to natural selection, phenotypic variability can increase the evolvability of an innovative, plastic response without improving evolvability to simpler challenges such as a shifted optimum in a single environment. Populations that evolved robustness by negative feedback between the trait and its rate of change show a particularly strong constraining effect on the evolvability of plasticity, revealing another mechanism by which evolutionary history can limit later innovation. These results document a novel mechanism by which weakening selection could actually stimulate the evolution of a major innovation.     

Correlated evolution of phenotypic plasticity in metamorphic timing

Phenotypic plasticity has long been a focus of research, but the mechanisms of its evolution remain controversial. Many amphibian species exhibit a similar plastic response in metamorphic timing in response to multiple environmental factors; therefore, more than one environmental factor has likely influenced the evolution of plasticity. However, it is unclear whether the plastic responses to different factors have evolved independently. In this study, we examined the relationship between the plastic responses to two experimental factors (water level and food type) in larvae of the salamander Hynobius retardatus, using a cause-specific Cox proportional hazards model on the time to completion of metamorphosis. Larvae from ephemeral ponds metamorphosed earlier than those from permanent ponds when kept at a low water level or fed conspecific larvae instead of larval Chironomidae. This acceleration of metamorphosis depended only on the permanency of the larvae's pond of origin, but not on the conspecific larval density (an indicator of the frequency of cannibalism) in the ponds. The two plastic responses were significantly correlated, indicating that they may evolve correlatively. Once plasticity evolved as an adaptation to habitat desiccation, it might have relatively easily become a response to other ecological factors, such as food type via the pre-existing developmental pathway.     

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.