Expression of sexual ornaments in a polymorphic species: phenotypic variation in response to environmental risk

Secondary sexual traits may evolve under the antagonistic context of sexual and natural selection. In some polymorphic species, these traits are only expressed during the breeding period and are differently expressed in alternative phenotypes. However, it is unknown whether such phenotypes exhibit phenotypic plasticity of seasonal ornamentations in response to environmental pressures such as in the presence of fish (predation risk). This is an important question to understand the evolution of polyphenisms. We used facultative paedomorphosis in newts as a model system because it involves the coexistence of paedomorphs that retain gills in the adult stage with metamorphs that have undergone metamorphosis, but also because newts exhibit seasonal sexual traits. Our aim was therefore to determine the influence of fish on the development of seasonal ornamentation in the two phenotypes of the palmate newt (Lissotriton helveticus). During the entire newt breeding period, we assessed the importance of phenotype and fish presence with an information‐theoretic approach. Our results showed that paedomorphs presented much less developed ornamentation than metamorphs and those ornamentations varied over time. Fish inhibited the development of sexual traits but differently between phenotypes: in contrast to metamorphs, paedomorphs lack the phenotypic plasticity of sexual traits to environmental risk. This study points out that internal and external parameters act in complex ways in the expression of seasonal sexual ornamentations and that similar environmental pressure can induce a contrasted evolution in alternative phenotypes.     

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

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

Rethinking phenotypic plasticity and its consequences for individuals,populations and species

Much research has been devoted to identify the conditions under which selection favours flexible individuals or genotypes that are able to modify their growth, development and behaviour in response to environmental cues, to unravel the mechanisms of plasticity and to explore its influence on patterns of diversity among individuals, populations and species. The consequences of developmental plasticity and phenotypic flexibility for the performance and ecological success of populations and species have attracted a comparatively limited but currently growing interest. Here, I re-emphasize that an increased understanding of the roles of plasticity in these contexts requires a ‘whole organism'' (rather than ‘single trait'') approach, taking into consideration that organisms are integrated complex phenotypes. I further argue that plasticity and genetic polymorphism should be analysed and discussed within a common framework. I summarize predictions from theory on how phenotypic variation stemming from developmental plasticity and phenotypic flexibility may affect different aspects of population-level performance. I argue that it is important to distinguish between effects associated with greater interindividual phenotypic variation resulting from plasticity, and effects mediated by variation among individuals in the capacity to express plasticity and flexibility as such. Finally, I claim that rigorous testing of predictions requires methods that allow for quantifying and comparing whole organism plasticity, as well as the ability to experimentally manipulate the level of and capacity for developmental plasticity and phenotypic flexibility independent of genetic variation.     

Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits

Background  

Many important evolutionary adaptations originate in the modification of gene regulatory circuits to produce new gene activity phenotypes. How do evolving populations sift through an astronomical number of circuits to find circuits with new adaptive phenotypes? The answer may often involve phenotypic plasticity. Phenotypic plasticity allows a genotype to produce different - alternative - phenotypes after non-genetic perturbations that include gene expression noise, environmental change, or epigenetic modification.     

Hormone signaling and phenotypic plasticity in nematode development and evolution

Phenotypic plasticity refers to the ability of an organism to adopt different phenotypes depending on environmental conditions. In animals and plants, the progression of juvenile development and the formation of dormant stages are often associated with phenotypic plasticity, indicating the importance of phenotypic plasticity for life-history theory. Phenotypic plasticity has long been emphasized as?a crucial principle in ecology and as facilitator of phenotypic evolution. In nematodes, several examples of phenotypic plasticity have been studied at the genetic and developmental level. In addition, the influence of different environmental factors has been investigated under laboratory conditions. These studies have provided detailed insight into the molecular basis of phenotypic plasticity and its?ecological and evolutionary implications. Here, we review recent studies on the formation of dauer larvae in Caenorhabditis elegans, the evolution of nematode parasitism and the generation of a novel feeding trait in Pristionchus pacificus. These examples reveal a conserved and co-opted role of an endocrine signaling module involving the steroid hormone dafachronic acid. We will discuss how hormone signaling might facilitate life-history and morphological evolution.     

Plasticity is a locally adapted trait with consequences for ecological dynamics in novel environments

Phenotypic plasticity is predicted to evolve in more variable environments, conferring an advantage on individual lifetime fitness. It is less clear what the potential consequences of that plasticity will have on ecological population dynamics. Here, we use an invertebrate model system to examine the effects of environmental variation (resource availability) on the evolution of phenotypic plasticity in two life history traits—age and size at maturation—in long‐running, experimental density‐dependent environments. Specifically, we then explore the feedback from evolution of life history plasticity to subsequent ecological dynamics in novel conditions. Plasticity in both traits initially declined in all microcosm environments, but then evolved increased plasticity for age‐at‐maturation, significantly so in more environmentally variable environments. We also demonstrate how plasticity affects ecological dynamics by creating founder populations of different plastic phenotypes into new microcosms that had either familiar or novel environments. Populations originating from periodically variable environments that had evolved greatest plasticity had lowest variability in population size when introduced to novel environments than those from constant or random environments. This suggests that while plasticity may be costly it can confer benefits by reducing the likelihood that offspring will experience low survival through competitive bottlenecks in variable environments. In this study, we demonstrate how plasticity evolves in response to environmental variation and can alter population dynamics—demonstrating an eco‐evolutionary feedback loop in a complex animal moderated by plasticity in growth.     

Evolution of phenotypic fluctuation under host-parasite interactions

Robustness and plasticity are essential features that allow biological systems to cope with complex and variable environments. In a constant environment, robustness, i.e., insensitivity of phenotypes, is expected to increase, whereas plasticity, i.e., the changeability of phenotypes, tends to diminish. Under a variable environment, existence of plasticity will be relevant. The robustness and plasticity, on the other hand, are related to phenotypic variances. As phenotypic variances decrease with the increase in robustness to perturbations, they are expected to decrease through the evolution. However, in nature, phenotypic fluctuation is preserved to a certain degree. One possible cause for this is environmental variation, where one of the most important “environmental” factors will be inter-species interactions. As a first step toward investigating phenotypic fluctuation in response to an inter-species interaction, we present the study of a simple two-species system that comprises hosts and parasites. Hosts are expected to evolve to achieve a phenotype that optimizes fitness. Then, the robustness of the corresponding phenotype will be increased by reducing phenotypic fluctuations. Conversely, plasticity tends to evolve to avoid certain phenotypes that are attacked by parasites. By using a dynamic model of gene expression for the host, we investigate the evolution of the genotype-phenotype map and of phenotypic variances. If the host–parasite interaction is weak, the fittest phenotype of the host evolves to reduce phenotypic variances. In contrast, if there exists a sufficient degree of interaction, the phenotypic variances of hosts increase to escape parasite attacks. For the latter case, we found two strategies: if the noise in the stochastic gene expression is below a certain threshold, the phenotypic variance increases via genetic diversification, whereas above this threshold, it is increased mediated by noise-induced phenotypic fluctuation. We examine how the increase in the phenotypic variances caused by parasite interactions influences the growth rate of a single host, and observed a trade-off between the two. Our results help elucidate the roles played by noise and genetic mutations in the evolution of phenotypic fluctuation and robustness in response to host–parasite interactions.     

The evolutionary ecology of alternative migratory tactics in salmonid fishes

Extensive individual variation in spatial behaviour is a common feature among species that exhibit migratory life cycles. Nowhere is this more evident than in salmonid fishes; individual fish may complete their entire life cycle in freshwater streams, others may migrate variable distances at sea and yet others limit their migrations to larger rivers or lakes before returning to freshwater streams to spawn. This review presents evidence that individual variation in migratory behaviour and physiology in salmonid fishes is controlled by developmental thresholds and that part of the variation in proximal traits activating the development of alternative migratory tactics is genetically based. We summarize evidence that alternative migratory tactics co‐exist within populations and that all individuals may potentially adopt any of the alternative phenotypes. Even though intra‐specific genetic divergence of migratory tactics is uncommon, it may occur if female competition for oviposition sites results in spawning segregation of alternative phenotypes. Because of their polygenic nature, alternative migratory tactics are considered as threshold traits. Threshold traits have two characteristics: an underlying 'liability' trait that varies in a continuous fashion, and a threshold value which is responsible for the discreetness observed in phenotypic distribution. We review evidence demonstrating that body size is an adequate proxy for the liability trait controlling the decision to migrate, but that the same phenotypic outcome (anadromy or residency) may be reached by different developmental pathways. The evidence suggesting a significant heritable component in the development of alternative migratory tactics is subsequently reviewed, leading us to conclude that alternative migratory tactics have considerable potential to respond to selection and evolve. We review what is known about the proximal physiological mechanisms mediating the translation of the continuous value of the liability trait into a discontinuous migratory tactic. We conclude by identifying several avenues for future research, including testing the frequency‐dependent selection hypothesis, establishing the relative importance of adaptive phenotypic plasticity in explaining some geographic gradients in migratory behaviour and identifying the physiological and genetic basis of the switching mechanisms responsible for alternative migratory tactics.     

Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism

Many polyphenisms are examples of adaptive phenotypic plasticity where a single genotype produces distinct phenotypes in response to environmental cues. Such alternative phenotypes occur as winged and wingless parthenogenetic females in the pea aphid (Acyrthosiphon pisum). However, the proportion of winged females produced in response to a given environmental cue varies between clonal genotypes. Winged and wingless phenotypes also occur in males of the sexual generation. In contrast to parthenogenetic females, wing production in males is environmentally insensitive and controlled by the sex-linked, biallelic locus, aphicarus (api). Hence, environmental or genetic cues induce development of winged and wingless phenotypes at different stages of the pea aphid life cycle. We have tested whether allelic variation at the api locus explains genetic variation in the propensity to produce winged females. We assayed clones from an F2 cross that were heterozygous or homozygous for alternative api alleles for their propensity to produce winged offspring. We found that clones with different api genotypes differed in their propensity to produce winged offspring. The results indicate genetic linkage of factors controlling the female wing polyphenism and male wing polymorphism. This finding is consistent with the hypothesis that genotype by environment interaction at the api locus explains genetic variation in the environmentally cued wing polyphenism.     

Insulin signalling underlies both plasticity and divergence of a reproductive trait in Drosophila

Phenotypic plasticity is the ability of a single genotype to yield distinct phenotypes in different environments. The molecular mechanisms linking phenotypic plasticity to the evolution of heritable diversification, however, are largely unknown. Here, we show that insulin/insulin-like growth factor signalling (IIS) underlies both phenotypic plasticity and evolutionary diversification of ovariole number, a quantitative reproductive trait, in Drosophila. IIS activity levels and sensitivity have diverged between species, leading to both species-specific ovariole number and species-specific nutritional plasticity in ovariole number. Plastic range of ovariole number correlates with ecological niche, suggesting that the degree of nutritional plasticity may be an adaptive trait. This demonstrates that a plastic response conserved across animals can underlie the evolution of morphological diversity, underscoring the potential pervasiveness of plasticity as an evolutionary mechanism.     

Evolution and maintenance of the environmental component of the phenotypic variance: benefit of plastic traits under changing environments

How environmental variances in quantitative traits are influenced by variable environments is an important problem in evolutionary biology. In this study, the evolution and maintenance of phenotypic variance in a plastic trait under stabilizing selection are investigated. The mapping from genotypic value to phenotypic value of the quantitative trait is approximated by a linear reaction norm, with genotypic effects on its phenotypic mean and sensitivity to environment. The environmental deviation is assumed to be decomposed into environmental quality, which interacts with genotypic value, and residual developmental noise, which is independent of genotype. Environmental quality and the optimal phenotype of stabilizing selection are allowed to randomly fluctuate in both space and time, and individuals migrate equally before development and reproduction among different niches. Analyses show that phenotypic plasticity is adaptive within variable environments if correlations have become established between the optimal phenotype and environmental quality in space and/or time. The evolved plasticity increases with variances in optimal phenotypes and correlations between optimal phenotype and environmental quality; this further induces increases in mean fitness and the environmental variance in the trait. Under certain circumstances, however, the environmental variance may decrease with increase in variation in environmental quality.     

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。     

Relaxed genetic constraint is ancestral to the evolution of phenotypic plasticity

Phenotypic plasticity--the capacity of a single genotype to produce different phenotypes in response to varying environmental conditions--is widespread. Yet, whether, and how, plasticity impacts evolutionary diversification is unclear. According to a widely discussed hypothesis, plasticity promotes rapid evolution because genes expressed differentially across different environments (i.e., genes with "biased" expression) experience relaxed genetic constraint and thereby accumulate variation faster than do genes with unbiased expression. Indeed, empirical studies confirm that biased genes evolve faster than unbiased genes in the same genome. An alternative hypothesis holds, however, that the relaxed constraint and faster evolutionary rates of biased genes may be a precondition for, rather than a consequence of, plasticity's evolution. Here, we evaluated these alternative hypotheses by characterizing evolutionary rates of biased and unbiased genes in two species of frogs that exhibit a striking form of phenotypic plasticity. We also characterized orthologs of these genes in four species of frogs that had diverged from the two plastic species before the plasticity evolved. We found that the faster evolutionary rates of biased genes predated the evolution of the plasticity. Furthermore, biased genes showed greater expression variance than did unbiased genes, suggesting that they may be more dispensable. Phenotypic plasticity may therefore evolve when dispensable genes are co-opted for novel function in environmentally induced phenotypes. Thus, relaxed genetic constraint may be a cause--not a consequence--of the evolution of phenotypic plasticity, and thereby contribute to the evolution of novel traits.     

Why are individuals so different from each other?

An important contributor to the differences between individuals derives from their plasticity. Such plasticity is widespread in organisms from the simple to the most complex. Adaptability plasticity enables the organism to cope with a novel challenge not previously encountered by its ancestors. Conditional plasticity appears to have evolved from repeated challenges from the environment so that the organism responds in a particular manner to the environment in which it finds itself. The resulting phenotypic variation can be triggered during development in a variety of ways, some mediated through the parent''s phenotype. Sometimes the organism copes in suboptimal conditions trading off reproductive success against survival. Whatever the adaptedness of the phenotype, each of the many types of plasticity demonstrates how a given genotype will express itself differently in different environmental conditions—a field of biology referred to as the study of epigenetics. The ways in which epigenetic mechanisms may have evolved are discussed, as are the potential impacts on the evolution of their descendants.     

Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

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.     

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

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