Cooperating to compete: altruism, sexual selection and causes

12 Pages·2013·0.55 MB·English

AnimalBehaviour88(2014)67e78
ContentslistsavailableatScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
Review
Cooperating to compete: altruism, sexual selection and causes of male
q
reproductive cooperation
Samuel L. Díaz-Muñoza,*, Emily H. DuValb, Alan H. Krakauerc, Eileen A. Laceyd,e
aSectionofEcology,Behavior,andEvolution,UniversityofCalifornia,SanDiego,CA,U.S.A.
bDepartmentofBiologicalScience,FloridaStateUniversity,Tallahassee,FL,U.S.A.
cDepartmentofEvolutionandEcology,UniversityofCalifornia,Davis,CA,U.S.A.
dMuseumofVertebrateZoology,UniversityofCalifornia,Berkeley,CA,U.S.A.
eDepartmentofIntegrativeBiology,UniversityofCalifornia,Berkeley,CA,U.S.A.
a r t i c l e i n f o
Competition among males for access to reproductive opportunities is a central tenet of behavioural
Articlehistory: biologythathascriticalimplicationsforstudiesofmatingsystems,sexualselectionandtheevolutionof
Received10July2013 numerousphenotypictraits.Giventheexpectationthatmalesshouldcompetevigorouslyforaccessto
Initialacceptance20August2013 females, it may at first seem paradoxical that males in some species cooperate to reproduce, often
Finalacceptance15October2013 resultingintheapparentsacrificeofdirectfitnessbysomemembersofthesecooperativepartnerships.
Publishedonline Becausethisformofcooperationliesattheinterfacebetweennatural,sexualandkinselection,studiesof
MS.number:ARV-13-00579R the adaptive consequences of male reproductive cooperation may yield important insights into how
complexandsometimesconflictingselectivepressuresshapeindividualbehaviour.Here,wedefineand
Keywords: reviewexamplesofreproductivecooperationamongmaleanimals.Wetakeanintegrativeapproachto
cooperation reviewing the potential causes of maleemale cooperation, including potential adaptive hypotheses,
cooperativebreeding
ecologicalcorrelates,phylogeneticpatternsandphysiologicalmechanisms. Theimpactofmalerepro-
cooperativedisplay
ductive cooperation on sexual selection theory is also discussed. We conclude by outlining several
cooperativepolyandry
kinselection importantdirectionsforfutureresearch,includingeffortstoimproveunderstandingoftheecologicaland
maleparentalcare demographic contexts in which male reproductive cooperation occurs. Collectively, such analyses
mutualtolerance promisetoimproveourunderstandingofmultiplefundamentalconceptsinevolutionarybiology.
reproductiveskew (cid:1)2013TheAuthors.PublishedonbehalfofTheAssociationfortheStudyofAnimalBehaviourbyElsevier
sexualselection Ltd.Allrightsreserved.
Classic sexual selection theory predicts that males should expectationisthatsuchtraitsaremaintainedbecausetheyincrease
competevigorouslywithoneanotherforaccesstopotentialmates thedirectfitnessofindividualmales.
(Andersson,1994;Bateman,1948;Darwin,1871;Dewsbury,2005; Giventheubiquityofthisexpectation,biologistshavelongbeen
Trivers,1972). Such intrasexual competition is generally believed intriguedbyspeciesinwhichmalescooperatetosecureaccessto
tobeapowerfulselectiveforcethat,inconcertwithfemalechoice, mates. Such cooperation, which includes performing coordinated
hassignificantlyshapedmalephenotypesinmostanimalspecies displays to attract females (peafowl, Pavo cristatus: Petrie et al.,
(Andersson, 1994; Dale et al., 2007). In particular, reproductive 1999; turkeys, Meleagris gallopavo: Krakauer, 2005; Chiroxiphia
competitionamongmalesisthoughttohaveplayedafundamental manakins: DuVal, 2007; Foster, 1981; McDonald & Potts, 1994),
role in the evolution of traits such as morphological weaponry formingcompetitivecoalitionstogainordefendaccesstofemales
(Callander, Kahn, Maricic, Jennions, & Backwell, 2013), sexual (dolphins, Tursiops sp.: Connor, Smolker, & Richards,1992; lions,
dimorphisminbodysize(Andersson,1994;Daleetal.,2007),and Panthera leo: Packer, Gilbert, Pusey, & Obrien, 1991) and even
thehighlyconspicuouscourtshipdisplaysobservedinmanyspe- sharingparentalcareoftheoffspringofasinglefemale(tamarins,
cies(Andersson,1994;Petrie,Krupa,&Burke,1999).Aconsistent Saguinus sp.: Díaz-Muñoz, 2011; Goldizen, 1987; humans, Homo
sapiens:Crook&Crook,1988; Smith,1998), appearsat firstpara-
doxicalbecauseitisoftenassociatedwithalossofdirectfitnessfor
at least some participating males. Following the realization that
q This is an open-access article distributed under the terms of the Creative indirectfitnessbenefitscanexplainapparentlyaltruisticbehaviour
Commons Attribution License, which permits unrestricted use, distribution, and (Hamilton,1963,1964b),kinselectionhasfrequentlybeeninvoked
reproductioninanymedium,providedtheoriginalauthorandsourcearecredited
to explain such examples of reproductive altruism. Kin selection,
* Correspondence:S.L.Díaz-Muñoz,DepartmentofPlantandMicrobialBiology,
however, cannot account for all occurrences of reproductive
331KoshlandHall,UniversityofCaliforniaBerkeley,Berkeley,CA94720-3102,U.S.A.
E-mailaddress:[email protected](S.L.Díaz-Muñoz).
0003-3472/$38.00(cid:1)2013TheAuthors.PublishedonbehalfofTheAssociationfortheStudyofAnimalBehaviourbyElsevierLtd.Allrightsreserved.
http://dx.doi.org/10.1016/j.anbehav.2013.11.008
68 S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78
cooperationamongmales,mostobviouslyincasesinwhichnon- we emphasize the breadth of cooperative behaviours observed
relatives cooperate (Clutton-Brock, 2002). This raises intriguing amongmalesaswellasthediversityoftaxainvolvedtofacilitatea
questionsaboutthewaysinwhichnaturalselection,sexualselec- more comprehensive exploration of this behaviour, given that it
tion and inclusive fitness interact to shape the reproductive doesnotfittypicalsexualrolesemphasizedintheliterature.
behaviourofmales.Asmoreexamplesofreproductivecooperation
havebeenexamined,ithasbecomeclearthatfitnessconsequences TypesofMaleReproductiveCooperation
to males vary markedly among species (Canestrari, Marcos, &
Baglione,2005;Díaz-Muñoz,2011;DuVal,2007;Francisco,Gibbs, To clarify our definition, we outline a few broad categories of
& Galetti, 2009; Kohda et al., 2009; Krakauer, 2005; Krakauer & malereproductivecooperationandconsiderbothexamplesthatfit
DuVal, 2011; Wagner, Creel, Frank, & Kalinowski, 2007), suggest- ourdefinitionandthosethatdonot.Wenotethatourcategories
ing a detailed, comparative exploration is needed to understand closely parallel the four types of cooperative reproduction pro-
thisphenomenon. posedbyTaborsky(2009)forfish.
Becausemalereproductivecooperationstandsattheintersec-
tionofsexualselectionandinclusivefitnesstheory,itisintegrally Cooperativedisplaycoalitions
tied tosome of the most active areas of researchin evolutionary Cooperative displaycoalitions occur whentwoor more males
biology. However, male reproductive cooperation has received congregate and coordinate their behaviours to attract and mate
surprisinglylittleattentionandhasnot,toourknowledge,beenthe withfemales.Maleswithinadisplaygrouparepotentiallyforgoing
subjectofageneral,syntheticreview.Morelimitedreviewswere solodisplaytoattractfemalesandmaynothavethechancetomate
conducted on male cooperation in fish (Taborsky, 2009) and on whiletheyholdsubordinatestatus.Forexample,manakinsinthe
cooperativedisplaysinbirds(Krakauer&DuVal,2011).Thisreview genusChiroxiphiaengageinelaboratemultimaleleapfrogdancesto
builds upon these papers by synthesizing the significance and attractfemales(DuVal,2007;McDonald,1989a),andsimilarcoor-
exploring the taxonomic applicability of the concept of male dinated displays may be common in this family (Ryder, Blake,
reproductive cooperation. Specifically we aim to (1) define and Parker, & Loiselle, 2011; Ryder, McDonald, Blake, Parker, &
summarize the multiple forms of male reproductive cooperation Loiselle, 2008). Other examples include wild turkeys (Krakauer,
reported in the literature, (2) outline potential adaptive explana- 2005)andpeafowl(Petrieetal.,1999).
tions for such cooperation, (3) explore the multifaceted ‘causes’
(ecological, demographic, phylogenetic, physiological) for malee Competitivecoalitions
male cooperation and (4) discuss the implications for sexual se- Competitive coalitions occur when two or more males join
lection,inparticularregardingpatternsofvarianceinreproductive forcestocombatothermalesvyingforaccesstoafemale.Perhaps
successandfemalematechoice.Inadditiontoprovidingthefirst themostfamiliarexampleofcooperativeintrasexualcompetition
comprehensivereviewofmalereproductivecooperation,thispa- for mates occurs in African lions, Panthera leo; males form co-
per intends to enhance understanding of this phenomenon by alitionstocompeteforaccesstofemalesandthevictor(s)ofsuch
outliningimportantdirectionsforfutureresearch. contests mate with pride females. Males that form coalitions
probablybenefitbyimprovingtheirchancesofwinningaggressive
WHATISMALEREPRODUCTIVECOOPERATION? contestswithcompetitors(relativetofightingalone),buttheypay
the certain cost of sharing breeding opportunities with females.
We define male reproductive cooperation as occurring when Thisbehaviourisalsoobservedinferalhorses,Equuscaballus(Feh,
twoormoremales,thatwouldotherwisebe(orare)reproductive 1999), dolphins (Connor et al., 1992) and baboons, Papio cyn-
competitors, engage in coordinated efforts to gain an advantage ocephalusanubis(Bercovitch,1988).
over other males in exclusive relation to reproduction. That is, Our definition generally excludes male coalitions that are
malescooperatetoattract,gainormaintainaccesstoafemale(s),or formedprimarilytogainaccesstoresourcesortoincreasesocial
toassistherreproduction.Suchcoordinationcanincludecourtship rank. While these coalitions are sometimes shown to increase
displays,coalitionaryaggressiontodefendorgainaccesstofemales reproductive success, they typically do so secondarily, meaning
orsharedcareofyoung.Ourdefinitionthusencapsulatesthemale theyaretheresultofrankandnotcooperativebehaviour,andtheir
reproductive cooperation outlined, but not explicitly defined, by reproductivebenefitscomminglewithothersurvivalbenefitssuch
Taborsky (2009) for fish. Individuals that cooperate to perform as food and territory. Following this reasoning, male red howler
these activities accrue greater inclusive fitness than conspecifics monkeys,Alouattaseniculus,thatformcoalitionstogainaccessto
thatengagein thesebehavioursontheirown. Inthisregard,our and defend females (Pope, 1990) engage in male reproductive
definition is consistent with the classic ecological concept of cooperation.Incontrast,malemacaques,Macacaassamensis,that
cooperation,whichconsistsofinteractionsinwhichbothpartici- form coalitions to ascend an intragroup dominance hierarchy do
pants benefit (Lidicker, 1979). The magnitude of these benefits, not meet our definition, even though they may increase their
however, may not be equal. In particular, because benefits are fitnessasaconsequenceoftheirnewrank(Schülke,Bhagavatula,
assessed in terms of inclusive fitness, individual males may gain Vigilant,&Ostner,2010).
from cooperating even though they engage in reproductive
altruism,meaningtheyappeartoforgodirectfitnessasamember Cooperativepolyandry
ofacooperativemalepartnership. Cooperative polyandry is a breeding system in which two or
Wehavedeliberatelysetabroaddefinitionformalereproduc- more males mate with a single female and assist in rearing her
tivecooperation.Thekeyelementsofourdefinitionarethatmales young. For instance, male Saguinus tamarins, which are usually
are potential reproductive competitors and that they coordinate relatives, mate with a single female and carry dependent young
theircooperativebehaviour.Futurequantitativestudiesmaywish (Díaz-Muñoz, 2011; Huck, Löttker, Böhle, & Heymann, 2005;
toincludeorexcludethebehavioursdescribedhereindepending Suarez, 2007). Other examples include Galapagos hawks, Buteo
onthequestiontheyaddress.Previousstudieshavereviewedand galapagoensis(Faaborgetal.,1995),someacornwoodpecker,Mel-
explainedcooperationamongmales,buttheywererestrictedtoa anerpesformicivorus,groups(Haydock&Koenig,2003),andcertain
single taxon (fish: Taborsky, 2009) or specific cooperative behav- humanculturalgroupsfromtheHimalayas(Crook&Crook,1988;
iour(competitivecoalitions:Olson&Blumstein,2009).Incontrast, Levine&Silk,1997).
S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78 69
Cooperativeparentalcare these elements of male behaviour and may also be productively
Cooperative parental care occurs in species in which males analysed.
engageincooperativeparentalcare,mateandgainpaternitybutdo
notformapolyandrousrelationshipwiththefemale.Thesemales WHOCOOPERATES?
are not helpers in the cooperative breeding sense (nonbreeding
members, usually from previous brood: Cockburn,1998; Skutch, OccurrenceofMaleReproductiveCooperationinVertebrates
1935; Solomon & French, 1997), but instead are co-breeders
(Dickinson,2004)thatmayormaynothave asocialrelationship Malereproductivecooperationhasnot,toourknowledge,been
withbreedingfemales(i.e.apairbond).Forinstance,subordinate systematicallydefinedorcategorizedacrosstaxa(butseeTaborsky,
males may assist a socially monogamous pair, as exemplified by 2009).Thus,tofindpeer-reviewedpapersdocumentingexamples
immigrantmalemeerkatsthatcompeteforbreedingopportunities of male reproductive cooperation, we conducted searches in ISI
andparticipateinbroodcarewithinagroup(Griffinetal.,2003). Web of Knowledge and Google Scholar to obtain the following
Malesmayalsoprovidecaretooffspringofmultiplegroupfemales exactphrasematches:‘malecooperation’,‘cooperativepolyandry’,
independentofsocialbonds.Forexample,maleCrotophagaanisare ‘male alliance’, ‘male coalition’, ‘cooperative display’, ‘male mate
sociallymonogamous,butmultiplepairsshareanest(acrèche);all sharing’,‘male mutualtolerance’.If thesesearchesyieldednore-
malessireyoungandprovidecarefornestlings(Riehl,2012).Other sults, we searched for anycombination of the terms. Searches in
examples include wild dogs, Lycaon pictus (Creel & Creel, 2002), Web of Science included the topic field, which examines article
pollinator fig wasps, Kradibia tentacularis (Suleman, Raja, & title,keywordsandabstract.GoogleScholarsearchesinvolvedfull
Compton, 2012), spider mites, Schizotetranychus celarius (Saito, text where available. In addition, for papers describing male
1986), and some populations of white-winged choughs, Corcorax reproductivecooperation,weexaminedassociatedreferencesand
melanorhamphos(Heinsohn,Dunn,Legge,&Double,2000). citedarticlestolocateadditionalexamples.
In contrast to co-breeders, nonbreeding male ‘helpers’ in Table1detailstheexamplesidentifiedbyoursearchesandwas
cooperatively breeding societies do not fit our definition of male usedtogeneratefiguresinthismanuscript.Althoughweattempted
reproductivecooperationbecausetheyarenotreproductivecom- to be exhaustive, this list likely omits some species, because the
petitors. We realize designating individuals as reproductive com- descriptions of male behaviour may employ terminology not
petitors can be challenging, particularly in cooperative societies; includedinoursearchparameters.Weexpectthatasresearchers
this difficulty applies to many complex breeding groups (e.g. becomemoreawareofthepossibilityofmalecooperation,exam-
Hauber & Lacey, 2005). We emphasize the distinction between ples previously overlooked will be identified and we encourage
nonbreeding helpers and co-breeders, because these terms are interested researchers to build on the data set complied for this
oftenconfusedintheliterature,andonlythelatterfallwithinour review.
definition,providedthereiscoordinatedcooperativebehaviour.
THEWHYANDHOWOFCOOPERATION
Mutualtoleranceandmatesharing
Mutualtoleranceandmatesharingoccurwhentwomalesshare The ‘cause’ofanybehaviour is complex and canbe examined
aterritoryandfemale,whichtheycollectively,butoftenseparately, fromavarietyofperspectivesdependinguponthequestionsbeing
defend.Thisbehaviourisasocialandtheonlycoordinationevident examined. Following Tinbergen (1963), we view these different
is mutual tolerance by males. This pattern is observed in striped perspectivesasnonexclusive,oftencomplementary,explanations.
hyaenas, Hyaena hyaena, in which two males defend a territory Below, we explore proposed explanations for male reproductive
containing a female; both males mate in the absence of a social cooperationusingmultiplelevelsofanalysis(Sherman,1988),both
relationship(Wagner,Frank,&Creel, 2008).Similar ‘asocial poly- proximateandultimate,andsuggestareasforfutureresearch.
andry’ have been reported for kinkajous, Potos flavus (Kays &
Gittleman,2001),side-blotchedlizards,Utastansburiana(Sinervo FitnessBenefits
&Clobert,2003)andcheetahs,Acinonyxjubatus(Caro,1994).
Thistypeofmaleemalecooperationpushestheboundariesof Male reproductive cooperation may involve the apparent sac-
our definition in that the behaviour is in essence asocial and co- rifice of direct fitness by at least some members of cooperative
ordination is minimal (i.e. males do not attack each other). partnerships. This apparent reproductive altruism parallels that
Furthermore, behaviours in this category likely entangle survival found in many cooperatively breeding societies, leading to the
benefitsformales.However,weconcurwithOlsonandBlumstein logical application of inclusive fitness theory (Hamilton, 1964a),
(2009),thatcooperationbetweenmalesisprobablyacontinuum, summarizedbyBrown(1987).
with tolerance at one end of the spectrum and obligate joint
participationattheother.Becauseintermediateformsofbehaviour Indirectfitnessbenefits
maybehighlyinformativeregardingtheevolutionofmaleemale Indirectfitnessbenefitsmayatleastpartiallycompensatemales
cooperation,wehavechosentoadoptalessrestrictiveperspective forapparentlossesincurrent(orfuture)directfitnessbenefits.A
andtoincludemutualtoleranceinourdiscussion. classicexampleofkinselectioninvolvespairsofmalewildturkeys
Wepresentthecategoriesaboveasaheuristictooltoorganize thatdisplaytogethertoattractfemales(Watts&Stokes,1971).This
thebroadarrayofbehavioursencompassedbymalereproductive wouldseemtoimposeacost,asmalewildturkeyscandisplayand
cooperation.Thesecategoriesmayforminterestingunitsofanal- mateontheirown.However,pairsaremoresuccessfulatmating
ysis in their own right. For example, the role of social and envi- andsiringchicks,andalthoughonlyonememberofthepairsires
ronmentalfactorsinshapingcompetitivemalecoalitionshasbeen young, the second male is closely related and accrues greater
evaluated by Olson and Blumstein (2009). Such analyses, to our fitnessbenefitsthansolomales(Krakauer,2005).
knowledge, have not been conducted for cooperative polyandry,
cooperativemaleparentalcareorcooperativemaledisplays,leav- Delayed(orfuture)fitnessbenefits
ingampleroomforfuturestudy.Althoughsomereadersmayview Delayed(orfuture)fitnessbenefitsmayleadtoincreasedlife-
thesecategoriesasdistinctphenomena,webelievethattheover- time fitness despite current losses of reproductive opportunities.
arching theme of male reproductive cooperation serves to unite Such delayed benefits may be particularly relevant in cases in
70 S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78
Table1
Thediversityofanimalspeciesinwhichmalesengageinreproductivecooperation,asreportedinthepeer-reviewedliterature
Species Group Order Family Typeofmalereproductive Source
cooperation
Chiroxiphialinearis Birds Passeriformes Pipridae Display McDonaldandPotts(1994)
Chiroxiphialanceolata Birds Passeriformes Pipridae Display DuVal(2007)
Chiroxiphiacaudata Birds Passeriformes Pipridae Display Foster(1981);Franciscoetal.(2009)
Chiroxiphiapareola Birds Passeriformes Pipridae Display Loiselleetal.(2006)
Piprafilicauda Birds Passeriformes Pipridae Display Ryderetal.(2008,2011)
Piprafasciicauda Birds Passeriformes Pipridae Display Robbins(1983)
Pipraserena Birds Passeriformes Pipridae Display Prum(1985)
Meleagrisgallopavo Birds Galliformes Phasianidae Display Krakauer(2005);WattsandStokes
(1971)
Pavocristatus Birds Galliformes Phasianidae Display Petrieetal.(1999)
Moxostomacarinatum Fish Cypriniformes Catostomidae Display Hackney,Tatum,andSpencer(1968)
Etheostomablennioides Fish Perciformes Percidae Display Fahy(1954)
Gallinulamortierii Birds Gruiformes Rallidae Cooperativepolyandry Goldizen,Buchan,Putland,Goldizen,
andKrebs(2000);Goldizen,Putland,
andGoldizen(1998);MaynardSmith
andRidpath(1972)
Prunellacollaris Birds Passeriformes Prunellidae Cooperativepolyandry Daviesetal.(1995);Hartleyetal.(1995)
Sericornisfrontalis Birds Passeriformes Acanthizidae Cooperativepolyandry MagrathandWhittingham(1997);
Whittingham,Dunn,andMagrath
(1997)
Melanerpesformicivorus Birds Piciformes Picidae Cooperativepolyandry HaydockandKoenig(2002)
Buteogalapagoensis Birds Falconiformes Accipitridae Cooperativepolyandry DeLayetal.(1996);Faaborgetal.(1995)
Eclectusparrots Birds Psittaciformes Psittaculidae Cooperativepolyandry Heinsohn,Ebert,Legge,andPeakall
(2007)
Prunellamodularis Birds Passeriformes Prunellidae Cooperativepolyandry Burke,Davies,Bruford,andHatchwell
(1989);Davies,Hatchwell,Robson,and
Burke(1992)
Porphyrioporphyrio Birds Gruiformes Rallidae Cooperativepolyandry CraigandJamieson(1990);Lambert,
Millar,andJack(1994)
Gallinulatenebrosa Birds Gruiformes Rallidae Cooperativepolyandry Garnett(1980)
Psophialeucoptera Birds Gruiformes Psophiidae Cooperativepolyandry EasonandSherman(1995);Sherman
(1995)
Corvuscoronecorone Birds Passeriformes Corvidae Cooperativepolyandry Baglione,Canestrari,Marcos,and
Ekman(2003);Canestrarietal.(2005)
Corvusbrachyrhynchos Birds Passeriformes Corvidae Cooperativepolyandry Townsend,Clark,McGowan,and
Lovette(2009)
Gypaetusbarbatus Birds Falconiformes Accipitridae Cooperativepolyandry Bertran,Margalida,andArroyo(2009)
Cyanocoraxmorio Birds Passeriformes Corvidae Cooperativepolyandry Williams(2004)
Catharactalonnbergi Birds Charadriiformes Stercorariidae Cooperativepolyandry Millaretal.(1994)
Melieraxcanorus Birds Falconiformes Accipitridae Cooperativepolyandry Malan(2005)
Calcariuspictus Birds Passeriformes Calcariidae Cooperativepolyandry Briskie(1992);Briskie,Montgomerie,
andPõldmaa(1998)
Saguinusfuscicollis Mammals Primates Callitrichinae Cooperativepolyandry Goldizen,Mendelson,VanVlaardingen,
andTerborgh(1996);Terborghand
Goldizen(1985)
Saguinusmystax Mammals Primates Callitrichinae Cooperativepolyandry Huck,Löttker,andHeymann(2004);
Huck,Löttker,Böhle,etal.(2005);Huck,
Löttker,Heymann,etal.(2005)
Saguinuslabiatus Mammals Primates Callitrichinae Cooperativepolyandry Suarez(2007)
Saguinusgeoffroyi Mammals Primates Callitrichinae Cooperativepolyandry Díaz-Muñoz(2011)
Leontopithecusrosalia Mammals Primates Callitrichinae Cooperativepolyandry Baker,Dietz,andKleiman(1993)
Symphalangussyndactylus Mammals Primates Hylobatidae Cooperativepolyandry Lappan(2007,2008)
Homosapiens Mammals Primates Hominidae Cooperativepolyandry CrookandCrook(1988);LevineandSilk
(1997);Smith(1998)
Julidochromistranscriptus Fish Perciformes Cichlidae Cooperativepolyandry Kohdaetal.(2009)
Chalinochromisbrichardi Fish Perciformes Cichlidae Cooperativepolyandry Awata,Munehara,andKohda(2005)
Neolamprologuspulcher Fish Perciformes Cichlidae Cooperativepolyandry Balshine-Earn,Neat,Reid,andTaborsky
(1998);Dierkes,Heg,Taborsky,Skubic,
andAchmann(2005);Dierkes,
Taborsky,andAchmann(2008);Stiver,
Dierkes,Taborsky,LisleGibbs,and
Balshine(2005)
Julidochromisornatus Fish Perciformes Cichlidae Cooperativepolyandry Awataetal.(2005);Awata,Heg,
Munehara,andKohda(2006)
Crotophagamajor Birds Cuculiformes Cuculidae Cooperativeparentalcare Riehl(2011,2012)
Corcoraxmelanorhamphos Birds Passeriformes Corcoracidae Cooperativeparentalcare Heinsohnetal.(2000)
Mungosmungo Mammals Carnivora Herpestidae Cooperativeparentalcare Keaneetal.(1994)
Lycaonpictus Mammals Carnivora Canidae Cooperativeparentalcare CreelandCreel(2002)
Ochotonacurzoniae Mammals Lagomorpha Ochotonidae Cooperativeparentalcare Dobson,Smith,andGao(1998);Yin,
Yang,Wei,andZhang(2009)
Suricatasuricatta Mammals Carnivora Herpestidae Cooperativeparentalcare Griffinetal.(2003)
Kradibiatentacularis Insects Hymenoptera Agaonidae Cooperativeparentalcare Sulemanetal.(2012)
Pleistodontesimperialis Insects Hymenoptera Agaonidae Cooperativeparentalcare ZammitandSchwarz(2000)
S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78 71
Table1(continued)
Species Group Order Family Typeofmalereproductive Source
cooperation
Schizotetranychuscelarius Arachnids Trombidiformes Tetranychidae Cooperativeparentalcare Saito(1986)
Nocomismicropogon Fish Cypriniformes Cyprinidae Cooperativeparentalcare Reighard(1943)
Notropisleptocephalus Fish Cypriniformes Cyprinidae Cooperativeparentalcare Wallin(1989)
Pelvicachromispulcher Fish Perciformes Cichlidae Cooperativeparentalcare MartinandTaborsky(1997)
Hemilepidotushemilepidotus Fish Scorpaeniformes Cottidae Cooperativeparentalcare DeMartiniandPatten(1979)
Cebuscapucinus Mammals Primates Cebidae Coalitions Perry(1996)
Eulemurfulvusrufus Mammals Primates Lemuridae Coalitions Ostner(2004)
Macacasylvanus Mammals Primates Cercopithecidae Coalitions Bissonnette,Bischofberger,andvan
Schaik(2010);Witt,Schmidt,and
Schmitt(1981)
Alouattaseniculus Mammals Primates Atelidae Coalitions Pope(1990)
Papiocynocephalus Mammals Primates Cercopithecidae Coalitions Bercovitch(1988);Alberts,Watts,and
Altmann(2003)
Hylobateslar Mammals Primates Hylobatidae Coalitions Savinietal.(2009)
Pantroglodytes Mammals Primates Hominidae Coalitions Watts(1998);Mitani,Merriwether,and
Zhang(2000);Gilbyetal.(2012)
Equuscaballus Mammals Perissodactyla Equidae Coalitions Feh(1999)
Tursiopssp. Mammals Cetacea Delphinidae Coalitions Connoretal.(1992);Connor,Smolker,
andBejder(2006)
Pantheraleo Mammals Carnivora Felidae Coalitions Bygott,Bertram,andHanby(1979);
Packeretal.(1991)
Artibeusjamaicensis Mammals Chiroptera Phyllostomidae Coalitions OrtegaandArita(2002);Ortega,
Maldonado,Wilkinson,Arita,and
Fleischer(2003)
Etheostomaolmstedi Fish Perciformes Percidae Coalitions Stiver,Wolff,andAlonzo(2013)
Bettabrownorum Fish Perciformes Osphronemidae Coalitions WitteandSchmidt(1992)
Bettapersephone Fish Perciformes Osphronemidae Coalitions WitteandSchmidt(1992)
Parablenniussanguinolentus Fish Perciformes Blenniidae Coalitions Oliveiraetal.(2002);Santos(1985);
SantosandAlmada(1988)
Cyprinodonmacularius Fish Cyprinodontiformes Cyprinodontidae Coalitions Barlow(1961)
Amphiprionakallopisos Fish Perciformes Pomacentridae Coalitions Fricke(1979)
Symphodusocellatus Fish Perciformes Labridae Coalitions Fiedler(2010);Lejeune(1985);
Taborsky(1987)
Symphodusroissali Fish Perciformes Labridae Coalitions Lejeune(1985)
Symphodustinca Fish Perciformes Labridae Coalitions Lejeune(1985)
Halichoeresmaculipinna Fish Perciformes Labridae Coalitions Thresher(1979)
Ourebiaourebi Mammals Artiodactyla Bovidae Mutualtoleranceandmatesharing Arcese(1999)
Herpestessanguineus Mammals Carnivora Herpestidae Mutualtoleranceandmatesharing Waser,Keane,Creel,Elliott,and
Minchella(1994)
Propithecusverreauxi Mammals Primates Indriidae Mutualtoleranceandmatesharing Kappeler,Mass,andPort(2009);
Port,Johnstone,andKappeler(2012)
Acinonyxjubatus Mammals Carnivora Felidae Mutualtoleranceandmatesharing Caro(1994)
Potosflavus Mammals Carnivora Procyonidae Mutualtoleranceandmatesharing KaysandGittleman(2001)
Utastansburiana Lizards Squamata Phrynosomatidae Mutualtoleranceandmatesharing SinervoandClobert(2003)
Catostomuscommersonii Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing Reighard(1920)
Hypenteliumnigricans Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing RaneyandLachner(1946)
Moxostomaaureolum Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing Reighard(1920)
Moxostomaduquesnei Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing Bowman(1970);KwakandSkelly
(1992)
Moxostomamacrolepidotum Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing BurrandMorris(1977);Jenkins(1970)
Moxostomaerythrurum Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing Jenkins(1970);KwakandSkelly(1992)
Moxostomavalenciennesi Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing Jenkins(1970);JenkinsandJenkins
(1980)
Erimyzonoblongus Fish Cypriniformes Catostomidae Mutualtoleranceandmatesharing PageandJohnston(1990)
Foreachspecies,thetaxonomicclassification,typeofmaleemalecooperationandsourcearelisted.Thedatainthistableareavailableinelectronicform(FigSharerepository
http://dx.doi.org/10.6084/m9.figshare.843622).
which,asaresultofreproductivecooperation,amalefailstosire previous examples that explain cooperation by males that are
young within a given breeding season but is not related to his excluded from reproduction. For example, in cooperatively poly-
presumablymoresuccessfulcooperativecompanion.Forexample, androus Galapagos hawks, multiple males mate with a single
lance-tailed manakins, Chiroxiphia lanceolata, form cooperative breedingfemaleandallofthemalesprovisionheryoung.Because
displaysofunrelatedmalesinwhichonlyonemaletypicallymates. malegroup-matesarenotrelated(Faaborgetal.,1995),theycannot
Intheabsenceofimmediatedirectfitnessopportunitiesandkin- gainindirectfitnessbenefitsfromsharingcareofyoung.Instead,
selected benefits, subordinate males instead benefit from an males apparently have equal and random probability of siring
increasedfutureprobabilityofbecomingthebreeder(DuVal,2007; young, resulting in shared paternity within and among breeding
McDonald&Potts,1994). attempts(Faaborgetal.,1995).
As has been noted in the cooperative breeding literature,
Currentdirectfitnessbenefits Brown’shypotheses(Brown,1987)arenotmutuallyexclusiveand
Current direct fitness benefits are shared among some or all thusourunderstandingofthefitnessbenefitsofcooperationmay
males in a group in many cooperative species, in contrast to lieindeterminingtheirrelativeimportance(Canestrarietal.,2005;
72 S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78
Dickinson,2004).Indeed,itmayberelativelycommonthatmales in asocial polyandry (Wagner et al., 2007) and cooperative male
accrue multiple types of fitness, with the relative contributions coalitions where resources dictate female distributions (Arcese,
varying in response to social and other conditions. For instance, 1999).
Packeretal.(1991)reportedthattherelativecontributionsofin- Although limited mating opportunities are apparently key to
directanddirectfitnessbenefitsincoalitionsofmalelionsappear most,ifnotall,malereproductivecooperation,theselimitsmaybe
to vary in response to coalition size. Specifically, males in small mediated by different factors. Cooperative male displays, for
coalitionstendtobeunrelatedandachieveroughlyequalmating instance, seem tobe associated with limits on social interactions
success, whereas males in largecoalitions are generallyclose kin (either via maleemale competition, or via female mate choice)
thatpartitiondirectfitnessmuchlessequitably,suchthatindirect ratherthanlimitedphysicalresourcessuchasfood,breedingter-
fitnessrepresentsa moreimportant component in larger groups. ritoriesornestingsites.Thus,theecologicalbasisofthoselimited
Increasingly,morestudieshaveexaminedbothindirectanddirect matingopportunitiesisapparentlylinkedtothetypeofmaleemale
fitnessbenefitsandhaverevealedadiversityoffitnessbenefitsto cooperationthatresults.
cooperatingmales.Tothisextent,reproductiveskewmodelsmay
helpto quantify howfitness is partitioned and what factors pro- PhylogeneticHistory
moteorhindercooperativegroups(Kokko&Johnstone,1999;Shen
&Reeve,2010). Whileaphylogeneticallycontrolledanalysisofmalereproduc-
tivecooperationisbeyondthescopeofthispaper,somedescriptive
Ecology,DemographyandSocialStructure statisticsonitstaxonomicdistributionareworthnoting.Wefound
87 species that fit our definition in the peer-reviewed literature,
Ecologicalfactorsmayhaveprofoundimpactsondemography representing22ordersand44familiesofanimals(Table1).Mostof
and social structure and, thus, on opportunities for male repro- the species identified are vertebrates, but we found two cases of
ductive cooperation. Insights into the effects of ecology on such male reproductive cooperation in insects and one in arachnids.
behaviour can be gleaned bystudying cases of maleemale coop- Somewhat surprisingly, fish and birds each had 28 species with
erationthatvaryduetoshiftsinecologicalconditions.Forinstance, examples of male reproductive cooperation, while mammals had
lone maleefemale pairs of callitrichines cannot reproduce in the 27. Male reproductive cooperation appears to be fairly widely
wild because of the high energetic demands of infant carrying distributedamongvertebrates,butattheordinallevelitisevident
(Goldizen, 1988), but they routinely do so in captivity, probably thatsomebranchesbearmultiplespeciesexhibitingthebehaviour,
becauseofreducedenergyneeds.Thisobservationhighlightsthe whilethemajorityoflineagesarerepresentedbyonlyoneorafew
apparent importance of male cooperation in meeting infant care suchspecies(Fig.1).Thus,evenintheabsenceofaformalphylo-
demands in different ecological settings. Similarly, a theoretical genetic analysis, it is evident that male reproductive cooperation
modelincorporatingresourcelimitation(i.e.alimitoninfantpro- has evolved multiple times within animals and, apparently, mul-
duction) predicted cases of cooperative polyandry in the acorn tipletimeswithinthreemajorlineagesofvertebrates.
woodpecker(Chao,1997). Whenthetaxonomicdistributionofeachoftheformsofmale
Territory quality also plays an important role in promoting reproductive cooperation is considered, several interesting pat-
maleemalecooperation.Forinstance,whilegibbons,Hylobateslar, terns emerge (Fig. 2). In fish, multiple examples of each type of
are traditionally thought of as monogamous, the probability of maleemalecooperationareevident.Coalitionsarethemostcom-
polyandrous male partnerships increases in lower-quality terri- monformofreproductivecooperationamongmammals,withno
tories (Savini, Boesch, & Reichard, 2009). Variation in resource instances of cooperative displays. In contrast, cooperative poly-
availabilityhasalsobeeninvokedtoexplainmutualmaletolerance andryismostcommoninbirds,withnoreportsofeithercoalitions
Primates
Perciformes
Passeriformes
Cypriniformes
Carnivora
Gruiformes
Falconiformes
Hymenoptera
Galliformes
Perissodactyla
Lagomorpha
Chiroptera Mammals
Cetacea Fish
Artiodactyla
Squamata Birds
Scorpaeniformes
Insects
Cyprinodontiformes
Psittaciformes Herpetofauna
Piciformes
Cuculiformes Arachnids
Charadriiformes
0 5 10 15
Trombidiformes
5 10 15
Number of species
Figure1. Malereproductivecooperationiswidespreadacrossanimalorders,butmanyordersarerepresentedbyasingleexample.Coloureddotsdepictthenumberofspeciesin
eachorderthatshowanexampleofmaleemalecooperation.Colourscorrespondtothemajoranimalgroupslabelledintheinset.Theinsetshowsthenumberofspecieswithmale
reproductivecooperationineachmajorgroup.
S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78 73
cooperative behaviour. Mechanisms such as kin recognition, hor-
Cooperative parental care
monalvariationsandcognitiveabilitiesarelikelytovarydepending
Mammals onthespecificnatureofmaleemalecooperationandthebiological
Fish abilitiesofdifferentspecies.However,noneoftheseaspectsofmale
Birds cooperationhasbeenwellstudied.Weexpectthatthephysiolog-
Insects ical mechanisms mediating male cooperation will vary substan-
Lizards tiallyinspeciesforwhichtheaveragemalepartnershipisshorter
Arachnids versuslongerthanasinglebreedingcycle.
In situations where male partnerships are long relative to a
Competitive coalitions
singlebreedingcycle,severalmechanismsmaybeinvolved.When
Mammals interactions among male relatives are common, kin recognition
Fish mayfacilitatemalecooperation,encompassingmechanismsfrom
Birds individualrecognitionofkinduetoashareddevelopmentalenvi-
Insects ronment to self-referential phenotype matching (Hauber &
Lizards Sherman,2001).Giventhatmalerelationshipscaninvolveexten-
Arachnids sive prosocial behaviour over extended periods (e.g. Garber,
Encarnación, Moya, & Pruetz, 1993; Goldizen, 1989), hormonal
Cooperative polyandry
mechanisms may facilitate this social bond. Hormones such as
Mammals oxytocin and vasopressin have been studied primarily in the
Fish context of maleefemale monogamous pair bonds, but they also
Birds influence social aggregations (Goodson, Schrock, Klatt, Kabelik, &
Insects Kingsbury, 2009), increase trust in social situations (Kosfeld,
Lizards Heinrichs, Zak, Fischbacher, & Fehr, 2005) and, importantly, in
Arachnids femaleefemale relationships (Beery & Zucker, 2010). Whether
thesehormonesalsomediatemaleemalerelationshipsremainsan
Cooperative display
intriguing question. Furthermore, do males and females in coop-
Mammals erativelypolyandroussituationsdevelophormonalprofilessimilar
Fish topair-bondedmonogamousspecies?
Birds Males mayalso have other hormonal mechanisms to mediate
Insects behaviouralchangesinstate,suchastestosteroneandglucocorti-
Lizards coids, in the presence of a male partner. An examination of the
Arachnids hormonalstateofcooperativelypolyandrousmoustachedtamarin,
Saguinus mystax, males suggested little difference in testosterone
Mutual tolerance and mate sharing
and cortisol levels among males, despite differences in breeding
Mammals success(Huck,Löttker,Heymann,&Heistermann,2005).Hormonal
Fish profileswilllikelyvaryaccordingtothetypeofmalecooperative
Birds behaviours: species with parental care might differ from species
Insects that form male coalitions for combat. Additionally, we speculate
Lizards that behavioural feedbacks on hormone levels may differ from
Arachnids noncooperative species; for example, ‘winner’ and ‘loser’ effects
(Hsu, Earley, & Wolf, 2005) may be less dramatic if male in-
0 2 4 6 8
teractionsoccurinthecontextofbothwithin-andamong-group
Number of species
hierarchies. Experimental studies that manipulate male partner
Figure2. Thedifferenttypesofmalereproductivecooperationareunevenlydistrib- presence are likelytoprovide greatinsight intothephysiological
utedamongmajoranimalgroups. basesofmaleemalecooperation.
The physiological mechanisms regulating cooperative ten-
or mutual tolerance. We find it intriguing that the relative fre- dencies in temporaryassociations of males raise more questions.
quency of the different forms of this cooperation varies across These mechanisms may be similar to those mediating long part-
vertebrate lineages, suggesting that fundamental evolved (phylo- nerships,butexpressedinacontext-dependentmanner.Alterna-
genetic) differences in the biology of these organisms may have tively,transientmale cooperation mayinvolve complexcognitive
played a role in shaping opportunities for cooperative male functions thatintegratecues fromthe socialand ecological envi-
behaviour. ronmentinnearreal-time.Thisseemsprobableincasesofcoop-
We would like to emphasize that the taxonomic patterns are erative aggression, and in particular in cases of intercession, in
based on our initial survey of the literature and thus may not which a male must make decisions mid-conflict based on the
provideadefinitivedescriptionofthephylogeneticdistributionof identities ofwarringparties.These complexcognitive behaviours
thisbehaviour.Ourpurposeistoprovideanoverviewofourcurrent havebeenwelldocumentedinprimates(deWaal&Tyack,2003),
knowledgetopromoteidentificationofpreviouslyoverlookedex- but alsooccur in spottedhyaenas, Crocutacrocuta (Engh,Siebert,
amplesofmalereproductivecooperation.Futureresearchonmale Greenberg, & Holekamp, 2005). These cognitive abilities are also
reproductive cooperation should benefit by considering both the likely to be manifested in reproductive contexts and represent
ecologicalandevolutionaryfactorsassociatedwiththisbehaviour. productivetargetsforfutureresearch.
Insummary,themechanisticunderpinningsofmalereproduc-
PhysiologicalMechanismsofMaleCooperation tive cooperation seem to be particularly poorly understood. By
conducting such analyses in a comparative framework it will
Malereproductivecooperation raises the question ofmale re- eventually be possible todetermine howthese mechanisms vary
lationshipsandthegenetic,hormonalandneuralunderpinningsof with eachtype ofcooperation. We believethat, as outlined here,
74 S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78
the recognition of male reproductive cooperation as a single, dimorphism, many cooperatively polyandrous species are mono-
overarchingphenomenonwillfostercomparativeinvestigationof morphic(e.g.Galapagoshawks),butspeciesengagingincoalitio-
the diverse mechanisms underlying specific examples of such nary aggression show marked dimorphism (e.g. lions). It seems
cooperation. likelythatthespecificadaptivefunctionofcooperationcontributes
tothedegreeofdimorphismobserved.Thus,becausegreaterbody
MALEREPRODUCTIVECOOPERATIONANDSEXUALSELECTION sizemayenhancetheabilityofmalestoacquireordefendaprideof
females,selectionmayfavourgreaterdimorphismascomparedtoa
Sexual selection theory goes far beyond the basic construct speciessuchasGeoffroy’stamarin,Saguinusgeoffroyi,inwhichthe
taught in introductory biologycourses, that of ardent males bat- primary benefit of male cooperation (cooperative care of young)
tlingeachotherfortheattentionofcoyfemales.Exceptionstothis seemsunlikelytoimposestrongselectionforsexualdimorphism.
simplisticstatementwerepointedoutbyDarwinhimself(e.g.sex- Kinshipamongcooperatingindividualsmayalsobeanimportant
rolereversedspecies:Darwin,1871)andthevarietyofsexualroles factor,withkinshipandindirectfitnessbenefitsgenerallyexpected
explainedbythistheoryhasbeenexpandedbydecadesofinves- toreducevarianceinmalereproductivesuccess,intensityofsexual
tigationintoreproductivestrategies(Emlen&Oring,1977;West- selection, and thus sexual dimorphism. Among species lacking
Eberhard, 1979), including elaboration of female sexual traits, maleparentalcare,however,thereisnoobviousrelationshipbe-
alternativematingtacticsandstrategiesusedbybothsexes,andthe tweenthetypeoffitnessbenefit(e.g.direct,indirect)derivedfrom
importance of the social environment. Empirical and theoretical male cooperation and the degree of sexual dimorphism. For
studies in areas such as sexual conflict and parental investment example,threebirdtaxawithcooperativemaledisplay(wildtur-
theory (Chapman, Arnqvist, Bangham, & Rowe, 2003; Kokko & keys,Chiroxiphiamanakins,andruffs,Philomachuspugnax),repre-
Jennions,2008),haverevealedthatthereproductivestrategiesof senting a range of reproductive sharing among males, have high
malesandfemalesarenotasclearlydistinctastextbookaccounts levelsofsexualdimorphismevencomparedtoothermembersof
wouldsuggest.Therefore,muchoftherenewedinterestinsexual theirfamilywithoutmalecooperation.Thus,theinfluenceof the
selectionhas(rightly)focusedonhowtheunexpectedbehaviours typeofmalecooperation,reproductivesharingandmalerelated-
thatsomefemalesexhibitfitintosexualselectiontheory.However, nessonsexuallyselectedtraitsareprimetargetsforinvestigation.
malecooperationinreproductivecontextshasreceivedrelatively Littleempiricalworkhasexaminedtheroleofmalecooperative
little attention, despite its potential to contribute to our under- behaviouronsexualselection.Afascinatingexampleistheevolu-
standing of sexual selection. Notably, because male reproductive tion of male polymorphisms coincident with different status or
cooperationbrings togethersexualselectionandinclusivefitness roles. In bearded manakins (Manacus sp.), males of the yellow
theory (Rubenstein, 2012), it extends our thinking beyond the morph preferentially lek with (yellow) relatives, leading to
classic boundaries of male reproductive competition. Among the increased reproductive success over white males and facilitating
resultingquestions,weposetwohere.(1)Howdoestheoccurrence positive selection of the yellow morph in the population
of male reproductive cooperation influence the action of sexual (Concannon,Stein,&Uy,2012).Malecooperationcanfacilitateother
selection? (2) What is the full range of reproductive and social selection patterns, such as in lazuli buntings, Passerina amoena,
behavioursthatcanbethoughtofassexuallyselectedtraits? where mutual male tolerance of divergent male morphs causes
disruptiveselectiononmaletraits(Greeneetal.,2000).Empirical
VariationinReproductiveSuccess,MaleCompetitionandTrait evidencealsoshowsthepotentialforhighlevelsofsexualdimor-
Evolution phism to evolve in the face of reproductive cooperation. Repro-
ductive skew is pronounced population-wide in the long-tailed
Forsexualselectiontoalterphenotypictraits,thesetraitsmust manakin, Chiroxiphia linearis (McDonald,1989a,1989b), notwith-
beassociatedwith differences inindividual reproductive success. standingmalecooperationindisplaystofemales.Thus,despitethe
Reproductivecooperationamongmaleshasthepotentialtoaffect relativerarityofmalecooperation,webelievethereisatremendous
reproductive success of both males and females, thereby influ- opportunitytomeldnewtheoreticalresearchontheimpactofthis
encingtheevolutionofsexuallyselectedtraits.Ingeneral,variance behaviouronclassicmodelsofsexualselectionwithempiricalwork
inreproductivesuccessisassumedtobegreaterformales,leading totestmodelsandrevealpatternsthatselectionproducesinnature.
totheexpectationthattheintensityofsexualselectionwillalsobe
greater for individuals of this sex. Depending upon the specific RoleofFemaleChoice
patterns of fitness involved, male reproductive cooperation may
eitherincreaseordecreasevarianceinmalereproductivesuccess. Classicsexualselectiontheorypositsthatfemalechoice(inter-
Inspeciesinwhichdirectfitnessisrestrictedtothedominantin- sexualselection)isapowerfulforcedrivingtheevolutionofmale
dividualinmalepartnerships,weexpectgreatervarianceinmale phenotypic traits. The selective pressures imposed by female
reproductive success due to the presence of nonbreeding sub- matingpreferencesaretraditionallyassumedtoleadtoenhanced
ordinates and to the failure of some males to form cooperative competition among males (intrasexual selection). Given this
relationships.Sexualdimorphisminthesespeciesshouldberela- perspective on the relationship between inter- and intrasexual
tivelypronounced.Incontrast,inspeciesinwhichreproductionis selection,howcanfemalechoicedrivetheevolutionofreproduc-
shared among partners, reproductive cooperation may serve to tivecooperationamongmales?
reduce variance in male reproductive success by increasing the The potential role of female choice in promoting cooperative
numberofindividualswhoachievedirectfitness;inthesespecies, male care of young is relatively straightforward. Females may be
if all else is equal, sexual dimorphism may be comparatively moresuccessful,andthusprefer,multiplemalestocareforyoung.
modest. Although variance in reproductive success, intensity of Forexample,inthecichlidJulidochromisornatus,femalesthathad
sexualselectionandsexualdimorphismarenodoubteachshaped two male helpers produced more offspring when controlling for
by multiple factors, reproductive cooperation among males gen- groupsize(Awata,Kohda,Shibata,Hori,&Heg,2010).Similarly,in
eratestestablepredictionsregardingtheeffectsofvarianceinmale closely relatedJulidochromisornatus, experimental manipulations
reproductivesuccessonphenotypictraitevolution. revealedthatpolyandrousfemalesobtainedmoreparentalcareby
The role of male cooperative behaviour in shaping sexually manipulating paternityallocation, leading to higher success than
selected traits is unclear. For instance, in the case of sexual monogamousfemales(Kohdaetal.,2009).
S.L.Díaz-Muñozetal./AnimalBehaviour88(2014)67e78 75
Not all examples of male reproductive cooperation relate to instance, while cooperatively polyandrous male tamarins are
malecare;inthesespecies,whatarethebenefitstofemalesthat famously prosocial (Goldizen, 1989) and have similar hormonal
prefer maleemale cooperation? It is possible that females prefer profiles(Huck,Löttker,Heymann,etal.,2005),availableevidence
elaborate displays that require coordination by male partners, as points to intense sperm competition within male partnerships
may be the case in Chiroxiphia manakins (Trainer, McDonald, & (Garber,Moya,Pruetz,&Ique,1996;Harcourt,Purvis,&Liles,1995).
Learn, 2002); in these species, multiple males can serve as an Similarly,althoughmalelionscooperatetoacquireordefendprides
extended phenotype used by females to select males (Trainer & of females from other males, competition among coalition mates
McDonald, 1995). Furthermore, coordinated teams of displaying leads to rank-related differences in reproductive success (Packer
males mayallow moreefficient mateassessmentorharassment- etal.,1991).
free mating. With regard to the latter, cooperative coalitions of Clearly, cooperationand competitionamong males are closely
wild turkeys exclude other males from access to females and, intertwined. While competition has historically received consid-
because within-coalition dominance is determined prior to the erableattentionfrombiologists,wehopetodrawincreasedfuture
breedingseason(Krakauer,2005),thereisrarelysquabblingamong attention to cooperation.Overstating theimportanceof competi-
male partners over who gets to mate. Finally, females may also tioncanleadtoneglectingimportantbehavioursandsubtlyshape
prefer groups of males because they are better than lone in- our views on evolutionary theory (Sussman, Garber, & Cheverud,
dividuals at defending infants (e.g. redfronted lemurs, Eulemur 2005), influencing other fields of study (MacKinnon & Fuentes,
fulvus rufus: Ostner, 2004; capuchin monkeys, Cebus capucinus: 2005). We hope this review will encourage theoretical and
Fedigan, Rose, & Avila,1996), or gaining access to resources in a empiricalworkonthisunderappreciatedbehaviour,therebylead-
given area (Savini et al., 2009). In summary, females may prefer ingtoagreaterunderstandingofthebalancebetweencooperation
cooperativemalesformultiplereasons,suggestingthatintersexual andconflictinevolution.
selectionisakeyforcefavouringreproductivecooperationamong
males.
CONCLUSIONS
NovelTheoreticalApproaches
The ultimate goal of this paper was to highlight examples of
malereproductivecooperationacrossanimaltaxa.Wehaveiden-
We believe that studies of systems characterized by male tifiedaninitiallistofexamplesthatwehopeareusedandextended
reproductive cooperation offer tremendous opportunities to bythe researchcommunity. We believethat significant advances
enhanceourunderstandingofthefullcomplexityofsexualselec-
will emerge from future studies examining the causes, conse-
tionanditseffectsonbehaviouralandotheraspectsofphenotypic
quences and correlates of male reproductive cooperation. In-
variation.Althoughsexualselectiontheoryhastraditionallybeen vestigationsofthefitnessconsequencesof thisphenomenonwill
dominated by the contributions of Bateman (1948) and Trivers highlightthecomplexinterplaybetweenconflictandcooperation
(1972), there is growing awareness of alternative theoretical ap- and should reveal the utility of inclusive fitness to explain more
proaches. For example, the concept of dynamic mating markets
than just classic cases of cooperative breeding. Studies of the
(Noë & Hammerstein, 1994), newly applied to sexual selection
ecological factors associated with male reproductive cooperation
(Patricelli,Krakauer,&McElreath,2011),emphasizesmultiplepo-
will contribute to the long-standing debate regarding the role of
tentialintersexualprospectsandintrasexualcompetitors.Thus,the
ecologyingeneratingsocialorganization.Researchintothephys-
occurrenceofcooperativepartnershipsaswellastheopportunities
iological mechanisms underlying male reproductive cooperation
and constraints that they impose become important factors for
represent,inouropinion,alargelyunexploredwealthofinforma-
investigation. In addition to possessing attractive phenotypes,
tionthatwilladvancethestudyof the physiologyandbehaviour
malesmustalsohavesufficientresponsivenessandskilltoachieve
alike, merging proximate and ultimate approaches. Finally, we
maximum fitness (Patricelli, Uy, Walsh, & Borgia, 2002). Recent
proposethatmalereproductivecooperationprovidesanimportant
debates about the utility of sexual selection theory highlight the
contextforexploringnewperspectivesonsexualselectiontheory,
needtoexpandthescopeofsexualselectionresearchbeyondthe
whichinturnmaybegreatlyenhancedbyconsideringcooperative
single maleefemale dyad (Rubenstein, 2012). Accordingly, social
interactionsamongindividuals.
network analysis has been used to explore how relations well
beyondthedyadiclevelinfluencesocialrelationships(Croftetal.,
2006), including maleemale cooperation (McDonald, 2007). We Acknowledgments
believethatsystemscharacterizedbymalereproductivecoopera-
tionareidealtofullyrealizethepotentialofavarietyofselection S.L.D.M.wassupportedbyaNationalScienceFoundation(NSF)
models because (1) they include social behaviours not often PostdoctoralResearch FellowshipinBiologyundergrantno. DBI-
considered in reproductive contexts, (2) male fitness is explicitly 1003098.S.L.D.M.wouldliketoacknowledgetheinfluenceofex-
dependent on interactions with both same- and opposite-sex in- changeswithAnneW.Goldizen,PaulA.GarberandLinChaoonhis
dividualsand(3)femalematechoicemaybebasedonanextended thinking about animal cooperation. A.H.K. was supported by NSF
multimalephenotype,challengingtraditionalconceptualandsta- grants NSF IOS-0925038 (to Gail Patricelli and A.H.K.) and IOS-
tisticalapproachesthatassessdifferentialreproductivesuccessin 1258217(toGailPatricelli,JenniferForbeyandA.H.K.).E.H.D.was
relation to one or a few traits. Theoretical models incorporating supportedbyNSFgrantIOS-0843334.E.A.L.wassupportedbythe
theseelementsshouldgeneratesignificantnewinsightsintohow DonnaandGaryFreedmanChairinUndergraduateEducationatthe
sexual selection shapes the morphology and behaviour of UniversityofCaliforniaBerkeley.
individuals.
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