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Introduction
My research interests lie at the intersection of evolutionary biology, ecology, and developmental biology. Much of my current effort focuses on the causes and consequences of phenotypic plasticity, specifically: 1) the genetic/epigenetic mechanisms of plasticity, 2) how plasticity evolves, and 3) how plasticity influences ecological and evolutionary processes. This work combines field studies of natural populations of amphibians with various modern approaches. Additionally, through my teaching and public outreach, I strive to convey the excitement and importance of science to others.
Current institution
Publications
Publications (174)
Asplanchna brightwellii rotifers have a diet-induced polyphenism; they develop different morphological and life history traits depending upon maternal ingestion of vitamin E. Here, we empirically induce the polyphenism to determine if this multivariate plasticity varies among clonal lines and populations (ponds) and to evaluate whether and how the...
Amphibians represent a diverse group of tetrapods, marked by deep divergence times between their three systematic orders and families. Studying amphibian biology through the genomics lens increases our understanding of the features of this animal class and that of other terrestrial vertebrates. The need for amphibian genomic resources is more urgen...
Organisms can react to environmental variation by altering their phenotype, and such phenotypic plasticity is often adaptive. This plasticity contributes to the diversity of phenotypes across the tree of life. Generally, the production of these phenotypes must be preceded by assessment, where the individual acquires information about its environmen...
A growing number of studies have applied evolutionary and ecological principles to understanding cancer. However, few such studies have examined whether phenotypic plasticity––the ability of a single individual or genome to respond differently to different environmental circumstances––can impact the origin and spread of cancer. Here, we propose the...
Amphibians represent a diverse group of tetrapods, marked by deep divergence times between their three systematic orders and families. Studying amphibian biology through the genomics lens increases our understanding of the features of this animal class and that of other terrestrial vertebrates. The need for amphibian genomics resources is more urge...
Many organisms facultatively produce different phenotypes depending on their environment, yet relatively little is known about the genetic bases of such plasticity in natural populations. In this study, we describe the genetic variation underlying an extreme form of plasticity––resource polyphenism––in Mexican spadefoot toad tadpoles, Spea multipli...
Novel forms of phenotypic plasticity may evolve by lineage‐specific changes or by co‐opting mechanisms from more general forms of plasticity. Here, we evaluated whether a novel resource polyphenism in New World spadefoot toads (genus Spea ) evolved by co‐opting mechanisms from an ancestral form of plasticity common in anurans—accelerating larval de...
Parental effects are often considered an evolved response, in which parents transmit information about the environment to enhance offspring fitness. However, these effects need not be adaptive. Here, we provide a striking example by presenting evidence that overfeeding of adult Mexican spadefoot toads, Spea multiplicata, is associated with decrease...
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...
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 ad...
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 dev...
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 respon...
Phenotypic plasticity and sexual selection can each promote adaptation in variable environments, but their combined influence on adaptive evolution is not well understood. We propose that sexual selection can facilitate adaptation in variable environments when individuals prefer mates that produce adaptively plastic offspring. We develop this hypot...
The possibility that sexual selection promotes adaptive evolution in variable environments remains controversial. In particular, where the scale of environmental variation results in parents and their offspring experiencing different environmental conditions, such variation is expected to break down associations between adult sexual traits and adap...
Batesian mimics – harmless species that converge on the warning signals of a dangerous species – are spectacular examples of adaptation, but few documented cases involve acoustic signals. Even fewer studies have documented microevolutionary change in mimicry of any kind. Here, we describe a potential evolutionary change in acoustic mimicry. Many no...
David and Karin Pfennig introduce character displacement, the divergent evolution of traits in overlapping species.
An individual’s early-life environment and phenotype often influence its traits and performance as an adult. We investigated whether such ‘carryover effects’ are associated with alternative, environmentally-induced phenotypes (‘polyphenism’), and, if so, whether they influence the evolution of polyphenism. To do so, we studied Mexican spadefoot toa...
Intraspecific competition has long been considered a key driver of evolutionary diversification, but whether it can also promote evolutionary innovation is less clear. Here we examined the interplay between competition and phenotypic plasticity in fuelling the origins of a novel, complex phenotype – a distinctive carnivore morph found in spadefoot...
Phenotypic plasticity allows organisms to alter their phenotype in direct response to changes in the environment. Despite growing recognition of plasticity's role in ecology and evolution, few studies have probed plasticity's molecular bases—especially using natural populations. We investigated the genetic basis of phenotypic plasticity in natural...
Nongenetic inheritance—involving epigenetic, behavioral, or environmental factors—is increasingly viewed as being important in development and evolution. Here, we describe a possible novel form of nongenetic inheritance in the tadpoles of the Mexican Spadefoot (Spea multiplicata): the transmission of information about the environment from dead indi...
Explaining the origins of adaptive features is a perennial challenge in evolutionary biology. A study on thermophilic cyanobacteria reveals how environmentally induced phenotypic change (plasticity) can pave the way for evolutionary innovation and subsequent adaptation to extreme conditions. Explaining the origins of adaptive features is a perennia...
A growing number of biologists have begun asking whether environmentally induced phenotypic change—phenotypic plasticity—precedes and facilitates the origin and subsequent fixation of novel, complex phenotypes. However, such plasticity-led evolution (PLE) remains controversial. Here, we begin with a summary of the PLE hypothesis and describe how it...
Frogs and toads (anurans) are widely used to study many biological processes. Yet, few anuran genomes have been sequenced, limiting research on these organisms. Here, we produce a draft genome for the Mexican spadefoot toad, Spea multiplicata, which is a member of an unsequenced anuran clade. Atypically for amphibians, spadefoots inhabit deserts. C...
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...
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 a...
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 pop...
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 th...
Artificial prey techniques—wherein synthetic replicas of real organisms are placed in natural habitats—are widely used to study predation in the field. We investigated the extent to which videography could provide additional information to such studies. As a part of studies on aposematism and mimicry of coral snakes ( Micrurus ) and their mimics, o...
In a rapidly changing world, understanding the processes that influence a population's ability to respond to natural selection is critical for identifying how to preserve biodiversity. Two such processes are phenotypic plasticity and sexual selection. Whereas plasticity can facilitate local adaptation, sexual selection potentially impedes local ada...
Plasticity-first evolution (PFE) posits that novel features arise when selection refines pre-existing phenotypic plasticity into an adaptive phenotype. However, PFE is controversial because few tests have been conducted in natural populations. Here we present evidence that PFE fostered the origin of an evolutionary novelty that allowed certain amph...
Character displacement – trait evolution that arises as an adaptive response to competition between species – is central to the origins, abundance and distribution of biodiversity. Yet, until recently, little was known of character displacement's underlying mechanisms. Although character displacement is assumed to arise solely through changes in de...
Reciprocal selection on harmless Batesian mimics and their defended models has long been hypothesized to spawn coevolutionary arms races. Mimics are thought continuously to experience selection to resemble their models better. Models are thought continuously to experience 'chase-away' selection for phenotypes that let them escape from these 'parasi...
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 evalu...
Intraspecific variation in resource-use traits can have profound ecological and evolutionary implications. Among the most striking examples are resource polymorphisms, where alternative morphs that utilize different resources evolve within a population. An underappreciated aspect of their evolution is that the same conditions that favor resource po...
Ecological character displacement is considered crucial in promoting diversification, yet relatively little is known of its underlying mechanisms. We examined whether evolutionary shifts in gene expression plasticity ('genetic accommodation') mediate character displacement in spadefoot toads. Where Spea bombifrons and S. multiplicata occur separate...
Batesian mimicry is widespread, but whether and why different species of mimics vary geographically in resemblance to their model is unclear. We characterized geographic variation in mimetic precision among four Batesian mimics of coral snakes. Each mimic occurs where its model is abundant (i.e., in "deep sympatry"), rare (i.e., at the sympatry/all...
Ecological evolutionary developmental biology explores how interactions between an organism and its environment influence development, and how this environmentally responsive development, in turn, impacts ecology and evolution. This article describes the recent research aimed at evaluating the role of environmentally initiated phenotypic change in...
Review of: Sultan S. E. 2015. Organism & Environment: Ecological Development, Niche Construction, and Adaptation. Oxford University Press. 224 pp. ISBN 9780199587063; $59.95 PB. This article is protected by copyright. All rights reserved
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, all...
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...
Deadly coral snakes warn predators through striking red-black banding. New data confirm that many harmless snakes have evolved to resemble coral snakes, and suggest that the evolution of this Batesian mimicry is not always a one-way street.
Many biologists are asking whether environmentally initiated phenotypic change (i.e., 'phenotypic plasticity') precedes, and even facilitates, evolutionary adaptation. However, this 'plasticity-first' hypothesis remains controversial, primarily because comprehensive tests from natural populations are generally lacking. We briefly describe the plast...
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 conditi...
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 gene...
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 s...
Table S1. Raw data that accompanies this manuscript.
Phenotypic plasticity is commonplace, and plasticity theory predicts that organisms should often evolve mechanisms to detect and respond to environmental cues that accurately predict future environmental conditions. Here, we test this prediction in tadpoles of spadefoot toads, Spea multiplicata. These tadpoles develop into either an omnivore ecomor...
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,...
We evaluated whether Batesian mimicry promotes early-stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where non-mimetic traits are favored), divergent, predat...
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 p...
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 wh...
Understanding how populations respond to rapid environmental change is critical both for preserving biodiversity and for human health. An increasing number of studies have shown that genetic variation that has no discernable effect under common ecological conditions can become amplified under stressful or novel conditions, suggesting that environme...
Abstract 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 relate...
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...
Mating competition between males often has harmful consequences for females. But it seems that fruit flies alter their behaviour among kin, with brothers being less aggressive and females reproducing for longer as a result. See Letter p.672
Coral snakes and their mimics often have brightly colored banded patterns, generally associated with warning colora- tion or mimicry. However, such color patterns have also been hypothesized to aid snakes in escaping predators through a “flicker-fusion” effect. According to this hypothesis, banded color patterns confuse potential predators when a s...
Mimicry--when one organism (the mimic) evolves a phenotypic resemblance to another (the model) due to selective benefits--is widely used to illustrate natural selection's power to generate adaptations. However, many putative mimics resemble their models imprecisely, and such imperfect mimicry represents a specific challenge to mimicry theory and a...
Identifying the causes of diversification is central to evolutionary biology. The ecological theory of adaptive diversi-fication holds that the evolution of phenotypic differences between populations and species-and the formation of new spe-cies-stems from divergent natural selection, often arising from competitive interactions. Although increasing...
Understanding how new species arise is central to evolutionary biology, and the study of speciation remains a vibrant frontier (1⇓⇓⇓–5). Although most evolutionary biologists agree that speciation occurs when populations become reproductively isolated from each other—meaning that they do not interbreed when they come into contact or, if they do int...
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...
Inheritance is crucial to the evolutionary process. Although most
evolutionary biologists assume that inheritance occurs exclusively through
changes in DNA base sequence, it has long been known that inheritance
can also occur through epigenetic mechanisms, such as chromatin
marking, maternal effects, parasite transmission, or learning. In recent
ye...
Evolutionary biology has long sought to explain how new traits and new species arise. Darwin maintained that competition is key to understanding this biodiversity and held that selection acting to minimize competition causes competitors to become increasingly different, thereby promoting new traits and new species. Despite Darwin's emphasis, compet...
Resource competition is common in nature and is often strong. Additionally, heterospecifics frequently interact in ways that impede ability of each species to reproduce successfully. Both types of competitive interactions can have severe fitness costs. Indeed, in some cases, competition can even cause a species to go locally extinct. As a consequen...
Intraspecific competition can have a profound influence on shaping diversity within species. Intraspecific competition can promote niche-width expansion, sexual dimorphism, and resource or mating polymorphism. Such polymorphisms are of interest in their own right, because they provide some of the most dramatic examples of diversity within species....
Character displacement is well supported theoretically and empirically, and it plays a key, and often decisive, role in generating and maintaining biodiversity. Yet a number of important issues regarding the causes and consequences of character displacement remain unresolved. Additional research into character displacement promises to have far-reac...
Clarifying the facilitators of character displacement is crucial for illuminating the origins of diversity. Six non–mutually exclusive factors are important: (1) standing variation; (2) strong selection; (3) ecological opportunity; (4) initial trait differences; (5) gene flow; and (6) a lack of antagonistic genetic correlations. Moreover, the occur...
Relatively little is known of the source of the phenotypic variation that fuels character displacement, as well as how different sources of variation affect the tempo and mode of character displacement. Character displacement can be mediated by genetically canalized changes or environmentally induced shifts. Yet these two proximate mechanisms likel...
Character displacement fosters species coexistence by promoting differences between species in resource use (resource partitioning) and in reproductive traits (reproductive partitioning). By promoting niche differences, character displacement lessens costly competitive interactions, reduces the risks of competitive or reproductive exclusion, and th...
Character displacement can affect sexual selection by generating shifts in an organism's phenotype or in the habitat in which mating takes place. Character displacement also alters the underlying fitness effects of mate choice. Such changes can enhance divergence between populations that do and do not co-occur with another species. Consequently, wh...
The relationship between microevolution and macroevolution has long been controversial. Much of this controversy centers on whether the same processes cause evolution at both scales. Although many evolutionary biologists have asserted that most macroevolutionary phenomena reflect microevolutionary processes acting over extended periods of evolution...
To explain biodiversity, Darwin proposed that organisms face recurring competition for scarce resources, and that such competition favors individuals least like their competitors. This evolutionary process is now known as “character displacement.” Character displacement is expected to produce a pattern of exaggerated divergence where species co-occ...
New species form during an extended process, which often begins when populations become physically separated and ends when they come into secondary contact and possess or subsequently evolve barriers to gene exchange. Selection can play an important role in promoting population divergence and reproductive isolation. Character displacement, in parti...
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 tadpo...
Batesian mimics are harmless prey species that resemble dangerous ones (models), and thus receive protection from predators. How such adaptive resemblances evolve is a classical problem in evolutionary biology. Mimicry is typically thought to be difficult to evolve, especially if the model and mimic produce the convergent phenotype through differen...
Mimicry is widely used to exemplify natural selection's power in promoting adaptation. Nonetheless, it has become increasingly clear that mimicry is frequently imprecise. Indeed, the phenotypic match is often poor between mimics and models in many Batesian mimicry complexes and among co-mimics in many Müllerian mimicry complexes. Here, we consider...
Identifying the factors that promote or preclude the evolution of resource polymorphism is essential for under-standing the origins of diversity. Although such polymorphisms have long been viewed as an adaptive response to intraspecific competition, they are by no means ubiquitous, even in populations experiencing strong competition. In the present...
Animals often facultatively engage in less risky behavior when predators are present. Few studies, however, have investigated whether, or how, such predator-mediated behavior promotes diversification. Here, we ask whether tadpoles of the spadefoot toad Scaphiopus couchii have a diminished ability to utilize a potentially valuable resource--anostrac...
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 differenti...
Some species evolve to resemble another species so as to protect
themselves from predation, but this mimicry is often imprecise. An
analysis of hoverflies suggests why imperfect imitation persists in the
face of natural selection. See Letter p.461
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...
Ecological character displacement occurs when competition imposes divergent selection on interacting species, causing divergence in traits associated with resource use. Generally, divergence is assumed to occur when selection acts on the same, continuously varying trait in both species. However, selection might target multiple traits, and even clos...
Spadefoot toads have emerged as a model system for addressing fundamental questions in ecological and evolutionary developmental biology (eco-evo-devo). Their tadpoles produce a wide range of adaptive phenotypes in direct response to diverse environmental stimuli. Such phenotypic plasticity offers an excellent opportunity to examine how an organism...
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...
Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a...
I examined nestmate and nest recognition among worker paper wasps Polistes exclamans on neighboring colonies in a dense nesting aggregation. In the laboratory, there was a significant positive correlation between the difference in preference toward nestmates and non-nestmates and internest distance (i.e., distance in the field between the nestmates...
Batesian mimicry is often imprecise. An underexplored explanation for imperfect mimicry is that predators might not be able to use all dimensions of prey phenotype to distinguish mimics from models and thus permit imperfect mimicry to persist. We conducted a field experiment to test whether or not predators can distinguish deadly coral snakes (Micr...
Character displacement occurs when two species compete, and those individuals most dissimilar from the average resource-use phenotypes of the other species are selectively favored. Few studies have explored the sequence of events by which such divergence comes about. We addressed this issue by studying two species of spadefoot toads that have under...
Phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) is commonplace. Yet its evolutionary significance remains controversial, especially in regard to whether and how it impacts diversification and speciation. Here, we review recent theory on how plasticity promotes: (i)...
There was an error published in J. Exp. Biol. 212, 3743-3750.
In Fig. 4, the data for the top two graphs – depicting residual corticosterone regressed on residual mass – were plotted on inverted axes. The correct version of the figure is below.
The authors apologise for this error but assure readers that the results and conclusions of the paper rem...
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 each other phenotypically. Darwin maintained that the origin of species and the evolution of differences between them is ultimately caused by divergent selection...
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...
