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Pomiankowski A, Iwasa Y, Nee S. The evolution of costly mate preferences. I.

Fisher and biased mutation. Evolution 45: 1422-1430

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Evolution,45(6), 1991, pp. 1422-1430

THE EVOLUTION OF COSTLY MATE PREFERENCES

I. FISHER AND BIASED MUTATION

ANDIREwPOMIANKOWSKII,
ABRG, Departmentof Zoology, Oxford,OX] 3PS, UK
YOH IWASA,
Departmentof Biology,Faculty of Science, Kyushu University,
Fukuoka 812, JAPAN
AND

SEAN NEE
AFRC UnitofEcology and Behaviour,Departmentof Zoology, Oxford,OX] 3PS, UK

Abstract.-Fisher's runawayprocessis thestandardexplanation of theevolutionofexaggerated

femalepreferences. Butmathematical formulationsofFisher'sprocess(haploidand additivedip-
loid) showit cannotcause stableexaggeration
iffemalepreferencecarriesa cost.At equilibrium
femalefitness mustbe maximized.Our analysisshowsthatevolutionary stableexaggerationof
femalepreference can be achievedifmutationpressureon themalecharacter is biased,thatis,
mutation has a directional
effect.
Atthisequilibriumfemalefitness
is notmaximized. We discuss
thereasonsand evidenceforbelievingthatmutationpressureis typically biased.Our analysis
highlightsthepreviously unacknowledgedimportance ofbiasedmutation forsexualselection.
Keywords.
-Mate choice,mutation
pressure,
runaway
process,sexualcharacters,
sexyson.

ReceivedSeptember
24, 1990. AcceptedFebruary
25, 1991.
Male matingbehavior ofteninvolves the genesfortheiroffspring; in the second view,
display of extravagantornaments accom- theyare lookingforgood viabilitygenes.
panied by loud and complex songs and the A keyquestionto pose is underwhatcon-
releaseofvolatile secretions.To understand ditions will these forceslead to the estab-
the evolution of these exaggeratedsecond- lishmentof costlysexual preferences.This
arysexual characterswe need to explainhow is a crucial question not only because there
femalesdevelop sexual preferencesforsuch is much evidence that there are costs as-
traits.Two theorieshave been proposed for sociated with mate choice (Pomiankowski,
cases where the benefitsof preferenceare 1987) but because in previousstudiesit has
heritable.The first, originatingwithDarwin been shownthatchoice costsdistinguishbe-
(1871) and Fisher(1915, 1930), suggeststhat tween the two theoriesof sexual selection.
theadvantageofpreference lies in thechoice All currentgeneralformulationsof Fisher's
of mates who will fatherattractivesons. If process show that female fitnessmust be
femaleson average prefera particularmale maximized at a stable evolutionaryequilib-
trait,thenmales withthattraithave a mat- rium.Fisher's processcannot cause the sta-
ing advantage and, if the traitis heritable, ble evolution of costly female preferences.
femaleswith the preferencehave male off- This is true whetherthe costs incurredin
springsimilarlyadorned who also enjoy a matechoice affectfemaleviability(Pomian-
matingadvantage. The second view, force- kowski, 1987; Bulmer, 1989b) or fecundity
fully advocated by Zahavi (1975) in the (Kirkpatrick,1985). In contrast,models of
"handicap" principle,arguesthattheprime the "handicap" principlehave shown that
benefitof choice lies in increased offspring it can lead to the evolution of costlyfemale
survival.In thisview, male ornamentspro- preferences (Andersson,1986; Pomiankow-
vide thefemalewithinformationabout her- ski, 1987). Raised offspringviability can
itable male quality. In the firstview, then, compensate forchoice costs, so that at the
femalesare looking forgood attractiveness evolutionaryequilibrium female fitnessis
not maximized.
' Presentaddress:Departmentof Geneticsand Bi- This paper setsout to investigatetheevo-
ometry,University CollegeLondon,London NW1 lution of costly female mate choice. We
2ME, UK. presentquantitativegeneticmodels of both

1422

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 FISHER AND BIASED MUTATION
Fisher's process and in the companion pa-
per (Iwasa et al., 1991) of the "handicap"
principleof sexual selection.First,we con-
firmthatin the simplestmodels of Fisher's
process, costlyfemale preferencesmay in-
crease temporarilyby runawaybut at equi-
libriumtheyare alwayseliminated.We then
show that this qualitative resultis not ge-
neric; it disappears when slightmodifica-
tions are made to the model. In particular,
we show that if mutationhas a directional
bias on the male trait then costly female
preferences are present at evolutionary
equilibrium.Reasons whymutationbias is
particularlystrongin exaggeratedand elab-
orate ornamentaltraitsare explored in the
discussion.
Two TRAIT MODEL
Consider a population withtwo sex-lim-
ited quantitativetraits,a male matingor-
namentt and a femalematingpreference p.
Both traits have an autosomal, polygenic
basis. The phenotypicvalue of each traitis
statisticallydecomposed into an additive
geneticcomponentand an "error"termdue
to environmentalvariationand dominance
(Bulmer,1980). As our goal is to make qual-
itative points as clearlyand easily as pos-
sible, we have chosen to model only the
evolutionoftheadditivegeneticeffects. This
we do using a novel, computationallysim-
ple, quantitativegenetic formulation.The
main conditionrequiredis weak selection;
thatis, thefitnessfunctionschangelittleover
the range of phenotypicvariation in the
population. A fulljustificationof the tech-
nique is givenin thecompanionpaper (Iwa-
saetal., 1991).
The evolution of the mean values of two
sex-limitedtraitsin a population with dis-
crete, nonoverlappinggenerationswill be
modeled as the productof the additive ge-
netic variance-covariancematrix and the
selectionvector,
a In W,,(t; t,p
(AtA_ 1 Gt Btp At
kAp! 2kBtP Gp a in Wf(p)
(1)
The factorof l/2 indicates the sex-limited
nature of the fitnessfunctions;choice (p)
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1423
beingexpressedonlyin femalesand thecho-
sen ornamenttrait(t) only in males. The
fitnessof a male, Wm(t;t; p), is a function
of both his individualphenotype(t) and the
populationmean values of the male trait(t)
and female preference(p)-separation of
these differentvariables being indicatedby
a semi-colon.A female'sfitnessis unaffect-
ed by the distributionof male phenotypes
and depends solely on her individual phe-
notype.These fitnessfunctionsmeasurethe
average survivalto thebreedingseason and
mating success of a given male or female
phenotyperelativeto others.The effectof
selectionis calculated by takingpartialde-
rivatives of the log fitnessfunctionswith
respectto theindividualtraits,evaluated at
the population means, t = t and p = p.
G,and Gpare thevariancesoftheadditive
geneticvalues of the male traitt and female
preferencep. Btpis the covariance of the
additivegeneticvalues of thetwo. In sexual
selectionthegeneticcovariancemainlyaris-
es fromnonrandommating.We simplyas-
sume that the values of Gt, Gp and Bp are
positive constants. The covariance BP is
positive because femaleswithlargervalues
of p tend to mate with males with larger
values of t. Althoughthese geneticparam-
etersmaychangewithtimedue to selection,
mutation,and recombination,we make a
constancyassumptionbecause as yet there
is no tractablemethod of calculatingthese
parametersforthequestionswe wantto ad-
dress (see, Barton and Turelli, 1987; Bul-
mer, 1989a). It is unlikelythatour conclu-
sions willbe compromisedby morerealistic
models when these become available. This
view is supportedby similar resultsbeing
found in major gene models of sexual se-
lection,in which the variance and covari-
ance termsare freeto evolve.
UnderlyingEquation (1) and similarfor-
mulationsis an importantassumptionthat
has rarelybeen emphasized.Mutationcaus-
es a shiftin the additive geneticvalues of
theloci contributing to each trait.However,
upward and downward changes are as-
sumed to occur equally frequently and with
similar magnitude. Summed over all loci
and averaged over all individuals in the
population, mutationproduces no net di-
rectional force on the mean phenotypes.
Hence, Equation (1) has no mutationterm.
1424 ANDREW POMIANKOWSKI ET AL.

As explained later,modificationof this as- When thereare no costs to choice and b = 0

sumptioncauses a radicalchangeto theevo- the two lines are identical, specifyingthe
lutionaryoutcome of sexual selection. classic straightline of equilibriap = (2c/a)T
By specifyingthe fitnessfunctionsWm(t; (Lande, 1981). The line of equilibrium is
t,p) and WJXp) we can calculate the change stable (more exactly,an attractinglimitset,
in the mean values of the ornament and Guckenheimerand Holmes, 1983) if the
preference.Male fitnessis the product of slope of the evolutionarytrajectoryis less
survivorshipand matingsuccess,and in the than the slope of the line of equilibria (B,,/
standardmodel (Lande, 1981) corresponds G, < 2c/a).
to, But if choice is costlyand b > 0 the two
Wm(t; t, p) = ea(t0-bect2
isoclines intersectat theorigin(Fig. 1). There
(2)
is only a singleequilibriumat peq = 0, the
Males are polygamousand can mate many point where female fitnessis maximized.
times. For positive values of preference, This example suggeststhatmate preference
matingsuccessincreasesexponentiallywith cannot be costly at the evolutionaryequi-
ornamentsize t, the rate coefficientbeing librium. The resultis due to the fact that
proportionalto p, the average strengthof when At = Ap = 0 in Equation (1) the prod-
the femalemate preference.We furtheras- uct of the geneticvariance-covariancema-
sume thatfemalesassess males withrespect trix(G) and the selectionvector mustbe a
to the mean male phenotype(t). Females zero vector. If both traitsremain indepen-
with positive preferenceprefermales with dently geneticallyvariable then the vari-
largerthanaverageornaments,and females ance-covariance matrix is nondegenerate
with negativepreferenceprefermales with and the determinantof G is nonzero, so at
smaller than average ornaments.Females equilibriumtheselectionvectormustbe zero
withzero preferencemate at random. This (0 ln Wf(p)/op= 0). This means thatfemale
model of femalepreferenceis similarto the fitnessis at a maximum at equilibrium(for
"psychophysical" model used by Lande sensible fitnessfunctions).
(1981). In contrast,survival chances de- This general conclusion states that at
crease as ornamentsize deviates fromthe equilibriumfemalematepreferenceevolves
optimal male phenotype,whichis arbitrar- to one maximizingher lifetimereproduc-
ily set at t = 0. tive success. Effectsof mate choice on off-
Females have to spend some time or en- springattractiondo not influencethe evo-
ergy,or riskpredationengagingin mate dis- lutionaryequilibriumat all. The male trait
crimination.We assume that this cost to evolves to thelevel thatmaximizeshis own
femalefecundity or survivalis an increasing lifetime reproductive success given the
functionofthestrength offemalepreference equilibrium strengthof female mate pref-
and is independentof the distributionof erence. We note that,forconvenience,the
male phenotypes. optimum femalepreferencewas set at p =
= (3) 0, which correspondsto random mating.If
Wf(p) eb-p2
we had taken some othervalue forthe op-
For conveniencewe assume costs are min- timum female preference,say p > 0, then
imized when femalesmate at random (i.e., the equilibriummale characterwould have
p = 0). The cost coefficients a, b and c are deviatedfromitsnaturalselectionoptimum
small positive constants.From these defi- by an amount reflecting the strengthof fe-
nitionsthechangein mean values are found male preference(Kirkpatrick,1987).
by substitutionin Equation (1),
G
At = (ap - 2ct) - Btp(bp), (4a)
MUTATION BIAS CAN ESTABLISH
B COSTLY CHOICE
= 2P (ap - 2ct) - Gp(bp). (4b)
2
The previous resultimplies that Fisher's
By settingAT= 0 and Ap = 0 we can define processcannotexplainthestableevolution-
two isoclines that intersectat equilibrium. ary exaggerationof costly female prefer-

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 FISHER AND BIASED MUTATION 1425

5
-0

FIG. 1. Evolution of the male trait(r) and female

preference(p) when preferencesare costly.Even with
a slightcost, b = 0.0125, preferencealways evolves to
an equilibrium at which female fitnessis maximized
(p = 0). Only transientevolution of costly mate pref-
erenceoccurs. Parametervalues a = 0.5, c = 0.5, Gt=
GP = 0.2, Btp= 0.06.
FIG. 2. Costlyfemalepreference evolveswhenthe
maletraitis subjectto mutationbias. At equilibrium
thecostsoffemalepreference areoffset bythemating
advantageof havingmoreattractive male offspring.
Parameter valuesas in Figure1 withu = 0.005.

ences. However, this requiresthatthe evo- / In Wm(t; t, p)

lution of preferenceis exactly, not just
approximatelydescribed by Equation (1). kAP!2\2BtpGp di n Wfp)
This requirementcan be easilytransgressed.
An example that we will concentrateupon
ap /
is biased mutation,where the net effectof
mutation is nonzero. There are two types ( ? ) (5)
of mutationbias thatare importantin sex-
ual selection.It is well knownthatmutation Substituting Equations (2) and (3) for
is biased on viability,most mutationsre- Wm(t;t,p) and Wf(p) respectivelyand set-
ducingviability.We will considerthiseffect tingAt = Ap = 0 again gives two isoclines,
in thecompanion paper (Iwasa et al., 1991). but these now intersectat a nonzero equi-
In addition,mutationpressureon morpho- librium(Fig. 2),
logical characters,particularlyexaggerated t - u(aBtp - 2bGp) (6a)
secondary sexual traits,is likely to be bi- teq - (a
-2bc(GtGp B2t)
ased. Primarilythis is because random al-
terationsto a complex systemare morelike- uBtp (6b)
lyto reduceitsperformance thanto improve
it (forreasonssee discussion).We now show
thatthe incorporationof a directionalbias If there is no mutational bias (u = 0) the
in mutation acting on the male trait can equilibriumis at teq= Peq =0, and female
easilyresultin theevolutionofcostlyfemale fitnessis maximized. However, withbiased
mate preference. mutation (u > 0) female fitnessdoes not
Mutationcan be simplyincorporatedinto reach its maximum at equilibrium.Rather
thestandardquantitativegeneticmodel. Let the equilibrium strengthof female prefer-
u be the per generationreductionin the ad- ence lies beyond the natural selection op-
ditivegeneticvalue of male traitdue to mu- timum, increasingwith the degree of mu-
tation. Now the change in mean values is, tationbias (u) and decreasingwiththecosts

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1426 ANDREW POMIANKOWSKI
of mate preference(b). At equilibrium,di-
rectselectionon femalemate preferencere-
mains negative; that is, female choice is
costly.This cost is offsetbytheindirectben-
efitof mating with the males bearing ex-
aggeratedornamentaltraitsand so having
more attractivesons. Interestingly, ieq is in-
dependentof the efficiency of mate prefer-
ence (a) or of the cost of the male trait(c).
In contrast,the equilibriumlevel of male
trait,teq, depends on these extra quantities
which affectmale reproductivesuccess. At
equilibrium,selectionon the male traitre-
mains positive; that is, males with larger
ornaments enjoy greatertotal fitness,be-
cause the benefitof highermating success
exceeds thecost of lowersurvival.Selection
constantlyfavorsgreaterexaggerationin the
male trait.But this forceis checked by bi-
ased mutationand the correlatedeffectof
selectionon femalepreference, bothofwhich
tend to reduce the mean value of the male
trait. At equilibrium these forces are bal-
anced.
This indicates that costly female prefer-
ence can evolve if the preferredmale char-
acteris subjectto directionalmutationbias.
We would like to stressthatthisresultholds
irrespective ofanyassociationsthemale trait
has with general viability. The reason for
the establishmentof costly female prefer-
ence lies purelyin the Fisherianbenefitthat
she gains fromhavingmore attractivemale
offspring.In nature, it may be that traits
subject to significantmutation bias also
stronglyreflectbiased mutation on viabil-
ity. However, it is importantto separate
thesetwo distinctforcesforcleartheoretical
analysis. It is also importantthatthese two
forces be separatelyassessed in empirical
studies.
MUTATIONBIAs
The preceding investigationshows that
Fisher's process can cause stable exaggera-
tionoffemalemate preferenceseven ifpref-
erence is not a neutralcharacter.But to as-
sess the importanceof biased mutationon
the male traitwe need to estimateits likely
value in nature. To do this we need to be
aware thatthe measurementof bias is scale
dependent. Given a particulardefinitionof
a characterand given a particularscale of
measurement,it is an empirical question
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ET AL.
whetherand to what degreemutationis bi-
ased. But it is at once obvious on logical
groundsthat if mutationis unbiased given
one definitionand scale of measurement
then it mustbe biased formany otherdef-
initions and scales. If mutation does not
alter the mean of a characteron an arith-
metic scale then it must alter it on a loga-
rithmicscale. If we define the color of a
crypticcaterpillarin termsof saturationwe
mayfindthatmutationis unbiased.But then
we know that mutationis biased if we re-
definecolor in termsofthedegreeofcrypsis,
the match to the background.
What mattersfor sexual selection is the
definitionand scale of femalepreference,a
subject about which littleis known. How-
ever, femalepreferenceoftenappears to be
forexaggeratedand intricatelydesignedor-
namental characters(Darwin, 1871; Triv-
ers, 1985). There are two relatedreasons for
expectinga pronounced mutation bias in
such characters.First,a greatlyexaggerated
traitis likelyto be at the physiologicallimit
of its production. For example, calling in
frogsand toads is known to be one of the
most, if not the most, energeticallycostly
behaviors that the male performs(Ryan,
1988). Probably it is extremelydifficult for
these frogsand toads to call any better(be
it louder, longer,more frequently).So, it is
likelythatmanymutationsin genesaffecting
callingwilldecreasecallingaptitudeand, so,
mutation will be biased. Second, many
charactersused in matingshow greatintri-
cacy and designof structureand coloration,
forexample,the"eye" on thepeacock's tail.
To getsuch perfectionprobablyrequiresthe
very exact action of a large number of en-
zymaticpathways.There will be manyways
of disruptingsuch pathways but very few
ways of improvingthem. So, again muta-
tion in characterswith very intricateand
specificdesigns is likelyto be biased.
Anotherway of thinkingabout mutation
bias is to relateit to the historyof selection
on the traitin question. Mukai (1964) pre-
dicted an equal frequencyof positive and
negativemutations,and hence no mutation
bias in characterssubjectto weak selection.
In contrast,he predictedthatcharactersre-
centlysubjectto directionalselectionshould
show a negative correlationbetween bias
and the directionof selection.For example,
 FISHER AND BIASED MUTATION 1427

we mayexpectlittleor no bias in Drosophila if mutationbias on the preferredmale trait

bristlenumber because this traithas been is similar in strengthto mutation bias on
shown to be under weak stabilizingselec- viability. In practice these two biases will
tion, but if bristle number was increased be intimatelyrelated. The bias reportedin
throughartificialselection then mutation induced mutationstudies is oftenin traits
bias towardslower numbersmightwell ap- that are probably closely related to fitness
pear. If this is the case then the mutation (e.g., Ohnishi in Crow and Simmons, 1983)
term,u, mightmorerealisticallybe replaced and P-element induced mutations in D.
by u It -t,t I in Equation (5). That is, weak melanogaster at genetic loci controlling
mutationbias close to the naturalselection quantitativecharactersfrequently have del-
optimum, but strongmutation bias away eteriouseffects on viabilityas well (Mackay,
fromthe optimum. Many sexual traitswill 1986). It is largelyforanalyticalclaritythat
have been recentlysubjectto directionalse- we have examined mutation on the male
lectiondue to femalemate preference, lead- trait under the assumption that mutants
ing to exaggerationaway fromthe viability have no pleiotropiceffectson other traits.
optimum. We expect these traitsto be par- Mutations thataffectthe male traitand fit-
ticularlysusceptibleto mutationbias. ness in other respectsare examples of so-
Mutation studies provide some evidence called "good genes," and are analyzed in a
fortheoccurrenceof mutationbias in quan- three trait model in the companion paper
titative traits. Unfortunatelymost studies (Iwasa et al., 1991). At the level of a single
of mutation on polygeniccharactershave geneticlocus it will not be possible to apply
concentratedon measuringchanges in the this distinctionbecause some alleles affect-
genetic variance not the mean. However, ingthe matingornamentwill have no pleio-
measurementsof changesto the mean were tropiceffects and otherswillhave significant
reportedin several radiationbiologyexper- pleiotropiceffectson viabilitytraits.How-
iments carriedout in the 1960s and 1970s ever, it may be possible, at the level of a
using X-irradiationor EMS (ethylmethane traitto make such a distinctionand findout
sulphate) treatmentto artificiallyraise the thefractionof mutantsin thattraitthatalso
mutationrate. These studiescommonlyre- have pleiotropic effectson other viability
porta decreasein thephenotypicmean after traits.This will potentiallyallow a gauge of
irradiation(Yamada and Kitagawa, 1963; the relative importance of these different
Abrams and Frey, 1964; Gaul, 1965; Doll, typesof mutationaleffect.
1972; Chakrabati, 1975; Ohnishi in Crow
and Simmons, 1983). More recentlyLai and SEXY SON
Mackay (1990) have used the P-M hybrid The findingsreportedhere also apply to
dysgenesis system of Drosophila melano- "sexy son" models of sexual selection.The
gaster to look at transposable element in- ''sexy son" hypothesis is derived from
duced mutationsin quantitativecharacters. Weatherhead and Robertson's (1979) sug-
They found that average stemopleuraland gestion that female preferenceevolves for
abdominal bristlenumbers were lower for males that are attractiveeven if theygive
P strain X chromosomes from dysgenic less assistance in raising offspringand so
crosses that sufferhigh mutationrates be- lower fecundity.The assumptions of the
cause of elevated P-element transposition. "sexy son" hypothesisdifferfromthe two
There is also some evidence fromsponta- traitmodel examined here only in that fe-
neous mutationaccumulation experiments male mate choice affectsherfecundityrath-
that the effectof mutationon bristlescore er than her viability.
is negativein D. melanogaster(T. Mackay, Fecunditycosts are more complicated to
pers. comm.), thougha similarexperiment model because theydepend on assumptions
by Mukai and coworkerson ADH activity about the distributionof male phenotypes
failedto show any bias (Mukai et al., 1984). and how the numberof femalesmated to a
Althoughthese reportssuggestthat mu- male affectsfecundity.However,in thesim-
tationbias on traitsexists,theydo not allow plest case of "unlimited male reproductive
an estimation of its magnitudein natural potential" (Kirkpatrick,1985), fecundityis
populations.It would be interesting to know a constantforeach male phenotypeand fe-

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1428 ANDREW POMIANKOWSKI ET AL.

cunditycosts act in an identical mannerto ditive models do conformto the sexy son
viabilitycosts: females with strongerpref- hypothesis,but it seems unlikelythat this
erences mate with males having largeror- is common.
naments and so have lower fecundity.If
thereis mutationbias on themale traitthen
a stable equilibriumwill be foundat which DIscusSION
losses in fecundityare offsetby the advan- The female'srolein matinghas oftenbeen
tage of bearing more attractiveoffspring. overlooked or femaleshave been relegated
Whether this is a strongenough force to to supposedly passive partners (Wallace,
account for the proposed examples of the 1891; Mayr,1972), wherepassivityhas been
"sexy son" is unclear.But it is clear thatthe taken to mean that females have simple,
strongargumentsforrejectionof the "sexy fixedpreferences, whichmales have evolved
son" hypothesis(Kirkpatrick,1985) need to to exploit (Parker, 1983; Arak, 1983). In a
be qualified. similar vein, much of the influentialwork
Our re-establishmentof the "sexy son" on the evolution of female choice has as-
hypothesisdiffers fromthatrecentlyputfor- sumed thatpreferenceis a neutraltraitthat
wardby Curtsingerand Heisler (1988) using is not subject to direct selective pressures
a two locus diploid model that explicitly (Lande, 1981; Kirkpatrick,1982). In these
considersnonadditivegeneticaffects.Curt- models preferenceevolves only as a corre-
singerand Heisler (1988) claim thatdiploid latedresponseto directselectionon themale
models permita stable evolutionaryequi- trait. The main result reported in these
libriumtrade-off betweenthefecundity costs models is that any strengthof femalepref-
of choice and the advantage of matingwith erencecan evolve (i.e., a lineofequilibria)-
more attractivemales. However, a reanaly- the evolutionaryoutcome of sexual selec-
sis by Kirkpatrick(1988) has shown that tion beinghighlyindeterminateand greatly
the resultsof diploid models are consistent affectedby random forces,such as genetic
with those found previously in haploid drift.
models in two importantrespects. Either We believe thatthe considerablebody of
thereis a stableequilibriumat whichfemale interpretation based on theassumptionthat
fecunditylies at a maximum (local or glob- preferenceis a neutralcharacteris mislead-
al), or this equilibriumis unstableand run- ing.First,thereis littleevidence thatfemale
away increasespreferenceand themale trait preferenceis not subject to selection. Al-
indefinitely (or untilgeneticvariance is ex- though there are few unambiguous mea-
hausted).Curtsinger and Heisler(1989) have sures, many observations stronglysuggest
questioned this conclusion and highlighted thatcostlymate choice has evolved (review
the complexities found in diploid models Pomiankowski,1987). For example,choosy
withnon-additiveeffects. female sandflieshave to vigorouslyresist
In our view,Kirkpatrick'sconclusionsare unwantedmale matingattempts,a behavior
generally valid for haploid and diploid that reduces fertility at low densities (En-
models withoutmutationbias. Though the gelhardet al., 1989); femalesage grousedo
evolutionarydynamics in diploid models not mate withthe firstmale theyencounter
are more complex, especially due to over- but spend several days assessingmales, of-
dominant selection maintaining genetic ten at different leks,beforechoosinga mate
variation, it appears that stable equilibria (Bradburyand Gibson, 1983; Johnsonand
occur only when femalefitnessis at a max- Boyce, 1990) and femalewhiteibises seek-
imum. This contrastswith our demonstra- ing extra-paircopulations risk greaternest
tion, in a quantitativegenetic model with parasitismand predation(Frederick,1987).
mutationbias on the male trait,that there In each of these cases female mate prefer-
are stable equilibria at whichfemalefitness ences do not appear to have evolved to the
is not maximized. However, because Curt- least costlyform.Females could minimize
singerand Heisler's (1988) resultsand Kirk- time,energy,and predationrisksby,forex-
patrick's(1988) reanalysisare based on sim- ample, accepting the firstmale they en-
ulation alone, the possibilityremains that counter or by avoiding extra pair copula-
some parametervalues in diploid nonad- tions. But theydo not.

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 FISHER AND BIASED MUTATION 1429

Second,directselectionon femalepref- causeofexaggeration evenwhenchoicecar-

erencesradicallyalters the evolutionary riesa cost.
equilibriafoundin modelsof sexualselec- The importance ofmutationon thepre-
tion.Principally,thelineofequilibriais de- ferredmale traithas been sporadically al-
stroyedand it is replacedby a singleequi- luded to before(e.g., Parker,1983) and
librium. Thisresultholdswithbothviability clearlyanalyzedin a two locus modelby
andfecundity costsevenifthecostsofchoice Bulmer(1989b),thoughhedidnotconsider
areminute.Although thisfactwasacknowl- whether mutation biascouldsupportcostly
edgedearlyon (Lande, 1981), the impor- choice.We expectthatbiased mutationis
tance of choice costs overridingFisher's commonin nature.Bias is especiallylikely
runaway processhasonlyrecently beenfully in traitsthathave recently been subjectto
stated(Kirkpatrick, 1985; Pomiankowski, directionalselectionand evolvedcompli-
1987;Bulmer,1989b).Runawaycan cause catedstructures or exaggeration, as is true
transitory increasesin femalepreference ofmanysecondary sexualcharacters. Itmay
awayfromthefitness maximum, butat the also be thecase thatotherforcesact in a
evolutionaryequilibrium,female fitness similarfashionto biasedmutation. For in-
mustbe maximized.Thiscounter-intuitivestance,migration pressure mayhavebiased
resultappearstoshowthatFisherianmating effects ifthereis selectivediffusion ofpar-
advantages, via attractivesons,cannotoff- ticular phenotypes (SegerandTrivers, 1986).
set naturalselectionagainstchoice.It im- Another bias thatis important in sexualse-
plies that Fisher'srunawayprocessonly lectionis mutationbias on overallfitness.
causes stableexaggeration if femalepref- We haveexplicitly notconsidered thishere
erencesare not costlyat all. to allow clearanalysisof Fisher'sprocess
We have demonstrated thatthisconclu- distinct fromthe"handicap"principle. The
sion holdsonlyundertheparticular setof importance ofmutation bias on viability is
assumptions implicitin thestandardquan- consideredin thecompanionpaper(Iwasa
titativegeneticformula,Equation(1). An et al., 1991) wherewe also discusstherel-
important assumptionis thattheexpecta- ativeimportance ofthesetwoforcesin sex-
tionofvariousindependent suchas ual selection.
effects,
mutation and migration arezeroforall val-
ues of theaveragemale ornamentand fe- LrrERATuRE CrTED
male preference traits.If thisassumption ABRAMS,R., AND K. J. FREY. 1964. Variation in
holdsthentheonlyevolutionary equilibri- quantitativecharactersof oats (Avena sativa) after
various mutagentreatments.Crop Science 4:163-
um lies at thepointwherefemalefitness is 168.
maximized.However,ifthisassumption is ANDERSSON, M. B. 1986. Evolution of condition-de-
violatedthe standardformulais onlyan pendent sex ornaments and mating preferences:
approximation and theevolutionary equi- Sexual selectionbased on viabilitydifferences.
Evo-
libriummaynotmaximizefemalefitness. ARAK, lution 40:804-816.
A. 1983. Male-male competitionand mate
We have shownthatif thereis biased choice in anuran amphibians, p. 181-210. In P.
mutationon the male ornament,female Bateson(ed.), Mate Choice. CambridgeUniv. Press,
choicecan be costlyat equilibrium. Biased Cambridge,UK.
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scapes, geneticdistanceand the evolutionof quan-
ornamented males.Although theyare sub- titativecharacters.Genet. Res. Camb. 49:157-173.
ject to weakerviabilityselection,theseless BRADBURY,J. W., AND R. M. GIBSON. 1983. Leks
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