Control Mechanisms

of
PolyphenicDevelopment
in Insects
In polyphenicdevelopment,environmental
factorsaltersome
aspects of developmentin an orderlyand predictableway
H. FrederikNijhout

It is well known that there is no with wings and distinctive behavior

necessaryone-to-onerelationship The developmental and physiology, that contrast with
between the genetic makeup of the typically short-winged or wing-
an organism-its genotype-and the system of insects is less sedentary morphs, which have
various characters and properties their own suite of distinctive behav-
that constitute its phenotype.In fact, preadapted in many ways ioral and physiological adaptations
it is precisely for this reason that (Zera and Denno 1997). In each of
terms like genotype and phenotype for the rapid evolution of these behavioral and physiological
are used to specify whether we are polyphenisms, the environment ex-
concernedwith an organism's genes phenotypic plasticity perienced by an individual before
or its external appearance.Students adulthood dramatically affects the
of biology are most familiar with type to develop two or more dis- adult phenotype that develops after
one of the causes of uncertainty in tinctly different alternative pheno- metamorphosis.
the relationship between genes and types without intermediates. The The existence of species that can
characters,namely,the relativedomi- phenotype that is expressed depends expressalternativephenotypesraises
nance of different alleles of a given on the environmentalconditions that interesting questions about the de-
gene. With dominance, a particular the organism encounters during its velopment and evolution of such sys-
phenotype can be produced by sev- development. tems. Froma developmentalperspec-
eral different genotypes. The uncer- Polyphenisms have many mani- tive, it is of interest to discover how
tainty works in the other directionas festations. Many insect species have it is possible for animals with the
well: A single genotype can produce distinctive seasonal adult pheno- same genotype to develop vastly dif-
many differentphenotypes, depend- types; these may be winged or wing- ferentphenotypes,what developmen-
ing on variouscontingenciesencoun- less, may differ in the proportions of tal mechanism allows the animal to
tered during development. That is, various body parts, and may have switch between these alternatives,
the phenotype is the outcome of a differentfood preferences,reproduc- and how this developmentalswitch-
complex seriesof developmentalpro- tive characteristics, and color pat- ing mechanism senses specific sig-
cesses that are influenced by envi- terns (Figure1). Many of the pheno- nals from the environment.From an
ronmentalfactorsas well as by genes. typic differences between seasonal evolutionary perspective, it is of in-
Different environmentscan have an forms are believed to be adaptations terest to discover whether a given
effect on the outcome of develop- to the limitations and opportunities phenotype has a higher fitness in its
ment that is as profound as that presented by a seasonally changing corresponding environment than the
produced by different genes. This environment. The seasonal pheno- alternative phenotype, whether one
phenomenon,which is nearlyuniver- types of insects can be so different phenotype is evolutionarily derived
sal, is called phenotypicplasticity. from each other that many were ini- from the other, and how the use of a
Polyphenism is a special case of tially described as different species. specific environmental cue evolved.
phenotypic plasticity; it refersto the The caste polyphenisms of social in- The answers to some of these ques-
abilityof animalswith the samegeno- sects are equallydramatic,often con- tions are beginning to be understood.
sisting of highly specialized soldier, Control mechanisms for poly-
Nijhout(e-mail:hfn@acpub. worker, and reproductivecastes, all
H. Frederik phenic development have been stud-
duke.edu)is a professorin the Depart- of which are genetically identical ied at several levels: environmental,
ment of Zoology, Duke University, (Wilson 1971, Nijhout and Wheeler developmental, and genetic. Most
Durham, NC 27708-0325. ? 1999 1982). Insects from many orders are investigations of the development
AmericanInstituteof BiologicalSciences. able to develop dispersal morphs, and evolution of polyphenism have

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 tended to focus on only one butterflies is actually better
of these levels, and relatively correlated with overall de-
few attemptshave been made velopment time than with
to integrate information temperature per se, which
across these levels. In this suggests that any mechanism
article, I outline some of the that slows the rate of devel-
general principles that have 3 opment will produce the same
been uncovered at each of alteration of the color pat-
these levels of control, and I terns as when development is
suggest how integration slowed by lowered tempera-
among them could enhance tures (Windig 1993, Roskam
our understanding of devel- and Brakefield 1996).
opment and evolution. In a second mechanism by
which developmental pro-
Environmental control cesses can result in reaction
norms, the environmental
Environmental variables have variable leads to a change in
such diverse and profound the level of expression of cer-
effects on phenotypic devel- j tain genes, so that they are
opment that the relationship transcribed more (or less) in
between a genotype and a 4 some environments than in
specific phenotype can be others. The altered quantity of
defined only under a re- i their gene products, which are
stricted set of environmental required for normal develop-
conditions (Bradshaw 1965, ment, then causes a change in
Schlichting 1986, West- phenotype. In a third mecha-
Eberhard 1989, Moran 1992, nism, the environmental vari-
Scheiner 1993). The mecha- able can lead to the expres-
nisms by which environmen- sion of new genes (and the
tal variation causes pheno- repression of others), so that
typic variation are very different patterns of gene ex-
similar to those by which ge- pression and therefore dif-
netic variation affects the g ferent developmental pro-
phenotype. Both environmen- grams run under different
tal and genetic variation can environmental conditions.
alter the dynamics and tim- Figure1. Seasonalpolyphenismin the tropicalbutterflyPrecis The first two of these
ing of developmental pro- almanar. The wet-season form (top) has a rounded wing mechanisms can be subsumed
cesses so that the final out- margin and colorful ventral color pattern. The dry-season under the term "allelic sensi-
come is different from what form (1bottom) has a more angular wing shape and a dull tivity." That is, the environ-
it would have been in the brown color patternthat resemblesa dead leaf. mental effect is direct and
absence of the variation. As a affects some aspect of devel-
result, environmentally induced vari- sponse to environment is called a opment quantitatively. By contrast,
ants often cannot be distinguished reaction norm (Stearns1989). There the developmental switch produced
from genetically induced ones (Roun- are three different mechanisms by by the third mechanism has been
tree and Nijhout 1995a, 1995b), even which developmental processes can called "regulatory plasticity"
when the environmental stimulus is lead to reaction norms. First, an en- (Schlichting and Pigliucci 1995). In
clearly extreme, as in the case of vironmentalvariable (e.g., tempera- this case, the environmental effect is
phenocopy induction (i.e., the in- ture) can have a direct but differen- indirect and alters development
duction, by an environmental shock, tial effect on the rate or timing of qualitatively by bringing new genes
of a phenotype that resembles that of biochemical processes so that they into the picture. Unfortunately, many
a known genetic defect; Capdevila no longer proceed at the same rela- authors use the term "gene expres-
and Garcia-Bellido 1974, Mitchell tive rates. The altered dynamics of sion" to mean phenotype, so that
and Lipps 1978, Mitchell and Peter- the ensemble of developmental pro- any change in phenotype is, by defi-
sen 1982). Normal day-to-day envi- cesses then results directly in an al- nition, a change in gene expression.
ronmental variation also plays im- teredphenotype. Changesof enzyme Indeed, all three mechanisms even-
portant roles in directing phenotypic activity with temperaturecould un- tually result in phenotypic differ-
development, and in this section I derlie this first mechanism. A pos- ences that may be perceived as quali-
examine the diversity of those roles. sible organismal-levelexample of the tative; therefore, observation of
first mechanism is the temperature- phenotype alone cannot reveal what
Reaction norms. When phenotypes dependentreactionnorm of the color mechanism was at work. Moreover,
change gradually with graded changes patternof Bicyclus butterflies.How- each of the alternative developmen-
in an environmentalvariable, the re- ever, color pattern variation in these tal pathways produced by regula-

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 tory plasticity can, in turn, exhibit
allelic sensitivity. The environment
can therefore have a hierarchical ef-
fect on development, with one envi-
ronmental variable producing two
or more phenotypic variants that each
respond differently to a second envi-
ronmental variable.
From the viewpoint of a develop-
mental biologist, the three mecha-
nisms for phenotypic plasticity are
vastly different and must have been
arrived at and refined via very differ-
ent evolutionary trajectories. For
instance, it is possible that one of the
two mechanisms of allelic sensitivity
is always the initial cause of pheno-
typic plasticity. The refinement and
adaptive evolution of the variant
phenotypes could then occur via two
quite different pathways: through
selection for alleles (of genes already
involved in variation of the pheno-
type) that modify the phenotype, or
through the recruitment of new genes
(without previous effect on varia-
tion of the phenotype) that can take
the phenotype in new, and previ-
ously impossible, directions.
From a practical standpoint in
evolutionary biology, knowledge of
the actual developmental mechanism
underlying a particular reaction norm
does not appear to matter much. An
abstract empirical function fitted to
the reaction norm is usually assumed
to be an acceptable descriptor of the
reaction norm in studies of the evo-
lution of phenotypic plasticity
(Gavrilets and Scheiner 1993, deJong
1995, Via et al. 1995), although the
need for models that incorporate
more mechanistic features of develop-
ment and genetics is beginning to be
recognized (Gavrilets and Scheiner
1993, Schlichting and Pigliucci 1995).
Polyphenisms. Some polyphenisms
arise when reaction norms become
discontinuous so that the phenotype
no longer changes gradually with
graded changes in the environment.
A polyphenism is sometimes visual-
ized as a reaction norm with a thresh-
old function superimposed on it, so
that a discrete phenotypic switch
takes place across a relatively small
segment of the total range of envi-
ronmental variation. In polyphenic
development, the environmental vari-
able is often a token stimulus rather
than the environmental variable to
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which the polyphenism is an adapta-
tion (for instance, photoperiod can
serve as a token stimulus to predict
the onset of winter, and a pheno-
typic form that is an adaptation to
low temperatures can develop in re-
sponse to changes in photoperiod).
The sensitive period during which
this stimulus is effective is often far
removed from the time at which the
affected phenotypic characters de-
velop. It is therefore unlikely that, in
polyphenic development, the envi-
ronmental variable has a direct ef-
fect on development via allelic sensi-
tivity. Indeed, as I will show later,
the environmental effect is indirect
and acts by changing the patterns of
hormone secretion.
It is also possible for polyphenic
development to occur in the presence
of a perfectly smooth reaction norm, if
the organism occurs in an environ-
ment that varies abruptly or discretely
so that different generations develop
under different environmental condi-
tions. Seasonal polyphenisms of in-
sects can be of this kind, particularly
in species that have two or three gen-
erations per year, so that each gen-
eration is likely to develop during a
different season. When such organ-
isms are exposed to intermediate en-
vironmental conditions, they develop
intermediate phenotypes. Thus, a
phenotypic plasticity that, in nature,
would typically be expressed as a
polyphenism can be expressed as a
reaction norm under controlled or
artificial conditions (Windig 1993,
Roskam and Brakefield 1996).
Environmental cues. Organisms use
a variety of environmental factors as
cues for polyphenic development. In
insects, photoperiod and tempera-
ture are used most often, but crowd-
ing, pheromones, and changes in food
quality have also been implicated. For
example, temperature is used by Pre-
cis octavia, Bicyclus safitza, and Bicy-
clus anynana, and photoperiod by
Araschnia levana (McLeod 1968,
Koch and Biickmann 1987, Brake-
field and Reitsma 1991, Smith 1991,
Windig 1993, Kooi et al. 1994). In
Precis coenia, by contrast, both tem-
perature and photoperiod induce
polyphenic development and can sub-
stitute for one another in this induc-
tion: At high temperatures, short
photoperiodinducesthe autumnphe- eggs are still within the genital tract
notype and long photoperiodinduces
the summerphenotype, but low tem-
peraturesinduce the autumn pheno-
type even in the presence of a long-
day photoperiod (Smith 1991).
Crowding controls the wing length
polyphenism of the cricket Gryllus
rubens (Zera and Tiebel 1988).
Crowding, photoperiod, and tem-
perature all control the complex
alate-apterousandparthenogenetic-
sexual polyphenisms in aphids
(Hardie and Lees 1985), and food
qualityandpheromonescontrolcaste
polyphenism in the ant Pheidole
bicarinata (Wheeler and Nijhout
1983, 1984).
In many insect species, there is a
more or less well-definedperiod dur-
ing embryonicor larvaldevelopment
when the individual is sensitive to
environmental cues. The environ-
ment-sensitive period precedes the
development of the final adult phe-
notype by a period of time that may
be as brief as a few days or as long as
several months. For example, the
environment-sensitiveperiod for the
seasonal wing pattern polyphenism
of P. coenia, A. levana, Polygonia
c-aureum,B. safitza, and B. anynana
is during the mid- to later larval
instarsbut not the pupal stage (Smith
1991, Kooi and Brakefieldin press).
The pupal color polyphenismsof the
cabbage white, Pieris brassicae, and
the zebraswallowtail,Eurytidesmar-
cellus, are controlled during a brief
light-sensitiveperiod in the prepupal
stage,shortlybeforepupation(Kayser-
Wegman 1975, West and Hazel
1985). By contrast, the pupal color
polyphenisms of the black swallow-
tail, Papilio polyxenes, and the spi-
cebush swallowtail, Papilio troilus,
are determined during the last larval
instar (Hazel and West 1983). The
queen-worker polyphenic switch in
the ant P. bicarinata is controlled by
an inductive period in late embry-
onic or early larval life, whereas the
worker-soldier polyphenic switch is
controlled during the middle period
of the last larval instar (Wheeler and
Nijhout 1981). In aphids, alate-
apterous and sexual-parthenogenetic
polyphenisms are controlled either
during the larval stages or during the
embryonic stage, depending on the
species. Environment-sensitive stages
of aphids occur while the developing
183
 of the mother. The embryos do not
appear to sense the environmental
cues directly but are cued by the
mother, usually by means of hor-
mones she secretes (Hardie and Lees
1985). In G. rubens, the wing length
polyphenism is controlled by crowd-
ing during the last half of larval life,
and the effects of crowding are re-
versible as late as the last larval in-
star (Zera and Tiebel 1988). Two
mechanisms can be responsible for
the lag time between the environ-
mental signal and the development
of the alternative phenotype: The lag
may be due to the fact that the rel-
evant developmental events take a
certain amount of time to be com-
pleted, or it may arise because the
signal causes a reprogramming of
developmental events that will take
place at some time in the future.
Integration of environmental cues.
Inductive environmental cues must be
present for a more or less prolonged
period of time during the sensitive
period. A single day of shortened pho-
toperiod or lowered temperature is
typically not enough to induce a poly-
phenic switch. Some kind of summa-
tion or integration of the environmen-
tal signal evidently occurs during the
sensitive period. The summation seems
to be important because the effects of
a period of inductive environmental
cues can be cancelled if it is followed
by a period of noninductive environ-
mental cues during the sensitive pe-
riod. The precise environmental cir-
cumstances required to induce
polyphenic development have been
best studied in the context of diapause
induction (Denlinger 1985, Tauber et
al. 1986), but the same general phe-
nomenology probably applies to the
control of other polyphenisms in in-
sects. In diapause induction, photo-
period and temperature often act syn-
ergistically, such that for any given
photoperiod, diapause induction is
more effective at lower temperatures
than at higher temperatures. The
conventional explanation of this syn-
ergism is that low temperatures slow
growth, thus increasing the length of
time animals are exposed to induc-
tive photoperiods and causing sum-
mation to be more effective.
Seasonal polyphenisms and diapause.
Some seasonal polyphenisms are
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tightly coupled with diapause: Indi-
viduals that enter diapause develop
one adult phenotype, whereas those
that do not develop a different phe-
notype (Denlinger 1985, Tauber et
al. 1986, Nijhout 1994). The sea-
sonal polyphenism of the wing pat-
tern of butterflies such as A. levana
and Papilio xuthus (Japaneseswal-
lowtail), for instance, is closely asso-
ciated with diapause (Endo et al.
1985, Koch and Biickmann 1987).
In contrast, the alternative seasonal
wing pattern phenotypes of P. coenia,
P. c-aureum, Pieris protodice, and
Bicyclus species develop without dia-
pause (Shapiro 1968, Endo et al.
1985, Smith 1991, Windig 1993).
The wing length polyphenism of the
water strider Aquarius paludum and
the pupal color polyphenism of P.
polyxenes are associated with dia-
pause, but in both species polyphenism
and diapause are induced during dif-
ferent critical periods or require dif-
ferent lengths of exposure to the in-
ducing environmental cue (Hazel and
West 1983, Harada and Numata
1993). These findings indicate that
the two events are controlled inde-
pendently, and therefore may also be
able to evolve independently.
Developmental control
In polyphenic development, environ-
mental factors act by altering some
aspect of development in an orderly
and predictable way. Sometimes this
effect is direct, such as when a change
in temperature alters the rate of a
critical developmental process. Of-
ten, however, the environmental ef-
fect is indirect; it appears to cause a
change (or reprogramming) of some
future developmental sequence of
events. Such alterations are typi-
cally mediated by changes in hor-
mone secretion.
Hormones and developmental
switches. The developmental con-
trol mechanisms that cause poly-
phenic development have been stud-
ied in a number of insects. In all cases
in which the mechanism has been
elucidated, it appears to involve a
developmental switch that is con-
trolled by one or more hormones
(Nijhout 1994). Hormonal control
of polyphenic development is so
widespread, in fact, that all insect
polyphenisms are likely to be con-
trolledby changesin endocrinephysi-
ology. Two hormones, juvenile hor-
mone and ecdysone, are most
commonly involved in polyphenic
development; there is evidence that
neurosecretoryhormones also play a
critical role in aphids, locusts, and
some butterflies (Nijhout 1994).
Many events in postembryonic
development are initiated or inhib-
ited by hormones,andtherearemany
ways in which variation in an endo-
crine mechanism can be associated
with variation in development. For
instance, changes in the concentra-
tion of hormones or in the timing of
their secretion can affect develop-
ment. Changesin concentrationthat
cause hormone levels to rise above
or fall below a particular threshold
can result in the activation or inacti-
vation of some developmental pro-
cesses. Similarly,changes in the tim-
ing of hormone secretioncan cause a
hormone to coincide with, or miss, a
critical period of sensitivity for the
stimulation or inhibition of some
developmental event. Conversely, it
is possible for the hormonal signal to
be constant but for the response to
the hormone to vary, for example,
by raising or lowering the threshold
of sensitivity to the hormone or by
shifting a critical period of hormone
sensitivity to a later or earlier time in
development. The response to a hor-
mone can also be changed by alter-
ing the intracellular molecular re-
sponse that follows after a hormone
binds to its receptor. Polyphenisms
can evolve if one or more of these
components of an endocrine switch-
ing mechanism becomes sensitive to
environmental variables.
Regulation of polyphenic devel-
opment by means of changes in the
concentration of hormones appears
to be quite common. Regulation by
means of fluctuating hormone con-
centration is best known from stud-
ies on the control of metabolism and
homeostasis, although hormonal
fluctuations also accompany many
developmental events, such as molt-
ing and metamorphosis. There is,
however, an important difference
between the role of hormones in
physiological regulation and their
role in developmental regulation,
namely, that in physiological regula-
tion the response to a hormone is
BioScience Vol. 49 No. 3
 often proportional to its concentra-
tion, whereas in development the
response is typically all-or-none. One
functional explanation for this dif-
ference is that development is pro-
gressive; specific developmental
stages at which decisions must be
made typically occur only once, and
only for a brief period of time.
In development, hormones act as
switches that alter the pattern of
gene expression and either initiate
certain developmental events or di-
rect development into specific alter-
native pathways. As hormone levels
rise and fall, the developmental re-
sponse changes qualitatively, rather
than quantitatively. It is possible for
organisms to show a graded devel-
opmental and phenotypic response
to graded changes in hormone con-
centration, but the mechanism of
graded change appears to be quite
different from that involved in ho-
meostatic regulation. A graded de-
velopmental response can come
about when different tissues of an
organism or different features of a
tissue either have different response
thresholds to a hormone or require
different lengths of exposure to a
hormone to mount a normal re-
sponse. Such intermediates consist
of a mosaic of two types of tissues
(Truman et al. 1974, Willis et al.
1982). Similarly, graded changes in
the timing of hormone secretion can
cause a graded phenotypic response
when a hormone arrests an ongoing
developmental process at different
times.
There are many instances in which
artificial elevation of a hormone ti-
ter appears to be sufficient to cause a
polyphenic switch. For instance, im-
plantation of active corpora allata
(the glands that secrete juvenile hor-
mone) into larvae of the migratory
locust, Locusta migratoria, that were
crowded and would normally have
developed into the melanic gregari-
ous morph caused them to develop
the green pigmentation characteris-
tic of the solitary morph (Joly and
Joly 1954, Staal 1961). An injection
of 20-hydroxyecdysone early in the
pupal stage can cause P. coenia that
would otherwise have developed into
an adult of the autumn morph to
develop the summer phenotype in-
stead (Rountree and Nijhout 1995a).
Application of juvenile hormone to
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JH-sensitive
,nerinu
Criticalsize forworkerdetermination
i
([JH]< Threshold)
Threshold - - -
(raisedby soldier-
inhibitingpheromone)
Threshold - - -
x
JHtiterin larvaeis raised
by highproteinin diet
worker soldier
-
Size
Figure2. Model for the control of worker-soldierpolyphenismin the ant Pheidole
bicarinata.The solid linesrepresentidealizedjuvenilehormone(JH)titersduringlarval
development,leadingto eitherthe soldierphenotype(if abovea certainthreshold)or the
workerphenotype(if belowthe threshold).Nutritionduringlarvallife controlsthe level
of juvenilehormoneduringa sensitiveperiodin the last larvalinstar.A low-proteindiet
leads to low levels of juvenilehormone and results in the developmentof the small
worker phenotype, whereas a high-proteindiet leads to elevated levels of juvenile
hormone and results in the developmentof the big-headedsoldier phenotype. High
levels of juvenile hormone during the sensitive period lead to a reprogrammingof
subsequentendocrineevents and of the growth patternsof the head imaginal disks.
Larvaeswitched to soldier developmentcontinue to secrete juvenile hormone for a
longer period of time than larvae destined to become workers. As long as juvenile
hormone secretioncontinues, larval growth continues and pupation is inhibited. In
larvaeswitchedto the soldiertrajectory,the criticalbodysizeat whichjuvenilehormone
secretionstops is higherthan in presumptiveworkerlarvae.Thus, soldierlarvaegrow
to a larger size than worker larvae, and because the growth pattern of their head
imaginaldisksis reprogrammed,theyalso developdifferentbodyproportionsas adults.
Interestingly,in the presenceof a continuedhigh-proteindiet,not all larvaedevelopinto
soldiers.Instead,theproportionof soldiersin a colonyis regulatedbymeansof a soldier-
inhibitingpheromoneproducedby soldiersalreadypresentin the colony. High levels
of the inhibitorypheromoneraisethe thresholdof sensitivityto juvenilehormoneduring
the juvenilehormone-sensitiveperiod, so that even in the presenceof high juvenile
hormonelevels, the larvaremainson the workerontogenetictrajectory.AfterWheeler
and Nijhout (1983, 1984).
larvae of the pea aphid, Aphis fabae, As already noted, changing the
and several other aphid species in- thresholds of sensitivity to a hor-
hibits development of the alate phe- mone in the presence of a constant
notype (Hardie 1981). Exogenous concentration of hormone is equiva-
juvenile hormone also induces queen lent to changing hormone concen-
development in the honey bee Apis tration in the presence of a constant
mellifera (Wirtz 1973) and soldier threshold of sensitivity. Some poly-
development in various ants and ter- phenic systems, such as the soldier-
mites (Luscher 1972, 1974, Wheeler worker polyphenism of Pheidole, are
and Nijhout 1984). In crickets, there controlled in part by changes in the
is a tight correlation between the threshold of sensitivity to juvenile
levels of juvenile hormone esterase hormone (Figure 2; Wheeler and
(an enzyme that breaks down juve- Nijhout 1984, Nijhout 1994). Al-
nile hormone and can lower its level though the details of how a thresh-
in the blood) and wing length poly- old of sensitivity to a hormone is
phenism (Zera and Tiebel 1989, Fair- achieved physiologically are not
bairn and Yadlowski 1997, Zera and known, it is likely that in at least
Denno 1997). some systems sensitivity is propor-
185
 struct muscles when to contract. The
target tissues, like muscles, are pre-
sumed to always be responsive and
therefore to be passive participants
in the process of regulation, simply
waiting to be stimulated by a hor-
mone. It has become clear in recent
b' Ecdysteroids years, however, that target tissues
are far from passive participants in
the hormonal regulation of develop-
ment. In many instances, tissues have
EcR-B epidermis been found to be responsive to hor-
mones only at or very near the time
at which the hormone is normally
secreted (Nijhout 1994). It is as if the
tissues somehow "know" when the
C hormonal signal will come and be-
come receptive to it only at that time.
EcR-A epidermis This phenomenon is believed to be
regulated at the level of the hormone
receptor (Riddiford and Truman
1994), a notion that is supported by
recent findings of enormous tempo-
d ral and spatial variation in hormone
receptor expression during develop-
ment (Figure 3).
-=~~ERwn dss_
The dynamics of variation in hor-
mone receptor expression are best
understood for the ecdysteroid re-
ceptor system. The juvenile hormone
4th instar 5th instar prepupa pupa receptor, unfortunately, remains elu-
sive (Charles et al. 1996, Riddiford
Figure3. Ecdysteroidtiters and simultaneousecdysteroidreceptorexpressionduring 1996), and its molecular character-
thelatelarvalandpupalstagesof thetobaccohornwormManducasexta. (a)Ecdysteroid istics and patterns of variation are
titers. The solid curve represents20-hydroxyecdysone;the dashedcurvein the pupal unknown. The ecdysteroid receptor
stagerepresentsecdysone.(b-d) mRNAaccumulationfor differentecdysteroidreceptor (EcR) is a heterodimer (i.e., a func-
isoforms in the epidermisand wing imaginaldisks. After Fujiwaraet al. (1995) and tional receptor made up of two pro-
Jindraet al. (1996). teins coded for by different genes).
One member of the dimeric pair (the
tional to the amount of hormone decision points-that is, times dur- ultraspiracle, or usp, protein) tends to
receptor in the target tissues. Bind- ing which a developmental trajec- be the same in all ecdysteroid receptor
ing affinity of the hormone-receptor tory can be altered-are reachedonly complexes, whereas the other can be
complex and variation in the intrac- once, and the progression of devel- any of several possible proteins. Dif-
ellularresponsemechanismundoubt- opment beyond that point makes the ferent receptors can be assembled with
edly also play roles in determining decision irrevocable. The timing of different variable parts, and each of
the apparentthresholdof sensitivity. hormone-sensitiveperiodsis thus de- these alternative heterodimers ap-
terminedby the attainmentof certain pears to regulate a different type of
Hormone-sensitive periods. When stages in the developmentalprocess. cellular response (Cherbas and
hormones act as developmental The actualmechanismresponsiblefor Cherbas 1996, Truman 1996).
switches, the timing of their secre- the appearanceof hormone-sensitive What is perhaps the most remark-
tion is as important as their con- periods appears to be related to the able finding is that the expression of
centration. There are critical hor- behavior of hormone receptors in each receptor varies in a complex
mone-sensitiveperiods, just as there the cells that are the targets of the tissue-specific temporal pattern
arecriticalenvironment-sensitivepe- hormone. Recent work has revealed throughout postembryonic develop-
riods. Elevationor depressionof hor- this behavior to be much more com- ment. Some of these patterns of varia-
mone concentration outside of the plex than was once thought. tion are illustrated in Figure 3, to-
critical period for a given tissue or Experience with hormones as gether with the contemporaneous
response is irrelevant and without physiological regulators has led bi- pattern of ecdysteroid concentration.
effect. The general explanation for ologists to think of them as control- Assuming that a low level of recep-
the existence of hormone-sensitive ling agents that instruct their target tor expression signifies an insensi-
periodsis simplythat developmentis tissues when to respond, much in the tivity to (and perhaps an inability to
progressive and irreversible,so that way that nerve action potentials in- respond to) the hormone, then it is

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 clear that there are times during de-
velopment when fluctuations in
ecdysteroidconcentrationwould af-
fect some tissues and not others. For
instance, just before the molt from
the fourth to the fifth larval instars
(Figure3), there is a double peak of
ecdysteroid concentration that is
matched approximatelyby a peak of
EcR-B1mRNA accumulation in the
epidermis,except for a sharp decline
in the middle of the peak, which is
mirroredby a brief peak in a differ-
ent ecdysteroid receptor, EcR-A. At
the same time, there is little or no
expression of ecdysteroid receptors
in wing imaginal disks. The func-
tional significanceof the sharppeak-
like fluctuations of the epidermal
receptors is not yet clear, but the
differencebetweenthe epidermaland
imaginal disks makes sense: the epi-
dermis undergoes a molting cycle at
this time, whereas there is no percep-
tible change in the imaginal disks.
Although much remains to be
learned about the biology of hor-
mone reception and response sys-
tems, the earlyevidencesuggeststhat
the seemingly erratic patterns of
ecdysteroid secretion and receptor
synthesis representa regulatorydia-
logue between the endocrine system
and the body. Different peaks of
hormone concentration may be ad-
dressing different tissues, because a
given tissue may turn its response to
a hormone on or off by modulating
its receptors. Moreover, a tissue can
switch to the use of a differentrecep-
tor and, in so doing, change the way
it respondsto the hormone. The pat-
terns of receptor modulation illus-
trated in Figure 3 show that the
switch to a different receptor can be
rapid as well as transient, and is
tissue-specific.
A transient peak of receptor
availability would be interpreted
physiologically as a brief hormone-
sensitiveperiodfor whateverdevelop-
mental event was regulated by that
receptor.Ininsectdevelopment,there-
fore, hormone titers and receptor
levels appear to be regulated inde-
pendently. There is an interesting
interaction, however, between
ecdysteroid secretion and receptor
expression:Ecdysteroidreceptorsare
often up-regulatedwhen ecdysteroid
levels in the blood rise (Cherbas and
Cherbas 1996), so at least some of
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a Ecdysteroid-sensitiveperiod
Larva-shortday I Springform
Diapause' - - - |-
Larva Adult
Pupa Eclosion
Ecdysteroidsecretion
Larva-longday 1 ^
II Bk |Summer form
Larva Pupa Eclosio Adult
Eclosion
ysteroid-sensitive
period
sss.sggssmss Ecdvsteroidsecretion
Autumnform
Eclosion Adult
Larva-longday _ Summerform
Larva Pupa
IIIllI lllllllllll
Adult
Pupation Eclosion
Figure 4. Seasonal polyphenic switching mechanism in two butterflies. (a) Araschnia
levana has a spring form that emerges from pupae that have undergone a winter
diapause and a summer form that emerges from pupae that do not diapause. An
ecdysteroid-sensitive period for form determination occurs 3-9 days after pupation.
Diapausing pupae (which are induced by short days) do not secrete ecdysteroids
until several months after pupation, whereas direct-developing pupae (induced by
long days) secrete ecdysteroids within a few days after pupation to begin adult
development. A diapausing pupa that is injected with 20-hydroxyecdysone during
the sensitive period will begin adult development immediately and express the
summer phenotype. (b) Precis coenia has a pale summer form and a dark autumn
form. There is an ecdysteroid-sensitive period between 28 and 48 hours after
pupation. In the summer (when days are long or temperatures high), ecdysteroid
secretion begins during the sensitive period in the pupal stage and results in the pale
summer phenotype, whereas in the autumn (when days are short or temperatures
low) ecdysteroid secretion is delayed 24 hours so that it occurs after the sensitive
period, leading to development of the dark autumn form. After Koch and Biickmann
(1987) and Rountree and Nijhout (1995a).
the receptor fluctuations in Figure 3 developmental regulation.
occur in response to fluctuations of If receptor regulation is involved
the hormone. Up-regulation of re- in hormonalcontrol of development,
ceptors, which is observed in many thenwhat exactlyarethe relativeroles
endocrine response mechanisms of hormone regulation and receptor
(Tata 1996), is apparently part of a regulation during development?It is
positive feedback mechanism that possible that hormones act mainly as
enhances the response to a hormone. general synchronizing signals. Be-
But it is also clear from Figure 3 that causehormonesecretionis controlled
many fluctuations in receptor levels by the central nervous system (via
are not associated with fluctuations neurosecretoryfactors), it can inte-
in ecdysteroid levels, and it is in such grate signals from the external and
cases that receptors are in control of internalenvironmentto regulateand
187
 Environmentalsignal independently. Some specific ex-
amples of how hormone-sensitive
Summation periods and hormone levels interact
to control polyphenic development
are illustrated in Figures 2 and 4.

Five mechanisms of polyphenic de-

velopment. Developmental and
physiological studies have revealed
severalindependentmechanismsthat
regulate polyphenic development in
insects. For all insect polyphenisms,
there are environment-sensitivepe-
riods during which some kind of
external stimulus alters the develop-
mental fate of the animal. Each envi-
ronmental signal appearsto have its
effect on development by reprogram-
ming the hormone response mecha-
nism. This reprogramming can be
due to changes in one or more of five
very different mechanisms: the titer
of a hormone during a hormone-
sensitiveperiod, the thresholdof sen-
Timingof sitivity to a hormone, the timing of
hormonesecretion hormone secretion, the timing of a
hormone-sensitive period, or the cel-
lular response to the hormone (Fig-
ure 5).
~' ~.'
X Timingof Each of the five mechanisms that
hormone-sensitive control polyphenic switching can it-
period self be controlled through several
distinctsubmechanismsor pathways.
For instance, the concentration of
Figure 5. Control mechanisms of polyphenic switching. Forked horizontal bar at top circulatinghormone can be changed
represents an individual developmental trajectory with a choice of two alternative by altering its rate of synthesis, its
terminal ontogenetic pathways leading to final phenotype H or T. At some time during rate of secretion, or its rate of degra-
development there is an environment-sensitive period. Environmental signals experi- dation by catabolic enzymes. The
enced during that time are summed and cause reprogramming of a developmental
titer of juvenile hormone, for in-
pathway (starting at A) later in development. Environmental signals can be nutrition,
pheromones, photoperiod, temperature, or crowding. The developmental switch can be stance, is regulated independently by
mediated by one or more of the diagrammed endocrine mechanisms. For instance, if a both synthesis and degradation mecha-
peak in hormone secretion coincides with a hormone-sensitive period, a developmental nisms (Hammock 1985). The various
pathway will be executed that is different from the one that is executed when the mechanisms and pathways for devel-
hormone peak does not coincide with the hormone-sensitive period (indicated by the opmental reprogramming each use
feedback loop to point C in the upper diagram). In addition to changes in the timing of differentgene productsand requirea
the hormone peak, its concentration can vary, as can the threshold of sensitivity to the different regulatory system. Each
hormone during the sensitive period. The duration of the environment-sensitive period, mechanism is presumably under in-
its proximity to the developmental switch, the type of endocrine mechanism used to
dependent physiological and genetic
control the switch, and the sequence of events that constitute the divergent developmen-
tal pathways are controlled independently. Insofar as each of these steps is controlled
control and can therefore vary and
independently, it is also able to evolve independently of the others. Selection to alter the
evolve independently of the others.
frequency of alternative phenotypes, for instance, will alter either the environment- It is important to recognize that
sensing and integration mechanism or some aspect of the endocrine-switching mecha- these five mechanisms are present as
part of the normal "monophenic"
nism, whereas selection to alter one or more of the alternative phenotypes will most
developmental system of insects.
likely occur by changes in the ontogenetic pathway that leads from A to either H or T.
They do not need to evolve or be
coordinate the overall timing and to environmental variables and the maintained separately just to serve
pace of development. Target cells, characteristicsof that response are, polyphenic development. All that is
by contrast, can regulatetheir recep- therefore, controlled by different required for the evolution of a
tor levels either entirely autono- mechanisms.These two components polyphenism is that one or more of
mously or in response to growth fac- of the control of phenotypic plastic- these mechanisms becomes physi-
tors and inhibitors produced by ity and polyphenic development ologically linked to a process that is
nearby cells. The ability to respond should therefore be able to evolve sensitive to an environmental vari-

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 able such as temperature,photope- tal mechanisms directly (e.g., Zera
adoption of a new host plant (Carroll
riod, nutrition, crowding, or phero- and Zhang 1995), there is evidence
and Boyd 1992, Dingle and Winchell
mones. The developmentalsystem of from breeding studies that many as-
1997, Carroll et al. in press). The
insects is therefore preadapted in pects of a polyphenic response
genetic control of wing morphology
many ways for the rapidevolution of mechanism are variable in ways that
is mediated through juvenile hor-
phenotypic plasticity. A switchlike can lead to adaptive evolution of the
mone, and the evolution of the pro-
polyphenic control of development polyphenism. Indeed, genetic varia-
portions of wing morphs in a popu-
is relativelyeasy to establish because tion in the mechanisms that monitor
lation is believed to be due to genetic
the temporal relationship between a and integrate environment signals is
alteration in the juvenile hormone-
hormonepeak and a hormone-sensi- well documented by breeding experi-
mediated switching system (Dingle
tive period is easily manipulated, ei- ments (Danilevskii 1965). Genetic
and Winchell 1997).
ther by an environmental signal or variation in the environment-sensi-
Genetic variation of the develop-
by mutation of one of the many com- tive mechanism is often expressed as
mental response downstream of the
ponentsof the pathway.Evena quan- endocrine signal is also possible; in-
variation in the propensity to switch
titatively small relative shift of hor- between alternative developmental
deed, such variation is almost cer-
mone peak and hormone-sensitive tainly widespread. Unfortunately, the
pathways under a constant environ-
period can bring them completely mental signal. In addition, geo-
analysis of relevant developmental
out of register, thus causing a quali- graphic races of species typically dif-
pathways and control mechanisms is
tative switch in development (e.g., fer in the critical photoperiod at
fraught with technical and concep-
Figure 5). tual difficulties, so that most of the
which a seasonally polyphenic switch
will take place (Danilevskii 1965,
information about variation and evo-
Geneticcontrol Tauber et al. 1986). lution at the level of mechanism is
inferential and indirect. For instance,
The prevalence of phenotypic plas- Developmental response mechanism. when one alternative phenotype
ticity and reaction norms suggests Genetic variation in the endocrine shows complex adaptations, such as
that evolutionary change of the phe- control mechanism is also known to the accurate dead-leaf mimicry of
notype can be initiated either by a occur, although few if any studies the dry-season forms of Precis almana
change in environment or by a ge- have conclusively demonstrated the (Figure 1) and other butterflies (Nij-
neticmutation(West-Eberhard1986, underlying causes of this variation. hout 1991), it is reasonable to as-
1989, Schlichting and Pigliucci In P. bicarinata and other ants, dif- sume that such adaptations were re-
1998). Once initiated, the new phe- ferent colonies of the species regu- fined over time by natural selection
notype can be further altered and late the percentage of soldiers at dif- acting on a portion of the develop-
adaptively refined and stabilized by ferent but stable levels (Holldobler mental pathway unique to that form,
furtherchanges in the processes that and Wilson 1990), and this variation and therefore downstream of the en-
give rise to the phenotype. Among is presumably achieved through docrine switching signal.
the targets of this change are the variation in the mechanism outlined Indirect evidence about genetic
genes whose products participate in in Figure 2, for instance by variation variation at the level of mechanism
the various endocrine processes de- in the threshold of sensitivity to ju- also comes from quantitative genetic
scribed above. venile hormone or variation in the studies of plasticity. In both the plant
sensitivity of juvenile hormone con- Phlox and the fruit fly Drosophila,
Environmentalsensitivity.Evolution centration to food quality. Variation for instance, there is independent
of polyphenic development can oc- in the rate of juvenile hormone me- genetic control of the mean value of
cur through changes in the environ- tabolism is responsible for varia- a plastic character in a given envi-
ment-monitoring mechanism or tion in the expression of wing length ronment and of the plasticity of that
through changes at any level in the polyphenism in G. rubens, Gryllus character, which is defined as the
developmentalswitchingmechanism. firmus, and Gryllus assimilis (Zera difference in the mean values of the
Such evolutionary change can take and Tiebel 1989, Zera et al. 1989, character of siblings raised in differ-
many forms, from a simple alter- Zera and Zhang 1995). The rapid ent environments (Schlichting and
ation in the threshold for the re- evolution in the control of wing Levin 1986, Scheiner and Lyman
sponse to a changing environmental length polymorphism in the soap- 1991). If these findings can be ex-
signal (such as a shift in the critical berrybug,Jaderahaemalotoma,may tended to polyphenic traits, and if
photoperiod with latitude), to the also be due to genetic variation in the polyphenisms evolve from continu-
evolution of new physiological or endocrine control system. This spe- ously plastic traits by the addition of
morphologicaladaptationsof one or cies has long- and short-winged mor- a hormone-mediated switching
both alternativemorphs (such as the phs, and the long-winged morph has mechanism, then it is likely that the
evolution of dead-leaf mimicry in three distinct patterns of flight muscle mean value of a character and the
the wing pattern of the dry season breakdown during the adult stage. degree of differentiation of a charac-
form of a butterfly). Evolution de- Wing morphology and flight muscle ter in alternative phenotypes are also
pends in part on the availability of breakdown exhibit genetic variation, controlled independently. Thus, once
appropriate genetic variation, and and the frequencies of the alterna- a polyphenism is established, each of
although few studies have addressed tive morphs in a population have the alternative morphs can undergo
the genetic variation in developmen- been shown to evolve rapidly after further adaptive evolution by changes

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 in the developmental response system
downstream of the endocrine signal.
Fixation of a phenotype. Once a
polyphenism has been established, it
is also possible for one or the other
form to become fixed in a popula-
tion. Such fixation can happen if the
population enters a habitat that is
not sufficiently variable to induce
the polyphenic switch, or it can hap-
pen by genetic fixation of one of the
alternative forms (West-Eberhard
1986). In P. coenia, for instance, the
autumn morph is induced by low
temperature and short days, but there
is also a gene (rosa) whose recessive
allele produces the autumn pheno-
type when homozygous (Smith 1991,
Rountree and Nijhout 1995b). This
allele is present at a low frequency in
US populations of P. coenia, so in
the majority of individuals control
of the seasonal morph is purely envi-
ronmental. But populations that are
homozygous for the recessive rosa
allele can easily be established, and
these would express the autumn
phenotype constitutively (and would
no longer be sensitive to environ-
mental variation). The genetically
induced rosa phenotype is not pro-
duced by changes in the endocrine
system but involves changes in the
developmental pathways down-
stream of the endocrine signal
(Rountree and Nijhout 1995b).
It is not clear how common it is to
have alternative (i.e., environmental
versus genetic) control mechanisms
within a species, but in many in-
stances these alternative control strat-
egies exist side by side within larger
taxa. In these cases, a similar alter-
native phenotype is expressed as an
environmentally controlled poly-
phenism in some species and as a
genetically controlled polymorphism
in other species. The best studied
examples of such alternative control
strategies are the dispersal polymor-
phisms that are common in the Or-
thoptera, Hemiptera, and Homop-
tera and that occur sporadically in
many other insect orders (Roff 1986,
Roff and Fairbairn 1991, Zera and
Denno 1997). Dispersal polymorph-
isms constitute a coordinated set of
morphological, physiological, and
behavioral traits that are always ex-
pressed together (and are also often
referred to simply as wing length
190
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polymorphism or as the "migratory
syndrome"). One of the alternative
forms is long winged and tends to be
migratory and to have low fecun-
dity, whereas the other form is short
winged or wingless, sedentary, and
highly fecund.
Wing morph determination can
be purely genetic, purely environ-
mental, or some combination of the
two (Roff and Fairbairn 1991, Zera
and Denno 1997). In cases in which
there is both an environmental and
genetic component, it has been as-
sumed that the genes control the
developmental system's sensitivity to
the environmental signal (Zera and
Denno 1997). For instance, genes
could control the titer of juvenile
hormone during a critical period of
wing size determination so that dif-
ferent genotypes have different lev-
els of juvenile hormone during the
critical period. It should be noted,
however, that the control of wing
length development has proven ex-
tremely difficult to elucidate (Zera
and Denno 1997), even in such well-
studied systems as migratory locusts,
for which there is reason to suspect
that factors other than juvenile hor-
mone play an important role (Pener
and Yerushalmi 1998).
In species that have a strictly envi-
ronmentally controlled wing length
polyphenism, the environmental sig-
nal appears to be mediated by the
endocrine system, as with other poly-
phenisms. Indeed, it is well known
that exogenous juvenile hormone can
induce the wingless or short-winged
morph in wing-polyphenic grasshop-
pers, crickets, aphids, and several
species of Hemiptera (McCaffery and
Page 1978, Hardie and Lees 1985,
Dingle and Winchell 1997, Zera and
Denno 1997). Although this effect of
exogenous juvenile hormone does not
prove that juvenile hormone is also
the mediator in strictly genetically
controlled wing length polymor-
phisms, it does suggest that such a
possibility should be investigated.
Future directions
The important issue that needs to be
addressed with respect to the fixa-
tion of a polyphenism is whether
genetically controlled polymorph-
isms evolved from environmentally
controlled polyphenisms, whether
environmentally controlled poly-
phenisms evolved from genetically
controlled polymorphisms, or
whether both kinds of evolution oc-
curred. There are many ways in which
a polyphenism-to-polymorphism
transition could be made. One way is
by selection on genetic variation in
hormone titers or thresholds. An-
other is by the evolution of allelic
variants that differentially affect the
postendocrine response mechanism,
as in the case of P. coenia mentioned
above, in which genetic variation
can, in a single step, produce a poly-
morphism that is completely inde-
pendent of the pattern of endocrine
dynamics.
A polymorphism-to-polyphenism
transition could be achieved through
several different pathways, depend-
ing on the original mechanism un-
derlying the polymorphism. If the
genetic effect was originally medi-
ated by the endocrine system, there
are many ways in which hormone
secretion, metabolism, thresholds, or
sensitive periods could be made sen-
sitive to environmental variation. But
if the genes that control the poly-
morphism were to affect the process
of wing development more directly-
for instance, by altering the local
expression or response of growth
factors or homeotic genes-then the
evolution of a novel environmen-
tally sensitive endocrine switching
mechanism would be more difficult
and less probable.
At present, insufficient compara-
tive genetic, endocrine, or develop-
mental information is available to criti-
cally address the issue of directionality
of the polyphenism-to-polymorphism
transition. Fortunately, however, the
necessary information can be readily
obtained with present technology. Elu-
cidating the mechanism responsible
for one or more of these transitions
would be a significant contribution
to understanding the interplay of de-
velopment and evolution in the grow-
ing hybrid field of evolutionary devel-
opmental biology.
Acknowledgments
I would like to thank Paul Brakefield,
Chris Klingenberg, Armin Moczec,
Carl Schlichting, and Anthony Zera
for critical comments on the manu-
script. This work was supported in
BioScience Vol. 49 No. 3
 part by grant IBN-97-28727 from
the National Science Foundation.
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