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1.  High-model abundance may permit the gradual evolution of Batesian mimicry: an experimental test 
In Batesian mimicry, a harmless species (the ‘mimic’) resembles a dangerous species (the ‘model’) and is thus protected from predators. It is often assumed that the mimetic phenotype evolves from a cryptic phenotype, but it is unclear how a population can transition through intermediate phenotypes; such intermediates may receive neither the benefits of crypsis nor mimicry. Here, we ask if selection against intermediates weakens with increasing model abundance. We also ask if mimicry has evolved from cryptic phenotypes in a mimetic clade. We first present an ancestral character-state reconstruction showing that mimicry of a coral snake (Micrurus fulvius) by the scarlet kingsnake (Lampropeltis elapsoides) evolved from a cryptic phenotype. We then evaluate predation rates on intermediate phenotypes relative to cryptic and mimetic phenotypes under conditions of both high- and low-model abundances. Our results indicate that where coral snakes are rare, intermediate phenotypes are attacked more often than cryptic and mimetic phenotypes, indicating the presence of an adaptive valley. However, where coral snakes are abundant, intermediate phenotypes are not attacked more frequently, resulting in an adaptive landscape without a valley. Thus, high-model abundance may facilitate the evolution of Batesian mimicry.
PMCID: PMC2842773  PMID: 19955153
adaptive landscape; Batesian mimicry; coral snake mimicry; predation; colour pattern
2.  Towards a gene regulatory network perspective on phenotypic plasticity, genetic accommodation and genetic assimilation 
Molecular ecology  2014;23(18):4438-4440.
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.
PMCID: PMC4180264  PMID: 25208504
adaptation; fish; gene regulatory networks; macroevolution; molecular evolution; phenotypic plasticity
3.  Development and Evolution of Character Displacement 
Character displacement occurs when competition for either resources or successful reproduction imposes divergent selection on interacting species, causing divergence in traits associated with resource use or reproduction. Here, we describe how character displacement can be mediated either by genetically canalized changes (i.e., changes that reflect allelic or genotype frequency changes) or by phenotypic plasticity. We also discuss how these two mechanisms influence the tempo of character displacement. Specifically, we suggest that, under some conditions, character displacement mediated by phenotypic plasticity might occur more rapidly than that mediated by genetically canalized changes. Finally, we describe how these two mechanisms may act together and determine character displacement’s mode, such that it proceeds through an initial phase in which trait divergence is environmentally induced to a later phase in which divergence becomes genetically canalized. This plasticity-first hypothesis predicts that character displacement should be generally mediated by ancestral plasticity and that it will arise similarly in multiple, independently evolving populations. We conclude by highlighting future directions for research that would test these predictions.
PMCID: PMC3352989  PMID: 22257002
adaptive divergence; competition; ecological developmental biology; genetic assimilation; genetics of adaptation; phenotypic plasticity
4.  Competition and the origins of novelty: experimental evolution of niche-width expansion in a virus 
Biology Letters  2013;9(1):20120616.
Competition for resources has long been viewed as a key agent of divergent selection. Theory holds that populations facing severe intraspecific competition will tend to use a wider range of resources, possibly even using entirely novel resources that are less in demand. Yet, there have been few experimental tests of these ideas. Using the bacterial virus (bacteriophage) ϕ6 as a model system, we examined whether competition for host resources promotes the evolution of novel resource use. In the laboratory, ϕ6 exhibits a narrow host range but readily produces mutants capable of infecting novel bacterial hosts. Here, we show that when ϕ6 populations were subjected to intense intraspecific competition for their standard laboratory host, they rapidly evolved new generalist morphs that infect novel hosts. Our results therefore suggest that competition for host resources may drive the evolution of host range expansion in viruses. More generally, our findings demonstrate that intraspecific resource competition can indeed promote the evolution of novel resource-use phenotypes.
PMCID: PMC3565482  PMID: 23075527
bacteriophage; intraspecific competition; resource polymorphism; host range expansion
5.  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.
PMCID: PMC3381942  PMID: 22526866
6.  The role of developmental plasticity in evolutionary innovation 
Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.
PMCID: PMC3145196  PMID: 21676977
genetic accommodation; genetic assimilation; novelty; developmental plasticity
7.  Widespread disruptive selection in the wild is associated with intense resource competition 
Disruptive selection has been documented in a growing number of natural populations. Yet, its prevalence within individual systems remains unclear. Furthermore, few studies have sought to identify the ecological factors that promote disruptive selection in the wild. To address these issues, we surveyed 15 populations of Mexican spadefoot toad tadpoles, Spea multiplicata, and measured the prevalence of disruptive selection acting on resource-use phenotypes. We also evaluated the relationship between the strength of disruptive selection and the intensity of intraspecific competition—an ecological agent hypothesized to be an important driver of disruptive selection.
Disruptive selection was the predominant mode of quadratic selection across all populations. However, a directional component of selection favoring an extreme ecomorph—a distinctive carnivore morph—was also common. Disruptive selection was strongest in populations experiencing the most intense intraspecific competition, whereas stabilizing selection was only found in populations experiencing relatively weak intraspecific competition.
Disruptive selection can be common in natural populations. Intraspecific competition for resources may be a key driver of such selection.
PMCID: PMC3432600  PMID: 22857143
Competition; Disruptive selection; Resource polymorphism; Selection differential; Spadefoot toad; Quadratic selection
8.  Character displacement and the origins of diversity 
The American Naturalist  2010;176(Suppl 1):S26-S44.
In The Origin of Species, Darwin proposed his ‘principle of divergence of character’ (a process now termed ‘character displacement’) to explain how new species arise and why they differ from one other phenotypically. Darwin maintained that the origin of species, and the evolution of differences between them, is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin’s principle, specifically that: (1) competition promotes divergent trait evolution; (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors; (3) divergence can occur within species; and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how: (1) divergence can arise from selection acting to lessen reproductive interactions; (2) divergence is fueled by the intersection of character displacement and sexual selection; and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify.
PMCID: PMC3285564  PMID: 21043778
Competition; Darwin’s divergence of character; hybridization; phenotypic plasticity; sexual selection; speciation
The Quarterly Review of Biology  2009;84(3):253-276.
Character displacement – trait evolution stemming from selection to lessen resource competition or reproductive interactions between species – has long been viewed as an important mechanism for enabling closely related species to coexist. Yet, the causes and consequences of character displacement have not been fully explored. Moreover, character displacement in traits associated with resource use (ecological character displacement) has been studied largely independently of that in traits associated with reproduction (reproductive character displacement). Here, we underscore the commonalities of these two forms of character displacement and discuss how they interact. We focus on the causes of character displacement and explore how character displacement can have downstream effects ranging from speciation to extinction. In short, understanding how organisms respond to competitive and reproductive interactions with heterospecifics offers key insights into the evolutionary consequences of species coexistence and diversification.
PMCID: PMC3279117  PMID: 19764283
adaptive radiation; coevolution; coexistence; competition; Darwinian extinction; mate choice; phenotypic plasticity; reinforcement; resource polymorphism; sexual selection; speciation
10.  Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies 
When experiencing resource competition or abrupt environmental change, animals often must transition rapidly from an ancestral diet to a novel, derived diet. Yet, little is known about the proximate mechanisms that mediate such rapid evolutionary transitions. Here, we investigated the role of diet-induced, cryptic genetic variation in facilitating the evolution of novel resource-use traits that are associated with a new feeding strategy—carnivory—in tadpoles of spadefoot toads (genus Spea). We specifically asked whether such variation in trophic morphology and fitness is present in Scaphiopus couchii, a species that serves as a proxy for ancestral Spea. We also asked whether corticosterone, a vertebrate hormone produced in response to environmental signals, mediates the expression of this variation. Specifically, we compared broad-sense heritabilities of tadpoles fed different diets or treated with exogenous corticosterone, and found that novel diets can expose cryptic genetic variation to selection, and that diet-induced hormones may play a role in revealing this variation. Our results therefore suggest that cryptic genetic variation may have enabled the evolutionary transition to carnivory in Spea tadpoles, and that such variation might generally facilitate rapid evolutionary transitions to novel diets.
PMCID: PMC2982244  PMID: 20573627
phenotypic plasticity; genetic accommodation; corticosterone; novelty; anuran larvae; heritability
11.  Mimics without models: causes and consequences of allopatry in Batesian mimicry complexes 
Batesian mimicry evolves when a palatable species (the ‘mimic’) co-opts a warning signal from a dangerous species (the ‘model’) and thereby deceives its potential predators. Longstanding theory predicts that this protection from predation should break down where the model is absent. Thus, mimics are expected to only co-occur with their model. Yet, many mimics violate this prediction and occur in areas where their model is absent. Here, we discuss the causes and consequences of such allopatric mimics. We also describe how these ‘rule-bending’ mimics provide critical insights into diverse topics ranging from how Batesian mimicry evolves to its possible role in speciation.
PMCID: PMC2982051  PMID: 20484238
mimicry; predation; speciation; gene flow; species ranges
12.  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.
PMCID: PMC2817138  PMID: 20083634
adaptive radiation; extinction; key innovation; phenotypic plasticity; replicated sister-group comparison; speciation
13.  Parallel evolution and ecological selection: replicated character displacement in spadefoot toads 
Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition's role in divergent trait evolution.
PMCID: PMC2821351  PMID: 19726477
character displacement; competition; divergent evolution; parallel evolution; population history
14.  Maternal Investment Influences Expression of Resource Polymorphism in Amphibians: Implications for the Evolution of Novel Resource-Use Phenotypes 
PLoS ONE  2010;5(2):e9117.
Maternal effects—where an individual's phenotype is influenced by the phenotype or environment of its mother—are taxonomically and ecologically widespread. Yet, their role in the origin of novel, complex traits remains unclear. Here we investigate the role of maternal effects in influencing the induction of a novel resource-use phenotype. Spadefoot toad tadpoles, Spea multiplicata, often deviate from their normal development and produce a morphologically distinctive carnivore-morph phenotype, which specializes on anostracan fairy shrimp. We evaluated whether maternal investment influences expression of this novel phenotype. We found that larger females invested in larger eggs, which, in turn, produced larger tadpoles. Such larger tadpoles are better able to capture the shrimp that induce carnivores. By influencing the expression of novel resource-use phenotypes, maternal effects may play a largely underappreciated role in the origins of novelty.
PMCID: PMC2817737  PMID: 20161745
15.  Mimicry on the edge: why do mimics vary in resemblance to their model in different parts of their geographical range? 
Batesian mimics—benign species that predators avoid because they resemble a dangerous species—often vary geographically in resemblance to their model. Such geographical variation in mimic–model resemblance may reflect geographical variation in model abundance. Natural selection should favour even poor mimics where their model is common, but only good mimics where their model is rare. We tested these predictions in a snake-mimicry complex where the geographical range of the mimic extends beyond that of its model. Mimics on the edge of their model's range (where the model was rare) resembled the model more closely than did mimics in the centre of their model's range (where the model was common). When free-ranging natural predators on the edge of the model's range were given a choice of attacking replicas of good or poor mimics, they avoided only good mimics. By contrast, those in the centre of the model's range attacked good and poor mimics equally frequently. Generally, although poor mimics may persist in areas where their model is common, only the best mimics should occur in areas where their model is rare. Thus, counter-intuitively, the best mimics may occur on the edge of their model's range.
PMCID: PMC2275182  PMID: 17567563
Batesian mimicry; geographical variation; predation; Micrurus fulvius; Lampropeltis triangulum elapsoides

Results 1-15 (15)