Cryptic Female Choice: Criteria for Establishing Female Sperm Choice

Author(s): T. R. Birkhead
Source: Evolution, Vol. 52, No. 4 (Aug., 1998), pp. 1212-1218
Published by: Society for the Study of Evolution
Stable URL: http://www.jstor.org/stable/2411251 .
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populationsof Drosophila.I. Heat resistanceand geographical WESTERMAN,J.M., AND P. A. PARSONS. 1973. Variationin genetic
variation in Drosophila melanogaster and Drosophila simulans.

architecture at differentdoses of g-radiation as measured by

Evolution15:1-14.
longevity in Drosophila melanogaster. Can. J. Genet. Cytol. 15:
TORO, J. E., AND L. I. PAREDES. 1996. Heritability
estimatesof
289-298.
larval shell lengthin theChileanblue musselMytiluschilensis, WOODS, R. E., M. J. HERCUS, AND A. A. HOFFMANN. 1998. Estiunderdifferent
fooddensities.Aquat.LivingResour.9:347-350.
matingthe heritability
of fluctuating
in fieldDroasymmetry
WADDINGTON, C. H. 1961. Geneticassimilation.Adv. Genet. 10:
sophila.Evolution52:816-824.
257-293.
WEIGENSBERG, I., AND D. A. ROFF. 1996. Naturalheritabilities:
can
they be reliably estimated in the laboratory? Evolution 50:2149-

2157.

Corresponding
Editor:T Markow

Evolution, 52(4), 1998, pp. 1212-1218

CRYPTIC FEMALE CHOICE: CRITERIA FOR ESTABLISHING FEMALE SPERM CHOICE

T. R. BIRKHEAD

Department of Animal and Plant Sciences, The Universityof Sheffield,SheffieldS1O 2TN, United Kingdom
E-mail: t.r.birkhead@sheffield.ac.uk

Abstract.-Inthispaper,I considerthecriterianecessaryto demonstrate

thepostcopulatory
abilityof femalesto favor
thespermof one conspecificmale overanother,
thatis, spermchoice.In practiceit is difficult
to distinguish
between
spermcompetition
and spermchoice,and spermchoice can be demonstrated
onlyif theeffectsof spermcompetition
can be controlled.Few studieshave used experimental
protocolsthatdo this,so evidenceforspermchoiceis limited.
Moreover,in thosestudiesin whichspermchoice occurs,it does so to avoid incompatiblegeneticcombinations
and
is therefore
unlikelyto resultin directionalsexual selection.
Key words.-Compatibiliy,
crypticfemalechoice,sexual selection,spermchoice,spermcompetition.
Received June13, 1997. AcceptedMarch 16, 1998.
When Darwin (1871) suggested thatsexual selection comprised intrasexual selection (usually mediated by male-male
competition) and intersexual selection (usually via female
choice), he considered only the behavioral processes taking
place prior to copulation. Subsequently, Parker (1970) recognized that males can also compete after copulation and
inseminationthroughspermcompetition.Sperm competition
is now acknowledged as a powerful selective force responsible forshaping many aspects of male reproductiveanatomy,
physiology, and behavior (Smith 1984; Birkhead and Parker
1997). The evolutionary significance of the female counterpart of sperm competition,postcopulatory female choice, is
less obvious. In this review I consider whetherthereis sound
evidence to supporta necessary componentof postcopulatory
female choice, namely,thatfemales can discriminatebetween
and differentiallyutilize the sperm of differentmales, a process I referto as "sperm choice."
The possibility thatfemales mightexertphysiological control over the probabilityof fertilizationby certain sperm has
been discussed for many years (Tyler 1948; Bedford 1965;
Cohen 1969; Lloyd 1979). Studies in which females are inseminated by males of a closely related species (heterospecific crosses) oftenresultin reduced fertilization,strongly
suggesting that females possess mechanisms to discriminate
between sperm from hetero- and conspecific males (Dobzhansky 1951; Hewitt et al. 1989; Bella et al. 1992; Robinson
et al. 1994). In some cases, the mechanism of heterospecific
sterilityis known: following heterospecificinseminationsbe-

tween certain Drosophila species oviposition is blocked, but

can be stimulatedby injecting females with the seminal fluid
(but no sperm) of conspecifc males (Fuyama 1983; reviewed
in Markow 1997). These studies indicate that at an interspecific level the ability of females to discriminate between
spermis oftenwell developed. Many fewerstudies,however,
have considered whetherfemales have the abilityto discriminate between the sperm of differentconspecific males.
Thornhill(1983, 1984) referredto any postcopulatoryability
of females to favor one (conspecific) male over another as
crypticfemale choice, describing themas "cryptic" because
these processes take place inside the female's body and cannot be observed directly.At that time, few behavioral ecologists attemptedto test the idea of cryptic female choice.
This is surprisinggiven the numberof studies thatwere then
underway on precopulatory female choice (see Andersson
1994). There were two probable reasons forthe apparentlack
of interest. First, just as had occurred with precopulatory
female choice, crypticfemale choice was considered to be a
less powerful and hence a less importantselective forcethan
sperm competition (e.g., Parker 1979, 1984). Second, the
study of crypticfemale choice required an understandingof
the mechanisms associated withinsemination,spermstorage,
and fertilization,which were areas few evolutionary biologists were trained to explore. More recently,an interestin
female perspectives (e.g., Lifjeld and Robertson 1992; Birkhead and M0ller 1993; Hunter et al. 1993) and a rekindling
of interestin mechanistic explanations for behavioral phe-

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1213

nomena(e.g., Krebs and Davies 1997) has helpedto bring currencewhenits existencehas notbeenproperly
confirmed
crypticfemalechoiceto theattention
ofbiologists(Eberhard in any species. Onlyif we are aware of whatdoes and does
1985, 1996). In addition,it is now clearthatmanymale and not constituteevidenceforspermchoice can we be confifemale reproductivetraitscoevolve (Eberhard1985; Rice dentlyidentify
its occurrence.
1996; Wiley 1997). Althoughthis does not necessarilyinThe criteriaforcrypticfemalechoicein generalhavebeen
clude crypticfemalechoice, themechanismsof spermuti- consideredby Thornhill(1983, 1984) and Eberhard(1996,
lizationwill undoubtedly
influencesexual conflictand may pp. 80-8 1) and are similarto thosedevisedforprecopulatory
playa rolein thecoevolutionofmaleandfemalereproductive femalechoicewhenthiswas in dispute(Halliday1983; Seartraits(Parker1979; Stockley1997a; Brownet al. 1997; Price cy andAndersson1986; Heisleretal. 1987;RyanandKeddy1997).
Hector 1992; Andersson1994; see also Eberhard1996, p.
Femalescan potentially
influencewhichmalesfather
their 81). AlthoughEberhard(1996,p. 80) acknowledgesthatmakoffspring
beforeor aftercopulation.Precopulatory
female ing a strongcase forcrypticfemalechoice is complex,he
choice is reasonablywell establishedbecause femalesof also assertsthatcrypticfemalechoice is widespread.In part
many species appear to exertconsiderableinfluenceover thisstemsfromthefactthathis definition
of crypticfemale
which males they copulate with (reviewedin Andersson choice (above) is broad and explicitlyincludessome pro1994). Postcopulatory
choicecan occureitherpriortoorafter cesses underfemalebehavioralcontrol(but not obviously
fertilization.Postfertilizationfemale choice can occur cryptic).For example,theextentto whicha femaleremates
thedifferential
abortionofembryos(e.g., Hull 1964; or ovipositsaftercopulatingwitha particularmale or how
through
Willsonand Burley1983) and/ordifferential
investment
in longsheallowsan externalspermatophore
toremainattached
offspring
(Willsonand Burley1983; Simmons1987; Burley (e.g., Simmons1986; Sakaluk and Eggert 1996) comprise
1988).
instancesof postcopulatory
behavioralcontrolby females.
The existenceof postcopulatoryprefertilization
female These cases appearto be well substantiated
and aretherefore
spermchoice is more controversial,
in part because, if it not an issue. In my opinionthe controversy
in the fieldof
occurs,it does so at the same timeas spermcompetition. crypticfemalechoice lies in whetherspermchoice occurs.
betweentheseprocessesis extremely
Distinguishing
difficult. I describethe main criteriathatmustbe met in orderto
Eberhard(1996) has identified
20 different
ways by which demonstrate
spermchoice by thesemeansand reconsidera
crypticfemalechoice may occur and has definedit thus: numberof the examplesthatpurportto show spermchoice
"Sexual selectionby crypticfemalechoice can resultfrom in thelightof thesecriteria.
a female-controlled
thatselectivelyfaprocessor structure
vors paternity
by conspecificmales witha particulartrait
CRITERIA
over thatof othersthatlack the traitwhenthe femalehas
Whena femaleis inseminated
by morethanone male,the
copulatedwithbothtypes" (Eberhard1996, p. 7). As Simcan be the consequenceof any combimonsandSiva-Jothy
(1998) havepointedout,postcopulatory resultingpaternity
differential
orfemale
abortion,
femalechoice can be eithersequentialor si- nationof: spermcompetition,
prefertilization
as an immultaneous.Whenchoice is sequential,a femaleis insemi- spermchoice.The existenceof spermcompetition
is well established(Parker
paternity
natedby one male but ejects (or neutralizes)all or mostof portantfactoraffecting
the mostplausibleway to demonhis spermpriorto copulatingwithanothermale. In thissit- 1984, 1998). Therefore,
uationthespermfromdifferent
malesare unlikelyto coexist stratetheoccurrenceof femalespermchoiceis to controlfor
abortionand spermcompetition.In some
in thefemalereproductive
tract,theycannotinteract
directly, both differential
abortioncan be accountedfor
and theycannotprovidethe femalewithan opportunity
to species, at least, differential
discriminate
betweenthem.However,it is stillfeasiblethat by recordingthe proportionof undevelopedeggs siredby
forsperm-competition
effectsis more
femalesmay discriminate
betweenmales or theirspermon each male.Controlling
debut can be achievedin particularexperimental
this basis (Janetos1980). The simultaneousoccurrenceof difficult
experiments
mainlyhavebeenconspermfromtwo (or more)males in thefemaletractis more signs.Sperm-competition
forfemalesto ductedin two ways. First,in birdsand mammals(in which
likelyto occur and providesthe opportunity
insemination
is possible)femalescanbe inseminated
choose betweenthespermof different
males (Simmonsand artificial
Siva-Jothy1998). The simultaneous
recognitionof and dis- just once witha mixtureof knownnumbersof spermfrom
crimination
betweenspermof different
males,eitheron the each oftwomales(e.g. Martinet al. 1974; Dziuk 1996). This
effects,
basis of themales' phenotypeor thatof theirspermconsti- designavoids thecomplexityof insemination-order
which oftenoccur when separateinseminationsare made
tutesspermchoice and is thefocusof thisreview.
In recentyears several studieshave claimed to provide (Birkheadand Biggins 1998). Second, the classical spermstudyconductedon insects,otherinvertebrates,
evidence for spermchoice. For example,the observations competition
thatfemalesofsomespeciespossessmorethana singlesperm and birdscompriseseach of severalfemalesbeing insemior storespermfromdifferent
males in dif- natedsequentiallyby a pair of males in a reciprocaldesign
storagestructure
ferentpartsof thereproductive
tracthave been takenas ev- such thatin halfthecases the spermof one male is insemandin theotherhalf,second(BoormanandParker
idence forspermchoice (referencesin Eberhard1996). Al- inatedfirst
of offwiththeoccurrence 1976; Birkheadand Biggins 1998). The proportion
thoughtheseobservationsare consistent
to
of spermchoice,theyare notsufficient
to demonstrate
it.By springfatheredby the firstand secondmale are referred
theirclaims,authorsmay misleadthe scientific as PI and P2, respectively(Boormanand Parker1976). Beoverstating
to believe thatspermchoice is a frequentoc- cause in manytaxa, especiallyinsectsand birds(Birkhead
community

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and Parker1997), the second or last insemination

fertilizes If individualfemalesshowsignificant
repeatability
in P2 valthemajorityof eggs,theoutcomeof sperm-competition
ex- ues thiswould be good evidencethatfemaleswereresponperimentsare oftenexpressedin termsof P2. Intermediate sible for some of the overall variancein P2. It mightbe
values of P2 are usuallyindicativeof spermmixingand ran- assumedthatto demonstrate
femalespermchoice only the
dom utilization,whereashighvalues of P2 indicatenonran- secondexperiment
is necessary.However,to identify
thedifdom utilizationof sperm(Simmonsand Siva-Jothy1998). ferencesbetweenmales (or theirsperm)thataccountforfeThe reciprocalexperimental
designallows one to establish male spermchoice it is also necessaryto be able to attribute
whetherordereffectsare symmetrical
foreach male in a pair variancein P2 to males,so bothexperiments
are required.
(BoormanandParker1976). Untilrecently
theresultsofmost
sperm-competition
studieswerepresented
as meanP2 values.
EXAMPLES
However,Lewis and Austad (1990) drew attentionto the
The examplespresented
herewereselectedfortworeasons:
considerablevariancethatexists aroundP2 values in such
(1)
in all cases the authorshave stronglyassertedthe exisstudiesand identified
a way in whichsome of thisvariance
could be attributed
to differences
betweeneithermales or tence of crypticfemalechoice, specifically,spermchoice;
females.In theirstudyof Tribolium
castaneumtheyallowed and (2) the studiesvaryconsiderablyin the qualityof evi11 male pairsto copulatein thesame sequenceeighttimes, denceused to supporttheclaimof spermchoice.This is not
review-thishas alreadybeen providedby
each timewitha different
virginfemale.UsingANOVA,they a comprehensive
Eberhard
(1996):
however,mycriteriaforacceptingtheexshowedthatP2 values weresignificantly
repeatableforparthanthose of
ticularmale pairs and that17.8% of thevariancein P2 was istence of spermchoice are more stringent
of
attributableto differencesamong male pairs. They also Eberhard(1996). My aim is to illustratethe difficulty
spermchoice and to establishto whatextent
showedthatafteraccountingforthismale effect,therewas demonstrating
a large errorvariance(among femalesand withinmales; thethreecriteriaabove have been met.
57.7%), whichencompassedseveralsourcesof variation,
inHumans
cludingthedifferential
use of spermby females.
The designof Lewis and Austad's(1990) studyprovides
Bakerand Bellis (1995) have assertedthatcrypticfemale
a usefulgeneralapproachforidentifying
thecriterianeces- choice is important
in humans.They proposethatfemales
saryto demonstrate
femalechoice of sperm.It mayalso be controlthepaternity
oftheiroffspring
thedifferential
through
possible to demonstrate
female spermchoice using other retention
of sperm.Theyreportedthatfemalesejectedfewer
methods,as in theunusualinstanceofBeroein whichfemale spermfollowingcopulationsin whichtheyexperiencedorspermchoice can be observeddirectly(see below). In stan- gasm close to the timeof male ejaculationthanfollowing
dard sperm-competition
experimentslike those described copulationsin whichtheydid notexperienceorgasm(Baker
above,threecriteria
mustbe mettodemonstrate
femalesperm and Bellis 1995, pp. 234-236). Althoughthisis consistent
choice. There mustbe variancein P2 (or, in the case of a withfemalespermchoice, because none of the criteriain
single mixed insemination,
variancethe proportionof off- Table 1 are met it does not constituteevidenceforsperm
springfathered
by one of themales), and some of thisvari- choice.
ance mustbe attributable
to bothfemalesand males.Attributingvariancetomaleswillusuallycompriseattributing
variChrysomelidBeetle, Chelymorphaalternans
ance to a pair of males, as in Lewis and Austad's (1990)
study,althoughmorecomplexexperimental
The male of thisbeetleis unusualin havingan extremely
designscould
attribute
varianceto individualmales. This,however,is be- long flagellumassociatedwithits penis(V. Rodriguez,cited
yondthe scope of thepresentpaper.
in Eberhard1996, p. 6). Duringcopulationtheflagellumis
By employingan experimental
designin whichthesame threadedup thefemale'slong and convolutedspermathecal
pairs of males inseminateseveral different
femalesor the ductand intotheampullaand occasionallyalso intothespersame femalesare inseminated
by theseveralpairs of males matheca.The male depositsa spermatophore
in thefemale's
(forexample,over different
breedingcycles), it shouldbe bursa,and spermmigratealong the flagellumup the sperpossible to attribute
some of thevariancein P2 to males or mathecalductto thespermatheca.
In sperm-competition
exfemales.For example,imaginean experimentlike thatof perimentsinvolvingtwo or threemales, the proportionof
Lewis and Austad's(1990) in whichseveralpairsof males offspring
siredby each male was correlatedwiththelength
each inseminatea numberofdifferent
females.Repeatability of his flagellum(Eberhard1996,p. 351). Eberhard(1996, p.
(Falconer1981; Lessells andBoag 1987) in P2 valuesamong 353) suggeststhatspermdumpingby femalesmay be the
femalesinseminatedby the same pair of males would con- mechanismresponsibleforthisdifferential
success.A higher
stitutegood evidencethatsome of the variancein P2 was proportionof femalesejected a drop of spermwhen they
attributable
to male pairs.Althoughit is also possiblein an copulatedwitha male whoseflagellumhad been experimenexperimental
designlike thatof Lewis and Austad's(1990) tallyshortened(87.5%) thanwhentheycopulatedwithconto estimatethe variancein P2 betweenfemalesand within trolmales (13.1%; see also Dickinson 1997, p. 177-178).
males,whichincludesthepossibilityoffemalespermchoice, Eberhard(1996, p. 6) interpreted
this as evidenceforthe
theproportion
estimating
of varianceattributable
to females preferential
use by femalesof spermfrommaleswithlonger
morepreciselyrequiresanotherexperiment.
This additional flagella.However,thereare alternativeexplanations:males
experiment
comprisesseveralfemaleseach inseminatedby witha longerflagellummaysimplybe moreefficient
at getseveraldifferent
pairsofmalesin successivebreedingcycles. tingtheirspermto thebestplace to achievefertilization
and/

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spermchoice meetthe criteriadefinedin the present

TABLE 1. The extentto whichvarious studiesclaimingto have demonstrated
evidence; + +, reasonableevidence; +, some evidence.
study.Qualityof evidence: + + +, good experimental
Criteria
1. Variance in P2

2. Variance in P2
due to female

3. Variance in P2
due to male

No data

No data

No data

Chelymorphaalternans

+++

No data

++

Scatophaga stercorarial

+++

see text

+++

Species

Humans
Homo sapiens
Chrysomelidbeetle
Yellow dungfly
Ascidian

Diplosoma listerianum

No data

Beroe ovata
Sand lizard

++

++

see text

++

No data

References

Baker and Bellis (1995)

V. Rodriguez, cited in Eberhard (1996)

Ward(1993, 1997); Simmonset al. (1996);

Otronenet al. (1997); Ward(1997)
Bishop (1996); Bishop et al. (1996);

J. D. D. Bishop,pers. comm.
Carr6and Sardet(1984); Carreet al.
(1991)

Lacerta agilis

+++

++

++

Olsson et al. (1994, 1996, 1997)

Callosobruchus maculatus

+++

++

++

Wilson et al. (1997)

Cowpea weevil

1Also referredto as Scathophaga (see Ward 1993, 1997).

moresperm(see also Dickinson1997;

ortheymayinseminate
thedata imply
1998). In summary,
Simmonsand Siva-Jothy
variancein P2 and suggestthatboth the femaleand male
(Table 1).
have some influenceoverpaternity
Yellow Dungfly,Scatophaga stercoraria

involvingtwomaleyelexperiments
In sperm-competition
low dungflies,variancein P2 occurs (Parkerand Simmons
to copulatefora fixed
1994). Afterallowingfemaledungflies
males, Ward(1993) foundthatretimewithtwo different
gardlessof copulationorder:(1) femalesstoredmoresperm
fromlargethansmallmales; (2) spermfromthetwo males
acrossthefemale'sthreespernonrandomly
weredistributed
mathecae;and (3) thelargermale fertilizedmoreeggs (see
also Otronenetal. 1997;Ward1998).Ward(1993) considered
used sperm
his resultsas evidencethatfemalespreferentially
fromlargemales.However,Simmonsetal. (1996) challenged
and showedby anotherempiricalstudyof
thisinterpretation
Scatophaga thatWard'sresultscould be equally or better
spermdisplacementrates: when
explainedby differential
larger males copulated second they displaced previously
storedspermmorerapidlythansmallermales. Simmonset
al. (1996) suggestedthatthis is largelya consequenceof
largermales havinglargerspermducts thatallow a faster
flowof sperm(see Table 1). When largermales copulated
first,theyreleased more sperm,fewerof whichwere displaced by the second,smallermale.
Ascidians and Flowering Plants

Nonrandomutilizationof spermhas been clearlydocua sessile,comentedin theascidian,Diplosomalisterianum,

(Bishop 1996; Bishop et
lonial, clonal, marinefilter-feeder
and releasessperm
al. 1996). Diplosomais a hermaphrodite
intothewater,fromwherespermaretakenup intotheoviduct
occurs.However,ifan
and fertilization
of a potentialpartner
individualtakesup spermfromits own clone,thespermdo
halfoftheoviduct.
thantheanterior
notprogressanyfurther

betweenthesperm
interaction
This suggestsan antagonistic
and theoviductthatservesas a block to selfing.The block
is not perfect,however,and occasionally(in isolatedcolonies) selfingdoes occur,but cell divisionin the zygoteis
abnormaland embryosare alwaysaborted(J.D. D. Bishop,
clones are
pers. comm.). In addition,spermfromdifferent
portionoftheoviduct,
sometimesalso blockedin theanterior
betweenclones (Bishop
apparentlydue to incompatibility
1996; Bishopet al. 1996). Because of itsbiology,Diplosoma
is notdirectlycomparablewiththeotherorganismsin Table
to determinewhetherDiplosoma
therefore
1. It is difficult
thecriteriain Table 1, butthereis someevidencethat
fulfills
all are met.However,thecase of Diplosomaraisestheissue
forunrelatedsperm
thistypeoffemalepreference
ofwhether
constitutesclassical, directionalsexual selection(Darwin
below (Discussion).
1871). This issue is consideredfurther
on femalepollenchoice
A verysimilareffectofrelatedness
plants(reviewedin WillsonandBuralso occursin flowering
female
ley 1983; Delph and Havens 1998). Postpollination
choicevia theeffectof thestigmapollen-tubegrowthis well
combinations
(e.g., self)resultin
documented:incompatible
of thepollentube.Moreover,pollenreducedor nongrowth
tube growthhas been shown,at least in some species, to
betweenthepollenand theferequiregeneticcompatibility
maletissue.In addition,severalstudieshaveshowna positive
correlationbetweendegreeof pollen competitionand offbetweenthepollenfrom
springvigor,so thatdiscriminating
different
males enhancesfemalefitness(Willsonand Burley
1983; Delph and Havens 1998).
Beroe ovata

examplesof whatmightconOne of themostintriguing

stitutespermchoice occurs in the ctenophoreBeroe ovata
(Carre and Sardet 1984; Carre et al. 1991). This studyis
uniquein thatfemalespermchoicecan be observeddirectly.
eggs of Beroe revealedthat
Examinationof thetransparent
and
theovum(polyspermy)
severalspermtypicallypenetrate

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thatthe femalepronucleusthenmoves aroundwithinthe

ovum to each of the male pronucleiin turnbeforefusing
withone of them.The authorsstatethatthebehaviorof the
femalepronucleuslooks like matechoice. Otherthanknowing thatthe femalepronucleushas an active role in fertilization and thatthis "choice" is not to avoid selfing(the
blockto selfingoccursat theegg envelope;Carreetal. 1991),
thereis no otherrelevantinformation
(Table 1).
Reptiles

tad's (1990) in theirstudyof paternityin Callosobruchus

maculatus.Eady (1994) had previouslyshownthatwhentwo
male C. maculatuscopulatedwitha singlefemale,P2 values
variedbetweenzero and one. Wilsonet al. (1997) thendesignedan experiment
to determine
howmuchofthevariance
in P2 was attributable
to femalesaftercontrolling
formale
effects.This was achievedby comparingtherepeatability
of
P2 whenthesame two males copulatedwiththreeunrelated
femalesand withthreefull sisters.The repeatability
of P2
was relatively low (r = 0.05-0.55) and nonsignificantwith

unrelatedfemales,but it was bothhigher(r = 0.82-0.90)

In the sand lizard,Lacerta agilis, femalesroutinelyand
and significant
betweensisters,indicatinga strongfemale
indiscriminately
copulate with several males. Further,feeffectandthatfemalespermchoicehas a geneticbasis (Table
malesthatcopulatewithseveralmalesexhibitgreaterhatch1). Wilsonet al. (1997) also observedrepeatability
of male
ing success,lowerincidenceofdeformities
amongoffspring,
effectsin one of theirtwoexperiments.
Therefore,
thisstudy
and enhancedsurvivalof free-living
as compared
offspring
fulfillsall threecriteriain Table 1. However,Wilson et al.
withfemalesthatcopulatewithonly a singlemale (Olsson
(1997) wereunableto identify
anymale characters
on which
et al. 1994, 1996). Sperm-competition
in which
experiments
femalesmightbase theirchoice of sperm,and suggestthat
femaleswere inseminatedby two males revealedthatthe
fertilization
success in thisspecies is a consequenceof gamale geneticallymore similarto the female(estimatedvia
or sperm-female
metecompatibility
compatibility.
DNA fingerprinting)
siredfeweroffspring.
Arranged
matings
confirmed
thatthosebetweenrelativesproducedfeweroffDISCUSSION
spring.It was concludedthatfollowinginseminations
bytwo
males, femalesdifferentially
use the spermfromthe lessThisreviewraisestwofundamental
questions:Does sperm
relatedmale.Male effects
wereminimized(butnotrigorously choiceexist,and,ifit exists,does it lead to sexualselection?
controlled)by takingintoaccountnumbersof sperm(albeit
The evidenceforspermchoice remainslimitedand few
via malesize andhencetestesmass) andtimesince publishedstudiesfulfilall the necessarycriteria(Table 1).
indirectly,
the last ejaculation.Neitherof thesefactorsexplainedany In addition,somecarefullyconductedstudieshave foundno
of thevariancein male fertilization
success,thusreinforcing evidence for sperm choice (Cunningham1997; Stockley
the conclusionthatspermchoice occurs.The resultscould 1997b).The mostimportant
resultto emergefromthisreview
also be explainedby differential
buta sub- is thatthefew studiesin Table 1 thatprovideevidencefor
zygotemortality,
sequentanalysis(Olsson et al. 1997) showedthatthiswas spermchoiceindicatenotthatspermchoicefavorsgenerally
notthecase. Althoughthestudyby Olsson et al. (1996) did attractive
males or theirsperm,but thatthe selectivebasis
not establishwhethertherewas repeatability
of P2 effects for spermchoice favorsspermof particulargenotypesto
across eithermale or females,this studyprovidessome of avoid selfingor otherincompatiblegeneticcombinations.
thebest evidenceto date forspermchoice (Table 1).
thatfemaleorganisms
This is consistentwiththehypothesis
Similar,althoughless comprehensive,
resultswere ob- minimizethe riskof a geneticallyincompatiblepartnerby
tainedby Madsen et al. (1992) in anotherreptile,theadder acceptingspermor pollen fromseveraldifferent
males folwithsev- lowed by thedifferential
Viperusberus:femalescopulatedindiscriminately
utilizationof thesegametesor diferal males, and the morepartnersa femalehad, the lower ferentialabortionof zygotesmade up of incompatiblegethelevel ofmortality
in her notypes(WillsonandBurley1983; Zeh andZeh 1996, 1997).
andmorphological
abnormalities
Madsen et al. (1992) suggestedthatthisoccurred Thereis abundantevidencethatdifferent
offspring.
individualsmaybe
because the qualityof males or theirspermdiffered,and geneticallyincompatible,
and thatfailureto avoid suchcommultiplematingby femalesensuredthattheywerefertilized binationscan reducethefitnessof bothpartners
(Zimmering
by thebest-quality
sperm.
and Fowler 1968; Bateson,1983).Incompatibility
mayarise
BothMadsenet al.'s (1992) populationof addersand Ols- frompartnersthatare eithergeneticallytoo similaror too
son et al.'s (1996) populationof sand lizardsare small and dissimilarfromone's self (Bateson 1983; Thornhill,1993).
isolatedwitha relativelyhighdegreeof inbreeding.
A study For example,in Drosophilamojavensisfollowingone genof a less-isolatedpopulationof adders foundthata much erationof sib mating,femalesinseminated
usuby a brother
smallerproportion
of femalescopulatedwithmorethanone ally failedto lay any eggs, despitepossessingan abundant
male and thatthosethatdid failedto show any greateroff- supplyof motilesperm(Markow 1982). This suggeststhat,
springviability(Capula and Luiselli 1994). This suggests just as in some heterospecific
Drosophila studies(above),
thattheresultsof Madsen et al. and Olsson et al. mayhave
and
femaleD. mojavensisare able to differentially
transport
been a consequenceof theirinbredstudypopulations,and
relatedness.Sperm
utilize spermfrommales of different
thatfemaleaddersmaycopulatewithmultiplepartners
main- choice
may be the mostappropriateformof femalechoice
ly whenit is advantageousto do so.
in at least threesituations.First,wherefemalesare unable
to exertany precopulatory
choice,whichoccurswhenthey
Cowpea Weevil, Callosobruchus maculatus
areforcibly
inseminated
(BirkheadandParker1997). Second,
Wilsonet al. (1997) used an experimental
designthatwas if individualsdo not have behavioralmechanismsfor sesimilarto butsomewhatmoreelaboratethanLewis andAus- lectinga compatiblepartner,
especiallyif theirlife-history

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featuresare such thatthe probabilityof being inseminated

male) is high(e.g., Olsby a relative(or otherinappropriate
son et al. 1996; Markow1997). Third,in sessile organisms,
such as ascidians and plants,therecan be no behavioral
spermchoiceandthepostchoiceofmalegametes;therefore,
abortionmaybe especially
processofdifferential
fertilization
(Wirtz1997) and may explainthe moreobvious
important
natureof theseformsof femalechoice in thesetaxa (Table

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Editor:E. Ketterson
Corresponding

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