Phenotypic plasticity in development and evolution: facts and concepts

This theme issue pursues an exploration of the potential of taking into account the environmental sensitivity of development to explaining the evolution of metazoan life cycles, with special focus on complex life cycles and the role of developmental plasticity. The evolution of switches between alternative phenotypes as a response to different environmental cues and the evolution of the control of the temporal expression of alternative phenotypes within an organism''s life cycle are here treated together as different dimensions of the complex relationships between genotype and phenotype, fostering the emergence of a more general and comprehensive picture of phenotypic evolution through a quite diverse sample of case studies. This introductory article reviews fundamental facts and concepts about phenotypic plasticity, adopting the most authoritative terminology in use in the current literature. The main topics are types and components of phenotypic variation, the evolution of organismal traits through plasticity, the origin and evolution of phenotypic plasticity and its adaptive value.     

Evolution of alternative insect life histories in stochastic seasonal environments

Deterministic seasonality can explain the evolution of alternative life history phenotypes (i.e., life history polyphenism) expressed in different generations emerging within the same year. However, the influence of stochastic variation on the expression of such life history polyphenisms in seasonal environments is insufficiently understood. Here, we use insects as a model and explore (1) the effects of stochastic variation in seasonality and (2) the life cycle on the degree of life history differentiation among the alternative developmental pathways of direct development and diapause (overwintering), and (3) the evolution of phenology. With numerical simulation, we determine the values of development (growth) time, growth rate, body size, reproductive effort, adult life span, and fecundity in both the overwintering and directly developing generations that maximize geometric mean fitness. The results suggest that natural selection favors the expression of alternative life histories in the alternative developmental pathways even when there is stochastic variation in seasonality, but that trait differentiation is affected by the developmental stage that overwinters. Increasing environmental unpredictability induced a switch to a bet‐hedging type of life history strategy, which is consistent with general life history theory. Bet‐hedging appeared in our study system as reduced expression of the direct development phenotype, with associated changes in life history phenotypes, because the fitness value of direct development is highly variable in uncertain environments. Our main result is that seasonality itself is a key factor promoting the evolution of seasonally polyphenic life histories but that environmental stochasticity may modulate the expression of life history phenotypes.     

Developmental plasticity and acclimation both contribute to adaptive responses to alternating seasons of plenty and of stress in <Emphasis Type="Italic">Bicyclus</Emphasis> butterflies

Plasticity is a crucial component of the life cycle of invertebrates that live as active adults throughout wet and dry seasons in the tropics. Such plasticity is seen in the numerous species of Bicyclus butterflies in Africa which exhibit seasonal polyphenism with sequential generations of adults with one or other of two alternative phenotypes. These differ not only in wing pattern but in many other traits. This divergence across a broad complex of traits is associated with survival and reproduction either in a wet season that is favourable in terms of resources, or mainly in a dry season that is more stressful. This phenomenon has led us to examine the bases of the developmental plasticity in a model species, B. anynana, and also the evolution of key adult life history traits, including starvation resistance and longevity. We now understand something about the processes that generate variation in the phenotype, and also about the ecological context of responses to environmental stress. The responses clearly involve a mix of developmental plasticity as cued by different environments in pre-adult development, and the acclimation of life history traits in adults to their prevailing environment.     

SEASONALITY MAINTAINS ALTERNATIVE LIFE‐HISTORY PHENOTYPES

Many organisms express discrete alternative phenotypes (polyphenisms) in relation to predictable environmental variation. However, the evolution of alternative life‐history phenotypes remains poorly understood. Here, we analyze the evolution of alternative life histories in seasonal environments by using temperate insects as a model system. Temperate insects express alternative developmental pathways of diapause and direct development, the induction of a certain pathway affecting fitness through its life‐history correlates. We develop a methodologically novel and holistic simulation model and optimize development time, growth rate, body size, reproductive effort, and adult life span simultaneously in both developmental pathways. The model predicts that direct development should be associated with shorter development time (duration of growth) and adult life span, higher growth rate and reproductive effort, smaller body size as well as lower fecundity compared to the diapause pathway, because the two generations divide the available time unequally. These predictions are consistent with many empirical data. Our analysis shows that seasonality alone can explain the evolution of alternative life histories.     

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.     

Carryover effects of predation risk on postembryonic life-history stages in a freshwater shrimp

For organisms with complex life histories it is well known that risk experienced early in life, as embryos or larvae, may have effects throughout the life cycle. Although carryover effects have been well documented in invertebrates with different levels of parental care, there are few examples of predator-induced responses in externally brooded embryos. Here, we studied the effects of nonlethal predation risk throughout the embryonic development of newly spawned eggs carried by female shrimp on the timing of egg hatching, hatchling morphology, larval development and juvenile morphology. We also determined maternal body mass at the end of the embryonic period. Exposure to predation risk cues during embryonic development led to larger larvae which also had longer rostra but reached the juvenile stage sooner, at a smaller size and with shorter rostra. There was no difference in hatching timing, but changes in larval morphology and developmental timing showed that the embryos had perceived waterborne substances indicative of predation risk. In addition to carryover effects on larval and juvenile stages, predation threat provoked a decrease of body mass in mothers exposed to predator cues while brooding. Our results suggest that risk-exposed embryos were able to recognize the same infochemicals as their mothers, manifesting a response in the free-living larval stage. Thus, future studies assessing anti-predator phenotypes should include embryonic development, which seems to determine the morphology and developmental time of subsequent life-history stages according to perceived environmental conditions.     

Origin and evolution of alternative developmental strategies in amphibious sarcopterygian parasites (Platyhelminthes, Monogenea, Polystomatidae)

Most integrative studies involving phylogenetic, developmental and ecological trends showed that the diversity of developmental modifications among the Platyhelminthes was linked to transmission opportunity pressures. For parasitic flatworms with complex life cycles it was suggested that the evolutionary forces that constrained or enhanced developmental strategies implied heterochronic patterns. Similar patterns were also reported from the Monogenea with direct life cycles, especially for Polystomatidae, which infest amphibious Sarcopterygians. Polystoma, whose members are recovered almost exclusively from anuran hosts of the Neobatrachia, is capable of following two alternative developmental strategies depending on the physiological stage of its host. Processes by which parasites reach maturity are strikingly different, and lead to discrete adult phenotypes within the same parasite species. In the present study, we investigate the origin and evolution of developmental patterns of polystomatids in a phylogenetic framework, using an integrative approach of heterochrony and evolutionary ecology. The results suggest that both phenotypes have coexisted during the early stages of polystome evolution, and that neither of them can be considered as the ancestral one. The two developmental pathways, each associated with one life cycle, may have arisen independently prior to polystome diversification, when strictly aquatic sarcopterygians attempted colonization of temporary freshwater environments. The occurrence of these two patterns within species of the genus Polystoma is suggested to reflect the ancestral condition, and to have allowed both developmental strategies to be successful depending on shifts in transmission opportunities. Thus, host evolutionary ecology may be the main factor in shaping developmental strategies within polystomatids.     

On the Evolutionary Developmental Biology of Speciation

The mainstream approaches to the study of speciation and clade diversification have extensively focused on genetic mechanisms and ecological contexts, while much less attention has been paid to the role of development. In this paper we provide materials to support the thesis that taking development into the picture of evolutionary processes can bring important insights on how species multiply and diversify. Evidence that developmentally entangled evolutionary factors are important in speciation comes from different lines of investigation that can be broadly grouped under three headings: evolvability, phenotypic plasticity, and phenology. Evolvability enters the scene through the complexity of the genotype-phenotype map, the developmental link between transmissible genetic information and selectable phenotypes. Phenotypic plasticity can act as a facilitator for speciation, promoting diversification at different stages of the speciation process, as well as generating novel targets and novel trade-offs for evolutionary processes. The formal inclusion of the developmental time axis in speciation models widens the scope for investigating the onset and/or reinforcement of reproductive barriers through a range of situations along an organism??s life cycle. Overall, developmental processes can contribute to speciation and diversification at different stages of the speciation process, at different levels of biological organization and along the organism??s whole life cycle.     

Ontogenetic stage-dependent effect of temperature on developmental and metabolic rates in a holometabolous insect

Different hypotheses attempt to explain how different stages of organisms with complex life cycles respond to environmental changes. Most studies have focused at the among-species level showing similar responses to temperature throughout ontogeny. However, there is no agreement about the pattern expected at the intraspecific scale where a strong selective effect is expected. In this paper, we studied the effects of thermal treatments on a life history trait (developmental rate) and a physiological trait (metabolic rate) during development in the fruitfly Drosophila buzzatii. First, we estimated the rate of development during larval life (LDR) and the pupal stage (PDR) in flies derived from two natural populations exposed to several thermal treatments. Our results showed that the developmental rate ratio, LDR/PDR, did not vary between populations, and that the effects of thermal treatments were stage specific. Second, we studied the relationship between developmental rate (DR) and metabolic rate (MR) in each life cycle stage. We found that allometric relationships between DR and MR varied throughout ontogeny, a pattern that shed light on the mechanisms responsible for thermal plasticity. We conclude that, although different populations may show developmental rate isomorphy; larvae and pupae may choose alternative “decisions” in terms of life-history evolution and physiological traits when confronted to different thermal environments.     

The effects of perceived predation risk on pre- and post-metamorphic phenotypes in the common frog

Where organisms undergo radical changes in habitat during ontogeny, dramatic phenotypic reshaping may be required. However, physiological and functional interrelationships may constrain the extent to which an individual's phenotype can be equally well adapted to their habitat throughout the life cycle. The phenotypic response of tadpoles to the presence of a predator has been reported for several species of anuran but the potential post-metamorphic consequences have rarely been considered. We reared common frog Rana temporaria tadpoles in the presence or absence of a larval odonate predator, Aeshna juncea , and examined the consequences of the resulting phenotypic adjustment in the aquatic larval stage of the life cycle for the terrestrial juvenile phenotype. In early development tadpoles developed deeper tail fins and muscles in response to the predator and, in experimental trials, swam further than those reared in the absence of a predator. While the difference in swimming ability remained significant throughout the larval period, by the onset of metamorphosis we could no longer detect any differences in the morphological parameters measured. The corresponding post-metamorphic phenotypes also did not initially differ in terms of morphology. At 12 weeks post-metamorphosis, however, froglets that developed from predator-exposed tadpoles swam more slowly and less far than those that developed from tadpoles reared in the absence of predators, the opposite trend to that observed in the larval stage of the life cycle, and had narrower femurs. These results suggest that there may be long-term costs for subsequent life-history stages of tailoring the larval phenotype to prevailing environmental conditions.     

Alternative parasite development in transmission strategies: how time flies!

Among parasitic platyhelminths with complex life cycles, it has been well documented that transmission opportunities are the main forces shaping the diversity of life‐history traits and parasite developmental strategies. While deviations in the development pathway usually involve shortening of life cycles, their extension may also occur following perception of remaining time by parasites. Polystoma gallieni, the monogenean parasite of Hyla meridionalis, is able to trigger two alternative developmental strategies depending on the physiological stage of the tadpoles upon which larvae attach. The distribution and reproductive outputs of both resulting phenotypes were surveyed to address questions about the dynamics of transmission in natural environments. Because modifications in the completion of life cycles can have drawbacks which may perturb the dynamic equilibrium of the resulting host–parasite systems, experimental infestations were also performed to assess parasite–parasite interactions. Our results suggest that the bladder adult phenotype, which involves transmission between frogs and tadpoles, is supplied secondarily by the branchial phenotype which involves transmission between tadpoles and metamorphs. They also support the occurrence of finely tuned trade‐offs between hosts and parasites and highlight positive trends behind the extension of direct life cycles, in which host‐derived signals account for the remaining time to achieve parasitic transmission.     

Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles

Social environments experienced at different developmental stages profoundly shape adult behavioural and neural phenotypes, and may have important interactive effects. We asked if social experience before and after weaning influenced adult social cognition in male prairie voles. Animals were raised either with or without fathers and then either housed singly or in sibling pairs. Males that were socially deprived before (fatherless) and after (singly housed) weaning did not demonstrate social recognition or dissociate spatial from social information. We also examined oxytocin and vasopressin receptors (OTR and V1aR) in areas of the forebrain associated with social behaviour and memory. Pre- and post-wean experience differentially altered receptor expression in several structures. Of note, OTR in the lateral septum—an area in which oxytocin inhibits social recognition—was greatest in animals that did not clearly demonstrate social recognition. The combination of absentee fathers on V1aR in the retrosplenial cortex and single housing on OTR in the septohippocampal nucleus produced a unique phenotype previously found to be associated with poor reproductive success in nature. We demonstrate that interactive effects of early life experiences throughout development have tremendous influence over brain–behaviour phenotype and can buffer potentially negative outcomes due to social deprivation.     

Flexibility in annual cycles of birds: implications for endocrine control mechanisms

Life cycles of birds and other vertebrates are composed of series of life history stages each with unique combinations of morphological, physiological and behavioral characteristics. For example, in the white-crowned sparrow, Zonotrichia leucophrys, the nonbreeding stage (winter), vernal migration, breeding, moult and autumn migration stages occur in a fixed and repeated sequence where each cycle is 1 year. The sequence of stages cannot be reversed. Transition from one life history stage to the next and the duration of each stage are dependent upon a combination of genetic factors and environmental cues. The latter include the annual change in photoperiod and the former may involve endogenous circannual rhythms. All vertebrates also express the emergency life history stage in response to perturbations of the environment that allow individuals to cope with the unpredictable. Each stage has a unique repertoire of sub-stages (physiological and behavioral, and to a lesser extent morphological), which can be expressed in any sequence or combination to give the state of the individual at any point in its life cycle. This state is presumably maximally adapted to the environmental conditions at that time. Although the sequence of life history stages appears to be innate, the rate of transition from stage to stage, and the expression of sub-stages can be modified by the local environmental factors and, particularly, by social cues. These environmental cues acting on the phenotype result in neuroendocrine and endocrine secretions that regulate development of the life history stage, its onset once mature capability has been attained, and then terminate it at the appropriate times. The environmental cues (from the physical and social environment) impart a strong experiential component. Because, there is a set number of life history stages and their sub-stages, there is a finite number of states that can be expressed in response to the environmental variation experienced by the individual. The more life history stages a phenotype expresses, the less flexibility is there in the overall timing of these stages owing to the time taken to develop one stage and terminate the last (about 1 month). However, many phenotypes have increased flexibility in their life cycles by overlapping some life history stages (i.e., with overlapping mature capability of two or perhaps even more stages). Another potential strategy is to dissociate some components of a life history stage so they are expressed at other times of year thus spreading out potential costs associated with that life history stage. Examples of both overlap and dissociation of life history stages are given including implications for hormonal control mechanisms.     

Effects of Social Structure on the Behaviour and Performance of Alternative Reproductive Phenotypes in Male Rock Shrimp, Rhynchocinetes typus

Males that adopt alternative mating tactics within a conditional strategy often undergo costly morphological changes when switching to the next phenotype during ontogeny. Whether costs of changing to a subsequent reproductive phenotype are outweighed by a higher mating probability may depend on the frequencies of different phenotypes in a group of competitors. Benefits and costs associated with different phenotype frequencies depend on interactions within and between alternative phenotypes, but the underlying behavioural mechanisms have rarely been studied. Herein, we used the rock shrimp Rhynchocinetes typus as a model: ontogenetic male stages of this species differ in morphological and behavioural traits that indicate alternative reproductive phenotypes. The small, subordinate, male stage (typus) develops via several intermediate stages (intermedius) to the dominant male stage (robustus): in competitive interactions the typus males usually employ the sneaking tactic, while the robustus males invariably employ the monopolizing fighter tactic. In laboratory experiments, we manipulated phenotype frequencies to examine whether there are frequency‐dependent effects on searching behaviour, aggressiveness and mating probability. With increasing frequency of robustus males, the rate of aggressive interactions among them increased. Furthermore, robustus males increased walking velocity when more than one robustus male was present. In contrast, typus males did not adjust their searching or aggressive behaviour. The increase of aggressive interactions among robustus males provided more opportunities for typus males to seize a temporarily unguarded female. While typus males exploit fights among robustus males that produce mating opportunities for them, robustus males benefit from typus males, which reveal the presence of receptive females. We suggest that each phenotype benefits from the presence of the other phenotype and suffers costly interference among individuals of the same phenotype. Whether frequency‐dependent effects on the mating probability of subordinates also affect their ontogenetic switchpoint should be examined in future studies.     

Resource polyphenism increases species richness: a test of the hypothesis

A major goal of evolutionary biology is to identify the causes of diversification and to ascertain why some evolutionary lineages are especially diverse. Evolutionary biologists have long speculated that polyphenism—where a single genome produces alternative phenotypes in response to different environmental stimuli—facilitates speciation, especially when these alternative phenotypes differ in resource or habitat use, i.e. resource polyphenism. Here, we present a series of replicated sister-group comparisons showing that fishes and amphibian clades in which resource polyphenism has evolved are more species rich, and have broader geographical ranges, than closely related clades lacking resource polyphenism. Resource polyphenism may promote diversification by facilitating each of the different stages of the speciation process (isolation, divergence, reproductive isolation) and/or by reducing a lineage''s risk of extinction. Generally, resource polyphenism may play a key role in fostering diversity, and species in which resource polyphenism has evolved may be predisposed to diversify.     

The control of morph development in the parasitic nematode Strongyloides ratti.

The parasitic nematode Strongyloides ratti has a complex life cycle. The progeny of the parasitic females can develop into three distinct morphs, namely directly developing infective third-stage larvae (iL3s), free-living adult males and free-living adult females. We have analysed of the effect of host immune status (an intra-host factor), environmental temperature (an extra-host factor) and their interaction on the proportion of larvae that develop into these three morphs. The results are consistent with the developmental decision of larvae being controlled by at least two discrete developmental switches. One is a sex-determination event that is affected by host immune status and the other is a switch between alternative female morphs that is affected by both host immune status and environmental temperature. These findings clarify the basis of the life cycle of S. ratti and demonstrate how such complex life cycles can result from a combination of simple developmental switches.     

Epigenomic reprogramming of the developing reproductive tract and disease susceptibility in adulthood

During development, epigenetic programs are "installed" on the genome that direct differentiation and normal tissue and organ function in adulthood. Consequently, development is also a period of susceptibility to reprogramming of the epigenome. Developmental reprogramming occurs when an adverse stimulus or insult interrupts the proper "install" of epigenetic programs during development, reprogramming normal physiologic responses in such a way as to promote disease later in life. Some of the best examples of developmental reprogramming involve the reproductive tract, where early life exposures to environmental estrogens can increase susceptibility to benign and malignant tumors in adulthood including leiomyoma (fibroids), endometrial, and prostate cancer. Although specific mechanism(s) by which environmental estrogens reprogram the developing epigenome were unknown, both DNA and histone methylation were considered likely targets for epigenetic reprogramming. We have now identified a mechanism by which developmental exposures to environmental estrogens reprogram the epigenome by inducing inappropriate activation of nongenomic estrogen receptor (ER) signaling. Activation of nongenomic ER signaling via the phosphotidylinositol-3-kinase (PI3K) pathway activates the kinase AKT/PKB in the developing reproductive tract, which phosphorylates the histone lysine methyltransferase (HKMT) EZH2, the key "installer" of epigenetic histone H3 lysine 27 trimethylation (H3K27me3). AKT phosphorylation inactivates EZH2, decreasing levels of H3K27 methylation, a repressive mark that inhibits gene expression, in the developing uterus. As a result of this developmental reprogramming, many estrogen-responsive genes become hypersensitive to estrogen in adulthood, exhibiting elevated expression throughout the estrus cycle, and resulting in a "hyper-estrogenized" phenotype in the adult uterus that promotes development of hormone-dependent tumors.     

Flight performance in the altricial zebra finch: Developmental effects and reproductive consequences

The environmental conditions animals experience during development can have sustained effects on morphology, physiology, and behavior. Exposure to elevated levels of stress hormones (glucocorticoids, GCs) during development is one such condition that can have long‐term effects on animal phenotype. Many of the phenotypic effects of GC exposure during development (developmental stress) appear negative. However, there is increasing evidence that developmental stress can induce adaptive phenotypic changes. This hypothesis can be tested by examining the effect of developmental stress on fitness‐related traits. In birds, flight performance is an ideal metric to assess the fitness consequences of developmental stress. As fledglings, mastering takeoff is crucial to avoid bodily damage and escape predation. As adults, takeoff can contribute to mating and foraging success as well as escape and, thus, can affect both reproductive success and survival. We examined the effects of developmental stress on flight performance across life‐history stages in zebra finches (Taeniopygia guttata). Specifically, we examined the effects of oral administration of corticosterone (CORT, the dominant avian glucocorticoid) during development on ground‐reaction forces and velocity during takeoff. Additionally, we tested for associations between flight performance and reproductive success in adult male zebra finches. Developmental stress had no effect on flight performance at all ages. In contrast, brood size (an unmanipulated variable) had sustained, negative effects on takeoff performance across life‐history stages with birds from small broods performing better than birds from large broods. Flight performance at 100 days posthatching predicted future reproductive success in males; the best fliers had significantly higher reproductive success. Our results demonstrate that some environmental factors experienced during development (e.g. clutch size) have stronger, more sustained effects than others (e.g. GC exposure). Additionally, our data provide the first link between flight performance and a direct measure of reproductive success.