The Evolutionary Maintenance of Alternative Phenotypes

The University of Chicago
The Evolutionary Maintenance of Alternative Phenotypes

Author(s): Nancy A. Moran
Reviewed work(s):
Source: The American Naturalist, Vol. 139, No. 5 (May, 1992), pp. 971-989
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Vol. 139. No. 5 The AmericanNaturalist May 1992
THE EVOLUTIONARY MAINTENANCE OF

ALTERNATIVE PHENOTYPES
NANCY A. MORAN
Departmentof Ecology and EvolutionaryBiology, Universityof Arizona, Tucson, Arizona 85721
Stubmitted
January25, 1991; Revised Junle17, 1991; Accepted Augtust19, 1991
Abstract.-To understandthe evolutionof polyphenism,or adaptive switchingbetweenalterna-

tive developmentalpathways and correspondingphenotypes,environmentalfactorsgoverning
the developmentalswitch, or cues, must be distinguishedfromfactorsaffectingrelative fit-
nesses, or selective agents. Under most conditionsof purelyspatial variationin environment,
the maintenanceof polyphenismrequires adaptive developmentalsensitivityto cues, which
results in phenotype-environment matching.Other determinantsof the maintenanceof poly-
phenism under spatial variationinclude relativefitnessesof differentphenotype-environment
combinations,frequencies of alternativeenvironments,and possible costs of polyphenism.
Where variationis temporal,polyphenismis affectedby the same parametersbut is maintained
morereadilyand may be favoredwithoutadaptive developmentalsensitivity.Even whereenvi-
ronmentalconditionsare sufficient formaintainingpolyphenism,its evolutionmaybe precluded
by constraintson developmental sensitivitythat prevent phenotype-environment matching,
costs of developmentalswitching,or antagonisticpleiotropythatpreventsindependentevolution
of alternativephenotypes.These factorscould be highlytaxon-specific,whichwould preclude
generalizationsconcerningthedistribution ofpolyphenism.However, theabundanceof seasonal
polyphenismsin multivoltineorganismssuggeststhatwhereenvironments are favorable,devel-
opmentalsystemsare oftenflexibleenoughfortheestablishment of simplepolyphenisms.Elabo-
ratepolyphenismsmaybe restrictedto circumstancesin whichthedevelopmentalswitchoccurs
duringveryearly development.
In recentyears,phenotypic has beenresurrected

plasticity as a subjectdeserv-
ing the seriousattentionof evolutionary biologists.As pointedout by West-
Eberhard(1986,1989)and Stearns(1989a),thisrenewedinterest followsseveral
decades duringwhichthe importance was downplayedas largely
of plasticity
inconsequentialforthelong-term geneticchangesthatcompriseevolution. None-
theless,duringthissame period,manybiologistshave pursuedtheoretical and
empiricalstudiesconcerning instancesofplasticity,
particular especiallyadaptive
These studieshavebeenmotivated
plasticity. byobservation:nongenetic pheno-
typicvariationis commonandoftenimportant enoughinthebiologyofparticular
plantand animaltaxa thatitwas boundto be addressedbybiologists working on
thosegroups.Examplesincludethealternative reproductivestrategiesof males
(Hamilton 1979; Austad 1984; Dominey 1984), diapausingversus direct-
developinglifehistoriesin arthropods (Taylor1986),alternative wingpatterns
in butterflies
(Shapiro 1976; Brakefieldand Larsen 1984; Kingsolver1987;
Kingsolver and Wiernasz1991),fullywingedandflightless formsinmanyinsects
Am. Nat. 1992. Vol. 139, pp. 971-989.

? 1992 by The Universityof Chicago. 0003-0147/92/3905-0005$02.00.
All rightsreserved.
972 THE AMERICANNATURALIST
(Harrison1980;Roff1986),alternative morphologies associatedwithdifferent

defensivetacticsof invertebrates (Harvell 1986; Lively 1986a; Havel 1987;
Greene1989),differences in trophicstructures(Bernays1986;Meyer1990),and
paedomorphic versusmetamorphic insomesalamanders
lifehistories (Dent1968;
Semlitsch et al. 1990).In each ofthesecases,theoretical and/orempirical studies
have addressedthebasis of theevolutionary maintenance of alternativepheno-
types.In mostinstances,alternative phenotypes resultfromplasticityrather than
geneticvariability. In addition, mostofthesecases involveplasticity thatis appar-
entlyadaptive,witheach of twoor morediscretephenotypes showingfeatures
suitedto a different setofenvironmental conditions.
Phenotypic differences may
involvediverseattributes, including behavioral, andmorphological
physiological,
ones. For example,thegenetically identicalfemalemorphsof certainaphidlife
cyclesshow discretedifferences in hostplantpreferences, in morphology, and
in the size, number,and timing of production of offspring(Dixon 1972;Hardie
1981;Hardieand Lees 1985).
In thisarticle,I developa generalized framework forunderstanding theevolu-
tionary maintenance ofa developmental switchandassociatedphenotypic plastic-
ityor polyphenism. I willrestrict myselfto irreversibledevelopmental choices
thatresultin discretedifferences amongphenotypes ofentireindividuals. Many
cases ofplasticity, including mostcitedabove,fallwithin theseconfines. Conclu-
sions may have some relevanceforcases of reversibleplasticity (as in many
examplesinvolvingbehavior[Stephens1987]or seasonal cyclesin long-lived
individuals [Lyman1963]),ofplasticity thatcharacterizesonlypartofan individ-
ual (manyexamplesinplants[A. D. Bradshaw1965;Lloyd1984]),orofplasticity
causingcontinuous phenotypic butthesewillnotbe considered
variability, explic-
itlyhere.Thus,mycentralaimis thedelineation oftheconditions underwhich
discretephenotypic alternatives willbe favoredby naturalselection.This aim
can onlybe realizedbyfirst recognizing severalpointsconcerning therelationship
betweenenvironmental variation, phenotypes, and fitness.
DUAL INFLUENCES OF ENVIRONMENT: DEVELOPMENT AND FITNESS
Environmental factorsaffect organisms intwowaysincases ofadaptivepheno-

typicplasticity.Thisdualinfluence ofenvironment is recognizedby someearlier
authors(e.g., Levins 1963,1968;W. E. Bradshaw1973;Shapiro1976;Tauberet
al. 1986; Danks 1987) but is not incorporated intomuchrecentworkon the
evolutionofplasticity (e.g., Via 1988;Stearns1989a).First,someenvironmental
factor,or cue, influences development; theconsequenceofthisinfluence is plas-
withdifferent
ticity, phenotypes expressedunderdifferent setsofdevelopmental
environments. Second,someenvironmental factorhas a differentialeffecton the
fitnesses
oftheresulting phenotypic suchthatthestateoftheselec-
alternatives,
tiveenvironment determines whichphenotype willhavehighestfitness.
The factorsimportant as cues maybe thesameas or different fromthefactors
important as selectiveagents(Levins1968).However,theydiffer at leastinwhen
theyexerttheireffects:theactionof thedevelopmental environment precedes
ALTERNATIVE PHENOTYPES 973
thatof the selective environment.The lag between the action of the two factors
may be briefbut is never entirelyabsent; it exists because phenotypesare not
produced instantaneously.For example, in manymultivoltine arthropods,photo-
period determinesthe developmentalswitchbetween direct-developing and dia-
pausing individuals,whereas temperatureor wateravailabilityusually definethe
selective environment(Beck 1980; Tauber et al. 1986; Taylor 1986; Danks 1987).
The effectof the cue (i.e., photoperiod)necessarilyprecedes thatof the selective
agent (i.e., the temperaturechange or desiccationthataccompanies the onset of
a cold or dry season).
ADAPTIVE MATCHING OF PHENOTYPE AND ENVIRONMENT
As is evidentin the models developed below, a primarydeterminantof condi-

tions that maintainadaptive plasticityis the accuracy withwhich factorsacting
as cues predict the states of factorsacting as selective agents. There are two
requirementsin orderfora plastic strategyto achieve a level of matchingbeyond
thatattainablethroughrandomassignmentof alternativephenotypesto environ-
mentaltypes. First, some environmentalfactor(s) correlatedwith a futurefac-
fitnessesof phenotypesmustbe available. Second, the
differential
tor(s) affecting
appropriatedevelopmentalsensitivitymust exist such that the influenceof the
firstfactorresultsin phenotypicadjustmentappropriateto the correlatedstate of
the second factor.An understandingof how matchingoccurs depends on a con-
ceptual frameworkthatincorporatesenvironmentalcomplexity,thatis, thatdis-
tinguishesbetween developmentalenvironmentand selective environment.
CONDITIONS FOR THE MAINTENANCE OF ADAPTIVE POLYPHENISM
In orderto describe the conditionsunderwhichpolyphenismis maintainedby

selection,I use a nongeneticoptimalityanalysis (see Parkerand Maynard Smith
1990). Althoughexact resultsmay differifparticulargeneticbases forpolyphen-
ism are assumed, using an optimalityapproach generallygives the same qualita-
tive predictionas models thatinclude explicitgeneticassumptionsand incorpo-
rate sexual reproduction(Thomas 1985). The approach is particularlyappropriate
forattempting to describe generalrequirementsforthe maintenanceof polyphen-
ism, since geneticbases are usually unknownand almost certainlyquite variable
fromcase to case.
I restrictmyselfto the simplestcase, thatof two alternativephenotypesand
two correspondingstates of the selective environment.Polyphenismswithmore
than two phenotypesresult fromnested bifurcationsin development(Wheeler
1986, 1991) and so can be understoodby applyingthe conditionsderived below
to each successive developmentalswitch. (Thus, a three-phenotype systemcan
be understoodby reducingit to two two-phenotypesystems.)Individualsexperi-
ence a single environment,with probabilitiesequal to the frequencyof each
environment.The strategyset consists of the polyphenicstrategy,which pro-
duces eitherof two phenotypes,and each of the two monophenicstrategies.The
bythefactthattheshift
isjustified
inclusionofthesealternatives frompolyphen-
ismto monophenism, througheliminationofa appearsoftento occur
phenotype,
in theconcluding
readily,as discussedfurther section.
EnvironmentalVariationand Fitness Trade-offs
An easilyrecognizedprerequisite fortheevolutionof adaptiveplasticity is a
spatiallyor temporally variableenvironment thatresultsin thereversalof the
ofalternative
relativefitnesses phenotypes.Ifthesamephenotype has thehighest
fitnessin alternativeselectiveenvironments, then constantexpressionof that
phenotype willbe favored over polyphenism.This conditionof fitnessreversals
impliesa trade-off involvingadaptations to alternative
environments (Stearns
be
1989b)and may expressed as
f(1,1) > f(2,1) andf(2,2) > f(1,2), (1)
wheref(i,j) is thefitnessoftheithphenotype in thejth environment.
Fitnesstrade-offs are readilyapparentin someof thebetter-studied cases of
alternativephenotypes. For example,in wingdimorphic insectspecies,winged
individualshavebetterdispersalabilitiesbutlongerdevelopmental timesorlower
fecundities(Dennoetal. 1989).Consequently, whenthelocalhabitatis deteriorat-
ing,wingedindividuals are morefit,butwhenlocal conditions are favorablefor
reproduction, individuals
flightless enjoytheadvantage,presumably because of
savingsfrominvestment in wingsand wingmusculature.
If these conditionsare satisfied(i.e., the selectiveenvironment variesand
causesreversaloftheselectivedifferential betweenalternative phenotypes),what
furtherrequirements mustholdforplasticity to be favored?As willbe evidentin
the modelsdevelopedbelow, the criticalfactorsare the extentto whichthe
correlationbetween developmentalenvironment and selectiveenvironment
allowsadaptivematching ofphenotype andenvironment, theextentto whichthe
environmental variationis spatialversustemporal,the fitnessrelationsof the
alternativephenotypes underdifferent environments andtherelativefrequencies
oftheenvironments, andpossiblecostsofplasticity, suchas thosethatmayarise
fromantagonistic pleiotropy involvingalternative phenotypes.
First,I considerpurelyspatialvariationin whichthetwo selectiveenviron-
mentsoccurwithconstantfrequencies in successivegenerations. I thendevelop
a modelinwhichvariation in environment is purelytemporal inorderto contrast
theconsequencesofthetwotypesofenvironmental variation formaintenance of
polyphenism.
THE MAINTENANCE OF ADAPTIVE POLYPHENISM-SPATIAL VARIATION
PolyphenismwithoutCosts versusMonophenic Specialists

(as in
matching.-In thepresenceof trade-offs
Perfectphenotype-environment
eq. [1]) andintheabsenceofcostsofplasticity,
a polyphenic thatalways
strategy
successfully matchesthe best phenotypeto each environmental statewill be
favoredoveranymonophenic Usingnotation
strategy. as in equation(1), we see
ALTERNATIVEPHENOTYPES 975
thatiff(1,1) andf(2,2) achievethehighestfitnesses 1

possiblein environments
and 2, respectively,
thensucha strategywillachievea fitnessof
wp = r f(l,1) + (1 - r) f(2,2), (2)
wherewpis thefitness
ofthepolyphenic strategy,r and 1 - r arethefrequencies
ofenvironments1 and 2, respectively,
and individualsexperienceenvironments
randomlyeach generation.This is thehighestfitnesspossible,and so thispoly-
willbe favoredoveranymonophenic
phenicstrategy one.
Imperfectphenotype-environmentmatching.-If matchingof the phenotypeto
environmentis imperfectenough,an advantageof polyphenismover monophen-
ismmaybe precluded.As developedearlier,suchimperfect matching mayresult
fromless thanperfectcorrelation betweencues and selectivefactorsor from
constraints on developmental Withimperfect
sensitivity. thefitnesses
matching,
ofalternativephenotypes indifferent environmentswillcontribute
to theaverage
fitnessof a polyphenicstrategy.To explorethissituation considerthe
further,
relativefitnessesof threestrategies-onepolyphenic, two monophenic-ina
spatiallyvaryingenvironment withtwo states.Each individualencounters only
one state;thatis, theenvironmentis coarsegrainedinthesenseofLevins(1968).
Genotypesof typeP may produceeitherof two phenotypes and achieve an
overallexpectedfitness of
wp = a1r >f(l,1) + (1 - a1)r f(2,1) + a2(1 - r) f(2,2)
+ (1 - a2) (1 - r) f(1,2),
wherea, and a2 are the proportions of occurrencesof environments 1 and 2,
respectively, thatare "predicted"correctly. Thus, a1 and a2 incorporate any
factorsthatinfluence matching, aspectsofdevelopmental
including sensitivityas
wellas correlation betweenenvironmental factorsused as cues and thoseused
as selectiveagents.As before,we assumetrade-offs; thatis,f(l , 1) > f(2,1) and
f(2,2) > f(1,2). GenotypesMl and M2 produceonlyphenotype 1 and phenotype
2, respectively, and achieveaveragefitnesses
as follows:
WMi = r f(l,l) + (1 - r) f(1,2),
and (4)
WM2 = r >f(2,1) + (1 - r) f(2,2).
Whenwillthepolyphenic strategy be favored?To simplify,

ifwe assumethatthe
abilityto predictenvironment 1 is thesameas theabilityto predictenvironment
2 (i.e., a = a, = a2), thepolyphenic willbe favoredwheneverwp >
strategy
max IWMI, WM2|, or when
a/(I - a) > maxlrx/(l - r), (1 - r)/rx| (5)
wherex = f(1,1) - f(2,1)/f(2,2) - f(1,2),thatis, theratioofthefitnessadvantage

ofphenotype 1 in environment1 to thatofphenotype2 inenvironment2. Figure
1 showscombinations ofa and r satisfying
thiscondition,
givendifferent
values
of the two phenotypes
of x. If the fitnessdifferentials withineach of the two
976 THE AMERICAN NATURALIST
P favored
0 x=2 x=1 x0O.

-C
oE
OE
r(frequency 1)1
ofenvironment
FIG. 1.-Combinations of a and i*for which polyphenismis favored under a spatially
varyingenvironment,given different values ofx, wherex = f(l1,1) - f(2,1)/f(2,2)- f(l1,2),
the ratio of the fitnessadvantage of phenotype1 in environment1 to thatof phenotype2 in
2.
environment
environments are the same (i.e., f[1,1] - f[2,1] = f[2,2] - f[1,2]), thenthe
polyphenic strategy willbe favoredoverM, whenevera > r and overM2when-
evera > 1 - r (fig.1). To the extentthatx > 1 (i.e., thedifference betweenthe
fitnessesis greaterin environment 1), P willbe favoredoverMl onlywhenP's
abilitytopredictenvironmental states(a) is sufficientlygreater thanthefrequency
of environment 1 (r)- thatis, whena is sufficiently greaterthanr. If thefitness
differenceis greaterin environment2, thentherequiredaccuracyofP's predic-
tionsis decreasedrelativeto r. If environment 1 is muchmorefrequent than
environment 2, thenP willonlybe favoredifpredictions are veryaccurate(a
close to one), ifthedisadvantage to producing phenotype 2 in environment 1 is
verysmall,oriftheadvantagetoproducing phenotype 2 inenvironment 2 is very
great(x muchless thanone). For a givenvalueofa, thepolyphenic strategy is
morelikelyto be favoredwhenalternative environmental statesare ofapproxi-
matelyequal frequencies or whenthefitness advantageofthephenotype suited
to therarerenvironment is great.These conclusionsagreewithLively's(1986b)
resultsfora morenarrowly specifiedsetoffitness relations.
Manyrealinstancesofplasticity involveasymmetries inthefitness advantages
ofalternative phenotypes as wellas differences infrequencies ofalternative envi-
ronments. For example,in wingdimorphic insects,conditions ofresourcedeple-
tionor overcrowding maybe rarebutmayconfera largefitnessadvantageto
dispersivemorphsable to escape to a betterhabitat(Dennoand Roderick1990).
Undermostconditions, sedentary morphs probably showa relatively smallfitness
advantageas a resultof slightly higherfecundity and fasterdevelopment. If the
abilityto matchphenotypeto environment is imperfect, thenthemagnitude of
suchfitness differentials combinedwiththerelativefrequencies ofselectiveenvi-
ronments willplaya roleindetermining whether is favoredbyselection.
plasticity
In addition to describingthe conditionsunder which polyphenismwill be fa-

vored over a monophenicstrategyconsistingofone ofits componentphenotypes,
equation (5) also indicates where polyphenismwill be lost. Eliminationof an
alternativephenotype,or "phenotypefixation,"has been suggestedto have mac-
roevolutionaryconsequences throughbothanagenesisand cladogenesis(Matsuda
1982, 1987; West-Eberhard1986, 1989). From equation (5), such loss would be
selected as a resultof two kindsof environmental
change. First,an advantageof
polyphenismmay be reversedifaccuracy of matching(a) decreases, forexample,
as a consequence of decreased correlationbetweenthe factorsused as cues and
thefactorsaffectingfitnessof alternativephenotypes.Second, ifone of the alter-
native environmentsincreases in frequency,thenthe correspondingmonophenic
maybecomefavoredoverpolyphenism,
strategy providedthatmatching
is im-
perfect.
Polyphenismversus a Single GeneralistPhenotype
As pointedout above, the assumptionthatdifferent
phenotypesachieve higher
fitnesswithinany one environmentimplies trade-offsor negative correlations
between fitnessesachieved in different
environments.In the face of such trade-
offs,a solutionto opposingselectiveregimesina variableenvironmentis pheno-
typicgeneralism(Levins 1968).Generalismis achievedthrough attributesthat
conferintermediate fitness
acrossa rangeofenvironmental states.Thus,in some
cases themonophenic strategyto consideras alternative
to polyphenism maybe
a generalist g, withthefollowing
strategy, fitnessrelations:
J'(1, ) > f(g, ) > f(2, 1),
and (6)
f(2,2) >f(g,2) >f(1 ,2),
wheref(g,1) andf(g,2) are thefitnessesofthemonophenic generalistphenotype
in environments 1 and 2, respectively.
Thus,thegeneralist
phenotype has lower
fitnessthana specialistphenotype whenbothoccurintheenvironment to which
the specialistis adaptedbut higherfitnessthanthe same specialistphenotype
whenbothoccurin theotherenvironment. The averagefitness
ofthegeneralist
is determined byitsfitnesses in thetwoenvironmentsandthefrequencies ofthe
twoenvironments, so that
wg= r f(g,i) + (1 - r) f(g,2). (7)
The polyphenic willbe advantageous
strategy when
r f(g,1) + (1 -r) f(g,2) < aIr f(1,1) + (1 - aI)r f(2,1) (8)
+ a,(1 - r) -f(2,2) + (1 - a2) (1 - r) f(1,2).
Whentheabilityto accuratelypredicttheenvironment
is perfect(i.e., a, a2
- 1), this inequalitybecomes
r f(1,1) + (1 - r) f(2,2) > r Jf(g,1)+ (1 - r) f(g,2), (9)
whichis alwaystrueby theassumption concerning therelativefitnesses
above.
Thus, if a polyphenicstrategy
producingspecialistphenotypes nevererrsand
incursno cost (see below),it will,notsurprisingly,be favoredovera generalist

strategy.
Additional assumptions
simplifying thatcanbe madetoclarify conditionsunder
whichpolyphenism willbe favoredoveran invariant generalist strategyare sym-
metry betweenfitnessesin thetwoenvironments andequal abilityto matchphe-
notypesto each oftheenvironments. Iff(1,1) = f(2,2),f(1,2) = f(2,1),f(g,1)
f(g,2), and a = al = a2, thentheinequality becomes
a f(1,1) + (1 - a) f(1,2) >f(g,1). (10)
In orderforpolyphenism ofthespecialist
to be favored,thesumofthefitnesses
phenotypes inthe"right"and "wrong"environments,weightedbytheaccuracy
ofmatching betweenphenotype mustbe greaterthanthecon-
and environment,
stantfitnessofthegeneralist
phenotype.
Effectof Costs of Polyphenism
Even ifdevelopmental andcues allowperfect
sensitivity predictionofthestate
oftheselectiveenvironment,plasticitymayentailcosts.Thesepotential costsfall
intotwocategories.First,thedevelopmental switchingsystemmaybe expensive,
which would resultin reduced fitnesseven when appropriatematchingis
achieved,oritmaysometimes resultindevelopmental as intheproduc-
mistakes,
tionof intermorphs of low fitness.For example,partiallydeveloped,useless
wingsare notuncommonin wingdimorphic insects,and intersexesof reduced
occurin someanimalswithenvironmental
fitness sex determination(Dunnet al.
1990).
A secondpossiblelimitation to fitnessassociatedwithplasticity is antagonistic
pleiotropy thatarisesfromopposingselectivepressureson alternative pheno-
types.That manyof the same loci are expressedin alternative phenotypes is
probableforall cases ofplasticity.
Although theestablishment ofdevelopmental
switchesthatcontroltheproduction ofalternative phenotypes maydecreasethe
levelof suchpleiotropy, whichwouldfreeeach phenotype to evolvemoreinde-
pendently of the other(s),completeindependence is unlikely.Some overlapin
geneexpressionby alternative phenotypes is impliedbythefactthattheyshare
earlydevelopment, priorto divergence of alternative pathways,and even after-
wardmanyof the same loci are certainly expressed.This overlapimpliesthat
traitsofalternativephenotypes sometimes willbe genetically correlatedandthat
selectionon one phenotype maybe opposedby selectionon alternative pheno-
types.Such pleiotropy couldimposecoststo plasticity by limiting theresponse
to selectionexhibitedby one or morealternative phenotypes. Such costsmight
be expectedto be greaterin cases in whichtheinfluence of cues, thesensitive
period,and adoptionofalternative developmental pathwaysare delayed.
Limitedevidencedoes existforconstraint due to correlationsamongalterna-
tivephenotypes. In intraspecific
comparisons ofpolyphenic andmonophenic but-
terflypopulations,the monophenic lineagesmayshowmoreexaggerated wing
patterns(McLeod 1984).Also,inhost-alternating Pemphigus aphidsthatproduce
differentphenotypes on alternative
hostplanttaxa,longperiodsof selectionon
onehosttaxonareassociatedwithreducedfitness onthealternative hosts(Moran
and Whitham1988;Moran1991).
In view of these potential costs of plasticity,another possible challenge to

a polyphenicstrategy is a monophenic, specialiststrategythat,in the "right"
environment, achieveshigherfitness thananyphenotype ofthepolyphenic strat-
egy.Such specialization on one environmentat theexpenseoffitness in alterna-
tive environments is, of course,widespreadand is a possibleconsequenceof
trade-offsbetweenfitnesses inalternative
environments, as describedbyequation
(1) (MacArthur 1972;Stearns1989b).Forthecase ofa polyphenic strategyversus
a monophenicspecialiston environment 1, the formalassumptionsregarding
are as follows:
relativefitnesses
f(s l, 1) > f(1,1) > f(2, 1), f(2,2) > f(s, ,2),f(2,2) > f(1,2), (1 1)
inenvironments
ofthespecialiststrategy
wheref(sl, 1) andf(sl,2)arethefitnesses
1 and The
2, respectively. polyphenic will
strategy be advantageous when
r f(ss,1) + (1 -r)f(sl,2)<alr f(l,l) + (1 - al)r f(1,2) (12)
+ 2(1 - r) f(2,2) + (1 -
a2) (1 - r) f(2,1).
usingthesamesimplifying
We can examinethisinequality as before.
assumptions
matching.-In the case where the polyphenic
Perfectphenotype-environment
makesno errorsin matching
strategy (a, - a2 = 1),
andenvironment
phenotype
polyphenismis favoredwhen
(1 - r) [f(2,2) - f(sl,2)] > r[f(sl,1) - f(l,1)] (13)
Even with perfectmatching,the polyphenicstrategymay not be favoredif the

cost is great enough-that is, iff(s1,l) is sufficiently
greaterthanf(1,1) or if the
specialist's environment is frequent.
Symmetryqf alternativephenotypes.-If we assume symmetrybetween the
fitnessesof the polyphenicstrategyin the alternativeenvironments(i.e., f[l 1]
= f[2,2]andf[1,2] = f[2,1])and similarabilityto predicteach environment
(a,
- a2), thenwe findthatthepolyphenic strategy is favoredwhen
a *f(l,1) + (1 -- a) f(1,2) > r f(sl,l) + (1 - r) f(sl,2). (14)
Each strategy Forthepolyphenic
experiencestwofitnesses. theaverage
strategy,
fitnessis thesumoftheseweightedby thefrequencies
ofsuccessesand failures
match. For the specialist strategy,the
in predictingthe phenotype-environment
averagefitnessis thesumof itstwofitnessesweighted bythefrequenciesofthe
two environments. Polyphenism is morelikelyto be favorediftheaccuracyof
matchingis high,thefrequency ofthespecialist'senvironment
is low,theadvan-
tage of the specialist in the "right" environment(f[s ,J] - f[1,1]) is small, or
(f[2,2] - f[sl,2]) is
of thespecialistin thewrongenvironment
thedisadvantage
large.
Bet Hedging tinderSpatial Heterogeneityin Selective Environment
A monophenic is one that"'putsall itseggsintoone basket,"whereas
strategy
a polyphenic strategyspreads its risks between two or more phenotypes.The
termbet hedgingis frequently
used to referto a polyphenicstrategy
thatran-
domlyassignsphenotypesto environments(Segerand Brockmann 1987;Philippi
and Seger1989).Bet hedging, usedinthissense,refers to theproduction ofmore

thanone phenotypewithina groupof individuals, whichtherebyincreasesthe
chancesthatat least some are suitedto whateverenvironment is encountered.
Thus,a bet-hedging strategyis simplyphenotypic intheabsenceofcues
plasticity
and/ordevelopmental thatwouldenablebetterthanrandommatching
sensitivity
betweenphenotype and environment.
If environmental variationis purelyspatial,can a bet-hedging strategybe ad-
vantageous?The usual definition ofbethedging impliesthatno cues are used to
matchphenotypeto environmental type.Rather,the polyphenicstrategy pro-
duces each of the alternative phenotypeswithsome constantprobability. To
showthatbet hedgingis notgenerallyadvantageouswherevariationis purely
spatialand whereinteractions amongindividuals do notaffectfitness,we can
return to thecase oftwodiscreteenvironments (eqq. [3]-[5]).In thiscase, using
theearliernotationand letting thefrequencyofproduction ofphenotypes 1 and
we findthatthefitness
2 be equal to d and 1 - d, respectively, ofthepolyphenic
strategy willbe
wp = dr f(1,1) + (1 - d)r f(2,1) + (1 - d) (1 - r)f(2,2)
+ d(1 - r)f(1,2).
fitness
Whatis thehighest thatcan be achievedifd is freeto vary?Differentiating
wpwith to
respect d, we have
dwpldd = r [f(l,1) - f(2,1)] - (1 - r) [f(2,2) - f(1,2)]. (16)
If r [f(1,1) - f(2,1)] > (1 - r) [f(2,2) - f(1,2)], then equation (16) is always
positive,so thatselectionwillfavorincreasing
d to one,whichresultsina mono-
phenic strategyfor producingonly phenotype1. If r [f(1, 1) - f(2, 1)] < (1 -
r) [f(2,2) - f(1,2)],thend shoulddecreaseto zero,whichresultsina monophe-
nic strategyforproducingonlyphenotype2. Thus, monophenismwill be favored
overpolyphenism inall excepttheinfinitely
unlikelycase inwhichthetwodiffer-
ences in fitnesses,weightedby the relativefrequenciesof the environmental
types,exactlybalance. In the case thattheseare equal, everyvalue of d or
combination ofthephenotypic proportionswillhaveequal fitness,
includingboth
monophenic Thus,a bet-hedging
strategies. polyphenic strategywithno ability
to matchphenotype and environment willnotevolvewhereenvironmental varia-
tionis purelyspatialand wherefurther assumptions enforcinglocal frequency
dependence(below)are notmet.This conclusionagreeswiththatof McGinley
et al. (1987)and Segerand Brockmann (1987).
Bet Hedging withSpatial Heterogeneityand Sibling Competition
These claimsconcerning the inadequacyof spatialvariationto maintainbet
hedginghave one majorexception.Spatialvariationmayfavora bet-hedging
strategyin cases of frequency dependenceactingwithingroupsof relativesor
siblingcompetition in the sense of MaynardSmith(1976, 1978).If siblingsor
otherclose relativescompete, then production ofa mixture ofphenotypes
may
be favoredevenwhenenvironmental is spatialrather
variation The
thantemporal.
potentialforfrequency-dependent selectionto maintaina bet-hedgingstrategyhas

been explored mainlyin the contextof favoringgeneticallyvariablegroups,such
as sexuallyproduced broods, over geneticallyhomogeneousones, such as asexu-
ally produced broods. The advantages of variationamong competingrelatives
have been recognized as a potentialbenefitof sexual reproductionrelative to
asexual reproduction(Williams 1975,pp. 15-17; MaynardSmith1976, 1978; Bell
1982, 1985). Althougha model based on siblingcompetitionis less than fully
satisfactoryto explain the maintenanceof sex (Hamiltonet al. 1980; Bell 1985),
similarprocesses may contributeto the maintenanceof polyphenicbet-hedging
strategiesin some groups. For example, productionof multipleseed types by a
singleplantmay reduce competitionamongthe resultingprogeny(Venable 1985).
THE MAINTENANCE OF ADAPTIVE POLYPHENISM: TEMPORAL VARIATION
So far,in consideringtheeffectsof environmental variationon themaintenance

of phenotypicplasticity,I have considered only cases in which the variationis
spatial and occurs withingenerations.In these cases, with discrete variation,
some individualsof a particulargenotypeare encounteringenvironment1 while
othersencounterenvironment2, and relativefrequenciesof environments(r and
1 - ri)remain constant over time. The appropriateestimatorof fitnesswhere
variationis spatial ratherthan temporalis the arithmeticmean, thatis, the sum
of the individual fitnessesweightedby theirfrequenciesof occurrence, as in
equations (2)-(4). However, changingconditionsoftencause different genera-
tions to encounterdifferent environments.For example, the dryingof a tempo-
rarypond affectsonly some generationsof residentzooplankton. The onset of
winteraffectsonly one of the two generationsof a bivoltineinsect. In these
cases of temporallyvaryingenvironments,effectsof selectionduringsuccessive
generationsare multiplicative.As a result,the appropriateestimatorof fitnessis
the geometricalmean; that is, fitnessestimatedacross n generationsis the ;ith
root of the productof the arithmeticmean of fitnesswithineach generation(Gil-
lespie 1974, 1976; Hamiltonet al. 1980; Lacey et al. 1983; Seger and Brockmann
1987; Philippiand Seger 1989).
Polyphenism tithoutCosts versusMoniopheniic
Specialists tinder
Temporal Variation
The general effectof variationbeing temporalratherthan spatial is to favor
polyphenism.This may be illustratedby returningto the case of two discrete
environmentalstateswitha polyphenicstrategythatproducestwo corresponding
phenotypesand a monophenic strategythat produces only one of these (eqq.
[I]-[4]). As before, ability of the polyphenic strategyto match phenotypeto
environmentis representedby a, with 0 < a < 1. Withina proportionr of
the generations,a proportional of the individualswiththe polyphenicstrategy
experiences fitnessof f(1,1), and the remainderexperiences fitnessof f(2,1).
Withina proportion1 - r of the generations,a proportiona2 experiencesf(2,2)
and 1 - a, achievef(1,2). As before,fitnessis notaffectedby interactionsamong
individuals. Long-termfitnessesof the polyphenicand monophenic strategies
CD
0.oE
EMI 0 1
TOE
co -
D favoredfaoe
r (frequencyof environment1)
FIG. 2.-Combinations of a and r for which polyphenismis favored under a temporally
varyingenvironment,given different values of z, where z = f(1,1)/f(1,2), the proportional
fitnessadvantage of the "right" over the "wrong" phenotypein eitherenvironment.
maybe represented
by
wp = [a, f(1,1) + (1 - a1) *f(2,1)]r [a2 f(2,2) + (1 - a2) f(1,2)](1r),
WMI = f(1,1 )r f(1,2)(1 r), (17)
and
wM2 = f(2,1)r f(2,2)(1r).
as beforeby takingthe specialcase of a1 = a2,f(1,1) = f(2,2),

If we simplify
andf(1,2) = (2, 1), thenthepolyphenic
strategywillhavean advantageoverthe
respectivemonophenic when
strategies
a f(1,1) + (1 - a) f(1,2) > max If(1,1)r.f(1,2)(1-r),f(1 1)(l-0) .f(1,2)rI (18)
Ifwe setz = f(1l,1)/f(1,2),
rememberingthatz > 1, thenthepolyphenic strategy
is advantageouswhen
a > max I(Zr - l)/(z - 1), (z(1-r) - 1)/(z - 1)1. (19)
The combinations ofa and r forwhichthisis true,givendifferent
valuesofz (the
proportional fitnessadvantageof the "right"over the "wrong"phenotypein
eitherenvironment), in figure
are represented 2. Fromequation(5), we saw that
forpurelyspatialvariationand otherwisesimilarassumptions, the polyphenic
strategyhas an advantage whenevera > max jr, 1 - r . Lively (1986b) arrived
at a similarconclusion.This conditionis equivalentto a requirement thatthe
accuracyof phenotype-environment matching be greaterthanthehighestaccu-
racythatcan be achievedby any strategy thatassignsphenotypes to environ-
mentsblindly.Whenenvironmental fluctuationoccursbetweengenerations, the
polyphenicstrategyis advantageous undera broaderrangeof combinationsof a

and r (fig.2). However, the trendof the requiredconditionsis broadlysimilarto
thatin thecase of spatialvariationin environment.The requiredlevel of accuracy
of matching(a) decreases with increasingdifferences
in fitnessbetween "right'
and "wrong" phenotype-environment combinations,and thisdecrease is greatest
when frequencies of environmentaltypes are intermediate(fig.2). That spatial
and temporal variationaffectpolyphenismdifferently is not surprising;spatial
and temporalvariationare well-knownto differin theireffectson themaintenance
of variationin other cases, includinggeneticpolymorphismswithinpopulations
(Hedrick et al. 1976; Hedrick 1986),geneticvariationwithinlineages as achieved
throughsexual recombination(Maynard Smith 1978; Hamilton 1980), and the
coexistence of different species withincommunities(Chesson 1986).
DISCUSSION
The foregoingresults show thatan understandingof the evolutionarymainte-

nance of plasticityrequiresconsiderationof ecological factorsas well as of devel-
opmental and genetic factors. In particular,polyphenismis more likely to be
favoredundertemporalvariationthanunderspatial variation,underhighvalues
of a, and under intermediatefrequenciesof alternativeselective environments.
These conclusionsagree withearliermodelsforparticularcategoriesofpolyphen-
isms (Lloyd 1984; Lively 1986b) and withseveral of Levins's (1962, 1963, 1968)
conclusionsforconditionsfavoringa developmentalswitchthatis eitherstochas-
tically or environmentallydetermined.The frameworkpresentedhere has the
advantages of having general applicability,in thatthe level of matching,fitness
relations,and environmental frequenciescan be variedseparately,and facilitating
contrastswithspecificmonophenicstrategies,such as the "generalist" and "sper
cialist" strategiesconsidered above.
Seasonality and the Availabilityof Cites
All oftheabove conditions favoring polyphenism are metformultivoltine ani-
mals in seasonal climates,whichperhapsexplainsthe apparentabundanceof
cases ofseasonalpolyphenisms relativetopolyphenisms associatedwithirregular
temporal fluctuationsor withspatialheterogeneity (Shapiro1976).For example,
a bivoltineinsectspeciesexperiencesa regularalternation oftwoenvironmental
states,so thatr and 1 - r are the same at 0.5. Probablymoreimportantly,
the annualcycle involvesa highlypredictablesequenceof changesin various
environmental factors.As a result,selectivefactors,suchas a decreaseintemper-
atureor foodavailability,are regularly anticipated
bycues, suchas photoperiod
or conditionof the hostplant.As a consequence,selectionon the natureand
timing ofdevelopmental sensitivitycan resultinperfect ornearperfect prediction
ofenvironmental factorsthataffectfitness, so thata willbe close to one.
Bet-hedgingPolyphenisms
The conclusionsreached above for temporalfluctuations
in environment
showedthatpolyphenism maybe favoredforvaluesofa evenless thanr (eqq.
[18] and [19]; fig.2). Underthoseconditions, theadvantageof thepolyphenic

strategy is equivalentto theadvantageofbethedging in a temporally fluctuating
environment, whichhas beendelineated bySegerandBrockmann (1987).In other
words,a polyphenic, bet-hedging strategy maybe favoredover a monophenic
strategy even whenthelatterachievesa higherlevelofphenotype-environment
matching.
The advantageofplasticity in thefaceoftemporal fluctuationsis based on the
fact that the geometricalmean fitnessis increasedby loweringbetween-
generation varianceinfitness.Thisdecreaseinvariancemaybe achievedthrough
theproduction of variablephenotypes withingenerations so thatthearithmetic
meanoftheaggregate is intermediatewithin a generation (Segerand Brockmann
1987).Dependingon theperiodand theregularity oftheenvironmental fluctua-
tions,severalgenerations maybe requiredbeforea benefit ofvariation is experi-
enced. Whenit does occur,thisbenefitonlyaccruesto an aggregate:multiple
carriersof an allele, a whole population,membersof a brood,and so forth.
McGinleyet al. (1987)also contrasted theeffects oftemporal andspatialvariation
on maintenance ofnongenetic variation-intheircase, parentally controlled vari-
ationin offspring size ratherthanan individual'scontrolof its ownphenotypic
expression.Theirgeneralconclusionswerethesameas thosereachedherefor
cases lackingphenotype-environment matching: temporalvariationmoreeasily
supportsa strategy of phenotypic variation, and spatialvariationsupportssuch
a strategy onlywithdensitydependenceamongsiblings.The twocircumstances
thatcan favorpolyphenic bethedging (i.e., temporal fluctuationsor spatialvaria-
tionwithsiblingcompetition) parallelthetwomajorcategoriesofmodelsforthe
maintenance of sexuality(Williams1975;Bell 1985).The conditions requiredfor
themaintenance ofbet-hedgingstrategies areexploredindetailelsewhere(Gilles-
pie 1974;Lacey et al. 1983;McGinleyet al. 1987;Segerand Brockmann1987;
Segerand Philippi1989).
Limits to the Evolutionof Plasticity
I have suggestedthat polyphenism is more widespreadthan is generally
thought. Nonetheless, itis clear thatthebulk oforganicdiversity arisesnotfrom
plasticitybut from genetic, largelyinterspecific
diversity. Why is polyphenism
notmorecommon,andinparticular whyareextreme cases,withhighly dissimilar
phenotypes, so rare?Formalrequirements forthemaintenance ofan established
polyphenism havebeenoutlinedinthepreceding sections.Does thelimited distri-
butionof polyphenism resultfromtheseconditions'onlyrarelybeingsatisfied,
thatis, fromtheabsenceofthenecessarypatterns ofvariationin selectiveagents
and/orcues? Alternatively, is theevolutionofplasticity moreoftenprecludedby
developmental constraints thatpreventits origin,limitdivergence ofalternative
phenotypes, or imposesubstantial costs?
Potentialdevelopmental constraintsthatmight precludeadaptiveplasticity in-
clude limitsto developmental thatpreventphenotype-environment
sensitivity
matching evenwhenpotentialcues are present,costsofmaintaining a systemof
developmental switching evenwhenappropriate matching occurs,andantagonis-
ticpleiotropy thatprevents independent evolution ofalternativemorphs.Thefirst
wouldlead to decreasedaccuracyof matching (i.e., decreaseda), whereasthe
lattertwo would cause each phenotypeof a polyphenicstrategyto attainlower

fitnessthanits monopheniccounterpart,as exploredin equations (11)-(14). Each
of these potentialconstraintson plasticitycould be highlytaxon-specific,which
would make thema difficult subject forgeneralization.
However, observationson the distribution of animalpolyphenismssuggestthat
taxon-specificidiosyncrasiesare not the dominantfactorsthatdeterminethe oc-
currence of simple cases of adaptive, conditional developmental switches.
Rather,the necessary patternsof environmentalvariation,primarilyavailability
of predictivecues, appear to be moreimportant.As notedearlier,the abundance
of cases of seasonal polyphenismin multivoltine lifecycles (examples in Shapiro
1976, 1984) suggeststhatunder regular,between-generation fluctuationsin envi-
ronmentand withdependable early predictorsof futureselective environments,
adaptive plasticitywithdevelopmentalsensitivityis a frequentevolutionaryout-
come. For example, switches between diapause and directdevelopment,most
oftencued by photoperiod,have evolved independentlyin a myriadof inverte-
brategroups (Beck 1980; Taylor and Spaulding 1986; Zaslavski 1989; Hairstonet
al. 1990). Thus, simple developmentalswitchesappear to be readilyestablished
and maintainedif requirementsforpatternsof environmentalvariationare met.
The abundance of seasonal polyphenismscontrastswitha lack of polyphenisms
in cases in which spatiallydiscreteenvironments,such as alternativehost taxa,
are experienced withoutthe benefitof predictorsthatoccur early enough to be
usefulfordirectingdevelopment.This comparisonsuggeststhatthe evolutionof
simple systemsof polyphenismis oftenlimitedby the availabilityof appropriate
environmentalvariation,particularlysuitable cues, ratherthan by flexibilityof
developmentalsystems.
In contrast,extremeexamples of plasticity,involvingmultipledevelopmental
switches and pronounced divergence among alternativephenotypes,are much
morerestrictedin taxonomicdistribution.Curiously,manyof the most outstand-
ing polyphenismsin metazoans are foundin those few, unrelatedtaxa in which
cyclical parthenogenesishas been established,particularlycertainrotifers(Gil-
bert 1980), the daphnids (Dodson 1988), the aphids (Hille Ris Lambers 1966;
Kawada 1987), and the paedogenetic cecidomyiids(Soulmalainen et al. 1987).
In aphids, for example, elaborate polyphenismshave evolved independentlyin
different lineages (Hille Ris Lambers 1966),whichsuggeststhatsome characteris-
tic of thisgroup lends itselfto the establishmentof multipledevelopmentalpath-
ways. A considerationof whycyclical parthenogensoftenshow highlydeveloped
polyphenismyields possible clues to understandingthe general limitson diver-
gence of alternativephenotypes.Cyclical parthenogensare unusual in combining
very shortgenerationtimes with extensive prenataldevelopment(possible be-
cause parthenogenesisallows developmentto proceed withoutfertilization).The
shortgenerationtimes promotemultivoltinism; consequently,different genera-
tions experience seasonal fluctuationsin a coarse-grainedmanner(sensu Levins
1968), which thus furnishesthe requiredvariationin selectiveenvironment.Pre-
natal development("telescoping of generations"in extremecases) may enhance
sensitivityto predictiveenvironmentalcues, since the mother'sfullydeveloped
neural and endocrine systems are responsive to the externalenvironmentand
could readilyinfluenceinternallydevelopingembryos.Thus, extremedivergence
of alternativephenotypesmay depend on a sensitive stage and developmental

switchthat occur very early, and this possibilitymay be facilitatedby prenatal
development.
Originand Loss of Polyphenism
I have considered here the requirementsformaintainingan establishedpoly-
phenism; the problem of how polyphenismsoriginate-for example, whether
throughan intermediatestage involvinggeneticpolymorphism(Bradshaw 1973),
continuousplasticity,or behavioralflexibility (Wcislo 1989)-is outsidethe scope
of this article. It is clear thatonce a polyphenicdevelopmentalsystemis estab-
lished, the linkage between cues, hormonesor other effectors,and phenotypic
consequences is oftenlabile. Thus, regulationof the developmentalswitch can
be adjusted in response to changes in patternsof environmental variability.Selec-
tion will always favor maximal accuracy of phenotype-environment matching.
Such selection on an established polyphenismmay adjust the identitiesand
thresholdsof the environmentalfactorsused as cues as well as the timingof the
developmentallysensitiveperiod. Evidence forthislabilityis providedby studies
thatdemonstratelocal adaptationof criticalthresholdsor of the timingof sensi-
tive stages (e.g., Taylor and Spaulding 1976; Shapiro 1979; Hairstonand Walton
1986). Thus, long-termchanges in environmentthatcause an establishedcue to
become less reliablemay resultin substitution of an alternativecue, whichwould
maintainhighlevels of phenotype-environment matchingand enable the persis-
tence of the polyphenism.
This labilityof thresholdsand of sensitivityto cues impliesthattransitionsto
monophenismoften can occur readily if patternsof environmentalvariability
change so as to no longerfavorpolyphenism.There are many examples of lin-
eages that apparentlyhave undergonethe loss of a phenotype,sometimeswith
accompanyingecological and/orlife-cycleshifts.For example,deletionof pheno-
types by lineages of aphids (Moran 1988, 1990) and rustfungi(Savile 1971) has
resultedin the loss of one of theirtwo alternativehost plant taxa; consequences
include changes in breedingsystems,habitatshifts,and rangeexpansions. West-
Eberhard(1986, 1989) and Matsuda (1982) have suggestedthatthe establishment
and subsequent loss of polyphenismcan have major evolutionaryrepercussions.
ACKNOWLEDGMENTS
I thank J. L. Bronstein, P. L. Chesson, D. M. Gordon, W. D. Hamilton,

D. R. Papaj, J. Seger, D. L. Venable, and D. E. Wheelerforcommentson the
manuscriptand/orforusefulcommentsduringdiscussions.This articlewas writ-
ten with the support of National Science Foundation award BSR-8806068 to
N.A.M.
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The Evolutionary Maintenance of Alternative Phenotypes

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The University of Chicago

The Evolutionary Maintenance of Alternative Phenotypes

THE EVOLUTIONARY MAINTENANCE OF

Abstract.-To understandthe evolutionof polyphenism,or adaptive switchingbetweenalterna-

In recentyears,phenotypic has beenresurrected

Am. Nat. 1992. Vol. 139, pp. 971-989.

(Harrison1980;Roff1986),alternative morphologies associatedwithdifferent

DUAL INFLUENCES OF ENVIRONMENT: DEVELOPMENT AND FITNESS

Environmental factorsaffect organisms intwowaysincases ofadaptivepheno-

ADAPTIVE MATCHING OF PHENOTYPE AND ENVIRONMENT

As is evidentin the models developed below, a primarydeterminantof condi-

CONDITIONS FOR THE MAINTENANCE OF ADAPTIVE POLYPHENISM

In orderto describe the conditionsunderwhichpolyphenismis maintainedby

THE MAINTENANCE OF ADAPTIVE POLYPHENISM-SPATIAL VARIATION

PolyphenismwithoutCosts versusMonophenic Specialists

thatiff(1,1) andf(2,2) achievethehighestfitnesses 1

Whenwillthepolyphenic strategy be favored?To simplify,

wherex = f(1,1) - f(2,1)/f(2,2) - f(1,2),thatis, theratioofthefitnessadvantage

0 x=2 x=1 x0O.

In addition to describingthe conditionsunder which polyphenismwill be fa-

incursno cost (see below),it will,notsurprisingly,be favoredovera generalist

In view of these potential costs of plasticity,another possible challenge to

Even with perfectmatching,the polyphenicstrategymay not be favoredif the

and Seger1989).Bet hedging, usedinthissense,refers to theproduction ofmore

potentialforfrequency-dependent selectionto maintaina bet-hedgingstrategyhas

THE MAINTENANCE OF ADAPTIVE POLYPHENISM: TEMPORAL VARIATION

So far,in consideringtheeffectsof environmental variationon themaintenance

as beforeby takingthe specialcase of a1 = a2,f(1,1) = f(2,2),

polyphenicstrategyis advantageous undera broaderrangeof combinationsof a

The foregoingresults show thatan understandingof the evolutionarymainte-

[18] and [19]; fig.2). Underthoseconditions, theadvantageof thepolyphenic

lattertwo would cause each phenotypeof a polyphenicstrategyto attainlower

of alternativephenotypesmay depend on a sensitive stage and developmental

I thank J. L. Bronstein, P. L. Chesson, D. M. Gordon, W. D. Hamilton,

Austad, S. N. 1984. A classificationof alternativereproductivebehaviorsand methodsforfield-testing

Harrison,R. G. 1980. Dispersal polymorphisms in insects.AnnualReview of Ecology and Systematics

Moran,N. A., andT. G. Whitham. 1988.Evolutionaryreduction ofcomplexlifecycles:an example

Associate Editor: Jon Seger

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