Evolution of Condition-Dependent Sex Ornaments and Mating Preferences: Sexual Selection Based on Viability Differences Author(s): Malte Andersson

Source: Evolution, Vol. 40, No. 4 (Jul., 1986), pp. 804-816 Published by: Society for the Study of Evolution Stable URL: http://www.jstor.org/stable/2408465 . Accessed: 30/05/2013 10:20
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Evolution, 40(4), 1986, pp. 804-816

EVOLUTION OF CONDITION-DEPENDENT SEX ORNAMENTS AND MATING PREFERENCES: SEXUAL SELECTION BASED ON VIABILITY DIFFERENCES
Department ofZoology, University P.O. Box 25059,40031 Gothenburg, ofGothenburg, Sweden
Abstract. -The possibilitythat the evolution of matingpreferences and secondarysex traitscan be based on heritabledifferences in viabilityis examined witha three-locus model. Earliergenetic models suggested thatviability-based processesalone cannot explain the evolution of mate choice and sex ornamentsthat reduce survival; a Fisherian mating advantage seemed necessary.The presentmodel is based on a monogamous matingsystemthatprecludessuch a matingadvantage. A keyassumptionis thatornamentdevelopmentdepends on thephenotypic conditionand overall ofthe possessor; thereis evidence thatsecondarysex traitsoftenmirror genotype nutritional status and health,sometimesthrough hormonalmediation.Ornamentand preference can thenhitchhike slowlyto high frequency with alleles that confera slightsurvival advantage, provided that such alleles become available oftenenough. The evolution of mating preferences and secondary sex traits thatreflect overallgenotypic constitution therefore can be based solelyon viability differences, no Fisherianmatingadvantage beingrequired.In practice,theseand several othermechanismsof sexual selectionmay occur together. Received September9, 1985. Accepted February13, 1986
MALTE ANDERSSON

Conspicuous secondarysex traitssuch as brightcolors, featherplumes, and mating calls present a challenging evolutionary problem,as theymay reducethe chances of survival (Burk, 1982). Darwin (1871) suggested that sex ornamentsevolve through matingpreferences in theothersex; he gave much evidence that preferences exist, but he did not explain why. Fisher (1930) outlined how a preference mightevolve: a new male traitwitha slightsurvival advantage happens to be preferred by some females. The alleles forthe male traitand thefemale preference become associated in their offspringand spread owing to the bettersurvival of sons possessing the trait. As the spreads,males withthe sex trait preference in addition gain a matingadvantage. Trait and preference thenevolve further untilthe traitbecomes so extreme thatreducedmale survivalbalances the matingadvantage. The logical consistencyof the Fisherian process has been demonstratedin genetic models by O'Donald (summarized, 1980), Lande (1981), Kirkpatrick (1982), and Heisler (1984). Its neatnessand plausibility need not imply,however,thatit is the only or the main way in which mating preferences evolve (Andersson, 1986). For instance,an initial survival advantage of the male traitis not required;pleiotropyor geneticdrift mightgive rise to the preference

(Emlen, 1973; Lande, 1981; Kirkpatrick, 1982), and thereare otherpossible mechanisms (e.g., Ghiselin, 1974; Halliday, 1978). One alternative is thatpreferences evolve because they make it possible to choose a mate of high geneticquality, the selective benefit not beinga Fisherianmatingadvantage for ornamented sons, but improved health and survival for offspring of both sexes. This idea was mentioned byWilliams (1966; but see 1975); othershave added to it (Trivers, 1972; Emlen, 1973; Zahavi, 1975, 1977; Bell, 1978; Eshel, 1978; Borgia, 1979; West-Eberhard,1979; Endler, 1980; Thornhill,1980; Andersson, 1982a; Hamilton and Zuk, 1982; Motro, 1982; Dominey,1983; Heisler,1984; Kodric-Brown and Brown, 1984; Nur and Hasson, 1984). The hypothesis, in particular the "handicap principle" of Zahavi (1975), has been severelycriticized;fora clarifying review see MaynardSmith(1985). In its originalform, theprincipledid notworkin geneticmodels assuming realisticviabilities,as the son of an ornamented male inherits not onlygenes for high survival but also the ornament whichreducessurvival.On balance thereis no net advantage fora female that prefers ornamentedmales (e.g., Davis and O'Donald, 1976; Maynard Smith, 1976, 1978). Maynard Smith(1976) suggested thatsome

804

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changein the assumptionsmightmake the A processbased onlyon viability differences processwork.Othergeneticmodels also in- can suffice, but in practice it may work in dicated thatviabilitydifferences do not suf- concertwith several othermechanisms. fice; combined with the Fisherian mechaGENETIC MODEL nism, however, they can enhance sexual Structure and Assumptions selection if the ornamentreduces survival more in low than in highqualitygenotypes Whethera condition-dependent trait in (Andersson,1982a, 1986). males (to take the most commonly ornaExcept fora brieftreatment by Maynard mentedsex) can evolve by matechoice more Smith(1985), no previousfew-locusmodel easily than a rigid traitis explored with a has dealt with a condition-dependent or- haploid three-locusmodel modified from nament,the expressionof which increases that of Maynard Smith (1976, 1978) and with the phenotypiccondition of the pos- Bell (1978). The essential mechanism that sessor. The presentmodel, which was de- bringsthe traitand the preference to high veloped independently of that of Maynard frequencies in a Fisherianprocessis theimSmith (1985), correspondsto an additive provedmatingsuccessofornamented males versionofhis case 1(c). The main difference thatarises as thefemalepreference spreads. is that,like Bell (1978) and Maynard Smith Such an advantage requiresthatornament(1978), I use a monogamous breedingsys- ed males mate withmore (or more fecund) tem to eliminate the possibilityof a Fish- femalesthan do cryptic males. To examine erian matingadvantage. The purpose is to a viability-basedmechanismisolated from explore whether sex ornaments: 1) can theFisherianprocess,Bell (1978), Maynard evolve througha process based purely on Smith (1978), and Andersson (1982a) viabilitydifferences, withoutdifferences in therefore modeled a monogamous system reproductive success;and, 2) are morelikely in whichall surviving males paired and got to evolve if they reflect general genotypic the same number of offspring. This apand phenotypiccondition than if theyde- proach,which is also used here,eliminates pend onlyon special trait loci. The idea that the possibilitythat the male trait spreads ornamentsare expressed in proportionto for reasons of mating success ratherthan phenotypic condition was mentioned by viability. Williams (1966, 1978), Zahavi (1977), and The main difference in assumptionshere Halliday (1978); it was developed further is that the ornamentdepends on the pheby Borgia (1979), West-Eberhard(1979), notypic conditionofthemale, whichin turn Andersson (1982a), Hamilton and Zuk is relatedto his overallgeneticconstitution. (1982), Parker (1982), Dominey (1983), The developmentof many sex traitsseems Kodric-Brownand Brown (1984), and Nur to depend on environment, genotype,and and Hasson (1984). Empiricalsupportis re- genotype-environmentinteractions, meviewed in the discussion.It is also assumed diated by physiological mechanisms that in conditionreflect thatdifferences heritable governgrowth priorities among organs(Anvariation and thatsome females genetic have dersson,1982a; Kodric-Brownand Brown, a geneticpreference forornamentedmales 1984; see Discussion below). To facilitate (these assumptions are discussed, for ex- analysis, I disregardenvironmentaleffects ample, by Lande, 1981; Andersson, 1982a; and assume that the heritablepart of the Hamilton and Zuk, 1982; Arnold, 1983; variationin phenotypiccondition depends Partridge, 1983; Heisler, 1984; Maynard on a singlelocus. This permitscomparison Smith, 1985). witha sex traitthatdepends onlyon alleles The model shows that alleles coding for at a traitlocus, not on otheraspects of the theornament and themating can genotype (Maynard Smith, 1976, 1978, preference hitchhike to highfrequency withgenes that 1985; Bell, 1978; Andersson, 1982a). confera slightsurvival advantage, if such The population is infinite, with discrete genes arise oftenenough. The monogamy generations, and a sex ratio of 1:1 at birth. model precludesa Fisherianmatingadvan- Locus 1 determinesthe facultyto develop tage, which thus is not necessary for sex the ornament.Males with allele a (of freornaments and mating to evolve. quency 1 - p) are always cryptic, preferences whereas

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806
TABLE

MALTE ANDERSSON 1. Genotypeviabilities(survival to reproductive age).

. Males A (facultative ornament*) a (all cryptic) Females A ora (all cryptic)

B (high viability) b (low viability)

a + a +

a + a +

a + a +

* The ornamentis expressedonly in highviability(AB) males.

males withallele A (of frequency p) develop theornament ifand onlyiftheyalso possess allele B (of frequency q) at locus 2. Allele B improvesphenotypic conditionand viabilityin bothsexes comparedto itsalternative, b. Ab males do not develop enough of an ornament forit to raise theirmortality over that of a males, nor for females to distinguishAb from a males. All femalesare cryptic. Locus 3 determinesthe matingpreference: femalescarrying allele C (of frequency r) preferornamented(AB) males, whereas c females choose mates at random among all males remainingafterC females have made their choices. If there are fewerornamented males than C females,the C females without an AB male also choose mates at random among those remaining. The threeloci recombinefreely (recombination = 0.5). These assumptions fractions are used to make possible comparisons with previous similar models(MaynardSmith,1976, 1978; Bell, 1978; Andersson, 1982a). For the same reason,the preference is assumed not to affect the viabilityof the female in the first version of the model below. A selective cost for the preference is explored further on. Withone exception, theviabilities(probabilities of survivingto reproductiveage) are as in Bell's (1978 p. 873) additive fitness scheme (Table 1): a is the "baseline" survival, ,Bis the reductionin survival caused by the ornament (expressed in AB males only),and E is the increase in survival conferred by the B allele. The viabilities must E < 1, and b) 0 ' be such that:a) 0 ?< a, ,B, a + ,B+ E < 1. The exceptionfromBell's scheme is that Ab males, which have the facultyfor developing the sex trait (allele A), do not develop it as theyalso carrythe low quality (b) allele at locus 2. Ab males therefore have the same viability(a + ,B)as do ab males. (In Bell's study,Ab males develop the ornamentand hence surviveonly

withprobability a.) All femalesobtaininga mate are equally fecund.The previous viabilityschedulecan be cast in more general terms (Maynard Smith, 1976, 1985; Bell, pers. comm.), but Table 1978; Kirkpatrick, forthe presentpurpose. 1 should suffice alThe model is used to explorewhether leles A (coding forthe condition-dependent can inornament)and C (the preference) crease fromlow frequencyin the population. Allele B is also introducedat low frequency, correspondingto a mutation or or a change in the environimmigration, ment makinga previouslyrare allele beneficial. Selection During theFirst Generation Assuming the population is in linkage with,theconditionsfor equilibriumto start allele to increase from the the preference can be derived first to thesecond generation (see Bell, 1978). The preference analytically is spreads if the mean survival of offspring higherfor a C female matingwith an ornamented (AB) male than fora nondiscrisurvivalfrom (c) female.Offspring minating matingsbetweenAB, Ab, aB, and ab males and femalesare derivedin analogywithBell (1978 pp. 873-874). The resultis summarized in Table 2; details are given in the Appendix. A sufficient condition forthe preference allele C to increase is that both B and b of highermean viafemalesbear offspring males (AB) ifmating withornamented bility than if matingwith crypticmales (Ab, aB, or ab). When the frequencyof allele A is males are of typeab low, almost all cryptic or aB (a feware of typeAb). It thensuffices to show under which conditions mean offfrommatingswith viabilityis higher spring ab AB males thanfromcryptic ornamented or aB males. This is done below forthetwo typesof females. B females.-From Table 2, the condition

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AB fathers foroffspring from to have higher matingwith ab males carrythe A or B alviabilitythan offspring from a fathersre- leles. Hence, foran ab female to have offspringthat survive betterif theirfatheris duces to AB thanifhe is ab requiresthat3E/8+ (E > (a) ,)/8 > 0, which reduces to (2b). 2(1 qa) Conditions(1a)-(2b) are lax compared to whereqa is the frequency of allele B among the correspondingexpression (3) of Bell a males after survivalselection(see Appen- (1978). In his case, it is necessarythat E be dix). If q, and hencealso qa, are much small- muchgreater than,B forthepreference allele er than 1, the conditionsimplifies to to increase.The present result therefore suggeststhata femalepreference is more likely > r (ib) to evolve for a condition-dependent male 2 traitthanfora condition-independent trait. Expression(lb) can be intuitively explained Expressions(1a)-(2b) concernthe female as follows.When alleles A and B are rare, preference; theydo not implythatthe male most B females are of genotypeaB. Con- traitis also selectedto higherfrequency. If sidertheoffspring frommatings betweenaB thereis initiallinkageequilibrium,allele A females and AB males. All such offspring willalwaysdecreasebetween generations one inheritthe B allele and hence have a sur- and two because AB males surviveless well vival advantage E (compared to carriersof than aB males, and Ab and ab males have the b allele). One quarter of the offspring, equal viability.Further, (1a)-(2b) are based AB sons, develop the ornamentwhich re- onlyon whathappens betweenthe first two duces viability by the amount ,B. On the generations; analyticalresultscannotbe deotherhand, aB femalesmatingwithcryptic rived forlater stages,as linkagedisequilibmales (almost all of which are ab) bear off- rium develops among the threeloci. Simspringhalf of which carrythe B allele with ulations (based on a modifiedversion of a advantage e; none develops the ornament. computerprogramgenerouslysupplied by Thus, foran aB femaleto have offspring of John Maynard Smith) are therefore used highermean viabilityif she mates with an next to follow long-term changes in allele AB ratherthan an ab male requires that frequencies. 3E/4+ (E -,B)/4 > e/2,which reduces to Later Generations: Simulations condition(lb). bfemales.-The conditioncorresponding The initialfrequencies of the eightdifferto (la) forb femalesis obtained fromTable ent zygotegenotypesare assumed to be in 2 as linkage equilibrium, calculated from the starting frequencies po, q0, and roof alleles >(2a) A, B and C. Genotypefrequencies foradult 4(1 qa) males and femalespriorto breedingare obIf q, and hence also qa, are much smaller tained by application of the viabilities in than 1, this simplifies to Table 1. The relativefrequencies of the different typesof matingsare then calculated > -, e (2b) withthe monogamymatingrulesdescribed 4, of matabove, whichyieldsthefrequencies which can also be explained intuitively as ings shown in Table 3. The genotypefrefollows.When allelesA and B are rare,most quencies among the resultingzygotes are femalesare of genotype ab. The production thencomputedand used as inputvalues for ofsurviving from suchfemales offspring then the next generation.Changes in allele frelargelydetermineswhat happens to the al- quencies can thusbe followedfora desired lele frequencies. Half the offspring fromab numberof generations. femalesmatingwithAB males obtain the B Whether thepreference and theornament allele and have a survivaladvantage E.One will surpasstheirstarting should frequencies quarterof these carriersof the B allele, AB depend on the viabilityparameters(a, ,B,E, whichreduces Table 1) and the initial allele frequencies sons, develop the ornament, No offspring fromab females (po, q0, and ro). To explore the conditions viability by ,B.
-

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808
TABLE

MALTE ANDERSSON 2. Viabilities of progenyfrommatingsbetweenthe different genotypes.*

Male genotype AB (ornamented) Ab (cryptic) a + a (aB or ab) (cryptic)

Female genotype

B (AB or aB) b (Ab or ab)

a + a

E +l(34P)

f(

8 )

a + E((

f4 08

81

+ (-)a f(7-p)

a +()

* Means based on sons and daughters, calculated fromthe Appendix. As locus 3 (alleles C and c) does not affect it need not be considered viability, here.

under which A and C can increase when rare,the simulationsare startedwithpo, q0, and roat low frequencies.New alleles will usually not confer large survival advantages, so E is assumed to be much smaller than a, allele B raisingthe viabilityby at most a few percentcompared to the basic survivorship a. The survival cost ,Bof the ornament(expressed only in AB males) is assumed to be of somewhat smaller magnitude than E. Under certainconditions, itturns out that the alleles forthe condition-dependent ornament(A) and the preference (C) increase in frequencyabove their startingvalues (Figs. 1 and 2). The mechanismbehind the

increase seems to be as follows. C females thatpair withAB males obtain mates with the (initially rare) advantageous B allele. Their daughters and, if E is sufficiently large comparedto f,also theirsons survivebetter thanoffspring fromc mothers and b fathers; henceallele C spreads.The matings between C females and AB males couple together allele C withA and B in linkage disequilibria. Over thegenerations, AB males thereforetendto obtain C femalesthatalso carry the advantageous B allele, which becomes inherited byall offspring from suchmatings. More slowly, alleleA therefore also getscoupled with B in linkage disequilibrium.Alleles A and C, forthisreason,can hitchhike

TABLE 3. Frequencies ofmating types. The notation is as in Bell(1978 p. 875),with a few exceptions. r' is the frequency of allele C (preference) amongfemales after survival selection. In thepresent case where onlyAB malesdevelop theornament, it is necessary to distinguish between thefrequencies PB' ofAB malesand Pb' of Abmalesafter survival selection (thefrequency ofalleleA among malesis then p' = PB' + Pb'). The proportions of C females areassumed to be thesameamong thosefemales a mateas among obtaining those notdoingso. (With theviability schedule ofTable 1,females outnumber malesatthebreeding season; thedifference is minute with thevaluesofa, f and e usedin thisstudy.) Mating type v x d Frequency if r' >PB' if r' -PB'

C x AB

PB

r'

C x Ab C x a (B orb)
c x AB cxAb

(r' -PB) (r' -PB')

1 - PB'
- PB' -Pb' - PB'

PbI

0 (1 (1
' I' r) P1B PB' Pb'
-PB'

PB -r' Pb
1PB'

c x a (B orb)

Pb'

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Allele
frequq

plO3

.0002

1.3

ency
1.2

.01
1.1

.0005

.001

P
.001

r .0001.

..

1.0I

200

400

600

800

180

360

540

Generation
p of the facultative FIG. 2. Increase in frequency mortality costs A ornament(allele A) under different (indicated at the curves) for males that develop the ornament.Thepeak frequency as well as the number of generations duringwhichp > po increaseswithreduced mortality cost F. Other parametervalues and are as in Figure 1. starting frequencies

Changes in the frequencies of the male ornament (p), the allele conferring higher survival (q, allele B), and the female preference (r). Allele B goes to fixation; in the process it bringsalleles A and C to frequencies higher thantheirstarting values fora number of generations, beforetheyeventuallybeginto decline. Parametervalues are (a, 3, e) = (0.1, 0.0005, 0.002), and starting frequencies(po, qo, ro) = (0.001,
0.001, 0.0001).

FIG. 1.

Generation

to higherfrequencieswith allele B, which always increases. When B approaches fixation, however,A and C decline again as fromAB males no longerhave a offspring survivaladvantage, because mostmales then carrythe B allele. Continued increase of A and C requiresthatnew beneficialB alleles arise often enough (see below); otherwise the ornament,because of its survival disadvantage f, will be lost fromthe population. A preference allele C that does not reduce viabilitycan persist,but usually at reduced frequency. AllelesA and C depend not onlyon B for theirincrease,but also on each other.Without allele C, the process that couples A to B willnotoccur,and A cannotspread.Without allele A, there are no AB males for C femalesto mate with,and so C cannot get coupled to B and spread. The frequency p of the condition-dependent ornament (allele A) usually firstdefora numberofgenerations. creases slightly If e is large enough compared to 3, and if alleles B and C are nottoo common to begin

with,theremay followan increasein p and r,takingalleles A and C above theirstarting val(Fig. 1). Withtheparameter frequencies ues used here, the increase is slight.It is followedby a decline as allele B approaches withit is no longer fixation and hitchhiking possible. The largerE is compared to A,the reached by allele higherthe peak frequency A (Fig. 2); this also applies forallele C. allele C entailsno direct As thepreference selectioncost, r increasesfora wider range of conditions than does p, the preference spreadingmore rapidlythan the ornament (Fig. 1). Simulationsshow thatwhenp and q are small (most femalesthenbeing ab), r will increase if and only if e > f/4, as predicted by expression (2b). Also, when the frequency starting qo of allele B is large,the predictedrelationbetweenE and : forr to increaseis observed.For example,withqo = 0.5, b and B femalesare equally common, and qa - 0.5 (with the viabilities assumed here).The mean ofexpressions(1a) and (2a) thenpredictsthatr will increaseonly ifE > by simulations. 3f/4; this is confirmed To spread,allele A mustbecome increasingly coupledwithB. This can occurthrough fromC femalesmated with (BC) daughters

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810

MALTE ANDERSSON

AB males. Such daughters prefer AB males; p.103 this tends to associate alleles A, B, and C. p=5 1 1.20 / The coupling and hence the increase in p should be strongest when C femalesand AB males are equally common, i.e., when r pq, so that most C femalesget an AB male and vice versa; thisprediction is also borne 1.10 5 10'4 out. Because r rises fasterthan p, forp to increaseovermanygenerations requires that requiredgrowswith Po > ro;the difference reduced qo. If, however,rois much smaller than po and q0,thenp and rwillnotincrease, 1.00 2_5_10\ as mostAB males do not obtain C females. 100 200 300 400 500 Alleles A and C spread only because of theircouplingto the B allele. It is therefore G e ne ra t io n necessary thatqo notbe too large;otherwise, FIG. 3. Increase in frequency p of the facultative allele B will become fixedtoo rapidly,mak- ornamentwhen the preference allele C leads to higher ing further increase in p and r impossible. riskof mortality forthe female.The mortality paramTheir fastestrise occurs roughlywhen the eter,uis indicatedat the curves.p in thiscase declines ifthereis no cost forthepreference, i.e., absolute rate of spread in B is highest(Fig. monotonically = 0 (not shown in the figure; see text).A moderate iftA 1). cost for the preference can, however, make p reach To summarize,the simulations confirm frequenciesgreaterthan po, as shown. When the cost the validity of conditions (1a)-(2b) and becomes too large, the increase in p again becomes demonstrate thatthepreference and the or- smaller (compare the curves with ,u = 5 x 10-4 and 5 x 10-5), and is preventedcompletelyby high costs nament can grow in frequency over many ,u.The other parametersare (a, 3, e) = (0.1, 0.0005, generationsif the ornament is condition- 0.002); startingfrequenciesare (po, qo, ro) = (0.001, dependentand develops in relation to the 0.001, 0.001). overallgenotype of the male. These conclusions are based on genotypic in differences viability ofonlya fewpercent, small enough AB males (PB'; Table 3). Such a cost can be to seem realistic.As the mating systemis modeled by eliminatinga fraction,ur'/pB' thefrequency monogamous and all males obtain equally from of C femalesat the matfecund theresult does notarisefrom ingseason; different females, magnitudes ofthemorin matingsuccessbut solelyfrom talityparameter,uwill be explored. (This differences in viability. differences assumption implies that, relative to c feFemale choice with a cost.-The com- males, C females have their survival remon assumption that mating preferences duced by a factor (l -r')( -,ur'/PB')/ carryno directselectivecost has been crit- [ 1-r'(1 - Ar'/pB')] owingto additional moricized by Parker (1983). Choice of a rare talitywhile searchingfora mate. This can typeof male likelytakestimeand energy or be shownto reduce theirrelativefrequency puts the femaleat higherriskof predation; by,gr'/pB', as required.) such costs mightmake the evolution of sex One effect ofthemortality cost is to lower ornamentsand preferences more difficult. the frequencyr of the preference allele C. To allow for a preference cost, assume This frequency usually does not exceed its thatthe choosy C femalessearchlongerfor starting value roif the cost parameter,uis a mate thando c femalesand thatthelonger of similarsize as the cost forthe ornament, search raises the risk of mortalitybefore d (and if po - qo - ro). A smaller cost for mating. This might apply for example in the preference can, however,make the prespeciesin whichmales advertisethemselves ferredtraitreach higherfrequency than it at territories or displaysitesforprospective would otherwise do (Fig. 3). The reason apmates. The extratime and energy required, pears to be as follows.As discussed, allele and hence the risk,should increasewiththe A increases most rapidly when AB males ofchoosyfemalesduring frequency themat- and C females are equally common, i.e., ing season (r') relativeto that of preferred when pq - r. If there is no cost for the

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is then Its frequency come close to fixation. value q0 again;p and setback to the starting p values whenthesimulation rremainat their ca is halted. The linkage disequilibriumDAC a / b/ .1 betweenalleles A and C in generationN is used in computingnew genotypefrequencies, assuming the "new" rare allele B to .01 occur randomlyin relationto the A and C loci to startwith. The programis then run again for N generations;the procedure is iteratedto show what happens to alleles A 5 4 3 2 1 and C in the long term(Fig. 4). thatan inThe simulationsdemonstrate Generation .10-4 from is poshigh frequency crease low to p of FIG. 4. Long-termincrease in the frequency the flexibleornament (allele A) when new advanta- sible for both the ornamentand the prefN generations. erence, geous B-alleles succeed each otherafter even withsmallgenotypic differences The three curves, each of which connects the allele in viability,and with initial gene frequenN, are based on the following at generation frequencies cies of magnitudesexpected formutations parameters(a, i, E): a (0.1, 0.001, 0.004), N = 250; b in finite natural populations. In curve c of (0.1, 0.0005, 0.002), N= 500; c (0.1, 0.00025, 0.001), N = 1,000. In all cases , = 0.1 ,I. Starting frequencies Figure4, the survivaladvantage,E,of allele are as in Figure 3. B is only 1% compared to the basic survicost d of the orvorship a; the mortality compared to the advantage of namentis 1/4 parameter,ufor allele C (,u= 0), it increasesfaster allele B, and the mortality preference is 1/lo the size ofthe mortality than the ornamentallele A, and r may rap- thepreference idly become much greaterthan pq, which cost forthe ornament. Only the increase of allele A is shown in spread of the ornament.If preventsfurther neverexceedspo withthe Figure 4; allele C, afteran initial decline, ,u= 0, p therefore A in frequency, witha lag defrequencies followsafter parametervalues and starting of Figure 3. With a cost forthe preference, pendent on the mortality parameter,u. of the orSustained growthin frequency r first declinesbelow however,its frequency requiresthatnew value ro.This permits pq to be- namentand thepreference the starting come largerrelativeto r and the ornament favorableB alleles arise oftenenough.With frequenallele A to increase more rapidly.A mod- the parametervalues and starting does not nec- cies of curve c in Figure 4, forp and r to cost therefore eratepreference it is enoughifnew B alleles essarilywork against the evolution of sec- keep increasing of overall genetic beginto spread within1,000 generations ondarysex traitsthatreflect each other.Such a low rateofestablishment it. quality,but may facilitate Long-term selection of ornament and in thegenomeforalleles witha relativesur-The previous results showed vival advantageofonly 1% maybe realistic. preference. that an ornament,as well as a preference, This suggeststhat selection based on herin overall condition differences fora numberof itable slight may increase in frequency forthe generations.Sustained increases can only and viabilitycan sometimessuffice and conoccur, however, if beneficial alleles with evolution of mating preferences even secondarysex traits, arise at other dition-dependent whichA and C can hitchhike mu- in the absence of a Fisherian mating adenough,forexample through loci often tation,temporalchangesin selection,or im- vantage forornamentedmales. migration. Whether such processes over DISCUSSION can permitornamentand manygenerations of Condition-Dependence to reach high frequenciesis expreference Sex Ornaments below. amined can be based The idea thatsexual selection To model the appearance of new favorofgenesthataffect able alleles, the simulationis halted aftera solelyon theinheritance without N, whenallele B has generalconditionand survivorship, numberofgenerations,

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in mating success, has not any differences been supported by earlier genetic models (e.g., Maynard Smith, 1976, 1985; Bell, 1986; Andersson,1986). 1978; Kirkpatrick, The presentresultsindicate,however,that if the preferred such a process may suffice is condition-dependent and mirrors sextrait and overallgeneticconstitution. phenotypic Mate choice based on such traitsshould not by the problemof negativecorbe affected relations among fitnesscomponents discussed, for example, by Maynard Smith (1985). Secondary sex traitsare expected to develop in relationto theconditionofthepossessor; theirgrowthcan be viewed as part of the reproductive effort(Andersson, 1982a), which oftenincreases in absolute termswith the nutritionalcondition (e.g., Askenmo, 1982, and referencestherein). growthof sex ornaCondition-dependent may be a consequence of ments,therefore, taxonomically widespread physiological of reprocessesthatgovernthepartitioning and repromaintenance, sourcesto growth, duction. One of the best documented exet al., amples is antlers(see Clutton-Brock 1982; Brown,1983; Goss, 1983); starvation has longbeen knownto reducetheirrelative size in red deer, Cervuselaphus. Compared to fossil skeletons from Scotland and red deer in otherpartsof Europe, Scottishdeer have smaller body size and relative antler of poor size. This is likelyto be an effect forScottishdeer released in New nutrition, grewantlersas one generation Zealand after large as those in fossil Scottishand extant mainland European populations. As deer became common in New Zealand, body and relativeantlersize was again reduced(Huxley, 1932). Other evidence comes fromthe nine-year study by Clutton-Brocket al. (1982); the size of antlersin juvenile as well in paras adult bucks declined drastically, of thepopulation.Captive allel withgrowth Scottishdeer fed ad libitumgrewas big as animals(Suttie,1980). Deer with continental supplementalfeed duringthe wintergrew antlersthana controlgroup;bothcatlarger egoriesshowed similarbody mass just after antlerproduction,so even fora given body antlersize affects mass,thelevel ofnutrition (Suttieand Kay, 1983 tables 3 and 4). Studiesofotherdeeralso pointto a strong

effect of nutrition on the relativegrowthof antlers(e.g., Magruderet al., 1957; Ullrey, 1983 table 2; reviewin Goss, 1983). Smith et al. (1983) found that nutritional conditionand antlerdevelopmentincreasedwith heterozygosity at seven electrophoretic loci, indicating thataspectsofthegenotype affect antlers throughphenotypic condition. In addition,thereis a moredirectgeneticcomin white-tailed ponentin antler size variation deer (Harmel, 1983), much of which may be based on a few loci (Templeton et al., 1983). It therefore seems thatantlersize in deer depends in parton special loci, in part on the phenotypic conditionof thebuck, as antassumed in thepresent model. Whether lersize directly affects femalechoiceofmates in deer is, however, uncertain (CluttonBrock, 1982). Evidence fromothergroupsalso suggests that secondary sex traits develop in proportion to the condition of the male and that theyhave low growthprioritiescomparedto otherorgans.For instance, thenuptial crestofmale newtsregresses rapidlyunder starvation (Champy, 1924). In male guppies, Poecilia reticulata,red or yellow carotenoidcolor spots raise the attractiveness of males to females;the brightness of such spots increases with the carotenoid contentsof the diet, and hence may reflect male food-finding ability (Endler, 1980, 1983; Kodric-Brown, 1985). Brightcarotenoid colors in birdsare also relatedto diet (e.g.,Ralph, 1969). The darknessofthedorsal plumage in male pied flycatchers, Ficedula hypoleuca,increases with nutritional condition(Slagsvold and Lifjeld,unpubl.). Hormonal regulation of secondary sex traitshas been found in many vertebrates (e.g., Vellano et al., 1970; Kimball and Erpino, 1971; Lofts and Murton, 1973; Fernald, 1976; Tanner, 1978). Hormone production depends on nutrition;animals in poor condition oftenhave lower levels of sex hormones(Wingfield, 1980), and probforthisreasondevelop relatively ablypartly smaller secondarysex traits.For example, comb size in red grouse cocks depends on the concentration of testosterone (Moss et al., 1979), as does the nuptial plumage in phalaropes (Johns,1964). The level of tesin turnis sensitiveto the plane of tosterone in birds and falls rapidly during nutrition

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CONDITION-DEPENDENT

SEX TRAITS

813

food shortage(Wingfield, 1980). The variation in secondarysex traitsamong males thus depends in part on variation in their phenotypic condition, but the extent to which such variationin conditionhas a geneticbasis is poorlyknownand needs to be studied. Assumptions and Comparison with OtherModels Does the male ornamentin the present sexual selection,that model evolve through is, owingto an advantagein competition for mates (Darwin, 1871)? In theDarwin-Fisher theory,ornamented males are favored because they mate with more females, or with highly fecund females. In the present model,ornamented males tendto matewith (BC) females that bear offspring of higher thanaverageviability; thefemalepreference allele (C) is required forthe male trait(A) to spread. This element of female choice and (indirect) competition for females of certaingenotypes the argues forclassifying process as sexual selection, even if in a different sense than usual. slightly The main differencebetween the assumptionshere and those of Bell (1978) is thathere the ornamentis expressedonly in high quality (AB) males, whereas in Bell's model it is expressedalso in Ab males. This difference has profoundeffects; the female preferenceallele (C) spreads much more that E > A/4, easily here. It is sufficient whereas E >? f is required in Bell's case. Moreover, the frequencyof the male ornamentneverexceedsitsinitiallevelin Bell's (1978) monogamy model, but here it can increasealso withrealistically small viability differences. With the present assumptions,continuedincreaserequires, however, that new alleles with a slightsurvival advantage become available within a few Ifnot,the hundredor thousandgenerations. ornament,aftera temporary increase, declines towards extinction. Its continued presence hence requires an input of beneficial alleles, for example through mutations, immigrationsor temporal fluctuations in selection. One possible source of in selectionis thetype temporalfluctuations of host-parasitecycle suggestedby Hamilton and Zuk (1982).

partAn increasein ornamentfrequency, ly due to hitchhiking with a high viability allele, occurredin an earliermodel of handicap selection combined with a Fisherian matingadvantage (Andersson, 1982a; also see Maynard Smith, 1985; Andersson, in assumptions 1986). The main differences are that, in the earlier model, the ornament was expressed in Ab as well as AB males, and it reduced survival by an additional amount in low viability(b) as com(B) males. Continued paredto highviability allelescan lead ofhighviability introduction increaseoftheornament also to a long-term in thatmodel (Andersson,unpubl.),but the requiredare muchmore viability differences extremeand unrealisticthan here. Condiof the ornamenttherefore tion-dependence likelyto enhance sexual seems particularly in viability. selectionbased on differences For computational convenience, the male expressionofthecondition-dependent model trait(coded byalleleA) in thepresent dependingon whetherthe was all-or-none, male also carrieda favorableallele (B) at a second locus. Variation in condition and in naturewilldepend on manyloci, viability and favorablenew alleles might appear anyfrom fewhere in the genome. Offspring males that prefer the largestsecondarysex traitsare likelyto accumulate such favorable alleles; they are also less likely than deleteriousalleles to inherit otheroffspring thatmayarise(Thornhill, 1980). This should and conmake the evolutionof preferences sex traitseasier than undition-dependent der the simplified assumptionsof the presentmodel. On theotherhand,morerealistic rules of mate choice (e.g., Maynard Smith, 1985; Seger,1985) mayworkin theopposite induced So may environmentally direction. quality,unless posvariationin phenotypic itively correlated with genotypic quality. Such correlations might, however, arise through genotype-environment interactions,whichseem likelyin manycases (Andersson,1982a; Kodric-Brownand Brown, 1984). If the expression of sex traits increases conwiththeoverallphenotypic and genetic for superdition of the male, a preference normaltraitsshould be favoredin females; the largerthe trait,the betterthe condition ofthemale (Andersson,1982b; Weldon and

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814

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ASKENMO,

C. 1982. Clutch size flexibility in the pied flycatcher Ficedula hypoleuca.Ardea 70:189-196. BELL, G. 1978. The handicap principlein sexual selection. Evolution 32:872-885. BOAKE, C. R. B. 1985. Geneticconsequences of mate choice: A quantitativegeneticmethod for testing sexual selectiontheory.Science 227:1061-1063. BORGIA, G. 1979. Sexual selectionand the evolution of matingsystems,pp. 19-80. In M. S. Blum and N. A. Blum (eds.), Sexual Selectionand Reproductive Competitionin Insects.Academic Press,N.Y. BROWN, R. D. (ed.) 1983. Antler Development in Cervidae. Caesar Kleberg Wildlife Res. Inst., Kingsville,TX. BURK, T. 1982. Evolutionarysignificance of predationon sexuallysignalling males. Florida Entomol. 65:90-104. CHAMPY, C. 1924. Sexualit6et Hormones. G. Doin, Paris, France. T. H. 1982. The functions CLUTTON-BROCK, of antlers. Behaviour 79:108-125. CLUTTON-BROCK, T. H., F. E. GuINNESS, AND S. D. ALBON. 1982. Red Deer. Behavior and Ecology of Two Sexes. Univ. Chicago Press, Chicago, IL. DARWIN, C. 1871. The Descent ofMan, and Selection in Relation to Sex. Murray,London. DAVIS, J. W. F., AND P. O'DONALD. 1976. Sexual selectionfora handicap: A criticalanalysis of Zahavi's model. J. Theoret. Biol. 57:345-354. DOMINEY, W. J. 1983. Sexual selection,additive genetic variance and the "phenotypichandicap." J. Theoret. Biol. 101:495-502. EMLEN, J. M. 1973. Ecology: An EvolutionaryApproach. Addison-Wesley,Reading, MA. ENDLER, J. A. 1980. Natural selectionon color patternsin Poecilia reticulata.Evolution 34:76-91. 1983. Natural and sexual selectionon color in poeciliidfishes. Envir.Biol. Fish. 9: 173patterns 190. ESHEL, I. 1978. On thehandicap principle-A critical defence.J. Theoret. Biol. 70:245-250. FERNALD, R. D. 1976. The effect of testosterone on ACKNOWLEDGMENTS the behavior and coloration of adult male cichlid I thankConny Askenmo,Mark Kirkpatfish (Haplochromis burtoni,Gunther). Hormone rick, Pekka Pamilo, Per Sundberg, Peter Res. 7:172-178. Taylor,and David Winklerforhelpfulsug- FISHER, R. 1930. The Genetical Theory of Natural Selection.Clarendon Press, Oxford,U.K. gestions on themanuscript, and Aino FalckGHISELIN, M. T. 1974. The Economy of Nature and Wahlstrom for drawing the figures.The theEvolutionofSex. Univ. CaliforniaPress,Berkewas supported study bytheSwedishNatural ley. FuncSciences Research Council, grantno. 4425- Goss, R. J. 1983. Deer Antlers:Regeneration, tion and Evolution. Academic Press, N.Y. 105. T. R. 1978. Sexual selection and mate HALLIDAY, choice, pp. 180-213. In J. R. Krebs and N. B. DaLITERATURE CITED vies (eds.), Behavioural Ecology. An Evolutionary ANDERSSON, M. 1982a. Sexual selection,naturalseApproach. Blackwell,Oxford,U.K. lection and quality advertisement.Biol. J. Linn. HAMILTON, W. D., AND M. ZUK. 1982. Heritabletrue Soc. 17:375-393. fitness and bright birds:A roleforparasites?Science * 1982b. Female choice selectsforextreme tail 218:384-387. lengthin a widowbird.Nature 299:818-820. HARMEL, D. E. 1983. Effects of genetics on antler * 1986. Sexual selection and the importance qualityand body size in white-tailed deer,pp. 339ofviability A reply.J.Theoret.Biol. In differences: 348. In R. D. Brown (ed.), AntlerDevelopment in press. Cervidae. Caesar Kleberg Wildlife Res. Inst., ARNOLD, S. J. 1983. Sexual selection:The interface Kingsville,TX. of theoryand empiricism, pp. 67-107. In P. Bate- HEISLER, I. L. 1984. A quantitative geneticmodel for son (ed.), Mate Choice. Cambridge Univ. Press, theorigin ofmating Evolution38:1283preferences. Cambridge,U.K. 1295.

Burghardt,1984). The Fisherian mechanism, on the otherhand, seems to favor a preference forsupernormal ornamentsonly duringthe runawaystage;when the process has come to rest,thepreference may be under symmetric selection(O'Donald, 1980). In an experimental study,widowbirdswith enlarged, supernormal tails attracted the most females,but further experimentsare requiredto clarify the mechanismin detail (Andersson, 1982b). Many secondarysex traitsare polygenic and show continuous variation; realistic modeling of such traitsrequires quantitative genetics (Lande, 1981). The present three-locus model does lend logical support, however,to the idea that sexual selection mightwork throughdifferences in overall genotypic constitution, mirrored by condition-dependentsex traitsthat reflect phenotypiccondition and survivorship.Since the starting and survivaldifferfrequencies ences seem realistically small, thispossibility should meritempirical testingtogether with Fisherian and other likely mechanisms,buildingforexample on approaches such as those ofPartridge (1980) and Boake (1985). The mechanismsare not mutually exclusive but may work in concert (Bell, 1978; Andersson, 1982a, 1986), which calls fora multiple-hypothesis approach in which the alternativesare considered toto estimatetheir gether relativeimportance.

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CONDITION-DEPENDENT J. S. 1932. Problems of Relative Growth. Methuen,London, U.K. 1964. Testosterone-inducednuptial JOHNS, J. E. in phalaropes. Condor 66:449-455. feathers 1971. Hormonal KIMBALL, F. A., AND M. J. ERPINO. sexual dimorphismin Scecontrolof pigmentary Gen. Comp. Endocrinol. 16: loporus occidentalis. 375-384. KIRKPATRICK, M. 1982. Sexual selectionand theevolution of femalechoice. Evolution 36:1-12. 1986. The handicap mechanism of sexual selection does not work. Amer. Natur. 127:222240. A. 1985. Female preferenceand KODRIc-BROWN, sexual selection for male coloration in the guppy Behav. Ecol. Sociobiol. 17:199(Poecilia reticulata). 205. A., AND J. H. BROWN. 1984. Truth KoDRIc-BRowN, in advertising: The kindsoftraitsfavoredby sexual selection.Amer. Natur. 124:309-323. LANDE, R. 1981. Models of speciation by sexual selection on polygenictraits.Proc. Nat. Acad. Sci. USA 78:3721-3725. 1973. Reproduction LoFrs, B., AND R. K. MURTON. in birds, pp. 1-107. In D. S. Famer, J. R. King, and K. C. Parkes (eds.), Avian Biology,Vol. 3. Academic Press, N.Y. MAGRUDER, N. D., C. E. FRENCH, L. C. McEWEN, AND of R. W. SwiFr. 1957. Nutritionalrequirements white-taileddeer for growthand antler development.II. Penn. State Univ. Agric.Exp. Stat.,UniPark, PA. versity MAYNARD SMITH, J. 1976. Sexual selectionand the handicap principle.J. Theoret. Biol. 57:239-242. 1978. The handicap principle-A comment. J. Theoret. Biol. 70:251-252. 1985. Sexual selection,handicaps and true fitness. J. Theoret. Biol. 115:1-8. Moss, R., H. H. KOLB, M. MARQUISS, A. WATSON, D. 1979. AgTRECA, D. WATT, AND W. GLENNIE. gressivenessand dominance in captive cock red grouse.AggressiveBehav. 5:59-84. MOTRO, U. 1982. The courtshiphandicap-PhenoJ. Theoret. Biol. 97:319-324. typiceffect. 1984. Phenotypic plasticity NUR, N., AND O. HASSON. and the handicap principle.J. Theoret. Biol. 110: 275-297. P. 1980. Genetic Models of Sexual SeO'DONALD, lection.Cambridge Univ. Press, Cambridge,U.K. evolutionPARKER, G. A. 1982. Phenotype-limited pp. 173-201. In King's Colarilystable strategies, Problemsin lege SociobiologyGroup (ed.), Current Sociobiology.CambridgeUniv. Press, Cambridge, U.K. 1983. Mate qualityand matingdecisions,pp. 141-164. In P. Bateson (ed.), Mate Choice. CambridgeUniv. Press, Cambridge,U.K. PARTRIDGE, L. 1980. Mate choice increases a comin fruit fitness flies.Nature 283: ponentof offspring 290-291. fit1983. Non-random matingand offspring ness,pp. 227-25 3. In P. Bateson (ed.), Mate Choice. CambridgeUniv. Press, Cambridge,U.K. RALPH, C. I. 1969. The control of color in birds. Amer. Zool. 9:521--530. geneticmodels forthe evoSEGER, J. 1985. Unifying lution of femalechoice. Evolution 39:1185-1193.
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Genetic variabilityand antlergrowthin a natural deer,pp. 365-388. In R. populationofwhite-tailed D. Brown (ed.), AntlerDevelopment in Cervidae. Caesar KlebergWildlifeRes. Inst.,Kingsville,TX. on growth J. M. 1980. Influenceof nutrition SUTTIE, ofcaptive red deer stags,pp. and sexual maturation 341-349. In E. Reimers, E. Gaare, and S. Skjenneberg (eds.), Proc. Sec. Int. Reindeer/Caribou forvilt Symp.,R0ros, Norway. 1979. Direktoratet Trondheim,Norway. og ferskvannsfisk, J.M., AND R. N. B. KAY. 1983. The influence SUTTIE, of antand photoperiodon the growth of nutrition lers of youngred deer, pp. 61-71. In R. D. Brown Developmentin Cervidae. Caesar Kle(ed.), Antler bergWildlifeRes. Inst., Kingsville,TX. TANNER, J. M. 1978. Foetus into Man: Physical Open Books, Conceptionto Maturity. Growthfrom London, U.K. D. DAJ. WILLIAMS, J. W., R. M. SHARP, TEMPLETON, AND S. WARvis, D. HARMEL, B. ARMSTRONG, DROUP. 1983. Single dominant major gene effect on the expression of antler point number in the white-taileddeer, p. 469. In R. D. Brown (ed.), AntlerDevelopment in Cervidae. Caesar Kleberg WildlifeRes. Inst., Kingsville,TX. R. 1980. Competitive,charmingmales THORNHILL, and choosy females:Was Darwin correct?Florida Entomol. 63:5-30. and sexual TRIVERS, R. L. 1972. Parentalinvestment selection, pp. 136-179. In B. Campbell (ed.), Sexual Selectionand the Descent of Man 1871-1971. Aldine, Chicago, IL. ULLREY,D. E. 1983. Nutritionand antlerdevelopdeer,pp. 49-59. In R. D. Brown mentin white-tailed Developmentin Cervidae. Caesar Kle(ed.), Antler bergWildlifeRes. Inst., Kingsville,TX. VELLANO, C., V. MAZZI, AND M. SACERDOTE. 1970. Tail height, a prolactin-dependent ambisexual characterin the newt (Trituruscristatuscarnifex Laur.). Gen. Comp. Endocrinol. 14:535-541. 1984. DeWELDON, P. J., AND G. M. BURGHARDT. ception divergenceand sexual selection. Z. Tierpsychol.65:89-102. M. J. 1979. Sexual selection,social WEST-EBERHARD, and evolution.Proc. Amer. Phil. Soc. competition, 123:222-234. WILLIAMS, G. C. 1966. Adaptation and Natural Selection: A Critique of Some CurrentEvolutionary Thought.PrincetonUniv. Press, Princeton,NJ. . 1975. Sex and Evolution. PrincetonUniv. NJ. Press, Princeton, 1978. Mysteriesof sex and recombination. Q. Rev. Biol. 53:287-289. WINGFIELD, J. C. 1980. Fine temporaladjustmentof pp. 367-389. In A. Epple functions, reproductive Acand M. H. Stetson(eds.), Avian Endocrinology. ademic Press, N.Y. ZAHAVI, A. 1975. Mate selection-A selectionfora handicap. J. Theoret. Biol. 53:205-214. remarks 1977. The cost of honesty(further on the handicap principle). J. Theoret. Biol. 67: 603-605. Editor: M. Uyenoyama Corresponding

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816

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APPENDIX

Calculation of offspring viabilitiesforthe first generationis explained in detail in Bell (1978 pp. 873-874). For example,the mean viabilityof all sons frommatingsbetweenB femalesand aB or ab males is obtained from the genotypeviabilitiesof Table 1, multipliedby the expected frequenciesof the different offspring genotypes fromthese types of parents.Expected frequenciesof offspring genotypesare obtained fromthe genotypefrequencies among adult males and females.A proportion p of the adult B femalesare of genotypeAB, and (1 of the B allele among adult a males is qa (see Bell, 1978 p. 873, forits p) are of genotypeaB. The frequency calculation). Since locus 3 (alleles C and c) does not affect viability,it need not be consideredhere. Viabilities frommatingsbetweenthe different of male and femaleoffspring genotypesare given in the table below.
genotype
Female

genotype

Male

Offspring viability Sons Daughters

B
B B

AR Ab aB orab
?'+e>(12

++i( a +2 + f+ )+/l[

2")
4

/2
(a2

c+ a

4P(

)? ?+2+1d
a + ,

b
b b

AB
Ab aB or ab
a +E

a +!+fl(3
a a +/3

"h)

( q)

+(

4 )p

>(a)

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