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.     

昆虫翅型分化的表型可塑性机制

翅多型现象在昆虫中广泛存在,是昆虫在飞行扩散和繁殖能力之间权衡的一种策略,对种群的环境适应性进化具有重要的意义。目前在植食性昆虫中研究较多,有关寄生蜂的翅型分化鲜见报道。综述了昆虫翅型分化的表型可塑性机制。遗传因素和环境因素均对昆虫翅的发育产生影响,基因型对翅型的决定具有显著作用,外界环境条件,包括温度、光周期、食物质量、自身密度、外源激素等因素对昆虫翅的发育也产生重要的调节作用,从而产生翅的非遗传多型性现象。此外,天敌的寄生或捕食作用可能会诱导某些昆虫的翅型产生隔代表型变化。对昆虫产生翅多型现象的生态学意义及其在生物进化过程中的作用进行了讨论,并探讨了寄生性昆虫翅型分化机制在生物防治上的可能应用途径。功能基因组学和表观遗传学的进一步发展可望为彻底揭示昆虫翅型分化机制提供新的机遇和技术手段。     

Seasonal butterfly design: morphological plasticity among three developmental pathways relative to sex,flight and thermoregulation

The temperate‐zone butterfly Pararge aegeria can use three developmental pathways corresponding to different seasonal cohorts: (1) development with a pupal winter diapause resulting in early spring adults; (2) development with a larval winter diapause resulting in late‐spring adults and (3) direct development resulting in summer or second generation adults. In order to test adaptive predictions, we compared variation in flight‐ and thermoregulation‐related morphology among adult males and females from the three pathways using both field data (i.e. wild‐caught butterflies) and experimental breeding data (i.e. reared under different photoperiod regimes). Morphological patterns among the pathways were largely similar in the field and rearing data. Seasonal patterns differed between the sexes for most traits, including (relative) size measures and wing colour. Our results suggest sex‐related, adaptive seasonal plasticity for morphological traits related to flight behaviour in a multivoltine insect.     

Transgenerational and developmental plasticity at the molecular level: Lessons from Daphnia

Listen to the news and you are bound to hear that researchers are increasingly interested in the biological manifestations of trauma that reverberate through the generations. Research in this area can be controversial in the public realm, provoking societal issues about personal responsibility (are we really born free or are we born with the burden of our ancestors’ experience?). It is also a touchy subject within evolutionary biology because it provokes concerns about Lamarckianism and general scepticism about the importance of extra‐genetic inheritance (Laland et al., 2014 ). Part of why the research in this area has been controversial is because it is difficult to study. For one, there is the problem of how long it takes to track changes across generations, making long‐term, multi‐generational studies especially tricky in long‐lived species. Moreover, there are presently very few (if any) known molecular mechanisms by which environmental effects can be incorporated into the genome and persist for multiple successive generations, casting doubt on their evolutionary repercussions. Fortunately, you only have to look in your local pond to find the creatures that are teaching us a great deal about how and why the experiences of parents are passed down to their offspring. In this issue of Molecular Ecology, Hales et al. (Hales et al., 2017 ) illustrate the power of Daphnia (“water fleas”) for making headway in this field.     

The fitness costs of developmental canalization and plasticity

Organisms are capable of an astonishing repertoire of phenotypic responses to the environment, and these often define important adaptive solutions to heterogeneous and unpredictable conditions. The terms ‘phenotypic plasticity’ and ‘canalization’ indicate whether environmental variation has a large or small effect on the phenotype. The evolution of canalization and plasticity is influenced by optimizing selection‐targeting traits within environments, but inherent fitness costs of plasticity may also be important. We present a meta‐analysis of 27 studies (of 16 species of plant and 7 animals) that have measured selection on the degree of plasticity independent of the characters expressed within environments. Costs of plasticity and canalization were equally frequent and usually mild; large costs were observed only in studies with low sample size. We tested the importance of several covariates, but only the degree of environmental stress was marginally positively related to the cost of plasticity. These findings suggest that costs of plasticity are often weak, and may influence phenotypic evolution only under stressful conditions.     

Characterization,costs, cues and future perspectives of phenotypic plasticity

BackgroundPlastic responses of plants to the environment are ubiquitous. Phenotypic plasticity occurs in many forms and at many biological scales, and its adaptive value depends on the specific environment and interactions with other plant traits and organisms. Even though plasticity is the norm rather than the exception, its complex nature has been a challenge in characterizing the expression of plasticity, its adaptive value for fitness and the environmental cues that regulate its expression.ScopeThis review discusses the characterization and costs of plasticity and approaches, considerations, and promising research directions in studying plasticity. Phenotypic plasticity is genetically controlled and heritable; however, little is known about how organisms perceive, interpret and respond to environmental cues, and the genes and pathways associated with plasticity. Not every genotype is plastic for every trait, and plasticity is not infinite, suggesting trade-offs, costs and limits to expression of plasticity. The timing, specificity and duration of plasticity are critical to their adaptive value for plant fitness.ConclusionsThere are many research opportunities to advance our understanding of plant phenotypic plasticity. New methodology and technological breakthroughs enable the study of phenotypic responses across biological scales and in multiple environments. Understanding the mechanisms of plasticity and how the expression of specific phenotypes influences fitness in many environmental ranges would benefit many areas of plant science ranging from basic research to applied breeding for crop improvement.     

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

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

The double cloak of invisibility: phenotypic plasticity and larval decoration in a geometrid moth,Synchlora frondaria,across three diet treatments

Abstract 1. Crypsis is one of the main defences that insects use to avoid predators, and both the juveniles and adults of many geometrid moths are remarkable in their ability to blend into different host backgrounds. The larvae of Synchlora frondaria have two methods to achieve crypsis: phenotypic plasticity in colouration that enable them to hide more effectively on their host plants, and a self‐decorating behaviour whereby the larvae camouflage themselves with materials from their host plants. 2. Larvae of Synchlora frondaria reared on three different host plants showed systematic differences in relative growth rate, survivorship and larval colouration. 3. Larval colouration varied across diet treatments in a way that was consistent with diet‐induced phenotypic plasticity, and larvae also exhibited characteristic decorating behaviour on all three hosts. 4. Larvae showed highest survivorship on Heterotheca subaxillaris (Asteraceae), and had significantly higher relative growth rates on H. subaxillaris (Asteraceae) and Lantana camara (Verbenaceae) than on Bejaria racemosa (Ericaceae). 5. Synchlora frondaria provides an example of a species where both decorating behaviour and phenotypic plasticity in larval colouration produce a cryptic form that is remarkably responsive to its background.     

Local adaptation for enhanced salt tolerance reduces non‐adaptive plasticity caused by osmotic stress

Organisms often respond to environmental change via phenotypic plasticity, in which an individual modulates its phenotype according to the environment. Highly variable or changing environments can exceed physiological limits and generate maladapted plastic phenotypes, which is termed nonadaptive plasticity. In some cases, selection may reduce the negative or disruptive impacts of environmental stress and produce locally adapted populations. Salt is an increasingly prevalent contaminant of freshwater systems and can induce nonadaptive plastic phenotypes for freshwater organisms like amphibians. Hyla cinerea is a frog species with populations inhabiting brackish, coastal habitats, so we use this species to test whether coastal populations are locally adapted to tolerate saltwater by determining how salt exposure during the embryonic and larval stages alters mortality and plastic developmental and metamorphic phenotypes of coastal and inland populations. Coastal frogs have higher survival, faster growth rates, and metamorphose sooner than inland frogs across salinities. Coastal frogs also metamorphose smaller (likely a consequence of earlier metamorphosis) yet maintain constant size, while higher salinities reduce metamorphic size for inland frogs. Coastal frogs evolved to minimize nonadaptive and disruptive impacts of saltwater during larval development and accelerate the larval period to reduce time spent in a stressful environment.     

Idealization in evolutionary developmental investigation: a tension between phenotypic plasticity and normal stages

Idealization is a reasoning strategy that biologists use to describe, model and explain that purposefully departs from features known to be present in nature. Similar to other strategies of scientific reasoning, idealization combines distinctive strengths alongside of latent weaknesses. The study of ontogeny in model organisms is usually executed by establishing a set of normal stages for embryonic development, which enables researchers in different laboratory contexts to have standardized comparisons of experimental results. Normal stages are a form of idealization because they intentionally ignore known variation in development, including variation associated with phenotypic plasticity (e.g. via strict control of environmental variables). This is a tension between the phenomenon of plasticity and the practice of staging that has consequences for evolutionary developmental investigation because variation is conceptually removed as a part of rendering model organisms experimentally tractable. Two compensatory tactics for mitigating these consequences are discussed: employing a diversity of model organisms and adopting alternative periodizations.     

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

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

The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole

Summary This study investigated the proximate basis of bimodally-distributed, environmentally-induced variation that occurs in natural populations of spade-foot toad tadpoles (Scaphiopus multiplicatus). Most individuals in most populations occur as a small, slowly-developing omnivore morph. In some of these same populations, a varying number of individuals occur as a large, rapidly-developing carnivore morph (Pfennig 1989). Censuses of 37 different natural ponds revealed that the frequency of the faster-developing carnivore morph correlated significantly positively with fairy shrimp density (their chief prey) and pond drying rate. By simultaneously varying two diet components and pond drying regime in artificial pools I found that only fairy shrimp density significantly affected the proportion of carnivores. Separate experiments established that the extent to which tadpoles developed the carnivore morphology correlated with shrimp density, and that morph determination depended on the ingestion of shrimp, not simply their presence. If a critical number of shrimp were ingested, the tadpole developed into a carnivore; if not, the tadpole developed by default into an omnivore. Thus a single cue — shrimp ingestion — triggers alternative ontogenetic trajectories. Using shrimp density to induce morph differentiation enables tadpoles to respond to their environment adaptively as shrimp are most abundant in highly ephemeral ponds, where the faster developing carnivores are favored.     

The role of phenotypic plasticity in shaping ecological networks

Plasticity-mediated changes in interaction dynamics and structure may scale up and affect the ecological network in which the plastic species are embedded. Despite their potential relevance for understanding the effects of plasticity on ecological communities, these effects have seldom been analysed. We argue here that, by boosting the magnitude of intra-individual phenotypic variation, plasticity may have three possible direct effects on the interactions that the plastic species maintains with other species in the community: may expand the interaction niche, may cause a shift from one interaction niche to another or may even cause the colonization of a new niche. The combined action of these three factors can scale to the community level and eventually expresses itself as a modification in the topology and functionality of the entire ecological network. We propose that this causal pathway can be more widespread than previously thought and may explain how interaction niches evolve quickly in response to rapid changes in environmental conditions. The implication of this idea is not solely eco-evolutionary but may also help to understand how ecological interactions rewire and evolve in response to global change.     

Evolution of phenotypic plasticity: Genetic differentiation and additive genetic variation for induced plant defence in wild arugula Eruca sativa

Phenotypic plasticity is the primary mechanism of organismal resilience to abiotic and biotic stress, and genetic differentiation in plasticity can evolve if stresses differ among populations. Inducible defence is a common form of adaptive phenotypic plasticity, and long‐standing theory predicts that its evolution is shaped by costs of the defensive traits, costs of plasticity and a trade‐off in allocation to constitutive versus induced traits. We used a common garden to study the evolution of defence in two native populations of wild arugula Eruca sativa (Brassicaceae) from contrasting desert and Mediterranean habitats that differ in attack by caterpillars and aphids. We report genetic differentiation and additive genetic variance for phenology, growth and three defensive traits (toxic glucosinolates, anti‐nutritive protease inhibitors and physical trichome barriers) as well their inducibility in response to the plant hormone jasmonic acid. The two populations were strongly differentiated for plasticity in nearly all traits. There was little evidence for costs of defence or plasticity, but constitutive and induced traits showed a consistent additive genetic trade‐off within each population for the three defensive traits. We conclude that these populations have evolutionarily diverged in inducible defence and retain ample potential for the future evolution of phenotypic plasticity in defence.     

Development and plasticity of endangered shrub Lindera melissifolia (Lauraceae) seedlings under contrasting light regimes

Lindera melissifolia (Walt.) Blume seedlings were raised in a growth chamber to determine the effects of light availability on shoot growth pattern, and basic leaf and stem growth. Lindera melissifolia seedlings exhibited a sympodial shoot growth pattern for 3 months following emergence from the soil medium, but this pattern was characterized by a reduction in leaf blade area approximately 30 days after emergence, followed by increases in leaf blade area. Seedlings receiving low light were 76% taller than seedlings receiving high light. Seedlings receiving low light also had larger leaf blade dimensions, blade area, seedling leaf area, and greater mass. Seedlings raised in high light had a greater proportional distribution of biomass in the roots, suggesting possible water stress from greater vapor pressure deficits. Furthermore, these seedlings displayed sharp angles of blade inclination and blade folding – acclimation that reduces exposure to light and subsequent higher leaf temperatures in open environments. These differences in morphological response to light resulted in high phenotypic variability in L. melissifolia seedlings. Lindera melissifolia seedling development showed a brief period of phenotypic plasticity, followed by ontogenetic plasticity. The short period of phenotypic plasticity may, however, have profound ecological implications for the conservation and recovery of this federally endangered shrub. Further experimentation should take into account the development of ontogenetic standards for comparisons of plant traits in addition to temporal standards.     

Phenotypic variation in colour pattern and seasonal plasticity in Eristalis hoverflies (Diptera: Syrphidae)

Abstract.

• 1 An examination of phenotypic variation in colour pattern was carried out on four Eristalis hoverfly species using museum material.
• 2 The amount of phenotypic variation varied substantially among the species with E.arbustorum being the most variable. The other species showed a wide colour pattern range but less variation within that range (E.abusivus and E.nemorum), or a narrow range of colour variation (E.horticola).
• 3 Sexual colour dimorphism was apparent in all four species, but most pronounced in E.abusivus and E.nemorum.
• 4 There were good phenotype-season relationships shown by both sexes in all species, except for female E.abusivus and E.nemorum, with paler insects being more abundant during the warmer summer months.
• 5 Female, but not male, E.arbustorum collected at inland sites were on average paler than those collected at coastal sites. This observation is considered with respect to temperature during the developmental stages.
• 6 The function of colour plasticity in hoverflies is discussed with reference to the need to maintain optimal thermal conditions for activity.

     

Effects of developmental stress on animal phenotype and performance: a quantitative review

Developmental stressors are increasingly recognised for their pervasive influence on the ecology and evolution of animals. In particular, many studies have focused on how developmental stress can give rise to variation in adult behaviour, physiology, and performance. However, there remains a poor understanding of whether general patterns exist in the effects and magnitude of phenotypic responses across taxonomic groups. Furthermore, given the extensive phenotypic variation that arises from developmental stressors, it remains important to ascertain how multiple processes may explain these responses. We compiled data from 111 studies to examine and quantify the effect of developmental stress on animal phenotype and performance from juveniles to adulthood, including studies from birds, reptiles, fish, mammals, insects, arachnids, and amphibians. Using meta‐analytic approaches, we show that across all studies there is, on average, a moderate to large negative effect of developmental stress exposure (posterior mean effect: |d| = ?0.51) on animal phenotype or performance. Additionally, we demonstrate that interactive effects of timing of stressor onset and the duration of exposure to stressors best explained variation in developmental stress responses. Animals exposed to stressors earlier in development had more‐positive responses than those with later onset, whereas longer duration of exposure to a stressor caused responses to be stronger in magnitude. However, the high amount of heterogeneity in our results, and the low degree of variance explained by fixed effects in both the meta‐analysis (R² = 0.034) and top‐ranked meta‐regression model (R² = 0.02), indicate that phenotypic responses to developmental stressors are likely highly idiosyncratic in nature and difficult to predict. Despite this, our analyses address a critical knowledge gap in understanding what effect developmental stress has on phenotypic variation in animals. Additionally, our results highlight important environmental and proximate factors that may influence phenotypic responses to developmental stressors.