Beyond sexual selection: the evolution of sex differences from brain to behaviour.

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NeuroscienceandBiobehavioralReviews46(2014)497–500

ContentslistsavailableatScienceDirect

Neuroscience

and

Biobehavioral

Reviews

j o ur na l ho me p a g e :w w w . e l s e v i e r . c o m / l o c a t e / n e u b i o r e v

Editorial

Beyond

sexual

selection:

The

evolution

of

sex

differences

from

brain

to

behavior

Sexualselectionhasreceivedagreatdealofattentioninthelast fewdecades(Owens,2006),andcontinuestobeacentraltopicof interestforbehavioralecologists.First,itisusefultogobacktothe historicaldeﬁnitionofsexualselection:

whenthemalesandthefemalesofanyanimalhavethesame generalhabits oflife, butdifferin theirstructure,colour, or ornament,suchdifferenceshavebeenmainlycausedby sex-ualselection;thatis,individualmaleshavehad,insuccessive generations,someslightadvantageoverothermales,intheir weapons,meansofdefence,orcharms;andhavetransmitted theseadvantagestotheirmaleoffspring.

CharlesDarwin, OntheOrigin ofSpecies byMeans ofNatural Selection,1859(chap.IV,pp.89–90)

Slightdifferences in reproductivesuccessmaybecaused by maleweaponsand/orcharms,exaggeratedsexualcharacteristics. ThesearethekeywordsofTheDescentofMan,andSelectionin RelationtoSex(1871):sexualselectionmeant“ardentmalesand choosyfemales”,i.e.male-maleﬁghtingandfemalechoice.Work sinceDarwin’stimehasenlargedthetheorytonotethatfemalescan beaggressiveandmaleschoosy,dependingonthecircumstances. In addition,sexualselection isrecognized tooccurboth before andaftercopulation.Despiteearlyskepticismand“sexualselection amnesia”(West-Eberhard,inthisissue),agrowingbodyofresearch andrecentmodelsarenowcenteredonthishighlyheuristic the-ory,makingitoneofthebeststudiedareasofbehavioralecology alongsideanimalsignalsandhost–parasiteinteractions(Fig.1).

Thereisbroadconsensusthattheoccurrenceofsexually dimor-phictraitsamong animals– especiallyinmales–oftenmaybe explainedbysexualselection,buttheprocessesbywhichsexual selectionoperatearestillcontroversial.Exaggeratedsexualsignals havebeenconsideredindicatorsof“goodgenes”(Hamiltonand Zuk,1982);thus,maleswithexaggeratedtraitsalsosireoffspring thathavehigherﬁtness.Sexualornaments,ifcostly,maybehonest cuesofmatequality(Zahavi,1975)andhealth(ZukandWedell, 2014),solvingtheconundrumofhowheritablevarianceinﬁtness ismaintained.

Ontheotherhand,inaccordancewiththe“aestheticcapacity”of females,theessenceofDarwin’sargument(1871),andtherunaway co-evolutionbetweenmale traitand femalepreference (Fisher, 1958),bizarrecourtshipdisplaysorconspicuousﬁghting special-izationsmayevolvebecausetheyaremerelypreferred,without

noadditionalinformation.Thefemale“tasteforthebeautiful”has beenrecentlyadvancedas“Darwin’sreallydangerousidea”(Prum, 2012):maletraitscouldbepreferred,regardlessofanyadditional quality.ButDarwin wasperhapsopentoboththeseoptions, if females“willselectthosethatarevigorousandwell-armed,and inotherrespectthemostattractive”(1871,chap.VIII,262).Ifsome traitsmayevolveasarmamentsandornaments,withadual func-tion(Berglundetal.,1996),“runawayselectionleadstogoodgenes” (Chandleretal.,2013).Kokkoetal.(2002)claimedthatthereisa continuumfromtheevolutionarymechanismsofgoodgenesand femaleestheticchoicethrough theindirectbeneﬁt ofﬁtter off-spring;thus,thedistinctionbetween“arbitraryandnon-arbitrary maletraitsis,initself,arbitrary”(Kokkoetal.,2006).

Giventhechallengingdebateonsexualselection,itisnosurprise that,overthelast30years,researchhasfocusedontheevolution ofmatingsystemsandmalearmaments/ornaments,sexualsignals asgood-genesindicators,alternativereproductivetactics,sexual dimorphismfromgametestoparentalroles,andmuchmore.But alongwiththesewell-researchedtopics,relatedorcomplementary

Fig.1. Thenumberofpublicationsper10,000papersonsexualselection(closed squares),host–parasiteinteractions(opentriangles),animalsignals(closed trian-gles)publishedoverthepast25yearsinthejournalsBehavioralEcology,Animal BehaviourandBehavioralEcologyandSociobiology.

Source:FromOwens(2006).

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498 Editorial/NeuroscienceandBiobehavioralReviews46(2014)497–500 onesmayhavebeenneglectedorreceivedmuch lessattention:

maleratherthanfemalematechoice;female-femalecompetition; femalepromiscuityandcrypticchoice;conﬂictandcoevolution betweenthesexesinbrainstructure,geneexpressionand cogni-tivefunctions;thesensorytraphypothesis;thetrade-offbetween immunityandmatingefforts;andtheapparentparadoxof same-sexbehavior,amongothers.Oftenitisinthesedeparturesfrom theusualwayofthinkingthatwegainnewinsights.Inaddition,a comparativeapproachandless-standardmodelsystemsmayallow tobetterunderstandtheevolutionarydevelopmentoftypicaland atypicalsexualbehavior.

Inthisspecialissue,weexploretheothersideofsexual selec-tionbyviewingsexualdifferencesatavarietyofscales,ranging from neural pathways and individual personality to a macro-evolutionaryperspective.Sexdifferencesinthebrainhavebeen welldocumented,buttheiradaptivevaluehasbeenonly super-ﬁcially investigated. Sexual dimorphism may mediate learning abilities involved in matechoice and competitionfor partners: neuro-motorskillstodisplay,advertisementsong,partner’s evalu-ationataﬁne-scale,perceptiveenhancement,sensoryexploitation and so on. If this is the case, then such neural differences are sexually selected traits, like antlers and nuptial plumage, and they are best understood within theframework of sexual selection.

NeuralsexualdimorphismisaparticulartopicofthisSpecial Issuebecausethebrainisatargetofsexualselection.Inthelast chapterofTheDescentofMan,Darwinunderlinestheevolutionary factorsthatopenthewaytotheapproachofcomparative neuro-anatomy.

Everyonewhoadmitstheprincipleofevolution,andyetfeels greatdifficultiesinadmittingthatfemalemammals,birds, rep-tiles,andfish,couldhaveacquiredthehighstandardoftaste whichisimpliedbythebeautyofthemales,andwhich gener-allycoincideswithourownstandard,shouldreflectthatineach memberofthevertebrateseriesthenerve-cellsofthebrainare thedirectoffshootsofthosepossessedbythecommon progeni-torofthewholegroup.Itthusbecomesintelligiblethatthebrain andmentalfacultiesshouldbecapableundersimilarconditions ofnearlythesamecourseofdevelopment,andconsequentlyof performingnearlythesamefunctions.

CharlesDarwin,TheDescentofMan,andSelectioninRelationto Sex,1871(chap.XXI,p.401)

Brainsexdifferencesinvolvedevelopmental,ecologicaland tax-onomicdifferences.“Birdsandmammalsexhibithighlycanalized sexualdifferentiation,amphibiansandreptilesaremore plastic, andteleostﬁshesare extremelylabile”(Francis,1995).Atleast someofthesedifferences mightbebestunderstoodwithinthe frameworkofsexualselection.

TheintroductoryessaybyWest-Eberhardismostlydevotedto thecoevolutionof sensory-responsesystems undernatural and sexualselection, better,under “socialselection”, of interest for neurobiological studieswhich putmale-female differences and conﬂictsinanevolutionaryperspective.Socialcompetitionexploits “amultitudeofsensory-responsecapacities”.AsWest-Eberhard emphasizes,“indicatorsofqualityseemunlikelytoaccountforthe greatcomplexityofcourtshipdisplays”.Attractivenessmayassume “astimulatoryvalueperse,aboveandbeyondanysigniﬁcancethey mayhaveassignsofgoodgenes”,better,“goodsurvivalgenes”.The evolutionofmultimodalsignalsandextravagantmalephenotypes “exceedsthatexpectedundersexualsection”:aprocess,forthe author,clearlydistinctfromnaturalselection,althoughboth mech-anismsmaymutuallyreinforceand“interplayinsignalevolution”. Consistentwithaco-evolutionaryprocessdrivingcomplexneural andbehavioral-morphologicaltraits,West-Eberhardmayconclude

that“aspectacularproductofnatural-socialselectionisthehuman brain”,inlinewiththeDarwiniantheory.

Hereinwepresentaseriesofbasicresearchandreviewpapers relevantforunderstandingsexualselectionanditsimplicationsin behavioral,physiologicalandneuro-endocrinestudies,organized inthreesections:ﬁrst,maleextremebehavioraltraitsassuitable modelsystemstoinvestigatehormonalandneuralbasesof exorbi-tantmatingefforts;second,apparentlymaladaptivebehaviorand exceptionstostandardsexualselection;third,cognitive neurobi-ologyandsex-relateddifferencesinbrainandbehaviorinhumans andotherprimates.

1. Malelife-history:“Livehard,dieyoung”

Thecostofreproductioninvariousformsiswelldocumented (Reznick, 1985). In many species, this cost is manifested as a reduction in longevity or immune response in males (Zuk and McKean,1996).Inthecaseofpigmyrattlesnakes,thistradeoffwas summarizedas“Livefast,lovehard anddieyoung”(Mayetal., 1997).Arecentpapershows thattheperceptionoffemale sex-ualpheromonesissufficienttolimitthelifespanofmalefruitflies (Gendronetal.,2014).Male sacrificeandautotomyofsignaling appendagesinspidersofferagoodexampleofhighmating invest-ment(Herbersteinetal.,inthisissue).Sexualselectionhasshaped malecourtshiptohonestlycommunicatetheidentityandthe qual-ityofa potentialmateand thustoreducetheriskofpredation bythefemale.Thetrade-offbetweenextremesexualdimorphism andlower ratesofcannibalism acrossspeciessuggeststhatthe evolution of complexity may inhibit femaleattack. Multimodal signaling,includingvisual,chemical,butalsovibrational compo-nents,impliesconsiderablecapacitytoemit,processandrespond tosuchelaboratemessages,althoughafewneurobiological stud-iesexploreindetailtheroleofthecentralandperipheralnervous systemsinintegratingthesesexualsignals,frombothafemaleand amaleperspective.

Multimodalsignalingissurelyinvolvedintheleks–i.e.the nup-tialarenas–ofpaperwasps,wherehundredsofmalesdisplayat landmarks(Beanietal.,inthisissue),aswellasintheexpandedlek matingsystemofmanakins,performingtheirlonelydancesinthe neotropicalforest(Fusanietal.,inthisissue).Malehymenopterans haveneitherarmamentsnorornaments,andareephemeraland elusive,difﬁculttoobserveincomparisontotheimpressive archi-tectureofthecolonies–afeminineworld.Theimpactofsexual selectionontheevolutionofthesocialinsectsocietiesisa sub-jectthatisslowlydeveloping,suchasthesubtleroleofmalesand thecognitivebasesoftheirbehavior,fromcourtshiptoalternative matingtactics,selectivematechoiceandspermallocation.Onecan viewthemaleneglectedphenotypeinwasps,beesandantsas“a naturalexperimenttocomparethedrivesofnaturalversus sex-ualselection,parentalversusmatingefforts,andtheirassociated neurogenomicmechanisms”(Beanietal.,inthisissue).

ThebizarreacrobaticperformanceoftheGolden-collared man-akin,thefocusoflong-termresearch(Fusanietal.,inthisissue), hasbeeninterpretedasanhonestindicatorofmalemotorskills, whichareinﬂuenced–intheirorganizationandactivation–by gonadalhormones,expressedinasex-dimorphicwayinthebrain, spinalcordandskeletalmuscles:“anandrogen-dependent pheno-type”,althoughthisneuralcircuitryissurprisinglypresent–butnot active–infemales(Fusanietal.,inthisissue).Thefemale,equipped withsuperbvisualprocessing,mayassessandcompare,ataﬁne scale,themaleperformance,drivingtheevolutionofthiscomplex courtship,whichimpliesarigidchoreographyofthenuptialarena (Barskeetal.,2011).“Onthewhole,birdsappeartobethemost aes-theticofallanimals,exceptingofcourseman,andtheyhavenearly thesametasteforthebeautifulaswehave”(Darwin,1871,chap.XI,

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Editorial/NeuroscienceandBiobehavioralReviews46(2014)497–500 499 p.466).Asoutlinedbytheauthors,theestheticvalueofmale

perfor-mance,charmingfemalesthroughnoveltyanddiversity,doesnot excludethegeneticqualityofmaleperformance.Again,runaway selectionandgoodgenesbeneﬁtscouldbeviewedasinteractive synergicmechanisms(Chandleretal.,2013).

Songbirdsofferafurtherexampleofspecies-specific neuromus-cularsystemscontrollingsexualdisplays,inthiscasethemalevocal performance.The songoftheBengalesefinchhasbeendefined as“awindowonthebehavioralneurobiologyofbirdsongsyntax” (Okanoya,2004).Thesongofthisspecies,domesticatedinJapanfor 250years,ismorecomplexandplasticthanthestereotyped sim-plesongofthewildancestor,anditsvocalcontrolnucleidifferfor sizeandgeneexpressionofneurotrophicfactors.MaleBengalese finchessingcomplexsongs“underindirectsexualselection”:in theabsenceofspeciesrecognition,predatoravoidance,stress,and otherpressuresinthewild,theylearnedawide-ranging phonol-ogytoattractfemales,“consideringthedomesticatedenvironment alsoasaspecialecologicalniche”(Suzukietal.,inthisissue). Sex-ualselection,domesticationandreducedstresslevel,allresulted inabalancebetweenglucocorticoid-andmineralocorticoid recep-torsinvocalcontrolnucleiandtheavianamygdalaaswellasin theevolutionofsongcomplexity,inlinewithdarwinian–fisherian runawayselectionforextremevocalperformance.AsDarwinnotes (1871,chap.XIII,p.67),“itisnotdifficulttoimaginethestepsby whichthenotesofabird,primarilyusedasamerecallorforsome otherpurpose,mighthavebeenimprovedintoamelodiouslove song”,althoughinthecaseofdomesticationthe“man’staste”could playarelevantrole.

2. Beyondsexualsterotypes

Sexual selection occurs before, during and after copulation, althoughtheformerisperhapsthebest-studied.Post-copulatory sexualselection,includingspermcompetitionandcrypticfemale choice,arenowincreasinglythesubjectsofresearch.Lesswidely examined,however,arethestructuresneededforcopulationitself, a lack that is addressed by Brennanet al. (in this issue).They examinesuchstructuresintwosubgroupsofthegalloanseriform superfamily,Japanesequailandducks.Likemostbirds,Japanese quail have a non-intromittent penis, and they have evolved a uniquefoamglandthatproducesameringue-likesubstance trans-ferredintothefemale’scloacaduringcopulation.Thesecretionsof theglandfunctioninpost-copulatorysexualselection.Maleducks, incontrast,possessanoftenelaborateintromittentorganthat ﬁg-uresinsexualconﬂict,withfemalereproductivetractsapparently havingevolvedasa“counter-move”tocontrolfertilization.Todate, however,researchershavenotattemptedtoexaminethe neuroen-docrinecontrolofthesestructuresasdifferentmanifestationsof sexualselection,somethingBrennanandcolleaguesbeginhere.

Genesare “fragrant.”Thatis,theirgene productsorspeciﬁc ligandssmellandmayinﬂuencematechoice,ifthese chemosig-nals are polymorphic enough to,for example, reveal the MHC (majorhistocompatibilitycomplex)genotypeofthepartnerand hence his or her compatibility in producing offspring with an optimallyvariableimmuneresponse(VollrathandMilinski,1995; Milinski,2006).Thistopiccontinuestogarnerbroadinterestand generate considerable discussion about the chemical nature of thepolimorphicodorsignal.Sticklebacksexhibitatwo-stepmate choice(Milinski,inthisissue).First,afemalesticklebackprefers thescentofamalethatofferstheoptimalcomplementationofher ownalleles.Second,shechecks thebrighterones,since thefull expressionofsex-dimorphicornament,liketheredbreeding col-orationofmales,isdependentonhealthandvigor(Hamiltonand Zuk,1982).Researchmaybebiasedtowardmodalitiesthatare rela-tivelyeasilyaccessibletothehumanobserver.Butsexualselection mayworkviachemicalaswellasvisualstimuli,ascomparative

experimental evidence on MHC fragrant genes suggest also in humans,“inanever-endingco-evolutionaryarmsraceaccordingto RedQueendynamics”(Milinski,inthisissue).Recentdataon neu-rohormonesmodulatingreproductiveandsocial behaviorinthe three-spinedsticklebacks(Klesczy ´nskaetal.,2012;Kulczykowska andKlesczy ´nska,2014)supporttherelevanceofthistraditional modelorganisminbehavioral,geneticandneuralstudies.

Perhapsnotopicinsexualitystudiesattractsasmuchattention ashomosexualbehaviorinhumans,andoftentheﬁrstquestionto biologistsiswhethersimilarbehavioroccursinnon-humans.Vasey (inthisissue)reviewsover20yearsofresearchonfemale-female sexualbehaviorinJapanesemacaques,notingthatsuchbehavior appearstobesexuallymotivated,ratherthanasamechanismfor socialinteraction.Thisworkplacessexualbehaviorinabroader context;notallsexuallyrelatedactivityleadsdirectlyto reproduc-tion.

3. Thebrainstormofsexdifferences

Therelationshipbetweennon-humanandhumanprimatesis alongstandingcontroversialtopic.AsDarwinpointedout(1871), “thedifferenceinmindbetweenmanandthehigheranimals,great asitis,isitcertainlyoneofdegreeandnotofkind”.Recent neuro-genomicresearch,reviewedbyStanyonandBigoni(inthisissue), supportbothsimilaritiesanddifferencesbetweenthegroups,as wellastheinﬂuenceofsexualselection.Inanthropoidprimates, largerbrainsareassociatedwithmonogamousmatingsystemsand loweredmatecompetitionamongmales(Schillaci,2006),although bothsexesmayhavearmamentsandornaments.Inthescenario of“thesocialbrainhypothesis”(Dunbar,2009),femaleafﬁliative socialityemphasizestheneocortex,themirrorneuronactivityand thecognitiveareas,whereasmalecompetitivesocialityismore closelyrelatedtotheemotionalresponsesofsubcorticalunitsand visual-spatialskills.Ifsocializationmodulatesbothneuroanatomy and sexdifferences,lifelong pair-bonding,highpaternal invest-mentandtheuniquemultifamilystructureinthehumanlineage leadtothedramaticexpansionofthecerebralcortexandto gen-derdimorphismalongcomplexnetworksinvolvedinvisual-spatial skills,socialcognitionanddecision-making.Feisetal.(2013)have shownthroughMR(magneticresonance)multimodalimagesthat theproportionofgrey matteris largerin thefemale,while the malebraincontainsmorewhitemattertissuealongagradientfrom frontaltooccipitalcortex.Inshort,inhumanandnon-human pri-mates“afeedbacksystemlinksbehavior,socialorganization,and geneexpressiontosexualdimorphism:fromtheformand func-tionofgenitaliatoneuroanatomyandthegenome”(Stanyonand Bigoni,inthisissue).

Genderdifferencesinthecapacityofempathy–“theinstinct of sympathy” ofDarwin (1872, p. 360) in The expression of the emotions in manandanimals – is the subject of a comprehen-sivereviewbyChristov-Mooreetal.(inthisissue).Phylogenetic andontogeneticrootsofempathyhavebeencomparedinhuman andnonhumanprimatesofvariousageandboth sexes,beyond anygenderstereotypeofmoreempatheticfemales–theprimary caregivers–and lessemotionalmales.Theauthorsexploretwo categoriesofempathyacrossabroadrangeofbehavioral/neural measuresandnon-invasivetechniques.Theaffectiveempathy,in whichfemalesareveryresponsive,sharingand“mirroring”the oth-ers’emotionsandmainlyinfants’signals,activatesfrontoparietal, temporalandsubcorticalareas.Thecognitiveempathy,aconscious processthroughwhichmalesinfertheothers’internalstates, eval-uatingand“mentalizing”theirintentions,involvesthecingulate, prefrontalandtemporalregions,i.e.theutilitariandecision-making systems.Empathyisamultilayeredprocess,involvingtheactivity ofvisuo-motorandaudio-visualmirrorneurons,beyondfurther neuralmechanisms,dueitsmultimodalnature.Theneuroscience

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500 Editorial/NeuroscienceandBiobehavioralReviews46(2014)497–500 ofempathy(ZakiandOchsner,2012)hasbeenreviewedusinga

Darwinianevolutionaryscenarioinanevo-devoperspective:sex differencesareaffectedbyprenatalandrogenexposureand hor-monereactivity,beginveryearlyininfants,appear tobestable throughout thelife and are inﬂuenced by thecultural context. The“ancientbiologicalphenomenon”ofempathy(Christov-Moore etal.,inthisissue)isnotaculturalby-productofoursocialization butmayhaveevolvedinprimatesinresponsetodifferentmaleand femaleroles.

Inhumans,facialattractivenesshasbeenmuchstudiedasabasis formatechoiceandotherformsofreproductivebehavior.Hahnand Perrett(inthisissue)takeaneurobiologicalapproachinexamining commonmechanismsbehindreproductivemotivation.Theyfind differencesinbrainactivityinresponsetopreferredfaces depend-ingongenderandsexualorientation,amongotherfactors.They alsonotethatourunderstandingofwhatconstitutesan“attractive” faceisstillnotwellunderstoodfromaneurologicalstandpoint, arguingforstudiesthatcombineneuroimaging,genetics,and hor-monalpatterns.Thebiologicalbasisofhumanbraindifferencesin relationtosexandgender(Balletal.,inthisissue)isthecontentious subjectofmanypopularbooks:“tempestsandtales”(McCarthyand Ball,2011).Ifneuralsystemsareinvolvedintheprocessesofmate choiceand socialcompetitionformatesinboth sexes (Clutton-BrockandHuchard,2013),thebraincouldbeviewedasasecondary sexcharacteristic,although“ecological”pressures–asunderlined byDarwin–andadditionaldrivesmayshapethephenotypeina sex-specificmanner.Followingtheclassicalhypothesisof organi-zationalandactivationaleffectsofsexsteroids,theauthorsexpand theirreviewtobirdsandmammals,afterusefulexplanationsof termssuchassexdetermination,sexdifferencesandsex dimor-phism.Therearesomanyandubiquitousgenderdifferencesinthe functionandstructureofhumanbrainthattheauthorshereadopt thecautiousapproachindicatedbyCahill(2010),i.e.toinvestigate “why”and“whynot”theyoccur,and“how”maybetestedintheir proximalandultimatemechanisms.“Intheinterveningyearstwo importantthingshavehappened.Oneisthatwehaveexpanded ourappreciationforsexdifferencesinthebrainbeyondtherealm ofreproduction,andsecond,wehavesubstantiallyadvancedthe frontierin termsofidentifyingthecellularpathwaysmediating sexdifferences”,whichare“uniquetoeachendpoint”(Balletal.,in thisissue).Neuroanatomicalsexdifferenceswithalltheircomplex variants,hormonalandgeneticinfluences,post-nataleffects sup-portthemarkedgenderplasticityinhumanbehaviorandbrain. Theinteractionbetweenhormones,genesandenvironmentmay inducesexdifferencesinthecognitivedomainaswellasinthe juvenileplay.Intheend,avarietyofmechanisms,consistentwith adaptiveandnon-adaptivescenarios,areinvolvedinsex-biased traitsinsidetheevolutionarypuzzleofsexualselection.

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LauraBeani DepartmentofBiology,UniversityofFlorence,Italy MarleneZuk DepartmentofEcology,EvolutionandBehavior, UniversityofMinnesota,USA Availableonline7November2014