Frog hatchlings use early environmental cues to produce an anticipatory resource-use phenotype.

Developmental plasticity can occur at any life stage, but plasticity that acts early in development may give individuals a competitive edge later in life. Here, we asked if early (pre-feeding) exposure to a nutrient-rich resource impacts hatchling morphology in Mexican spadefoot toad tadpoles, Spea multiplicata. A distinctive carnivore morph can be induced when tadpoles eat live fairy shrimp. We investigated whether cues from shrimp--detected before individuals are capable of feeding--alter hatchling morphology such that individuals could potentially take advantage of this nutritious resource once they begin feeding. We found that hatchlings with early developmental exposure to shrimp were larger and had larger jaw muscles--traits that, at later stages, increase a tadpole's competitive ability for shrimp. These results suggest that early developmental stages can assess and respond to environmental cues by producing resource-use phenotypes appropriate for future conditions. Such anticipatory plasticity may be an important but understudied form of developmental plasticity.

Disentangling the developmental origins of a novel phenotype: enhancement versus reversal of environmentally induced gene expression.

Increasing evidence suggests that many novel traits might have originated via plasticity-led evolution (PLE). Yet, little is known of the developmental processes that underpin PLE, especially in its early stages. One such process is 'phenotypic accommodation', which occurs when, in response to a change in the environment, an organism experiences adjustments across variable parts of its phenotype that improve its fitness. Here, we asked if environmentally induced changes in gene expression are enhanced or reversed during phenotypic accommodation of a novel, complex phenotype in spadefoot toad tadpoles (Spea multiplicata). More genes than expected were affected by both the environment and phenotypic accommodation in the liver and brain. However, although phenotypic accommodation primarily reversed environmentally induced changes in gene expression in liver tissue, it enhanced these changes in brain tissue. Thus, depending on the tissue, phenotypic accommodation may either minimize functional disruption via reversal of gene expression patterns or promote novelty via enhancement of existing expression patterns. Our study thereby provides insights into the developmental origins of a novel phenotype and the incipient stages of PLE.

Phenotypic plasticity, canalization, and the origins of novelty: Evidence and mechanisms from amphibians.

A growing number of biologists have begun asking whether environmentally induced phenotypic change--'phenotypic plasticity'--precedes and facilitates the origin and canalization of novel, complex phenotypes. However, such 'plasticity-first evolution' (PFE) remains controversial. Here, we summarize the PFE hypothesis and describe how it can be evaluated in natural systems. We then review the evidence for PFE from amphibians (a group in which phenotypic plasticity is especially widespread) and describe how phenotypic plasticity might have facilitated macroevolutionary change. Finally, we discuss what is known about the proximate mechanisms of PFE in amphibians. We close with suggestions for future research. As we describe, amphibians offer some of the best support for plasticity's role in the origin of evolutionary novelties.

Evolutionary rescue via transgenerational plasticity: Evidence and implications for conservation.

When a population experiences severe stress from a changing environment, evolution by natural selection can prevent its extinction, a process dubbed "evolutionary rescue." However, evolution may be unable to track the sort of rapid environmental change being experienced by many modern-day populations. A potential solution is for organisms to respond to environmental change through phenotypic plasticity, which can buffer populations against change and thereby buy time for evolutionary rescue. In this review, we examine whether this process extends to situations in which the environmentally induced response is passed to offspring. As we describe, theoretical and empirical studies suggest that such "transgenerational plasticity" can increase population persistence. We discuss the implications of this process for conservation biology, outline potential limitations, and describe some applications. Generally, transgenerational plasticity may be effective at buying time for evolutionary rescue to occur.

Transcriptomic bases of a polyphenism.

Polyphenism-in which multiple distinct phenotypes are produced from a single genotype owing to differing environmental conditions-is commonplace, but its molecular bases are poorly understood. Here, we examine the transcriptomic bases of a polyphenism in Mexican spadefoot toads (Spea multiplicata). Depending on their environment, their tadpoles develop into either a default "omnivore" morph or a novel "carnivore" morph. We compared patterns of gene expression among sibships that exhibited high versus low production of carnivores when reared in conditions that induce the carnivore morph versus those that do not. We found that production of the novel carnivore morph actually involved changes in fewer genes than did the maintenance of the default omnivore morph in the inducing environment. However, only body samples showed this pattern; head samples showed the opposite pattern. We also found that changes to lipid metabolism (especially cholesterol biosynthesis) and peroxisome contents and function might be crucial for establishing and maintaining differences between the morphs. Thus, our findings suggest that carnivore phenotype might have originally evolved following the breakdown of robustness mechanisms that maintain the default omnivore phenotype, and that the carnivore morph is developmentally regulated by lipid metabolism and peroxisomal form, function, and/or signaling. This study also serves as a springboard for further exploration into the nature and causes of plasticity in an emerging model system.

Plasticity-led evolution: A survey of developmental mechanisms and empirical tests.

Recent years have witnessed increased interest in evaluating whether phenotypic plasticity can precede, facilitate, and possibly even bias adaptive evolution. Despite accumulating evidence for "plasticity-led evolution" (i.e., "PLE"), critical gaps remain, such as: how different developmental mechanisms influence PLE; whether some types of traits and taxa are especially prone to experience PLE; and what studies are needed to drive the field forward. Here, we begin to address these shortcomings by first speculating about how various features of development-modularity, flexible regulation, and exploratory mechanisms-might impact and/or bias whether and how PLE unfolds. We then review and categorize the traits and taxa used to investigate PLE. We do so both to identify systems that may be well-suited for studying developmental mechanisms in a PLE context and to highlight any mismatches between PLE theory and existing empirical tests of this theory. We conclude by providing additional suggestions for future research. Our overarching goal is to stimulate additional work on PLE and thereby evaluate plasticity's role in evolution.

Plasticity-led evolution: evaluating the key prediction of frequency-dependent adaptation.

Plasticity-led evolution occurs when a change in the environment triggers a change in phenotype via phenotypic plasticity, and this pre-existing plasticity is subsequently refined by selection into an adaptive phenotype. A critical, but largely untested prediction of plasticity-led evolution (and evolution by natural selection generally) is that the rate and magnitude of evolutionary change should be positively associated with a phenotype's frequency of expression in a population. Essentially, the more often a phenotype is expressed and exposed to selection, the greater its opportunity for adaptive refinement. We tested this prediction by competing against each other spadefoot toad tadpoles from different natural populations that vary in how frequently they express a novel, environmentally induced carnivore ecomorph. As expected, laboratory-reared tadpoles whose parents were derived from populations that express the carnivore ecomorph more frequently were superior competitors for the resource for which this ecomorph is specialized-fairy shrimp. These tadpoles were better at using this resource both because they were more efficient at capturing and consuming shrimp and because they produced more exaggerated carnivore traits. Moreover, they exhibited these more carnivore-like features even without experiencing the inducing cue, suggesting that this ecomorph has undergone an extreme form of plasticity-led evolution-genetic assimilation. Thus, our findings provide evidence that the frequency of trait expression drives the magnitude of adaptive refinement, thereby validating a key prediction of plasticity-led evolution specifically and adaptive evolution generally.

Multiple models generate a geographical mosaic of resemblance in a Batesian mimicry complex.

Batesian mimics-benign species that receive protection from predation by resembling a dangerous species-often occur with multiple model species. Here, we examine whether geographical variation in the number of local models generates geographical variation in mimic-model resemblance. In areas with multiple models, selection might be relaxed or even favour imprecise mimicry relative to areas with only one model. We test the prediction that model-mimic match should vary with the number of other model species in a broadly distributed snake mimicry complex where a mimic and a model co-occur both with and without other model species. We found that the mimic resembled its model more closely when they were exclusively sympatric than when they were sympatric with other model species. Moreover, in regions with multiple models, mimic-model resemblance was positively correlated with the resemblance between the model and other model species. However, contrary to predictions, free-ranging natural predators did not attack artificial replicas of imprecise mimics more often when only a single model was present. Taken together, our results suggest that multiple models might generate a geographical mosaic in the degree of phenotype matching between Batesian mimics and their models.

How stabilizing selection and nongenetic inheritance combine to shape the evolution of phenotypic plasticity.

Relatively little is known about whether and how nongenetic inheritance interacts with selection to impact the evolution of phenotypic plasticity. Here, we empirically evaluated how stabilizing selection and a common form of nongenetic inheritance-maternal environmental effects-jointly influence the evolution of phenotypic plasticity in natural populations of spadefoot toads. We compared populations that previous fieldwork has shown to have evolved conspicuous plasticity in resource-use phenotypes ("resource polyphenism") with those that, owing to stabilizing selection favouring a narrower range of such phenotypes, appear to have lost this plasticity. We show that: (a) this apparent loss of plasticity in nature reflects a condition-dependent maternal effect and not a genetic loss of plasticity, that is "genetic assimilation," and (b) this plasticity is not costly. By shielding noncostly plasticity from selection, nongenetic inheritance generally, and maternal effects specifically, can preclude genetic assimilation from occurring and consequently impede adaptive (genetic) evolution.

The emergence of performance trade-offs during local adaptation: insights from experimental evolution.

Environmental heterogeneity is considered a general explanation for phenotypic diversification, particularly when heterogeneity causes populations to diverge via local adaptation. Performance trade-offs, such as those stemming from antagonistic pleiotropy, are thought to contribute to the maintenance of diversity in this scenario. Specifically, alleles that promote adaptation in one environment are expected to promote maladaptation in alternative environments. Contrary to this expectation, however, alleles that underlie locally adaptive traits often fail to exhibit fitness costs in alternative environments. Here, we attempt to explain this paradox by reviewing the results of experimental evolution studies, including a new one of our own, that examined the evolution of trade-offs during adaptation to homogeneous versus heterogeneous environments. We propose that when pleiotropic effects vary, whether or not trade-offs emerge among diverging populations will depend critically on ecology. For example, adaptation to a locally homogeneous environment is more likely to occur by alleles that are antagonistically pleiotropic than adaptation to a locally heterogeneous environment, simply because selection is blind to costs associated with environments that are not experienced locally. Our literature review confirmed the resulting prediction that performance trade-offs were more likely to evolve during selection in homogeneous than heterogeneous environments. The nature of the environmental heterogeneity (spatial versus temporal) and the length of the experiment also contributed in predictable ways to the likelihood that performance trade-offs evolved.

Behavioral Plasticity and the Origins of Novelty: The Evolution of the Rattlesnake Rattle.

Environmentally induced behavior (behavioral plasticity) has long been hypothesized to promote the origins of novel morphological traits, but this idea remains controversial. One context in which this hypothesis can be evaluated is animal communication, where behavior and morphology are often linked. Here, we examined the evolution of one of nature's most spectacular communication signals: the rattlesnake rattle. We specifically evaluated whether rattlesnake rattling behavior-and, hence, the rattle-originated from a simple behavior: vibrating the tail when threatened. By reconstructing the ancestral state of defensive tail vibration, we show that this behavior is nearly ubiquitous in the Viperidae (the family that includes rattlesnakes) and widespread in the Colubridae (the largest snake family, nearly all of which are nonvenomous), suggesting a shared origin for the behavior between these families. After measuring tail vibration in 56 species of Viperidae and Colubridae, we show that the more closely related a species was to rattlesnakes, the more similar it was to rattlesnakes in duration and rate of tail vibration. Thus, the rattlesnake rattle might have evolved via elaboration of a simple behavior. These data thereby support the long-standing hypothesis that behavioral plasticity often precedes-and possibly instigates-the evolution of morphological novelty.

Genetic assimilation: a review of its potential proximate causes and evolutionary consequences.

BACKGROUND: Most, if not all, organisms possess the ability to alter their phenotype in direct response to changes in their environment, a phenomenon known as phenotypic plasticity. Selection can break this environmental sensitivity, however, and cause a formerly environmentally induced trait to evolve to become fixed through a process called genetic assimilation. Essentially, genetic assimilation can be viewed as the evolution of environmental robustness in what was formerly an environmentally sensitive trait. Because genetic assimilation has long been suggested to play a key role in the origins of phenotypic novelty and possibly even new species, identifying and characterizing the proximate mechanisms that underlie genetic assimilation may advance our basic understanding of how novel traits and species evolve. SCOPE: This review begins by discussing how the evolution of phenotypic plasticity, followed by genetic assimilation, might promote the origins of new traits and possibly fuel speciation and adaptive radiation. The evidence implicating genetic assimilation in evolutionary innovation and diversification is then briefly considered. Next, the potential causes of phenotypic plasticity generally and genetic assimilation specifically are examined at the genetic, molecular and physiological levels and approaches that can improve our understanding of these mechanisms are described. The review concludes by outlining major challenges for future work. CONCLUSIONS: Identifying and characterizing the proximate mechanisms involved in phenotypic plasticity and genetic assimilation promises to help advance our basic understanding of evolutionary innovation and diversification.

Evolutionary rescue and the coexistence of generalist and specialist competitors: an experimental test.

Competition for resources is thought to play a critical role in both the origins and maintenance of biodiversity. Although numerous laboratory evolution experiments have confirmed that competition can be a key driver of adaptive diversification, few have demonstrated its role in the maintenance of the resulting diversity. We investigate the conditions that favour the origin and maintenance of alternative generalist and specialist resource-use phenotypes within the same population. Previously, we confirmed that competition for hosts among φ6 bacteriophage in a mixed novel (non-permissive) and ancestral (permissive) host microcosm triggered the evolution of a generalist phenotype capable of infecting both hosts. However, because the newly evolved generalists tended to competitively exclude the ancestral specialists, coexistence between the two phenotypes was rare. Here, we show that reducing the relative abundance of the novel host slowed the increase in frequency of the generalist phenotype, allowing sufficient time for the specialist to further adapt to the ancestral host. This adaptation resulted in 'evolutionary rescue' of the specialists, preventing their competitive exclusion by the generalists. Thus, our results suggest that competition promotes both the origin and maintenance of biodiversity when it is strong enough to favour a novel resource-use phenotype, but weak enough to allow adaptation of both the novel and ancestral phenotypes to their respective niches.

Sexual selection's impacts on ecological specialization: an experimental test.

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs-distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring.

Mimicry's palette: widespread use of conserved pigments in the aposematic signals of snakes.

Mimicry, where one species resembles another species because of the selective benefits of sharing a common signal, is especially common in snakes. Snakes might be particularly prone to evolving mimicry if all species share some of the same proximate mechanisms that can be used to produce aposematic/mimetic signals. We evaluated this possibility by examining color pigments in 11 species of snakes from four different families, three species of which participate in a coral snake mimicry complex involving convergence in coloration. We found that all 11 species used combinations of two pteridine pigments and melanin in their coloration, regardless of whether or not they were mimics. Furthermore, the presence or absence of red pteridines was strongly correlated with the relative excitation of medium- and long-wavelength photoreceptors in birds, thereby linking shared pigmentation to perception of those pigments by likely agents of selection. Thus, precise color mimicry might be relatively easy to evolve among snakes owing to symplesiomorphies in pigmentation.

Evolutionary change in continuous reaction norms.

Understanding the evolution of reaction norms remains a major challenge in ecology and evolution. Investigating evolutionary divergence in reaction norm shapes between populations and closely related species is one approach to providing insights. Here we use a meta-analytic approach to compare divergence in reaction norms of closely related species or populations of animals and plants across types of traits and environments. We quantified mean-standardized differences in overall trait means (Offset) and reaction norm shape (including both Slope and Curvature). These analyses revealed that differences in shape (Slope and Curvature together) were generally greater than differences in Offset. Additionally, differences in Curvature were generally greater than differences in Slope. The type of taxon contrast (species vs. population), trait, organism, and the type and novelty of environments all contributed to the best-fitting models, especially for Offset, Curvature, and the total differences (Total) between reaction norms. Congeneric species had greater differences in reaction norms than populations, and novel environmental conditions increased the differences in reaction norms between populations or species. These results show that evolutionary divergence of curvature is common and should be considered an important aspect of plasticity, together with slope. Biological details about traits and environments, including cryptic variation expressed in novel environmental conditions, may be critical to understanding how reaction norms evolve in novel and rapidly changing environments.

Towards a gene regulatory network perspective on phenotypic plasticity, genetic accommodation and genetic assimilation.

Many organisms can produce alternative phenotypes in direct response to different environmental conditions, a phenomenon known as phenotypic plasticity. The environmentally sensitive gene regulatory networks (GRNs) that mediate such developmental flexibility are largely unknown. Yet, characterizing these GRNs is important not only for elucidating plasticity's molecular basis, but also for shedding light onto whether and how plasticity might impact evolution. In this issue of Molecular Ecology, Schneider et al.) describe one of the first efforts to determine the GRN underlying a plastic trait. They focus on diet-induced plasticity in the cichlid fish, Astatoreochromis alluaudi. Depending on whether soft food (e.g. insects) or hard food (e.g. molluscs) is consumed, this species forms a lower pharyngeal jaw (LPJ) with many fine teeth or with fewer molar-like teeth, respectively (Fig. 1). The authors previously identified genes that are differentially expressed between LPJ morphs during early development. In the present study, they examine the expression of 19 of these genes across development and diet. By analysing these transcriptional data in combination with information on putative transcription factor binding sites, they construct a GRN that explains observed gene expression patterns and is likely to control LPJ morphology. This work advances our understanding of how plasticity can arise as a consequence of environmentally sensitive GRNs and promises to help illuminate how changes in such GRNs could facilitate evolution.

Rapid evolution of mimicry following local model extinction.

Batesian mimicry evolves when individuals of a palatable species gain the selective advantage of reduced predation because they resemble a toxic species that predators avoid. Here, we evaluated whether-and in which direction-Batesian mimicry has evolved in a natural population of mimics following extirpation of their model. We specifically asked whether the precision of coral snake mimicry has evolved among kingsnakes from a region where coral snakes recently (1960) went locally extinct. We found that these kingsnakes have evolved more precise mimicry; by contrast, no such change occurred in a sympatric non-mimetic species or in conspecifics from a region where coral snakes remain abundant. Presumably, more precise mimicry has continued to evolve after model extirpation, because relatively few predator generations have passed, and the fitness costs incurred by predators that mistook a deadly coral snake for a kingsnake were historically much greater than those incurred by predators that mistook a kingsnake for a coral snake. Indeed, these results are consistent with prior theoretical and empirical studies, which revealed that only the most precise mimics are favoured as their model becomes increasingly rare. Thus, highly noxious models can generate an 'evolutionary momentum' that drives the further evolution of more precise mimicry-even after models go extinct.