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Emerging model systems in eco-evo-devo: the environmentally
responsive spadefoot toad
Cris C. Ledo
´n-Rettig
!
and David W. Pfennig
Department of Biology, University of North Carolina, CB#3280, Coker Hall, Chapel Hill, NC 27599, USA
!
Author for correspondence (email: cledonrettig@mail.usf.edu)
SUMMARY 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’s ecology affects its development as well as how an
organism’s development influences its ecology and evolution.
By characterizing and understanding the interconnected-
ness between an organism’s environment, its development
responses, and its ecological interactions in natural populations,
such research promises to clarify further the role of the
environment in not only selecting among diverse phenotypes,
but also creating such phenotypes in the first place.
INTRODUCTION
Ecological and evolutionary developmental biology (‘‘eco-
devo’’ and ‘‘evo-devo,’’ respectively) seek to understand how
an organism’s genome and ecology interact to create pheno-
typic variation, and to determine the ecological and evolu-
tionary consequences of this variation (Sultan 2007, 2010;
Gilbert and Epel 2009). Implicit in these goals are that
phenotype expression is dependent on the environment in
which these phenotypes are produced. Further, ecologically
distinct populations and species evolve such that environ-
mental cues direct an individual’s development to produce
phenotypes that are adaptive for the variability encountered
in the organism’s unique habitat. Accordingly, organisms
most amenable to research in integrating eco-devo with
evo-devo are those whose ecology is well known and that
experience diverse ecological (and thus, selective) regimes.
Spadefoot toads (hereafter, spadefoots) meet these criteria,
and they have emerged as an excellent system for integrating
eco-devo with evo-devo. Indeed, spadefoots respond to
numerous environmental factors that influence fitness. The
larvae, in particular, express a high degree of phenotypic
plasticity. Furthermore, different species, populations, and
even individuals experience diverse selective environments.
Consequently, linking ecological processes to evolutionary
outcomes is often tractable. Most importantly, although
spadefoot biology is seemingly unique, the developmental,
ecological, and evolutionary processes that can be illuminated
by studying them will likely apply to numerous other taxa.
Below, we briefly describe spadefoot natural history. We
then summarize the many environmental factors that shape
phenotype production in New World spadefoots. In partic-
ular, we highlight two environmentally dependent phenotypes
that have been evolved in this clade and that have important
fitness consequences for larvae: variation in metamorphic
timing and the expression of resource polyphenism (sensu
Mayr 1963). Finally, we address four current avenues of
research that have been investigated with spadefoots.
DIVERSITY AND NATURAL HISTORY OF
SPADEFOOTS
Spadefoots (superfamily Pelobatoidea) are frogs and not true
‘‘toads’’; that claim is restricted to the genus Bufo (Anaxyrus).
The phylogenetic relationships among species have been well
resolved (Garcı´a-Parı´setal.2003),enablingresearchersto
generate phylogenetically informed hypotheses regarding their
various adaptations. Although spadefoots also inhabit
Europe and Africa (genera Pelobates and Pelodytes), we
focus on New World spadefoots, which exhibit numerous,
derived features associated with their desert habitats, such as
rapid larval development and special ways of procuring food.
North American spadefoots (family Scaphipodidae) con-
sist of two generaFSpea and Scaphiopus (Fig. 1). Within
these two genera, four species are desert-dwellers (Spea bomb-
ifrons,Spea intermontana,Spea multiplicata,andScaphiopus
couchii). Although the remaining species (Spea hammondii,
Scaphiopus holbrookii and Scaphiopus hurterii)liveinmore
mesic habitats, they share some of the same adaptations
to xeric environments as their desert brethren. For instance,
EVOL UTI ON & DE VELO PME NT 13:4, 391–400 (2011)
DOI: 10.1111/j.1525-142X.2011.00494.x
&2011 Wiley Periodicals, Inc. 391
S. holbrookii frequently breed in ephemeral ponds, despite
inhabiting the mesic eastern US (Fig. 2).
To survive in xeric habitats, adult spadefoots spend most
of the year underground, emerging during warm-weather
rains to feed and breed in temporary rain-filled ponds
(Bragg 1965). Because these ponds are often highly
ephemeral, spadefoot larvae are frequently under intense
selection to grow and develop rapidly enough to metamor-
phose before their pond dries (Newman 1989). Not surpris-
ingly, spadefoot larvae are capable of remarkably rapid
development (S. couchii,e.g.,canmetamorphoseless
than eight days posthatching; Newman 1989). Additionally,
some species have evolved unique feeding adaptations that
speed development and growth. It is these two features of
the larvaeFvariable developmental rate and feeding
adaptationsFthat provide exceptional opportunities for
eco-evo-devo research.
AN ENVIRONMENTALLY RESPONSIVE TADPOLE
Although desert spadefoots have rapid larval development,
they also exhibit considerable plasticity in developmental rate
(Newman 1994). This plasticity enables larvae to slow devel-
opment and thereby acquire additional nutrients and grow
more if their pond persists (Newman 1992; Denver et al. 1998;
Morey and Reznick 2000). Such plasticity is presumably an
adaptation for variability in pond duration (Newman 1994).
Spadefoots have an additional adaptation to cope with
desert habitats: Spea larvae facultatively produce a distinctive
ecomorph that preys on anostracan fairy shrimpFavaluable,
but often underutilized, resource in their relatively nutrient-
limited ponds. Most anuran larvae feed on detritus and
microorganisms and possess small jaw muscles, smooth ker-
atinized mouthparts, and an elongate gut (Duellman and
Trueb 1986; Altig et al. 2007). Although Spea larvae develop
Fig. 1.Representative members from
both North American spadefoot genera
(Scaphiopus and Spea). Scaphiopus cou-
chii (left) is sexually dimorphic, where
males are bright green (top frog) and
females are drab green and black. Spea
bombifrons males (right) congregate at
the periphery of ponds to solicit mating
calls.
Fig. 2.North American spadefoots in-
habit variable environments. For exam-
ple, the Eastern spadefoot (Scaphiopus
holbrookii)inhabitsmoremesicenviron-
ments, and breeds in ponds that are
longer in duration (top left). Within de-
sert environments, spadefoot natal ponds
may vary in nutrient richness and dura-
tion. These ponds may be surrounded by
vegetation and thus high in organic nu-
trients (top right), or may have very little
vegetation and nutrients, for instance, if
they are formed on desert playas (bottom
left). These ponds may also vary in du-
ration; for instance, larger ponds (bottom
left) usually last longer than smaller
ponds (bottom right).
392 EVOLUTION & DEVELOPMENT Vol . 13, No. 4 , Ju l y --A ugu st 2 011
these features (which is referred to as the ‘‘omnivore’’ ecotype)
by default, they have the potential to develop as an alternative
‘‘carnivore’’ ecotype (sensu Pomeroy 1981), which is charac-
terized by large jaw muscles, notched and keratinized mouth-
parts, few labial teeth, and a short gut (Fig. 3; Pomeroy 1981;
Pfennig 1992a, b). Thus, although typical anuran larvae feed
opportunistically on macroscopic prey (e.g., macroinverte-
brates and dead tadpoles; Schiesari et al. 2009), Spea’s
carnivore morph is specialized for pursuing and subduing
live, macroscopic prey. Interestingly, the expression of this
ecomorph is induced by the consumption of shrimp and other
tadpoles (Pomeroy 1981; Pfennig 1990), although numerous
other factors also influence carnivore production
(Table 1). Moreover, the frequency with which the carnivore
morph is expressed, and how ‘‘extreme’’ the resulting carni-
vores are (i.e., the degree to which the carnivore is phenotyp-
ically distinct from the omnivore), varies among species,
populations, and even sibships (Pfennig 1999; Pfennig and
Murphy 2000, 2002).
A MAJOR RESEARCH CHALLENGE: PLASTICITY
AND EVOLUTION
Because spadefoot larval development is sensitive to diverse
environmental stimuli (Table 1), these tadpoles can be used to
examine how an organism’s ecology affects its development,
as well as how an organism’s development influences its ecol-
ogy and evolution. Additionally, spadefoot tadpoles are ex-
cellent models for examining the role of phenotypic plasticity
in evolution.
Evolutionary biologists have long hypothesized that phe-
notypic plasticity might precede, and even promote, genetic
evolution (Baldwin 1896; Schmalhausen 1949; Waddington
1953; West-Eberhard 1989; Schlichting and Pigliucci 1998; Pa
´l
and Miklos 1999; Pigliucci and Murren 2003; Price et al. 2003;
West-Eberhard 2003; Schlichting and Murren 2004; Moczek
2008; Pfennig et al. 2010). According to one widely accepted
hypothesis, if selection acts on quantitative genetic variation
regulating the expression of initially environmentally depen-
dent traits, it can lead to the evolution of reduced or enhanced
plasticity (the extremes being assimilation and polyphenism,
respectively; Waddington 1953; Mayr 1963). This processF
dubbed ‘‘genetic accommodation’’ (sensu West-Eberhard
2003)Fcan ultimately result in the evolution of a novel trait.
Although laboratory studies have demonstrated that genetic
accommodation can occur (Waddington 1953; Rutherford
and Lindquist 1998; Suzuki and Nijhout 2006), relatively little
is known about whether and how this process is responsible
for ecologically and evolutionarily relevant traits in natural
populations.
Fig. 3.Tadpoles in the genus Spea express polyphenism: alternate
phenotypes that are environmentally dependent. Some individuals
develop as typical omnivorous anuran larvae, which possess small
jaw muscles, smooth and unserrated mouthparts, and a long, coiled
intestine (left morph). In contrast, some individuals develop as a
carnivorous morph, possessing large jaw muscles, notched and
serrated mouthparts, and a short, relatively uncoiled gut (right).
The frequency and degree of carnivore morph expression varies
among species, populations and families. The process by which an
individual develops as a carnivore morph is likely influenced by
multiple environmental factors (e.g., social context and body con-
dition) however a potent environmental cue for the induction of
this alternate phenotype is the consumption of shrimp.
Table 1. Various factors that influence the expression of the distinctive carnivore ecotype in Spea tadpoles
Cue Effect on development Reference
Large animal prey Ingestion of shrimp or tadpoles induces carnivore production Pomeroy (1981); Pfennig (1990)
Heterospecific competitors Presence of heterospecific competitors can either increase or decrease
afocalindividual’slikelihoodofbecomingacarnivore,dependingon
the species
Pfennig and Murphy (2000)
Genetic relatives Presence of genetic relatives decreases a focal individual’s likelihood
of becoming a carnivore
Pfennig and Frankino (1997)
Individual’s condition Tadpoles in good condition (i.e., those with large mass relative to
body length) are more likely to become a carnivore when reared with
conspecific competitors, but less likely to do so when reared alone
Frankino and Pfennig (2001)
Emerging model systems in eco-evo-devo 393Ledo
¤n-Rettig and Pfennig
Understanding the role of environmentally dependent
variation in the origins of novel, complex traits has been a
major research focus in spadefoots. However, it is not the
only problem in eco-evo-devo that has been addressed using
spadefoots. Three additional topics have been the subjects of
research, including (1) the role of epigenetic inheritance in
adaptive evolution; (2) the role of developmental switches in
evolution; and (3) how feedback can arise among develop-
mental mechanisms, ecological processes, and evolutionary
outcomes. We highlight research each area below.
PLASTICITY AS AN ANTECEDENT OF NOVELTY
Relatively little is known about whether and how genetic
accommodation promotes the evolution of complex, novel
traits in natural populations. Part of the difficulty is that,
once a trait has already evolved, its evolution cannot be
studied in situ.
To examine whether and how an evolutionary lineage’s
past environmentally dependent responses played a role in the
origins of novel traits, we must find a way to ‘‘turn back the
clock.’’ One way of doing so is to use a comparative approach
informed by phylogeny (Shapiro 1980; Ghalambor et al.
2007). In other words, an effective approach for evaluating
plasticity’s role in the origins of novelty is to examine the
phenotypic responses of a taxon that is ‘‘ancestral’’ to taxa
possessing the novel trait in question, and thereby infer
whether the actual ancestors of the species or population in
question could express such a trait facultatively.
Spadefoots have been studied in this fashion. In one study,
the remarkably short larval periods of North American
spadefoots were compared with those of ‘‘ancestral’’ Euro-
pean spadefoots (Pelobates and Pelodytes;Gomez-Mestre
and Buchholz 2006). Even thoughtheformerpossessconsid-
erable plasticity in developmental timing, this plasticity has
been reduced along with a trend toward overall shorter larval
period. Taxa with reduced larval periods appear to have
evolved from developmentally plastic Pelobatid ancestors.
The assimilation of a shorter larval period might have
occurred when selection acted on genetic variation underly-
ing developmental rate, causing larvae to produce higher
levels of thyroid hormone (specifically, triiodotyrosine, or T
3
,
the key instigator of amphibian metamorphosis) and/or
greater tissue sensitivity to thyroid hormone (Gomez-Mestre
and Buchholz 2006). Indeed, the species possessing the short-
est larval period (and least metamorphic plasticity) expresses
high thyroid hormone receptor mRNA levels throughout
development relative to other spadefoots (D. R. Buchholz,
personal communication).
In a second study, this comparative approach was used to
investigate the evolution of an omnivore feeding strategy in
S. couchii tadpoles. In contrast to the generalist feeding strat-
egy exhibited by most spadefoot larvae, S. couchii feeds
exclusively on detritus and microorganisms, and suffers poor
fitness if fed only shrimp (Ledo
´n-Rettig et al. 2008, 2009).
Ancestors of S. couchii might have maintained a generalist
feeding strategy, which included the shrimp resource, but
were ultimately excluded from this diet as Spea larvae,
which inhabit the same ponds, evolved their cannibalistic
morphologies and behaviors (C. C. Ledo
´n-Rettig and D. W.
Pfennig, unpublished data). Importantly, ancestors of S. cou-
chii might have mediated this predation risk by choosing mi-
crohabitat distinct from the highest densities of cannibalistic
larvae and, as a by-product, the highest densities of shrimp.
These behavioral modifications might have been followed by
an evolutionary loss of behavioral, physiological, and mor-
phological traits that allowed S. couchii to consume shrimp,
leading to assimilation of the detritivore feeding strategy.
Further, S. couchii might have evolved a more specialized
detritivore morph. Indeed, evidence based on larval gut length
suggests that S. couchii are far more specialized for consuming
detritus than other anurans, including Spea (Altig and Kelly
1974) (Fig. 4).
Spadefoots have left other possible signatures of genetic
accommodation. For instance, although certain populations
Fig. 4.An ancestral character state reconstruction depicting the
distribution of trophic polyphenism among spadefoots species
(Pelobatoidea), their ancestors, and an outgroup (Xenopus). Rel-
ative support for the ability to express the carnivore morph is
indicated with black circles, while relative support for the expres-
sion of typical, monomorphic larvae is indicated with white circles
(tree from Garcı´a-Parı´setal.2003;reconstructionfromLedo
´n-
Rettig et al. 2008). Resource polyphenismFthe ability to express
discrete resource-use traitsFis confined to the genus Spea.S.mul-
tiplicata,Spea multiplicata;S. bombifrons,Spea bombifrons;
S. hammondii,Spea hammondii;S. intermontana,Spea intermon-
tana;S.couchii,Scaphiopus couchii;S. hurterii, Scaphiopus hurterii;
S. holbrookii, Scaphiopus holbrookii;P.caucasicus,Pelodytes
caucasicus;P. ibericus, Pelodytes ibericus;P. punctatus, Pelodytes
punctatus;P.varalidii,Pelobates varalidii;P. cultripes,Pelobates
cultripes;P. fuscus, Pelobates fuscus;P. syriacus, Pelobates syriacus;
B.feae,Brachytarsophrys feae;M.lateralis,Megophrys lateralis;
L.pelodytoides,Leptolalax pelodytoides.
394 EVOLUTION & DEVELOPMENT Vo l. 13, N o. 4, Ju ly -- A ugu st 2 011
of S. multiplicata are plastic with respect to the resource pol-
yphenism, those in sympatry with S. bombifrons are canalized
for the omnivore morph as a manifestation of character
displacement (trait evolution resulting from selection that
reduces competition; Pfennig and Murphy 2000, 2002). Like-
wise, although carnivores are normally induced in Spea only
after tadpoles have been exposed to shrimp or high tadpoles
densities, carnivores appear to be expressed constitutively in
certain populations of S. bombifrons (Pomeroy 1981). Ulti-
mately, the most direct evidence that environmentally depen-
dent phenotypes can engender evolutionary novelties will
come from selection studies on variation exposed under novel
environmental regimes. Spadefoots are not ideal for perform-
ing such selection studies (individuals do not reach sexual
maturity for at least one year). Nevertheless, such challenges
must be confronted if we are to understand if and how genetic
accommodation occurs in vertebrates.
EPIGENETIC INHERITANCE AND EVOLUTION
In many species, development is dictated not only by the
parental genetic contribution, but also by the parents’ extra-
genomic contributions (Roach and Wulff1987; Rossiter 1996;
Mousseau and Fox 1998). Indeed, parents often facultatively
endow their offspring with materials (e.g., resources, hor-
mones, and parental care: Schwabl 1993; Weaver et al. 2004;
Dloniak et al. 2006) or information (e.g., altered states of gene
regulation: Agrawal et al. 1999) that allow offspring to cope
better with their specific environment. In this way, ‘‘maternal
effects’’ (so called because most cases involve only mothers)
enable fitness-enhancing information acquired during the
mother’s lifetime to be transmitted directly to her offspring
(Mousseau and Fox 1998; Agrawal et al. 1999; Plaistow
et al. 2006). The widespread occurrence of environmentally
initiated maternal effects is important because it illustrates
how information acquired during an individual’s lifetime
can be transmitted to its offspring, thereby forming an alter-
native inheritance system (Jablonka and Lamb 1995, 2005;
Pigliucci 2007).
Additionally, maternal effects might play a key role in
generating novel phenotypes through genetic accommodation
(West-Eberhard 2003, 2005). A maternal effect influences
phenotypic expression in many individuals simultaneously,
especially when mothers produce large numbers of offspring.
Consequently, traits among the offspring whose expression is
mediated by a maternal effect can be tested in numerous,
diverse genetic backgrounds, thereby increasing the chances
of genetic accommodation occurring. Moreover, maternal
effects can spawn an evolutionary momentum that persists
for many generations, even in the absence of the original
environmental factor that induced the maternal effect
(Kirkpatrick & Lande 1989; for possible empirical examples,
see Agrawal et al. 1999; Plaistow et al. 2006). Consequently,
maternal effects provide more frequent, recurrent opportuni-
ties for genetic accommodation to transpire. Thus, traits
whose expression is influenced by maternal effects might be
especially likely to undergo subsequent refinement, elabora-
tion, and, possibly, developmental stabilization through
genetic accommodation.
In amphibians, development is especially sensitive to ma-
ternal condition (Kaplan 1998). For example, in Mexican
spadefoots (S. multiplicata), the maternal phenotype influ-
ences the expression of resource polyphenism among her tad-
pole offspring. Specifically, the tadpoles of larger females are
more likely to become carnivores (Martin and Pfennig 2010a).
Moreover, the tendency for large mothers to produce tadpoles
with a greater propensity to become carnivores has been
shown to reflect differences in maternal investment (Martin
and Pfennig 2010a). Larger females invest in larger eggs,
which become larger tadpoles. Larger tadpoles, in turn, are
able to handle shrimp more efficiently and thereby acquire
more of the cueFshrimp ingestionFthat induces the carni-
vore morph (Martin and Pfennig 2010a).
This maternal effect appears to mediate adaptive diver-
gence between populations (specifically, character displace-
ment), and there is even evidence that it has promoted the
evolution of canalized divergence in morph production be-
tween populations that have experienced prolonged and per-
sistent differences in exposure to a heterospecific competitor.
In particular, Mexican spadefoots (S. multiplicata)andPlains
spadefoots (S. bombifrons)havedivergedintheexpressionof
resource polyphenism where they co-occur in southeastern
Arizona, US, as an adaptive response to selection that min-
imizes competition with the other species (Pfennig and
Murphy 2000, 2002, 2003; Pfennig and Pfennig 2005; Pfennig
et al. 2006, 2007; Rice et al. 2009). In populations where each
species occurs alone, both species produce among their larvae
similar, intermediate frequencies of carnivores (which prey on
fairy shrimp) and omnivores (which specializes on detritus;
Pfennig et al. 2006). However, in populations where they co-
occur, S. multiplicata shift to producing mostly omnivores,
whereas S. bombifrons shift to producing mostly carnivores
(Pfennig and Murphy 2000, 2002, 2003; Pfennig et al. 2006).
This divergence appears to reflect selection to lessen interspe-
cific competition for food (Pfennig and Murphy 2000, 2002;
Pfennig et al. 2007; Rice et al. 2009). Specifically, by produc-
ing mostly omnivores, sympatric S. multiplicata avoid com-
peting for shrimp with S. bombifrons,thespeciesthatisthe
superior competitor for the shrimp resource. By contrast, by
producing mostly carnivores, sympatric S. bombifrons avoid
competing for detritus with S. multiplicata,thespeciesthatis
the superior competitor for the detritus resource (Pfennig and
Murphy 2000).
Although these differences between sympatric and allo-
patric populations of S. multiplicata persist even when
Emerging model systems in eco-evo-devo 395Ledo
¤n-Rettig and Pfennig
tadpoles are reared under common conditions (Pfennig
and Murphy 2000, 2002), they appear to be mediated by a
condition-dependent maternal effect (Pfennig and Martin
2009). Specifically, because sympatric S. multiplicata are
forced by S. bombifrons onto the less nutritious detritus
resource (Pfennig and Murphy 2000), sympatric S. multipli-
cata tend to mature as smaller (Pfennig and Pfennig 2005) and
poorer condition adults (Pfennig and Martin 2009). Presum-
ably because of their reduced size and/or condition, female
S. multiplicata in sympatry invest less into offspring than do
female S. multiplicata in allopatry (Martin and Pfennig
2010a). Because smaller, poorer condition females produce
mostly omnivores (see above), these females create offspring
with a phenotype that minimizes competition with S. bomb-
ifrons and that differs from the phenotype in allopatry. How-
ever, these population differences in morph production
disappear once mothers are equilibrated in body condition
(Pfennig and Martin 2009), indicating that a condition-
dependent maternal effect mediates character displacement in
this species. Indeed, the relatively small females from each
generation should also tend to produce small eggs and omni-
vores in the next generation, fueling a self-reinforcing epige-
netic cycle that promotes divergence between sympatric and
allopatric populations (Pfennig and Martin 2009).
Environmentally mediated maternal effects, similar to
those observed in S. multiplicata,mighthaveprecededand
promoted canalized differences in populations of S. bombif-
rons.IncontrasttoS. multiplicata,theexpressionofcarnivore
morphs in S. bombifrons is not (or may no longer be) depen-
dent on maternal condition (Pfennig and Martin 2010). As
mentioned, S. bombifrons express a higher frequency of car-
nivores in sympatry relative to allopatry, but this difference is
not related to population differences in maternal condition.
Instead, divergence between sympatric and allopatric
S. bombifrons populations in morph production appears to
reflect genetically fixed differences between these two types of
populations.
How did these differences arise from environmentally me-
diated maternal effects? The answer may reside in the history
of this population of S. bombifrons with its resource compet-
itor. S. bombifrons has recently invaded S. multiplicata’s rel-
atively stable range (Rice and Pfennig 2008), and populations
of S. bombifrons at the front of this expansionFthat is, pop-
ulations in which the carnivore morph is expressed in the
absence of the maternal effectFhave had a relatively long
evolutionary history with their competitor. In contrast, pop-
ulations of S. multiplicata at the edge of this invasion front
have had very little time to evolve, genetically, in response to
their competition. Therefore, it appears that the expression of
the carnivore morph in S. bombifrons populations at the front
of an invasion has become divorced from maternal control by
substitution with novel genetic variants and combinations
(Pfennig and Martin 2010).
DEVELOPMENTAL SWITCHES AS FACILITATORS
OF DIVERSITY
Although the origins of developmental polyphenisms is a
motivating topic per se, once in place, they might subse-
quently facilitate the evolution of adaptive, phenotypic
variation (West-Eberhard 1989; Moczek 2009; Minelli and
Fusco 2010; Pfennig et al. 2010). On two fronts, through their
biphasic life cycle and their resource polyphenism, spadefoots
can be used to investigate the origins and evolutionary con-
sequences of developmental switches.
It is still unclear whether Spea’s resource polyphenism
evolved from continuous variation (Martin and Pfennig
2010b), or whether it has been resurrectedFfully intact or
in particular aspectsFfrom some quiescent developmental
switch expressed in ancestral amphibian larvae. However, in
other systems, it is often possible to reveal intermediate forms
from natural populations (Nijhout 2003) and evolve polyp-
henisms from continuous variation in the lab (Suzuki and
Nijhout 2006). This suggests that in some cases continuous
plasticity is ancestral, and that discrete polyphenism is the
result of selection for adaptive, alternative phenotypes (Nijh-
out 2003; Moczek 2007). Further, some nonpolyphenic spade-
foot populations exhibit heritable variation in diet-dependent
gut length, indicating that at least some elements of this re-
source polyphenism could have arisen from selection on con-
tinuous, diet-dependent variation (Ledo
´n-Rettig et al. 2010).
Once a developmental switch or sequence has evolved, its
components can be ‘‘rearranged’’ into novel combinations
(i.e., ‘‘developmental recombination’’; West-Eberhard 2003).
Such components might include alternate modes of behavior,
physiology, or morphology that can be deleted, duplicated,
amplified, or altered to produce a drastically different out-
come or respond to different cues. This recombination is
possible when context-dependent phenotypes are underlain by
modular elements (i.e., genes, proteins, or other traits) that are
free from pleiotropic constraints with traits expressed in other
contexts (i.e., environments or developmental stages). There is
rapidly accumulating evidence that developmental polyp-
henisms are often underlain by modular elements, at least at
the level of gene expression (Moczek 2009; Snell-Rood et al.
2011).
In spadefoot larvae, the stress axis may be a key regulator
of developmental switches such that variation in the elements
of this axis has resulted in phenotypic diversification. Across
vertebrate taxa, the stress axis plays an important role in
transducing environmental signals into developmental, be-
havioral, and physiological responses (Crespi and Denver
2005a). Interestingly, in anuran larvae, the major develop-
mental and stress hormones (T
3
and corticosterone [CORT],
respectively) are controlled by the same neuroendocrine fac-
tor, corticotropin-releasing factor (CRF; Denver 1999). As
mentioned, spadefoot larvae can accelerate metamorphosis in
396 EVOLUTION & DEVELOPMENT Vo l. 13, N o. 4, Ju ly -- A ugu st 2 011
response to nutritional restriction, crowding, water tempera-
ture elevation, or water volume reduction (Denver et al. 1998;
Morey and Reznick 2000; Boorse and Denver 2003; Crespi
and Denver 2005b; Gomez-Mestre and Buchholz 2006). In
the last case, metamorphic timing has been directly linked to
CRF regulation (Denver 1997). Because all these cues are
indicative of a deteriorating larval habitat, it is likely that
CRF coordinates the timing of anuran metamorphosis with
environmental information by coupling the environmental
sensitivity of CRF secreting neurons to the actions of T
3
and
CORT on an individual’s developmental response.
Given that the stress axis is ancient and functions across
birds, mammals, fish, amphibians, and reptiles, this develop-
mental switch might have been co-opted in amphibian larvae
so that they could respond to a unique set of signals that are
particularly good at predicting the condition of aquatic
habitats. Likewise, the same endocrine machinery used for
escaping drying ponds might have been co-opted to produce
the alternate trophic morph in Spea.Thethyroidhormone
T
3
has been implicated in the expression of the larval carni-
vore morph, which possesses certain attributes characteristic
of metamorphosing individuals (Pfennig 1992b).
If the endocrine signal for rapid development, T
3
,isindeed
involved in the production of the carnivore morph, then why
do tadpoles that become carnivores not, at the same time,
metamorphose? As it turns out, carnivore-morph tadpoles do
indeed metamorphose significantly earlier than omnivore-mo-
rph tadpoles reared under the same conditions (Pomeroy
1981; Pfennig 1992b). Moreover, the effects of T
3
on certain
tissues and organs might have been divorced through differ-
ential distribution of hormone receptors or genetic variation
in the downstream targets of hormone receptors, themselves.
These topics clearly need further investigation, but we antic-
ipate that a comparison of the hormonal regulation of
morphs, populations, and species that vary in plastic re-
sponses (i.e., developmental timing and resource polyphenism)
will reveal whether ancestral developmental switches (e.g., the
stress axis) can facilitate the diversification of phenotypes.
Traits need not only evolve when they become dissociable
during ontogeny and evolution. The converse situation of
modularity is when developmental switches have pleiotropic
effects on traits, resulting in relationships that are conserved
between populations and species, even if they are exposed to
different environmental conditions. If a threshold switch itself
evolves (occurring earlier or later during ontogeny, respond-
ing more or less or to different environmental cues), it might
bring about the evolution of correlated traits in its wake
(Nijhout and Emlen 1998; Moczek and Nijhout 2004; Suzuki
and Nijhout 2008). For instance, in spadefoots, adult snout
and leg lengths are positively correlated with how long a tad-
pole develops (a highly environmentally dependent variable;
Gomez-Mestre and Buchholz 2006). More remarkably, adult
snout and leg lengths among different species are positively
correlated with the length each species’ average larval period.
Although it is not clear if these evolutionary by-products are
adaptive, such correlations generate phenotypic variation that
can act as new targets for selection and would not otherwise
be made available.
RECIPROCAL ACCOMMODATION
Above, we focused on how the larval spadefoot’s phenotypic
response is shaped by its environmental variation and
ecological interactions. However, the reciprocal is also
true: environments and communitiesFand thus, selective
regimesFare modified by the phenotypic responses of the
individuals within them (Lewontin 1983; Day et al. 2003).
Although this was recognized by evolutionary biologists
during the modern synthesis (reviewed in Wcislo 1989;
Odling-Smee et al. 2003), the interdependency of organismal
responses and selective environments was not included in
most conceptual and theoretical models until much later
(sensu Lewontin 1983). Advocates of this perspective argue
that the behavioral, morphological, and physiological pheno-
types elicited by organisms are not merely the end products
of selection, but evolutionary processes that alter selection
pressures. This process is generally referred to as ‘‘niche
construction’’ (sensu Odling-Smee 1988).
Some interactions might lead to an eco-evolutionary feed-
back that modifies the evolutionary trajectories of associated
traits, a process that we will refer to as ‘‘reciprocal accom-
modation’’ (sensu Gilbert and Epel 2009). Although it is clear
that, in many cases, reciprocal accommodation modifies the
evolutionary trajectory of involved traits, whether the evolu-
tion of such traits is promoted or constrained depends on a
population’s environmental and phylogenetic history (Sultan
2007). For instance, organisms can alter their competitive
environment via character displacement (Schluter 2000), but
the ability to undergo character displacement tends to be
more prevalent and proceed more quickly in taxa that are
phenotypically variable (Rice and Pfennig 2007). This vari-
ability is, in turn, contingent on a species’ or population’s
evolutionary past with other environmental and ecological
challenges.
Such reciprocal accommodation can be observed in Spea.
As mentioned above, both S. multiplicata and S. bombifrons
exhibit resource polyphenism in allopatry, but competitive
interactions have promoted divergence between these species’
in sympatry. In particular, where the two species occur
together, selection favors omnivorous traits in S. multiplicata.
By contrast, selection favors carnivorous traits in S. bombif-
rons.Thetwospeciesemployphenotypicplasticitytopro-
mote this divergence in trophic morphology (and, hence, in
resource use; Pfennig and Murphy 2002). Species that can
facultatively alter their phenotypes in this way may persist in
Emerging model systems in eco-evo-devo 397Ledo
¤n-Rettig and Pfennig
the face of novel competitive interactions, because they can
switch to a selectively favored phenotype without having to
wait for mutation or recombination (Pfennig and Murphy
2000, 2002). That is, Spea’s developmental plasticity has
shaped their ecology; in the absence of such plasticity, the less
competitive species may have become locally extinct through
competitive exclusion.
The mechanisms by which niche construction can promote
or impede trait evolution can be explained in terms of tra-
ditional quantitative genetics (Donohue 2005), and factors
that may allow or prevent a population from responding to
niche construction are the same as those that would apply to
general adaptive evolution. Still, few empirical examples exist
that convincingly demonstrate the influence of niche con-
struction on the evolution of traits and suites of traits
(although see Post and Palkovacs 2009). As discussed above,
variation in larval competitive environments among popula-
tions of spadefoots makes them particularly amenable for
isolating the influence of niche construction on the evolution
of resource use traits.
CONCLUSIONS AND FUTURE DIRECTIONS
The fields of ecology, evolution, and development are not
only informed by one another; they are contingent on one
another. Even though the questions asked by these fields are
seemingly different, and cross-talk among these fields has
been relatively limited, the emergent phenomena that can be
explained by considering all fields in conjunction will be
greater than the sum of the parts. Furthermore, because of
recent advances in techniques that make the syntheses of
these fields possible, now is the time that integrating eco-devo
with evo-devo might yield the largest and most important
contributions.
For instance, determining whether or to what extent al-
ternate, environmentally dependent phenotypes share the
same developmental modules is critical for understanding the
evolutionary consequences of plasticity (Snell-Rood et al.
2010). It is now possible to characterize these developmental
modules at the level of gene expression (e.g., see Snell-Rood et
al. 2011). Research in our lab on spadefoots has thus far
identified over 70 distinct genes that are differentially ex-
pressed between omnivore and carnivore morphs in both lab-
reared and field-caught individuals (A. Leichty and D. W.
Pfennig, unpublished data). Given the importance of the om-
nivore–carnivore larval polyphenism in determining fitness,
genes that are differentially expressed between these alterna-
tive morphs might be the ultimate targets of selection in this
system. Future studies should seek to ascertain whether or not
these genes are indeed under strong selection in populations
where the omnivore–carnivore larval polyphenism has
evolved. Moreover, insights into the functionality and his-
tory of these genes might illuminate how the polyphenism
evolved in the first place.
In addition to divergence in developmental modules, per
se, phenotypic variation can arise due to differences in the
timing and placement of the same developmental modules
(e.g., see ‘‘Developmental Switches as Facilitators of Diver-
sity’’). Currently, researchers are identifying the endocrine and
molecular mechanisms (i.e., altered production of metamor-
phic hormones and expression of hormone receptors) asso-
ciated with variation in the neuroendocrine stress axis,
allowing spadefoot tadpoles to diversify in metamorphic plas-
ticity (D. R. Buchholz, personal communication).
In the future, the challenge of integrating eco-devo with
evo-devo will be to identify appropriate systems in which we
know a considerable amount about their genetic variation,
ecological interactions, and developmental responses. Spade-
foots are well suited for this task because numerous studies
have illuminated the environmental effects on early develop-
ment, and even their lasting effects on adult phenotypes (e.g.,
see ‘‘The Environmentally Responsive Spadefoot’’). Indeed,
although eco-devo has only recently gained attention in the
literature, research on spadefoots and other amphibians has
been contributing to this field for decades. Moreover, spade-
foots might help to illuminate an overlooked problem in eco-
devo: how development affects ecology. As noted above, a
common, but potentially important, way in which develop-
ment might impact ecology is by promoting character
displacement (see ‘‘Reciprocal Accommodation’’). Thus,
research on spadefoots has been, and may continue to be
instrumental in shedding light on both how an organism’s
ecology can affect its development, and also onto how its
development can influence its ecology. By characterizing and
understanding the interconnectedness among development
responses, ecological interactions, and their evolutionary
responses of natural populations, we can ultimately answer,
the major question uniting practitioners of eco-evo-devo,
posed at the outset: what is the environment’s role, not only in
selecting among diverse phenotypes, but also in creating these
diverse phenotypes?
Acknowledgments
We thank Karin Pfennig, Aaron Leichty, Dan Buchholz, Sabrina
Burmeister, Nanette Nascone-Yoder, Keith Sockman, and two
anonymous reviewers for commenting on the paper. The research
described here was funded by the National Science Foundation
under grants IOS-0818212, DEB-0640026, DEB-1019479, and the
Graduate Research Fellowship Program.
REFERENCES
Agrawal, A. A., Laforsch, C., and Tollrian, R. 1999. Transgenerational
induction of defenses in animals and plants. Nature 401: 60–63.
Altig, R., and Kelly, J. P. 1974. Indices of feeding in anuran tadpoles as
indicated by gut characteristics. Herpetologica 30: 200–203.
398 EVOLUTION & DEVELOPMENT Vo l. 13, N o. 4, Ju ly -- A ugu st 2 011
Altig, R., Whiles, M. R., and Taylor, C. L. 2007. What do tadpoles really
eat? Assessing the trophic status of an understudied and imperiled group
of consumers in freshwater habitats. Freshw. Biol. 52: 386–395.
Baldwin, J. M. 1896. A new factor in evolution. Am. Nat. 30: 441–451.
Boorse, G. C., and Denver, R. J. 2003. Endocrine mechanisms underlying
plasticity in metamorphic timing in spadefoot toads. Int. Comp. Biol. 43:
646–657.
Bragg, A. N. 1965. Gnomes of the Night. The Spadefoot Toads.Universityof
Pennsylvania Press, Philadelphia.
Crespi, E. J., and Denver, R. J. 2005a. Ancient origins of human devel-
opmental plasticity. Am. J. Hum. Biol. 17: 44–54.
Crespi, E. J., and Denver, R. J. 2005b. Roles of stress hormones in food
intake regulation in anuran amphibians throughout the life cycle. Comp.
Biochem. Physiol. A Mol. Int. Physiol. 141: 381–390.
Day, R. L., Laland, K. N., and Odling-Smee, J. 2003. Rethinking adaptation
Fthe niche-construction perspective. Perspect. Biol. Med. 46: 80–95.
Denver, R. J. 1997. Environmental stress as a developmental cue:
corticotropin-releasing hormone is a proximate mediator of adaptive
phenotypic plasticity in amphibian metamorphosis. Horm. Behav. 31:
169–179.
Denver, R. J. 1999. Evolution of the corticotropin-releasing hormone sig-
naling system and its role in stress-induced phenotypic plasticity. In C. A.
Sandman, F. L. Strand, B. Beckwith, B. M. Chronwall, F. W. Flynn,
and R. J. Nachman (eds.). Neuropeptides: Structure and Function in
Biology and Behavior.NewYorkAcademyofSciences,NewYork,pp.
46–53.
Denver, R. J., Mirhadi, N., and Phillips, M. 1998. Adaptiveplasticityin
amphibian metamorphosis: response of Scaphiopus hammondii tadpoles
to habitat desiccation. Ecology 79: 1859–1872.
Dloniak, S. M., French, J. A., and Holekamp, K. E. 2006. Rank-related
maternal effects of androgens on behaviour in wild spotted hyenas.
Nature 440: 1190–1193.
Donohue, K. 2005. Niche construction through phenological plasticity: life
history dynamics and ecological consequences. New Phytol. 166: 83–92.
Duellman, E., and Trueb, L. 1986. Biology of Amphibians.JohnHopkins
University Press, Baltimore.
Frankino, W. A., and Pfennig, D. W. 2001. Condition-dependent expres-
sion of trophic polyphenism: effects of individual size and competitive
ability. Evol. Ecol. Res. 3: 939–951.
Garcı´a-Parı´s, M., Buchholz, D. R., and Parra-Olea, G. 2003. Phylogenetic
relationships of Pelobatoidea re-examined using mtDNA. Mol. Phylo-
genet. Evol. 28: 12–23.
Ghalambor, C. K., McKay, J. K., Carroll, S. P., and Reznick, D. N. 2007.
Adaptive versus non-adaptive phenotypic plasticity and the potential for
contemporary adaptation in new environments. Funct. Ecol. 21: 394–407.
Gilbert, S., and Epel, D. 2009. Ecological Developmental Biology: Integrat-
ing Epigenetics, Medicine, and Evolution. Sinauer Associates, Sunderland.
Gomez-Mestre, I., and Buchholz, D. 2006. Developmental plasticity mir-
rors differences among taxa in spadefoot toads linking plasticity and
diversity. Proc. Nat. Acad. Sci. USA 50: 19021–19026.
Jablonka, E., and Lamb, M. J. 1995. Epigenetic Inheritance and Evolution:
The Lamarckian Dimension. Oxford University Press, Oxford.
Jablonka, E., and Lamb, M. J. 2005. Evolution in Four Dimensions: Genetic,
Epigenetic, Behavioral and Symbolic Variation in the History of Life.MIT
Press, Cambridge.
Kaplan, R. H. 1998. Maternal effects, developmental plasticity, and life
history evolution: an amphibian model. In T. A. Mousseau and C. W.
Fox (eds.). Maternal Effects as Adaptations. Oxford University Press,
New York, pp. 244–260.
Kirkpatrick, M., and Lande, R. 1989. The evolution of maternal characters.
Evolution 43: 485–503.
Ledo
´n-Rettig, C. C., Pfennig, D. W., and Crespi, E. J. 2009. Stress hor-
mones and the fitness consequences associated with the transition to a
novel diet in larval amphibians. J. Exp. Biol. 212: 3743–3750.
Ledo
´n-Rettig, C. C., Pfennig, D. W., and Crespi, E. J. 2010. Diet and
hormonal manipulation reveal cryptic genetic variation: implications for
the evolution of a novel feeding strategy. Proc. Roy. Soc. Lond. B 277:
3569–3578.
Ledo
´n-Rettig, C. C., Pfennig, D. W., and Nascone-Yoder, N. 2008. An-
cestral variation and the potential forgeneticaccommodation in larval
amphibians: implications for the evolution of novel feeding strategies.
Evol. Dev. 10: 316–325.
Lewontin, R. C. 1983. Organism and environment. In H. C. Plotkin (ed.).
Learning, Development, and Culture.JohnWileyandSons,Ltd,New
York, pp. 151–170.
Martin, R. A., and Pfennig, D. W. 2010a. Maternal investment influ-
ences expression of resource polymorphism in amphibians: implica-
tions for the evolution of novel resource-use phenotypes. PLoS ONE 5:
e9117.
Martin, R. A., and Pfennig, D. W. 2010b. Field and experimental evidence
that competition and ecological opportunity promote resource polymor-
phism. Biol. J. Linn. Soc. Lond. 100: 73–88.
Mayr, E. 1963. Animal Species and Evolution. Belknap Press, Cambridge.
Minelli, A., and Fusco, G. 2010. Developmental plasticity and the evolution
of animal complex life cycles. Phil. Trans. Roy. Soc. B Biol. Sci. 365:
631–640.
Moczek, A. P. 2007. Developmental capacitance, geneticaccommodation,
and adaptive evolution. Evol. Dev. 9: 299–305.
Moczek, A. P. 2008. On the origins of novelty in development and
evolution. Bioessays 30: 432–447.
Moczek, A. P. 2009. The origin and diversification of complex traits
through micro- and macroevolution of development: insights from
horned beetles. In W. Jeffery (ed.). Current Topics in Developmental
Biology. Vol. 86. Elsevier Academic Press Inc, San Diego, pp. 135–162.
Moczek, A. P., and Nijhout, H. F. 2004. Trade-offs during the development
of primary and secondary sexual traits in a horned beetle. Am. Nat. 163:
184–191.
Morey, S., and Reznick, D. 2000. A comparative analysis of plasticity in
larval development in three species of spadefoot toads. Ecology 81:
1736–1749.
Mousseau, T. A., and Fox, C. W. 1998. Maternal Effects as Adaptations.
Oxford University Press, New York.
Newman, R. A. 1989. Developmental plasticity of Scaphiopus couchii tad-
poles in an unpredictable environment. Ecology 70: 1775–1787.
Newman, R. A. 1992. Adaptive plasticity in amphibian metamorphosis.
Bioscience 42: 671–678.
Newman, R. A. 1994. Genetic variation for phenotypic plasticity in the
larval life history of spadefoot toads (Scaphiopus couchii). Evolution 48:
1773–1785.
Nijhout, H. F. 2003. Development and evolution of adaptive polyphenisms.
Evol. Dev. 5: 9–18.
Nijhout, H. F., and Emlen, D. J. 1998. Competition among body parts in
the development and evolution of insect morphology. Proc. Nat. Acad.
Sci. USA 95: 3685–3689.
Odling-Smee, J. 1988. Niche constructing phenotypes. In H. C. Plotkin
(ed.). The Role of Behavior in Evolution.MITPress,Cambridge,MA,pp.
73–132.
Odling-Smee, J., Laland, K. N., andFeldman, M. 2003. Niche Construction:
The Neglected Process in Evolution. Princeton University Press, Prince-
ton, NJ.
Pa
´l, C., and Miklos, I. 1999. Epigenetic inheritance, genetic assimilation and
speciation. J. Theor. Biol. 200: 19–37.
Pfennig, D. W. 1990. The adaptive significance of an environmentally-
cued developmental switch in an anuran tadpole. Oecologia 85:
101–107.
Pfennig, D. W. 1992a. Polyphenism in spadefoot toad tadpoles as a locally
adjusted evolutionary stable strategy. Evolution 46: 1408–1420.
Pfennig, D. W. 1992b. Proximate and functional causes of polyphenism in
an anuran tadpole. Funct. Ecol. 6: 167–174.
Pfennig, D. W. 1999. Cannibalistic tadpoles that pose the greatest threat to
kin are most likely to discriminate kin. Proc. Roy. Soc. Lond. B Biol. Sci.
266: 57–61.
Pfennig, D. W., and Frankino, W. A. 1997. Kin-mediated morphogenesis in
facultatively cannibalistic tadpoles. Evolution 51: 1993–1999.
Pfennig, D. W., and Martin, R. A. 2009. A maternal effect mediates rapid
population divergence and character displacement in spadefoot toads.
Evolution 63: 898–909.
Pfennig, D. W., and Martin, R. A. 2010. Evolution of character displace-
ment in spadefoot toads: different proximate mechanisms in different
species. Evolution 64: 2331–2341.
Emerging model systems in eco-evo-devo 399Ledo
¤n-Rettig and Pfennig
Pfennig, D. W., and Murphy, P. J. 2000.Characterdisplacementinpoly-
phenic tadpoles. Evolution 54: 1738–1749.
Pfennig, D. W., and Murphy, P. J. 2002. How fluctuating competition
and phenotypic plasticity mediate species divergence. Evolution 56:
1217–1228.
Pfennig, D. W., and Murphy, P. J. 2003. A test of alternative hypotheses
for character divergence between coexisting species. Ecology 84:
1288–1297.
Pfennig, D. W., Rice, A. M., and Martin, R. A. 2006. Ecological oppor-
tunity and phenotypic plasticity interact to promote character displace-
ment and species coexistence. Ecology 87: 769–779.
Pfennig, D. W., Rice, A. M., and Martin, R. A. 2007. Field and
experimental evidence for competition’s role in phenotypic divergence.
Evolution 61: 257–271.
Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T.,
Schlichting, C. D., and Moczek, A. P. 2010. Phenotypic plasticity’s im-
pacts on diversification and speciation. Trends Ecol. Evol. 25: 459–467.
Pfennig, K. S., and Pfennig, D. W. 2005. Character displacement as the
‘‘best of a bad situation’’: fitness trade-offs resulting from selection to
minimize resource and mate competition. Evolution 59: 2200–2208.
Pigliucci, M. 2007. Do we need an extended evolutionary synthesis? Evo-
lution 61: 2743–2749.
Pigliucci, M., and Murren, C. J. 2003. Perspective: Genetic assimilation and
a possible evolutionary paradox: Can macroevolution sometimes be so
fast as to pass us by? Evolution 57: 1455–1464.
Plaistow, S. J., Lapsley, C. T., and Benton, T. G. 2006. Context-dependent
intergenerational effects: the interaction between past and present envi-
ronments and its effect on population dynamics. Am. Nat. 167: 206–215.
Pomeroy, L. V. 1981. Developmental polymorphism in the tadpoles of the
spadefoot toad Scaphiopus multiplicatus.PhDdissertation,Universityof
California, Riverside.
Post, D. M., and Palkovacs, E. P. 2009. Eco-evolutionary feedbacks in
community and ecosystem ecology: interactions between the ecological
theatre and the evolutionary play. Phil. Trans. Roy. Soc. B Biol. Sci. 364:
1629–1640.
Price, T. D., Qvarnstrom, A., and Irwin, D. E. 2003. The role of phenotypic
plasticity in driving genetic evolution. Proc. Roy. Soc. Lond. B Biol. Sci.
270: 1433–1440.
Rice, A. M., Leichty, A. R., and Pfennig, D. W. 2009. Parallel evolution
and ecological selection: replicated character displacement in spadefoot
toads. Proc. Roy. Soc. B Biol. Sci. 276: 4189–4196.
Rice, A. M., and Pfennig, D. W. 2007. Character displacement: in situ
evolution of novel phenotypes or sorting of pre-existing variation?
J. Evol. Biol. 20: 448–459.
Rice, A. M., and Pfennig, D. W. 2008. Analysis of range expansion in two
species undergoing character displacement: why might invaders generally
‘win’ during character displacement? J. Evol. Biol. 21: 696–704.
Roach, D. A., and Wulff, R. D. 1987. Maternal effects in plants. Annu. Rev.
Ecol. Syst. 18: 209–235.
Rossiter, M. C. 1996. Incidence and consequences of inherited environ-
mental effects. Annu. Rev. Ecol. Syst. 27: 451–476.
Rutherford, S. L., and Lindquist, S. 1998. Hsp90 as a capacitor for mor-
phological evolution. Nature 396: 336–342.
Schiesari, L., Werner, E. E., and Kling, G. W. 2009. Carnivory and
resource-based niche differentiation in anuran larvae: implications for
food web and experimental ecology. Freshw. Biol. 54: 572–586.
Schlichting, C. D., and Murren, C. J. 2004. Evolvability and the raw ma-
terials for adaptation. In Q. C. B. Cronk, J. Whitton, R. H. Ree, and I.
E. P. Taylor (eds.). Plant Adaptation: Molecular Genetics and Ecology.
NRC Research Press, Ottawa, pp. 18–29.
Schlichting, C. D., and Pigliucci, M. 1998. Phenotypic Evolution: A Reaction
Norm Perspective. Sinauer Associates, Sunderland.
Schluter, D. 2000. The Ecology of Adaptive Radiation.OxfordUniversity
Press, Oxford, UK.
Schmalhausen, I. I. 1949. Factors of Evolution: The Theory of Stabilizing
Selection. Blakiston, Philadelphia.
Schwabl, H. 1993. Yolk is a source of maternal testosterone for developing
birds. Proc. Nat. Acad. Sci. USA 90: 11446–11450.
Shapiro, A. M. 1980. Physiological and developmental responses to photo-
period and temperature as data in phylogenetic and biogeographic
inference. Syst. Zool. 29: 335–341.
Snell-Rood, E. C., Cash, A., Han, M. V., Kijimoto, T., Andrews, J., and
Moczek, A. P. 2011. Developmental decoupling of alternative pheno-
types: insights from the transcriptomes of horn-polyphenic beetles. Evo-
lution 65: 231–245.
Snell-Rood, E. C., van Dyken, J. D., Cruickshank, T., Wade, M. J., and
Moczek, A. P. 2010. Toward a population genetic framework of devel-
opmental evolution: the costs, limits, and consequences of phenotypic
plasticity. Bioessays 32: 71–81.
Sultan, S. E. 2007. Development in context: the timely emergence of eco-
devo. Trends Ecol. Evol. 22: 575–582.
Sultan, S. E. 2010. Plant developmental responses to the environment: eco-
devo insights. Curr. Opin. Plant Biol. 13: 96–101.
Suzuki, Y., and Nijhout, H. F. 2006. Evolution of a polyphenism by genetic
accommodation. Science 311: 650–652.
Suzuki, Y., and Nijhout, H. F. 2008. Constraint and developmental dis-
sociation of phenotypic integration in a genetically accommodated trait.
Evol. Dev. 10: 690–699.
Waddington, C. H. 1953. Genetic assimilation of an acquired character.
Evolution 7: 118–126.
Wcislo, W. T. 1989. Behavioral environments and evolutionary change.
Annu. Rev. Ecol. Evol. Syst. 20: 137–169.
Weaver, I. C. G., et al. 2004. Epigenetic programming by maternal behav-
ior. Nat. Neurosci. 7: 847–854.
West-Eberhard, M. J. 1989. Phenotypic plasticity and the origins of diver-
sity. Annu. Rev. Ecol. Syst. 20: 249–278.
West-Eberhard, M. J. 2003. Developmental Plasticity and Evolution.Oxford
University Press, New York.
West-Eberhard, M. J. 2005. Phenotypic accommodation: adaptive innova-
tion due to developmental plasticity. J. Exp. Zool. B Mol. Dev. Evol. 304:
610–618.
400 EVOLUTION & DEVELOPMENT Vo l. 13 , No. 4 , Ju ly -- A ugu st 2 011
