Mechanisms and Evidence of Genital Coevolution: The Roles of Natural Selection, Mate Choice ...

22 Pages·2015·1.88 MB·English

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Mechanisms and Evidence of Genital
Coevolution: The Roles of Natural Selection,
Mate Choice, and Sexual Conflict
PatriciaL.R.Brennan1,2andRichardO.Prum3
1DepartmentsofPsychologyandBiology,UniversityofMassachusetts,Amherst,MA01003
2OrganismicandEvolutionaryBiologyGraduateProgram,UniversityofMassachusetts,Amherst,MA01003
3DepartmentofEcologyandEvolutionaryBiologyandPeabodyMuseumofNaturalHistory,
YaleUniversity,NewHaven,CT06520
Correspondence:[email protected]
Genital coevolution between the sexes is expected to be common because of the direct
interaction between male and female genitalia during copulation. Here we review the
diverse mechanisms of genital coevolution that include natural selection, female mate
choice, male–male competition, and how their interactions generate sexual conflict that
canleadtosexuallyantagonisticcoevolution.Naturalselectionongenitalmorphologywill
resultinsizecoevolutiontoallowforcopulationtobemechanicallypossible,evenasother
featuresofgenitaliamayreflecttheactionofothermechanismsofselection.Genitalcoevo-
lutionisexplicitlypredictedbyatleastthreemechanismsofgenitalevolution:lockandkeyto
preventhybridization,femalechoice,andsexualconflict.Althoughsomegoodexamples
exist in support of each of these mechanisms, more data on quantitative female genital
variationandstudiesoffunctionalmorphologyduringcopulationareneededtounderstand
more general patterns. A combination of different approaches is required to continue to
advanceourunderstandingofgenitalcoevolution.Knowledgeoftheecologyandbehavior
ofthestudiedspeciescombinedwithfunctionalmorphology,quantitativemorphological
tools,experimentalmanipulation,andexperimentalevolutionhavebeenprovidedinthe
best-studiedspecies,allofwhichareinvertebrates.Therefore,attentiontovertebratesinany
oftheseareasisbadlyneeded.
Ofalltheevolutionaryinteractionsbetween shown to covary in many taxa (Sota and Ku-
the sexes, the mechanical interaction of bota1998;IlangoandLane2000;Arnqvistand
genitalia during copulation in species with in- Rowe 2002; Brennan et al. 2007; Ro¨nn et al.
ternal fertilization is perhaps the most direct. 2007; Kuntner et al. 2009; Tatarnic and Cassis
For this reason alone, coevolution between 2010; Cayetano et al. 2011; Evans et al. 2011,
genital morphologies of males and females is 2013;SimmonsandGarcı´a-Gonza´lez2011;Yas-
expected. Morphological and genetic compo- sin and Orgogozo 2013; and see examples in
nents of male and female genitalia have been Table1).
Editors:WilliamR.RiceandSergeyGavrilets
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P.L.R.BrennanandR.O.Prum
References SauderandHausdorf2009Kamedaetal.2009 Kuntneretal.2009 Huber1999 Burnsetal.2013 SotaandTanabe2010 WojcieszekandSimmons2012 Lautenschlageretal.2010 RobertsonandPaterson1982;McPeeketal.2009 ¨Ronnetal.2007 Gayetal.2011 Cayetanoetal.2011 Continued
systems Likelymechanism SACorfemalechoice Lockandkey SAC Femalechoice SAC MechanicalincompatibilityresultingfromIntersexualselectionLockandkey Naturalselectionagainstfluidloss,lockandkey,andsexualselection Lockandkeyviafemalesensorysystem SAC SAC SAC
el
centliteratureandmod Evidence omparativeamongspeciesharacterdisplacement omparativeamongspeciesomparative(nophylogeneticanalysis)omparativeamongspecies omparativeinspeciescomplex unctionalcopulatorymorphology wo-speciescomparison,shapecorrespondence unctionalmorphology,comparativeamongspecies omparativeamongspecies/ullsibhalfsibmatingexperiments xperimentalevolution
e C C C C C C F T F C F E
r
more and heca
oftaxawithemphasison Femalestructures Spermatophore-receivingorgansVaginalength Multiple Epigynalpockets Sclerotizedpregenitalbarriers Genitalsegmentsize Accesorylobeofthevulvadistalprojection Vulva,vagina,andspermat Abdominalshapeandsensoryhairs ThickenedwallsofcopulatoryductSusceptibilitytodamage Nocorrelatedresponse
y
et
olutionfoundinavari Malestructures Spermatophore-producingorgansPenislength Multiple Cheliceralapophysis Hardenedpenesandlossofnuptialgifts Gonopodsize Gonopodshapeandsize Gonopode Claspingappendages Spinyaedagus Damageinflicted Reducedspines
v
Table1.Examplesofcoe Taxa MollusksLandsnails(Xerocrassa)SatsumaArthropodsArachnids(Nephilidspiders)Pholcidaespiders Harvestmen(Opiliones)MillipedesParafontariatonominea Antichiropusvariabilis CrustaceanFiddlercrabs,Uca HexapodesOdonates InsectsColeoptera:seedbeetlesCallosobruchus:Callosobruchusmaculatus
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MechanismsofGenitalCoevolution
References SotaandKubota1998;Sasabietal.2010 ´SimmonsandGarcıa-´Gonzalez2011 Kamimura2012 YassinandOrgogozo2013 MaslyandKamimura2014Kotrbaetal.2014 ˜BricenoandEberhard2009a,bIlangoandLane2000 Carayon1966;MorrowandArnqvist2003TatarnicandCassis2010ArnqvistandRowe2002PerryandRowe2012 Continued
m
e
s c
ni oi
a h
h c
elymec ndkey choice female choice choice pecified
Lik Locka Female SAC SACor SAC Female Female Nones SAC SAC SAC SAC
d y
Evidence Cross-speciesmatings Experimentalevolution Cross-speciesmatings Comparativeamongspecies MatingwithintrogresselinesComparativeamongspeciesandmorphologicalExperimentalcopulatorfunctionComparativeamongspeciesComparativeamongspeciesComparativeamongspeciesComparativeamongspeciesComparativeamongpopulations
s
Femalestructures Vaginalappendix(pocketattachedtothevaginalapophysis)Sizeandlocationofgenitalpit Cavitieswithsclerotizedplatelets Oviscaptpouches OviscaptfurrowsUterine,vulval,andvaginalshieldsWoundingofthefemaleabdomenCommonspermathecalduct Female-sensingstructures Spermathecalductslength,baseoftheductSpermalege(thickenedexosqueleton)Externalfemaleparagenitalia Antigraspingappendages Antigraspingappendages
Malestructures Apophysisoftheendophallus Shapeoftheparameresintheaedagus Sclerotizedspikesontheaedagus Epandrialposteriorlobes PhallicspikesCercalteeth,phallichook,andspinesPosteriorlobeofthegenitalarchGenitalprocess Cercalteeth Aedagalfilaments,aedagalsheathsPiercinggenitalia ChangesinmalegenitalshapeGraspingappendages Graspingappendages
s
a g
a n u
ble1.Continued xa Carabidbeetles(Ohomopterus) Dungbeetle:OnthophagustaurusDiptera:DrosophilsantomeaandD.yakubaDrosophilamelanogasterspeciescomplex D.mauritianaandD.secheliaStalk-eyedflies(Diopsidae) Tse-tseflies:GlossipallidipesPhelebotomine:sandfliesHeteroptera:Bedb(Cimiciidae)Plantbugs(Coridromius)Waterstriders(Gerrissp.)Gerrisincognitus
a a
T T
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P.L.R.BrennanandR.O.Prum
d d
References Foreroetal.2013 Yoshizawaetal.2014 ´SanchezandCordero2014 Matthews1950 Langerhans2011 Evansetal.2011 ¨Kohleretal.2012 ¨Pope1941;BohmeanZiegler2009;Kingetal.2009Pope1941Friesenetal.2014 Brennanetal.2007 PLRBrennan,KZyscowski,andROPrum,unpubl. Continue
e
oln
Likelymechanism None Femalecompetition(rreversal),coevolutioSACSAC None StrongcharacterdisplacementSAC Sexualselection Lockandkey,femalechoice,andSAC NoneSAC SAC /Femalechoicenaturalselection
n
g g g g g nce, nce riso g g
Evidence ComparativeamonspeciesComparativeamonspecies Comparativeamonspecies Morphologicalobservation ComparativeamonspeciesComparativeamonpopulations ShapecorrespondetwospeciesShapecorresponde Two-speciescompaExperimentalmanipulation ComparativeamonspeciesComparativeamonspecies
Femalestructures Bursacopulatrix Penis-likegynosome Signa:Sclerotizedstructuretobreakspermatophores Thickvaginalpads GenitalpapillaewithinopeningsFemalegonoporeshape Vaginashape Vaginashape ThicknessofvaginawallVaginalmuscularcontrol Vaginalelaboration Vaginalelaboration
e s
Malestructures Aedagus Malegenitalchamber Thicknessofspermatophorewall Clasperclaw Gonopodialtips Gonopodiumtipshap Hemipeneshape Hemipeneshape SpininessinhemipeneBasalhempenespine Penislength /Penislengthpresence
alis
Table1.Continued Taxa Beeassassins(Apiomerus)Caveinsects(Psocodea),NeotroglaButterflies(Heliconiinae)FishBaskingshark:CetorhinusmaximusGambusia Poeciliareticulata ReptilesAnoles Severalspecies AsiaticpitvipersGartersnake:ThamnophissirtBirdsWaterfowl Tinamous
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MechanismsofGenitalCoevolution
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0
References Renfree1987Augeeetal.2006;Johnstonetal.20Bedfordetal.2004 Bedfordetal.2004 Kinahanetal.2007 Breedetal.2013 Bonetetal.2013Fooden1967
m
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me ylo oice
Table1.Continued TaxaMalestructuresFemalestructuresEvidenceLikely MammalsMarsupialsBifidpenisTwolateralvaginaeShapecorrespondenceNoneEquidnaBifidpeniswithfourSinglevaginasplitsintotwoShapecorrespondenceNonerosettesuteriS-shapedcurveoftheCoincidentcurveintheShapecorrespondenceNoneInsectivores:Short-erectpenisvaginatailedshrew:BlarinabrevicaudaInternalcircularfoldsinLengthcorrespondenceNoneFiliformpenis(uptoCommontenrec:thevagina70%ofthemale’sTenrecbodylength)caudatusPenisandbaculumVaginallengthAllometricrelationshipsNoneRodents:Capedunelengthwithinspeciesmole:BathyergussuillusCopulatorAustralianhoppingSpinypenisDeriveddistalregioninMorphologicalmice(Notomys)thevaginaobservationandtwo-speciescomparisonPig:SusdomesticusFiliformpenisendCervicalridgesArtificialinseminationFemalechNoneShapecorrespondencePrimates:MacacaLongandfilamentousVestibularcolliculusandcomparisonarctoidesglans(fleshyfold)thatwithcloserelativespartiallyobstructstheentrancetothevagina Thelikelymechanismisthatsuggestedbytheauthors,anditincludessexuallyantagonisticcoevolution(SAC),naturalselection,sexualselection,femalechoice,ornonespecified.Theevidenceprovidedbythestudiescanbecomparativeamongspeciesoramongpopulations,/experimentalevolution,cross-speciesmatings,full-sibling(sib)half-sibmatings,shape,andlengthcorrespondence.Shapecorrespon-denceisoftentakenasevidenceofcoevolution,althoughitisnotasconclusiveasotherapproaches.
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P.L.R.BrennanandR.O.Prum
Malegenitaliaareamongthemostvariable nismsofgenitalcoevolutiondifferentiatingthe
structures in nature (Eberhard 1985). In con- potentially independent or overlapping roles
trast,femalegenitaliahavetypicallybeenfound of natural selection, female choice,and male–
not to be as interspecifically variable as male male competition (Fig. 1). This classification
genitalia in several studies that specifically ex- allowsustodistinguishspecificallythosemech-
amined and described them (Eberhard 1985, anismsof genital coevolutionthatinvolvesex-
2010a,b). Female genitalia are not studied as ual conflict (i.e., when the evolutionary inter-
often as male genitalia, perhaps because of a estsofindividualsofdifferentsexes,particularly
male-biased view of evolutionary processes over mating, are different). We then highlight
byresearchers(Ah-Kingetal.2014).However, examplesindifferenttaxaorganismswithpar-
studying female genitalia is undeniably chal- ticularemphasisonthosethatprovideevidence
lenging.Malegenitaliaaregenerallykeptinside ofsexualconflict.
of the body cavity, but are everted before, or
duringcopulation,sotheirfunctionalmorphol-
ogy can be more easilystudied than the inter- GENITALCOEVOLUTION
nal genitalia of females. Female genitalia also
Genital coevolution results when evolutionary
tend to be softer than male genitalia and thus
changesinagenitaltraitfoundinonesexselects
theirmorphologymaybemoredifficulttode-
for an evolutionary change in a genital trait
scribe,andcanmoreeasilybedistortedondis-
section and preservation. Female adaptations
to sense or oppose features of male genitalia Male–male competition Female choice
can be subtle, requiring careful study. Female
genital tracts areundermultiple sourcesof se-
SAC-
lection:notjustmating,butalsostoringsperm, Fisher Fisher-LK
egglaying,birthing,andofteninterfacingwith Male
the terminal portion of the digestive tract. elaboration w/o
Therefore, selection balancing multiple func- coevolution SAC- Good
genes
tionsmayfurtherconstrainmorphologicalevo- Good
lutioninfemalegenitalia.However,evensmall SAC- genes Direct benefits
morphologicalchangesinfemalegenitalia,for Direct Sensory lock
benefits
example,increasesinvaginalmuscle,maychan- and key
ge afemale’s ability to choose or reject a male
Morphological
duringmating,ortomanagethecostsofmating. Lock and key
accommodation
Thus,thefunctionalconsequencestomaleand
Genital
female genital morphologyare hardto predict
adaptation w/o
unlessoneknowshowgenitaliafunctionduring coevolution
intromission. Despite these challenges, recent
studieshaveexaminedvariationoffemalegen- Natural selection
italia and evidence is accumulating that fea-
Figure 1. Graphical classification of mechanisms
turesoffemalegenitaliaarevariableenoughto
of genital evolution and coevolution. Three circles
supportcoevolutionaryprocesses(Polihronakis depicttheindependentandco-occurringactionsof
2006; Puniamoorthy et al. 2010; Siegel et al. natural selection, female choice, and male–male
2011; Showalteret al. 2013; and seeadditional competition.Differentspecificversionsofgenitalco-
referencesinAh-Kingetal.2014). evolutioncanoccurdependingonwhichofthethree
broader evolutionary mechanisms are occurring.
In this article, wewill discuss different hy-
Sexual conflict (hatched lines) occurs through the
pothesesofgenitalevolutionthatpredictcoevo-
simultaneous action of male–male competition
lution;however,thisisnotareviewofthatentire
and female choice, or male–male competition and
subject(butseeEberhardetal.2010b;Simmons naturalselection.SAC,sexuallyantagonisticcoevolu-
2013). Rather, we discuss the various mecha- tion.Seetextforexplanation.
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MechanismsofGenitalCoevolution
in the other sex. This reciprocal evolutionary female choice of preferred males, and sexually
changecanbeshownbybothmacroevolution- antagonistic coevolution resulting from sexual
aryandmicroevolutionaryresearchapproaches. conflict.Neitherpleiotropy,socialsignaling,or
Comparativestudiesofspeciesand/orpopula- male–male competition explicitly predict co-
tionscanprovideevidenceofdynamicchanges evolution,althoughchangesbroughtonbythese
in genital morphology in both sexes. These processes mayelicit a coevolutionary response
include investigations of morphological cor- onfemalesthroughadifferentmechanism.
respondence,compatibilityinoverallshape,or Here, we discuss mechanisms of genital
between morphological structures and corre- coevolution in terms of the independent or
spondingsensingstructures.Comparativestud- overlapping forces of natural selection, female
ies can reveal evidence of arms races in which choice, and male–male competition (Fig. 1).
evolutionary changes in genital morphology We identify those examples of sexually antag-
ofeachsexareantagonistic.Amicroevolution- onistic coevolution between male and female
aryapproachcanincludestudiesofcorrelation genitalia as the result of the co-occurrence of
betweengenital features (bothcorrespondence femalechoiceandmale–malecompetition,or
or antagonistic), experimental manipulation male–malecompetitionandnaturalselection.
tomeasurethefitnessconsequencesofchanges
ingenitalmorphologyinbothsexes,andmost
recently,experimentalevolutionaryapproaches NaturalSelection
that directly inform on the selective pressures
ForMechanicallyFeasibleCopulation
that act on genital features, and the presence
of coevolutionary changes in both sexes. In Naturalselectiontomakecopulationfunction-
Table 1 we summarize examples of systems in allypossiblemustalwaysinfluencegenitalmor-
whichallthesediversetypesofevidenceforco- phologytoachievethebasicfunctionofgamete
evolutionhavebeenreported,andsomeofthem transfer(Darwin1871),despitethelikelyaction
wewilldiscussindetail. of other mechanisms in genital elaboration.
Asourexamplesoutlinebelow,manydiffer- This processcan giverise to a pattern of mor-
entgenitaltraitsmaycoevolve,includingover- phological accommodation (Fig. 1). Genital
allsize,shape,functionalmorphology,sizeand sizeisofprimaryimportanceinthemechanical
shapeofparticularcomponentsofthegenitalia interaction during copulation, and therefore
including but not limited to spines, ridges, genital size covariation indicative of coevolu-
flaps, and manyother superficial elaborations, tion is likely to be important and widespread.
nongenitalcontactstructures,andphysiologyof Althoughsizecoevolutioncanalsoresultfrom
moveable and erectile and inflatable compo- sexual selection, natural selection on genitalia
nentsofgenitaliaknowninvertebratesandin- toinsuresuccessfulgametetransfercanhelpto
vertebrates. explain manyobservedpatterns, yetitisrarely
discussed(Pereti2010).
Threelinesofevidencesuggestthatgenital
MECHANISMSOFGENITALCOEVOLUTION
size fit is important. First, crossings between
Genitaldiversificationhasbeenhypothesizedto species with different genital sizes are almost
resultfrompleitropy,andnatural,sexual(Eber- alwaysimpossibleorlethaltofemales,especial-
hard 1985; Hosken and Stockley 2004), and ly when males are much larger (Masly 2012).
social selection (East et al. 1993). Within sex- Second, when size dimorphism is marked, se-
ual selection, male–male competition, female lectioncanoperatetomatchgenitalsize.Inorb-
choice,andsexualconflictcaninfluencegenital weavingspiderswithextremesizedimorphism,
morphology.Someofthesehypothesespredict tinymaleshavedisproportionallylargegenitalia
genitalcoevolutionbetweenthesexesincluding (upto20%oftheirbodymass)tomatchfemale
naturalselectionformechanicallyfeasiblecop- genital size (Ramos et al. 2005). This has not
ulation,lockandkeytopreventhybridizations, been examined when males are larger than fe-
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P.L.R.BrennanandR.O.Prum
males,butfemalesmaybepredictedtoenlarge elaboration in insects, the hypothesis has not
theirgenitaliatoaccommodatelargemalegen- reallybeenfalsified.Amorerecentreviewcen-
italia(Langerhans2011).Third,changesingen- ters on examining hybridization between spe-
ital size appear to be more constrained than cies,inwhichgenitalmorphologyseemstoplay
changes in shape. In the Onthophagus beetles, a rolein reproductive isolationvia mechanical
theshapeofmaleandfemalegenitaliachanges incompatibility (Masly 2012). Lock and key is
more rapidly than size (Macagno et al. 2011). supported by recent studies of millipede geni-
This pattern was also shown in a study of ex- talia (e.g., Tanabe and Sota 2008; Wojcieszek
perimental evolution of male genitalia in On- andSimmons2012,2013).
thophagus taurus, in which shape but not size There are several predictions of the lock-
of the aedeagus changed after 19 generations and-key hypothesis that have not been sup-
(Simmonsetal.2009),andinanexperimental ported (reviewed by Eberhard 1985, 2010a,b;
evolutionstudyinmiceMusmusculus,inwhich ShapiroandPorter1989),buttheymaysimply
baculum width but not length was shown to not have been adequately tested (Simmons
changeafter27generations(SimmonsandFir- 2013). According to lock and key, matings be-
man 2014). However, an experimental evolu- tweensympatricspeciesshouldbemechanically
tion study of genitalia in Drosophila found difficult,andoftenthisisnottrue.However,in
that both size and shape of the genital arch two closely related sympatric Carabid beetles,
changedinresponsetonaturalandsexualselec- interspecific mating are costly for both males
tion (House et al. 2013), so this pattern is not and females and result in genital damage ow-
universal.However,maleinsectstendtoshowa ingtomechanicalmismatch(SotaandKubota
patternofnegativeallometrythatsuggeststhat 1998). Further, genital divergence should be
genital size changes little relative to body size correlated with low hybrid fitness, otherwise
comparedtoothernongenitalcharacters(Eber- selection would be too weak to drive further
hardetal.1998). mechanical isolation; but again there is little
evidenceforthis,anexceptionbeingthehybrid
zone between the beetles described above, in
ForaLock-and-KeyMechanismtoPrevent
which females have deformed ovaries (Sota
Hybridization
andKubota1998).Becauselockandkeyisbased
Defournotedthatmalegenitaliaininsectswere onnaturalselectionforreinforcementofspecies
often species specific and stated that these isolation, there should also be character dis-
served to preserve “types” (Defour 1844). The placementin male genitalia of sister species in
“lock-and-key”hypothesisproposesthatvaria- zones of sympatry compared to allopatry. Al-
tion in genital form coevolvesthrough natural though Eberhard (2010b) argues that this has
selection againsthybridizationandto enhance notbeenshown,Simmons(2013)detailssome
reproductiveisolation(Eberhard1985;Shapiro insectexamplesinwhichreinforcementhasbeen
andPorter1989).Femalesavoidthefitnesscosts shown. Character displacement is involved in
of having theireggs fertilized bya male of the genitaldiversificationandcoevolutionofpenis
wrongspeciesbyevolvinggenitaliathatpermit andvaginalengthinlandsnails(Kamedaetal.
onlymaleswiththerightfittoachievemechan- 2009),andinmaleandfemalegenitaldiversifi-
icalcoupling leading tofertilization. Themale cation in fish of the genus Gambusia (Langer-
“key” must fit the female “lock.” As such, this hans2011).Finally,themostwidespreadreason
hypothesispredictsclosecoevolutioningenital whylockandkeyisdeemedunlikelyistheper-
shape and mechanical fit during copulation. ceptionthatfemalegenitaliaarenotasvariable
ShapiroandPorter(1989)provideanexcellent as male’s, that is, the keys are variable, but the
reviewofthehistory,testsandevidenceforand locksarenot(Eberhard1985).However,exam-
againstthishypothesisintheinsects.Theycon- ination of current literature suggests that this
clude that although there is no evidence that conclusion is only weakly supported even in
lockandkeyexplainsmostinstancesofgenital thewell-studiedinsects(Simmons2013).
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MechanismsofGenitalCoevolution
Surprisingly,manystudiesofthelock-and- hypothesisonthebasisoflackoffemalegenital
key mechanism do not examine females at all variation alone. Simmons (2013) has made a
(e.g., Mutanen et al. 2006; and see references similarpoint.
inAh-Kingetal.2014).Somestudiesalsocon- Although evidence for genital covariation
clude that females are not variable by using in shapehasbeen used as evidence to support
eitherlinearestimatesofgenitalsizeorqualita- lock-and-key(e.g.,Mikkola1992),mechanical-
tive examinations of genital shape (Eberhard ly feasible copulation, female choice and sex-
2004a,b, 2006, 2010a,b). However, linear esti- ually antagonistic coevolution can also result
matesdonotcapturethecomplexityofgenital inshapecoevolution.Therefore,genitalcoevo-
shape,andsizemaybeselectedtobelessvari- lution is not an exclusive prediction of lock
ablethanshapeasdiscussedabove.Whenquan- andkey.
titative measures and ultrastructure analyses
offemalemorphologyandshapeareconducted,
FemaleChoice
significant genital morphological variation
across species has been detected. Forexample, Femalechoicecanresultincoevolutionofdif-
femalegenitaliainDrosophilaweredeemedtobe ferent features of genitalia. Just like any other
fairly invariant across species (Eberhard and sensory mediated mate choice mechanism, fe-
Ramirez 2004; Jagadeeshan and Singh 2006), males may be able to use sensory stimuli re-
but a recent studyshowed that in nine species ceivedduringcopulationfrommalegenitalsas
of Drosophila, several aspects of female genital thebasisforfemalechoice.Thisprocessrequires
morphologycovarywithmalegenitaltraits(Fig. female to receive and evaluate these stimuli.
2) (Yassin and Orgogozo 2013). A geometric Thus,ifmalesstimulatefemaleswithvibrissae,
morphometricanalysisofgenitalshapeamong thenfemalesmusthavetheabilitytocontactthe
twosisterspeciesofwatersnakes(Nerodiasp.) vibrissaeanddetecttheirmovement,shape,or
thatseemedverysimilaronvisualexamination whatever component of male morphology is
alone, showed that vaginal shape of these two speculatedtostimulatethem.
speciesdifferedsignificantlyinthedegreeofbi- Throughsexualselection,matingpreferenc-
furcation and the aspect ratio of the vagina escancoevolvewithmaletraitsthrougheither
(Showalteretal.2013). thearbitraryFisherianmechanism,orbyadap-
Althoughtherearegoodreasonstosuggest tivegoodgenesanddirectbenefitsmechanisms
that lock and key is unlikely to explain wide- (Fig.1)(KirkpatrickandRyan1991;Andersson
spread patterns of genital evolution, quantita- 1994;Prum2010).Femalematechoicecanaf-
tive examination of female genitalia should be fectmalegenitalevolutionwhenfemaleschoose
performed before ruling out the lock-and-key on the basis of interaction with male genitalia
Figure2.FemalegenitaliainDrosophilawerepreviouslythoughttobeinvariant,butrecentworkhasdescribed
extensivevariationandcoevolutioningenitalmorphology.(A,C,E)Femaleoviscapts,and(B,D,F)maleepan-
drialposteriorlobes.Scalebars,50mm.(ReprintedfromYassinandOrgogozo2013.)
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P.L.R.BrennanandR.O.Prum
(Eberhard1996). Thus,male andfemale geni- mentous or finger-like endings on their penis
talia may participate in all the same coevolu- (Eberhard1985),suggestingthatfemalechoice
tionaryprocessesthatcharacterizematingpref- mayplayanimportantroleinshapingthispar-
erences and displays that are mediated by the ticularclassofgenitalelaboration.
sensory system during precopulatory interac- Amodifiedversionofmechanicallockand
tions.Genitalcoevolutionbyfemalechoicere- key is known asthe sensory lock and key; this
quires female promiscuity, so that females can hypothesis argues that differences in genital
chooseamongmultiplemaleswithwhomthey morphologyperceivedbyeithersexduringcop-
mate. ulation can resultin prematuretermination of
Femalematechoicecouldresultinarbitrary mating(Eberhard1985,2010a,b).Coevolution
“Fisherian,”orLandeKirkpatrick(LK),coevo- occursbetweencomponentsofgenitaliaassoci-
lution in male and female genitalia via either ated with sensing “fit,” rather than purely me-
sensorypreferencesorotheranatomicalfeatures chanicalaspectsofshapedifferencesthatmake
offemalegenitaliathatallowfemalestoevaluate copulationdifficult.However,ifmatingsuccess
malefeatures.Wediscussthispossibilitybelow ismediatedbyfemalesensoryperception,then
inbirds.Asproposedformatechoiceingeneral this mechanism is essentiallyaform of female
(Prum2010),thearbitraryfemalechoicemech- choice in which female mating preferences are
anism isactually the null hypothesis of coevo- under natural selection against hybridization
lution until evidence of good genes or direct (Fig. 1). Simmons (2013) argued that sensory
benefits mechanisms can be obtained (Prum lock and key is another type of female choice
2010).Thisprocesscanoccurwhenfemalemat- processthat should be viewed as acontinuum
ingpreferencesarenotundernaturalselection. that enhances species isolation in one end, or
Thebestsupportforgenitallymediatedfe- thatselectformalefeaturesthatincreasefemale
male mate choice is provided by a series of fitness on the other. Sensory lock and key to
experiments examining interactions between avoidhybridizationissupportedinsomeOdo-
genital features of males, and female receptors nates, inwhich mechanical isolationviaclasp-
in tsetse fly Glossina pallidipes. Modifications ingappendagesisreported,andcoevolutionbe-
ofthecercalteeth—thepartofthemalegenita- tweenthemaleabdominalclaspersandfemale
liathatsqueezesthefemaleabdomen—resulted shape, sensory hairs (Robertson and Paterson
inreductionoffemalespermstorageandovu- 1982),andshapeoffemaleabdomens(McPeek
lation while increasing remating probability. etal.2009)preventsheterospecificmatings.
These changes were shown to be dependent
onfemalestructuresthesensemalestimulation
SexuallyAntagonisticCoevolutionResulting
(Bricen˜oandEberhard2009a,b).
fromSexualConflict
Studies of domestic pig (Sus domesticus)
provide an example of genital coevolution via So far we have discussed cases in which co-
femalechoiceinvertebrates.Malepigshavepe- evolutionresultsincorrespondenceorfit.How-
nisesthatendonacorkscrewfilamentwhereas ever, sexually antagonistic coevolution (SAC)
sowshaveridgesontheircervixthatspecifically thatoccursasaconsequenceofsexualconflict
sensestimulationfromthepenisduringcopu- betweenmalesandfemalescanresultincoevo-
lation. When sows are artificially inseminated, lutionaryprocessesthatreducefit,orthatfunc-
stimulationofthecervixridgesmustoccuroth- tiontodecreaseeaseofcopulation,ortomiti-
erwise the pregnancy rates drop dramatically gate male damage to the female. SAC occurs
(Bonet et al. 2013). This is consistent with a when genital adaptations coevolve in each sex
roleforfemalechoiceinshapingpigpenismor- toadvancecontrolovermatingandfertilization
phology,althoughnoinformationonmalevar- initiatingacoevolutionaryarmsrace(Chapman
iation of genital features is available to deter- et al. 2003; Parker 2006; Brennan and Prum
mineitspotentialcorrelationwithfertilization 2012).Bothdirectandindirectselectionareim-
success. Manyother mammals have these fila- portant in shaping evolutionary responses to
10 CitethisarticleasColdSpringHarbPerspectBiol2015;7:a017749