This is a repository copy of The evolution of parental cooperation in birds.

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1 This is a repository copy of The evolution of parental cooperation in birds. White Rose Research Online URL for this paper: Version: Accepted Version Article: Remes, V., Freckleton, R.P., Tokolyi, J. et al. (2 more authors) (2015) The evolution of parental cooperation in birds. Proceedings of the National Academy of Sciences, 112 (44). pp ISSN Reuse Unless indicated otherwise, fulltext items are protected by copyright with all rights reserved. The copyright exception in section 29 of the Copyright, Designs and Patents Act 1988 allows the making of a single copy solely for the purpose of non-commercial research or private study within the limits of fair dealing. The publisher or other rights-holder may allow further reproduction and re-use of this version - refer to the White Rose Research Online record for this item. Where records identify the publisher as the copyright holder, users can verify any specific terms of use on the publisher s website. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by ing eprints@whiterose.ac.uk including the URL of the record and the reason for the withdrawal request. eprints@whiterose.ac.uk

2 Classification BiologicalSciences,Evolution Title- The-evolution-of-parental-cooperation-in-birds- - Short-title Parentalcooperationinbirds Authors- Vladimír-Remeš a,-robert-p.-freckleton b,-jácint-tökölyi c,-andrás-liker d,-tamás-székely e,f Author-affiliation adepartmentofzoologyandlaboratoryofornithology,palackyuniversity,17.listopadu50,77146 Olomouc,CzechRepublic bdepartmentofanimalandplantsciences,alfreddennybuilding,universityofsheffield,sheffields10 2TN,UK cmtatde Lendület BehaviouralEcologyResearchGroup,DepartmentofEvolutionaryZoology, UniversityofDebrecen,Egyetemtér1,4032Debrecen ddepartmentoflimnology,universityofpannonia,warthavinceu.1.,ht8201veszprém,hungary edepartmentofbiologyandbiochemistry,universityofbath,bathba27ay,uk fstatekeylaboratoryofbiocontrolandcollegeofecologyandevolution,sunyattsenuniversity, Guangzhou ,China Corresponding-author VladimírRemeš,DepartmentofZoologyandLaboratoryofOrnithology,PalackyUniversity,17.listopadu 50,77146Olomouc,CzechRepublic tel:+420t vladimir.remes@upol.cz 1

3 2 30 Abstract 31 Parentalcareisoneofthemostvariablesocialbehaviorsanditisandexcellentmodelsystemto 32 understandcooperationbetweenunrelatedindividuals.threemajorhypotheseshavebeenproposedto 33 explaintheextentofparentalcooperation:sexualselection,socialenvironment,andenvironmental 34 harshness.usingthemostcomprehensivedatasetonparentalcarethatincludes659birdspeciesfrom familiescoveringbothuniparentalandbiparentaltaxa,weshowthatthedegreeofparental 36 cooperationisassociatedwithbothsexualselectionandsocialenvironment.consistentwithrecent 37 theoreticalmodelsparentalcooperationdecreaseswiththeintensityofsexualselectionandwithskewed 38 adultsexratios.theseeffectsareadditiveandrobusttotheinfluenceoflifethistoryvariables.however, 39 parentalcooperationisunrelatedtoenvironmentalfactors(measuredatthescaleofwholespecies 40 ranges)asindicatedbyalackofconsistentrelationshipwithambienttemperature,rainfallortheir 41 fluctuationswithinandbetweenyears.theseresultshighlightthesignificanceofsocialeffectsfor 42 parentalcooperationandsuggestthatseveralparentalstrategiesmaycotexistinagivensetofambient 43 environment Significance-Statement 47 Parentsinmanyanimalspeciescarefortheiroffspring.Insomespeciesmalescaremore,inotherspecies 48 femalescaremore,whereasinstillotherspeciesthecontributionofthesexesisequal.yet,wedonot 49 knowwhatexplainsthesedifferencesamongspecies.usingthemostcomprehensiveanalysesofparental 50 caretodate,hereweshowthatparentscooperatemorewhensexualselectionisnotintenseandtheadult 51 sexratioofmalestofemalesisnotstronglyskewed.however,thedegreeofparentalcooperationis 52 unrelatedtoharshnessandpredictabilityoftheambientenvironmentduringthebreedingseason.our 53 workthereforesuggeststhatseveraltypesofparentalcaremaycotexistinagivensetofambient 54 environment. 55 \body 56

4 3 Parentalcooperation,definedhereastheextentofbiparentalcare,variesalongacontinuumfrom 57 approximatelyequalsharebythemaleandfemaletoobligateuniparentalcare,wherebyoneparent(the 58 maleorthefemale)providesallcarefortheyoung(1,2).bycooperatingwitheachother,themaleandthe 59 femaleparentincreasegrowthandsurvivaloftheiryounginvariousinsects,fishes,amphibians,birds, 60 andmammals(3 5).Thustheextentofparentalcooperationmayinfluencereproductivesuccessand 61 populationdynamics.parentalcareisanexcellentmodelsystemforinvestigatinginteractionsbetween 62 twounrelatedindividuals(6,7),anditisoneoftheprimeexamplesofgamettheoreticanalysesofconflict 63 andcooperationboththeoreticallyandempirically(8 11).Therefore,understandingthedriversof 64 parentalcooperationisoneofthelynchpinsofbreedingsystemevolutionandcooperativebehavior Sexualselection,socialenvironment,andambientenvironmenthavebeenproposedtoexplainvariation 67 intheextentofcooperationbetweenparents(7,12 14).First,cooperationbetweenparentsshould 68 decreasewiththeintensityofsexualselection(10,15,16)andareasonforthisreductionmaybethat 69 sexualselectionfavorsthesexwithhighervarianceinmatingsuccesstoreducehis(orher)care 70 provisioning(17 19).Moreover,highmatingeffortmightfurtherdecreasetheabilityofthesexunder 71 strongersexualselectiontocontributetoparentalcare(20).furthermore,highratesofextratpair 72 paternityshouldleadtotheevolutionofreducedcareprovisioningbymales(21 25).Thisevolutionary 73 reductionofpaternalcareinspecieswithhighextratpairpaternitywouldtranslateintoreducedparental 74 cooperation.second,thesexthatisinshortsupplyinthepopulationhasanincreasedmatingopportunity 75 andisthuslesslikelytoprovidecarethanthemoreabundantsex(26 28).Therefore,socialenvironment 76 (i.e.,sexratioofadultsinthepopulation)isexpectedtoinfluenceparentalbehavior(8,23,29,30).third, 77 environmentalfactorsareknowntoinfluencecomplexsocialbehaviorinvertebrates(31 33).More 78 specifically,demandingenvironmentalconditionsimposinghighercostsofliving,suchaslowfoodsupply 79 orharshandunpredictableclimates,shouldpromoteparentalcooperation(34 36)andlimitsocial 80 conflict(37),andthisideahasbeenrecentlybackedbyextensivemodeling(38 39).Althoughprevious 81 testsofthesehypothesesprovidedimportantinsightsintothepotentialdriversofparentalcooperation, 82 nostudyhasyettestedallthreehypothesesacrossabroadrangeoftaxaandassessedtheirrelative 83 importance Here,weusedataonparentalcooperationin659birdspeciesfrom113familiestotestthesethreemajor 86 hypotheses.birdsareoneofthemostsuitableorganismstotestthesepropositions,sincetheyexhibitthe 87 fullrangeofparentalcooperationfrombiparentalcaretouniparentalcare,anddetaileddataareavailable 88

5 4 onparentalbehaviorofabroadrangeoftaxafromwildpopulations.sinceparentalcareisacomplextrait, 89 wecompileddataon8componentsofcare(40)andquantifiedparentalcooperationbasedonsextspecific 90 contributiontocareintheseparentalactivitiesspanningthewholeparentalcareperiod(fullmaterials 91 andmethodsareavailableinsiappendix,supplements1).wefocusedoncareprovisioningbythemale 92 andthefemaleparent,andtheextentofparentalcooperationwasestimatedonascalethatvaried 93 between 1.5whenonlyoneparent(themaleorthefemale)providesallcareand1.5whenthemaleand 94 thefemaleparentshareprovisioningapproximatelyequally(frequencydistributionofparental 95 cooperationacross659speciesofbirdsisavailableinsiappendix,fig.s1) Usingphylogeneticanalyseswetestthefollowingpredictions:i)sexualselection:parentalcooperationis 98 higherinsociallymonogamousspeciesandinspecieswithlowratesofextratpairpaternity(epp),thanin 99 polygamousandhigheppspecies,respectively;ii)socialenvironment:specieswithbalancedadultsex 100 ratios(asr,proportionofmalesintheadultpopulation)exhibitmoreparentalcooperationthanspecies 101 withbiasedasr;andiii)ambientenvironment:speciesthatliveinenvironmentswithharshandvariable 102 climatesexhibithighparentalcooperation Results-and-Discussion 105 Theextentofparentalcooperationisusuallyconservedwithinmajorclades(Fig.1),whichisconsistent 106 withhighvaluesofphylogeneticsignal(λ 0.9,Table1;exactestimatedλvaluesareavailableinSI 107 Appendix,TableS1).Atthesametime,parentalcooperationishighlyvariablebetweencladesacross 108 birds.forexample,grebes,woodpeckers,andsparrowsarecharacterizedbyextensiveparental 109 cooperation,whereasothersexhibitlowcooperation(e.g.ducks,pheasantsandgrouse,andowls,fig1). 110 Severalclades,however,exhibithighinterTspecificvariationinparentalcooperation;forexamplesnipes, 111 sandpipersandallies,andoldworldwarblers(fig.1) Bothsexualselectionandsocialenvironmentpredictparentalcooperationasshownbyphylogenetic 114 generalizedleastsquaresanalyses(41)usingthemostrecentcompleteavianphylogeny(42)(table1, 115 Figs.2,3;fordetailsoftheserelationshipsseeSIAppendix,TableS1andFig.S2).First,intensesexual 116 selectionasindicatedbyextensivesexualsizedimorphism(43)andhighratesofextratpairpaternityare 117 consistentlyassociatedwithlowparentalcooperation(figs.2,3).toconfirmthatourpredictionsalso 118 holdwhentestingthemaleinvolvementincare,wealsoanalyzedrelativemalecare,whichisaproxyof 119 parentalcarebiasexpressedonthescalefromfemaletbiasedtomaletbiasedcare(frequencydistribution 120

6 5 ofrelativemalecareacross659speciesofbirdsisavailableinsiappendix,fig.s1).ourpredictionsare 121 supported,sincemalecare(relativetofemalecare)islowinspecieswithmaletbiasedsexualsize 122 dimorphismandhighinspecieswithfemaletbiaseddimorphism.moreover,malesprovidelittlecarein 123 specieswithhighextratpairpaternity(fig.3;summarizedresultsareavailableinsiappendix,tables2 124 whiledetailedresultsareavailableinsiappendix,tables3andfig.s3) Theseresultsareinlinewiththeoriesoftheevolutionofparentalcooperation(2,17,25,44).Specifically, 127 ourresultsareconsistentwiththepredictionthatthelargersex(usuallythemaleinbirds),whichisoften 128 understrongersexualselectionthanthesmallersex,reducesitscareprovisioning(17,19),translating 129 intolowercontributiontocareonmacroevolutionarytimescales.similarly,ourresultssupportthe 130 predictionthathighratesofextratpairpaternitywilllead,onamacroevolutionarytimescale,toa 131 reductioninmalecare(22 25)andconsequentlytoreducedparentalcooperation.Atthesametime,this 132 resultisfarfromtrivial,becausesomemodelspredictvariablerelationshipsbetweenmalecareandextrat 133 pairpaternitydependingonmodelassumptions(45)andresultsofpreviousempiricalstudiesarealso 134 conflicting(e.g.22,46 48,reviewedin25).Itisworthstressingthattherelationshipwedocumentisthe 135 mostcomprehensiveinanymajortaxonandmakesasignificantcontributiontoprevioustheoreticaland 136 empiricalinvestigationsofextratpairpaternityandparentalcare.themacroevolutionaryresponseof 137 malecaretoextratpairpaternitymaynotdependontheabilityofmalestoperceivepaternitylossintheir 138 contemporarybroodsandrespondtoitbyfacultativereductionofpaternalcare(21,22,24,46),although 139 thisabilityseemstobewidespreadamonganimals(25).reductionofmaleparentalcontributiondueto 140 femalepromiscuitymightleadtoloweroverallparentaleffort(49),andeventualbreakdownofbiparental 141 breedingsystems(21) Second,parentalcooperationdecreaseswithbiasedadultsexratios(Table1,Figs.2,3).Thisresultisin 144 linewiththeoreticalpredictionthatbiasedsexratioswillpromotedivergentparentalsexroles,because 145 individualsoftheraresexreducetheircareduetohighmatingsuccess,whilemembersofthemore 146 commonsexgetmostreproductivesuccessfromcaringforexistingoffspring(8,23).thisinterpretationis 147 supportedbymodelingofrelativemalecare,whichislowinspecieswithfemaletbiasedsexratioandhigh 148 inspecieswithmaletbiasedsexratio(fig.3;summarizedresultsareavailableinsiappendix,tables2 149 whiledetailedresultsareavailableinsiappendix,tables3andfig.s3).ourresultsarealsoinlinewith 150 previousfindingsinshorebirds,whereasrstronglypredictedconventionalandreversedparentalsex 151 roles(27).however,thedirectionalityoftherelationshipbetweenasrandcooperationisunclearandthe 152

7 6 causalitymightbereversed.unequalparentalrolesmightleadtobiasedsexratiosbecausethesexes 153 engageunequallyinparentalduties,havedifferenttimebudgets,andconsequentlyexperiencedifferent 154 mortalityrates(50).accordingly,sextbiasedmortalityratesareoftencorrelatedwithbiasedasracross 155 populationsandspecies(51 53).Moreover,someauthorssuggestpositivefeedbacksbetweenchangesin 156 ASRandparentalsexrolesandthustherelationshipmayevenbebidirectional(8,23,54) TheaforementionedresultsarenotconfoundedbyphylogenysinceweusephylogenyTbasedcomparative 159 analyses,andremainrobusttoalternativephylogenetichypothesesandincorporatingpotential 160 confoundsinthemodels(forphylogeneticrobustnessofourresultsseesiappendix,tabless1ands3).in 161 additiontosexualselectionandsocialenvironment,wefindapositiverelationshipofparental 162 cooperationtoadultbodymass,althoughthiseffectislessconsistentbetweenanalyses(table1,fig.3). 163 Bodymassisatypicalallometriccorrelateoflifehistory,includingbreedingcycleduration(forthe 164 relationshipofbreedingcycledurationtoadultbodymassinourdatasetseesiappendix,fig.s4)and 165 adultmortalityrate(correlationinourdatasetr= 0.57,n=323species),andofpairbonddurationand 166 divorcerate(55,56).consequently,itseemsthatlongtlivedspecieswithprolongedpairbondsandlow 167 divorcerateswouldbeexpectedtocooperatemore,butmoredirecttestsofthishypothesisareneeded. 168 Wefindthatchickdevelopment(altricialvs.precocial)isnotassociatedwiththeextentofcooperationor 169 relativemalecare(table1,fig.3),suggestingthatchickdemanddoesnotaffectparentalcooperation 170 strategiesacrossbirds.wehighlightthatsexualselectionandsocialenvironmenttogetherwithbody 171 massexplainalargeproportionofvarianceinparentalcooperation(approx.30t35%;summaryintable1 172 anddetailsinsiappendix,tables1),althoughthesevaluesaresomewhatlowerforrelativemalecare 173 (approx.12t26%;summaryinsiappendix,tables2anddetailsinsiappendix,tables3).wealso 174 emphasizethatrecentworksuggeststhatasrrelatestosexualselection(57)andthepreciserelationship 175 betweenasr,demographicprocesses,andsexualselectionarefarfromunderstood(53).nevertheless, 176 ourresultsdemonstratelargeadditiveeffectsofmajorselectiveforcesthatweretheoreticallypredicted 177 tofacilitateparentalcooperationinanimals Finally,climaticconditionsduringthebreedingseason,thoughttodrivetheevolutionofcooperation(33, ,58),donotpredictparentalcooperationasnoneoftheclimaticfactorsissignificantlyassociatedwith 181 parentalcooperationeitherinbivariateormultipleregressionanalyses(table1,fig.3;fordetailsofthese 182 relationshipsseesiappendix,tables1andfig.s2).ouranalysesthussuggestthatclimaticconditions 183 prevailingduringthebreedingseasonarequitepermissiveintermsofcotoccurringmultipleparental 184

8 7 cooperationstrategies.thisconclusionagreeswithobservationsthatspecieswithextremelycontrasting 185 parentalcaresystems(e.g.withreversedvs.conventionalsexroles)maybreedsidetbytsidesharingmuch 186 oftheenvironment(seeref.27forexamples).weakorinconsistenteffectsofclimatehavepreviously 187 beenidentifiedinlargetscaleanalysesofclimaticcorrelatesofcooperativebreedingandsexualsize 188 dimorphisminbirds(34,58 60).Takentogetherwithournewresultspresentedhere,thisbodyofwork 189 suggeststhatsexual,social,andparentingstrategiesinbirdsarelargelyindependentofclimaticeffectson 190 thescaleofwholebreedingrangesofspeciesandinsteadmightbedrivenbyecotevolutionaryfeedbacks 191 betweensocialbehavior,lifehistory,anddemography(29,61).itisalsopossiblethatparental 192 cooperationmaycovarywithenvironmentalfactorsatfinerspatialscalesnotcapturedbyouranalysesof 193 breedingrangetwideenvironment,forexampleasseemstobethecaseofmatingsystemsandsexual 194 selection(31,32,35,60).wesuggestthatdetailedanalysesoftheplasticityofparentalcooperation 195 withinspeciesinrelationtoenvironmentalconditionsonsmallerspatialscales(e.g.foodsupply,ambient 196 temperature)willshedcriticallightonthisimportantquestion Inconclusion,weshowthattheevolutionofparentalcooperationispredictedbysexualselectionand 199 socialenvironmentatleastinbirds,whereasclimaticconditionsatthescaleofthewholespecies 200 breedingrangesdonotpredictparentalcooperation.thus,severalparentalcooperationstrategiesmaybe 201 adaptiveinagivensetofclimaticconditions,dependingonthespecies'socialandgeneticmatingsystems 202 anddemographicstructure.thesepatternsarevalidacrossabroadrangeofbirdspeciesandcladesthat 203 breedindiversesettings.theyhighlightthesignificanceoffeedbacksbetweensexualselection,social 204 environment,andparentalcare,sinceallofthesehavemortalityconsequencesandarethuslinkedinecot 205 evolutionaryfeedbackloops(61) Furtherworksareneededtoadvanceparentalcooperationresearch.First,driversoftheeffectswe 208 identifyaresometimesunclear.forexample,itisnotclearwhetherevolutionarychangesinparental 209 cooperationaredrivenbysexualselectionactingonmalebehavior(24,46),onfemalebehavior(62)oron 210 bothsexessimultaneously.second,furtherstudiesshouldexplorewhichsexismoreresponsiveand 211 whethersextspecificparentingabilitiescanbiasresponsestointensesexualselection(10,11).third,new 212 phylogeneticcomparativeanalysesareneededtotestwhethersexualselectionandsocialenvironment 213 mayinfluenceparentalcooperationinnontaviantaxa,forinstanceinfishes,frogs,andmammals.whilst 214 thedetailsofcaredifferbetweenthesemajorclades,ourresultshereestablishtheworkinghypotheses 215 thatcanbefollowedupinadiverserangeoftaxa.fourth,environmentalfactorsotherthanclimatecan 216

9 8 haveimportanteffectsonparentalcooperation.forexample,foodavailabilitypredictscooperationduring 217 nestlingfeedinginseveralaviangroups(35,36),andthegeneralityofthisrelationshipshouldbetested 218 usinglargetscaledatasets.moreover,ourrangetwideanalysesmighthavemissedtheimportanceof 219 ecologicalfactorsoperatingonsmallerspatialscales.weencourageresearcherstoevaluatepotential 220 effectsofsmalltscaleecologicalfactorsonparentalcooperation.finally,insightsgainedbyour 221 comparativestudyshouldbefurthertestedinthenaturalhabitatofanimals.thesefieldtbased 222 observationsandexperimentalmanipulationscombinedwithcomparisonsacrosspopulationsandlongt 223 termpopulationmonitoringdatawillbeimmenselyusefultoteaseapartvarioussocialandecological 224 effectsandallowevolutionaryecologiststotestthepositiveandnegativefeedbacksthatunderpinmating 225 systemsandparentalcare Materials-and-Methods 228 Datacollection 229 WequantifiedsexTspecificcontributiontocareonanordinalscalefrom0to4asfollows:0Tnomale 230 contribution,1tmalecontribution1t33%,2tmalecontribution34t66%,3tmalecontribution67t99%,4 231 Tmalecontribution100%.Thus,thisscorevariedfromfemaleTonlycare(0)toapproximatelyequalcare 232 bymaleandfemale(2)tomaletonlycare(4).scoresweregatheredseparatelyfornestbuilding, 233 incubation,nestguarding(i.e.,guardinganddefendingthenestduringincubation),chickbrooding,chick 234 feeding,chickguarding(i.e.,guardinganddefendingthebroodafterhatching),posttfledgingfeedingof 235 chicks,andposttfledgingguardingofchicks(i.e.,guardinganddefendingthebroodafterfledging,for 236 detailsseeref.40).torepresenttheextentofbiparentalcare,theeightparentalactivitieswereretcoded 237 ona3levelscalesothat0representedexclusiveuniparentalcarebythemaleorfemale(originalscores0 238 or4),1representedbiparentalcarebiasedtowardeitherthemaleorthefemale(originalscores1or3), 239 and2representedapproximatelyequalcontributionbythemaleandfemale(originalscore2).finally,we 240 calculatedparentalcooperationbyaveragingthestatisticallycenteredextentofbiparentalcareacrossthe 241 eightactivities.theresultingparentalcooperationrangedfromminimumparentalcooperationto 242 maximumparentalcooperation(frequencydistributionofparentalcooperationacross659speciesof 243 birdsisavailableinsiappendix,fig.s1)andvariedacrossthephylogeny(fig.1).here,minimum 244 cooperationiswhenallactivitiesarecarriedoutbyonesex(themaleorthefemale,ca.aroundthevalue 245 of 1.5),whereasthemaximumcooperationiswhenallparentalcareactivitiesaresharedapproximately 246 equallybetweenthemaleandthefemale(ca.aroundthevalueof1.5).totesthypothesesthatpredict 247 specificdirectionofeffectsonthescalefromfemaletbiasedtomaletbiasedcare,wealsocalculated 248

10 9 standardizedrelativemalecarebasedontheoriginalscores.relativemalecarerangedfrom 2(strongly 249 femaletbiasedcare)to3(stronglymaletbiasedcare;frequencydistributionofrelativemalecareacross speciesofbirdsisavailableinSIAppendix,Fig.S1).Datacollectionwasdesignedtocoverthebroad 251 phylogeneticdiversityandfullvariabilityofbreedingsystemsexhibitedbybirds.ourdatasetcontained speciesfrom113avianfamilies Weusedtwoproxiesofsexualselectionthatarewidelyavailable:sexualsizedimorphismandextraTpair 255 paternity(63).wenotethattherelationshipbetweenthestrengthofsexualselectionandeppiscomplex. 256 However,byusingseveralindicesofsexualselection(sexualsizedimorphism,EPP)wehopetoprovide 257 comprehensiveanalysesandcharacterizebroadrangeofprocessesthatunderpinsexualselection, 258 includingmaletmalecompetitionandfemalechoice.wecalculatedsizedimorphismindexassdi=body 259 massoftheheaviersexdividedbybodymassofthelightersexminusoneandmadethevaluespositive 260 formaletbiaseddimorphismandnegativeforfemaletbiaseddimorphism.wethenalsocalculatedabsolute 261 SDIbytakingabsolutevaluesoftheoriginalSDI.GreatervaluesofabsoluteSDIthusmeangreater 262 differenceinbodymassesbetweensexes,suggestingdifferentialselectionactingonmalesandfemales 263 thatmayindicatesexualselection(15,43).extratpairpaternity(epp)wasexpressedas%ofbroods 264 containingatleastoneextratpairoffspring,inaccordancewithrecentstudies(64).however,tocheckthe 265 sensitivityofouranalysestothisparticularchoice,wealsorepeatedallanalyseswith%ofextratpair 266 offspringinthepopulation(epy).althoughthisvariablestronglydecreasedsamplesize,resultswere 267 largelyrobusttothechoiceofeppvs.epy(detailsofthesesensitivityanalysesareavailableinsi 268 Appendix,TablesS1andS3).Socialenvironmentwascharacterizedbyadultsexratio(ASR),whichwas 269 expressedastheproportionofmalesintheadultpopulation(52,65).wethencalculatedtheabsolute 270 deviationfromasrof0.5toexpressthedegreeofbiasinthefrequencyofmalesvs.femalesinthe 271 population.thisvaluewasalwayspositiveandincreasedwithincreasingdeviationfromasrof0.5(asr 272 bias) Tocharacterizeambientenvironment,firstwerecordedbreedingseasonforeachspeciesfromliterature. 275 Second,basedondigitizedranges(66)andglobalclimaticlayers(CRUDataset, duringitsbreedingseason.weextractedi)theaveragemonthlytemperature( C)andrainfall(mm);ii) 278 withintyearvariationassdofbreedingseasonmonthlyaveragesfortemperatureandrainfall;andiii) 279 amongtyearvariationassdacross49years(1961t2009)ofmonthlyaveragesfortemperatureand 280

11 10 rainfallduringthespecies'breedingseason.tocontrolforpotentiallifethistoryconfounds,weincluded 281 adultbodymass(g)andchickdevelopment(altricialvs.precocial)inthemodels Phylogeneticanalyses 284 Weusedphylogeneticgeneralizedleastsquares(PGLS)approachimplementedinafastlikelihood 285 algorithm(67)intherlanguage(68).inpglsmodels,weestimatedthephylogeneticsignalbyoptimizing 286 theλparameter(41).weused500phylogenetictreesextractedfromwww.birdtree.org(hackett 287 constraint,ref.42).weranthepglsanalysesacrossallthetreesandthensummarizedtheresulting parameterestimates Parentalcooperationandrelativemalecarewerethemainresponsevariablesinourmodels.First,we 291 fittedbivariatepglsmodelsbetweenparentalcooperationandthefollowingpredictors:sexualsize 292 dimorphism(logabsolutesdi),extratpairpaternity(sqrtepp),adultsexratio(sqrtasrbias),climatic 293 variables(meansandamongtandwithintyearvariationsintemperatureandrainfall),adultbodymass 294 (logttransformed),andchickdevelopment(altricialvs.precocial).predictorswerethesameforrelative 295 malecare,exceptthatweusedsdiinsteadofabsolutesdi,asrinsteadofasrbias,andwedidnotuse 296 climaticvariablesduetolackingpredictionsforrelativemalecare.second,wefittedpglsmodelswith 297 severalexplanatoryvariables.tousethemaximumnumberofspeciesineachanalysis,wefittedfour 298 modelsstructuredaccordingtoourthreemainhypotheseswhilecontrollingforlifethistoryvariables.for 299 parentalcooperation,thesewere:sexualselectionmodel absolutesdi,epp,adultbodymass,chick 300 development(n=226species);socialenvironmentmodel ASRbias,adultbodymass,chickdevelopment 301 (n=165species);climatemodel ambienttemperature,rainfall,adultbodymass,chickdevelopment(n 302 =659species);Fullmodel absolutesdi,epp,asrbias,ambienttemperature,rainfall,adultbodymass, 303 chickdevelopment(n=80species).forrelativemalecare,thesewere:sexualselectionmodel SDI,EPP, 304 adultbodymass,chickdevelopment(n=226species);socialenvironmentmodel ASR,adultbodymass, 305 chickdevelopment(n=165species);fullmodel SDI,EPP,ASR,adultbodymass,chickdevelopment(n= species).Wedidnotfittheclimaticmodelduetolackingpredictionsforrelativemalecare.Fulldetails 307 ofmaterialsandmethodsareavailableinsiappendix,supplements Acknowledgments 310 Weappreciatetremendousworkofgenerationsoffieldornithologists.Thisworkwouldnotbepossible 311 withouttheireffort.wethankthereviewersforveryhelpfulcomments.v.r.wassupportedbypalacky 312

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16 Figure-legends Fig.1.Phylogeneticdistributionofparentalcooperationin659speciesofbirdsincludedinthisstudy (Bayesianmaximumcredibilitytreeof500phylogenies).Thefigureshowsparentalcooperationforeach species(blackbarsrefertoparentalcooperation;tallbarsindicatehighcooperation)andphylogenetic reconstructionalongthebranches(usingplotbranchbytrait{phytools}functionofrsoftware;red=high cooperation,yellow=lowcooperation). Fig.2.Parentalcooperationinrelationtosexualsizedimorphism(logabsoluteSexualDimorphismIndex), extratpairpaternity(sqrtepp),andadultsexratio(sqrtasrbias)inbirds.variablesineachpanelwere statisticallyadjustedforotherpredictorsinaphylogeneticgeneralizedleastsquares(pgls)modeland theresidualsfromstatisticalmodelsareplotted(sexualselectionmodelforsexualsizedimorphismand ExtraTpairpaternity,andSocialenvironmentmodelforAdultsexratio,seeTable1).Ordinaryleast squaresregressionlinesareincluded. Fig.3.Parentalcooperationandrelativemalecare(fortheirfrequencydistributionacross659speciesof birdsseesiappendix,fig.s1)inrelationtosexualselection(orange),socialenvironment(red),climate (green),andlifethistorytraits(pink).thefigureshowseffectsizes(meanstandardizedregression coefficients±2se)fromthephylogeneticgeneralizedleastsquaresanalysesofparentalcooperationand relativemalecare.modelswereeitherbivariate(circles)ormultipleregressions(othersymbols).multiple regressionmodelsparallelourhypotheses:sexualselectionmodel(squares),socialenvironmentmodel (diamonds),climatemodel(upwardfacingtriangles),andfullmodel(downwardfacingtriangles;seealso Table1).Inanalysesofparentalcooperation,weusedabsoluteSDIandASRbias,whereasinanalysesof relativemalecare,weusedsdiandasr(seematerialsandmethodsandsiappendix,supplements1). LifeThistorycovariates(bodymass,chickdevelopment)wereincludedinallmodels.Horizontalerrorbars notinterceptingtheverticalzerolineindicatestatisticallysignificanteffects.notethatclimatewasnot fittedinmodelsofrelativemalecare. 15

17 Table&1Parental(cooperation(in(relation(to(sexual(selection,(social(environment,(and(climate(in( birds.'in'all'models'parental'cooperation'was'the'response'variable'and'predictors'included:'sexual' size%dimorphism%(log%absolute%size%dimorphism%index),%extrapair%paternity((sqrt(epp),(adult(sex( ratio&(sqrt&asr&bias),&temperature&(first&axis&from&pca&on&climatic&variables:&higher&values&mean&hot& environments*with$low$temperature$variability;factor'loadings'available'in'si#appendix,#table&s),# rainfall'(second'axis'from$pca$on$climatic$variables:$higher$values$mean$dry$environmentswith%high% rainfall'variability;'factor'loadings'available'in'si#appendix,table&s4),#body#mass#(logtransformed),- and$chick$development$(altricial$vs.$precocial).$we$use$phylogenetic$generalized&least&squares& approach'and'present'means'from'500'analyses'using'different'phylogenetic'trees'(see'detailed' results'in'si#appendix,#table&s1).&estimates&are&standardized&regression&coefficients&and&λindicates) the$strength%of%the%phylogenetic%signal Model&and&predictors Estimate((SE) F(P) Sexual'selection'(R =0.17,λ= 0.76,&df&=&4,221) Sexual'size'dimorphism 0.258&(0.057) 20.62%(<0.001) Extrapair%paternity 0.264&(0.061) 18.55%(<0.001) Body%mass 0.299%(0.115) 6.83%(0.011) Chick&development 0.157&(0.151) 1.12$(0.308) Social'environment'(R =0.07, =0.91,df=3,161) Adult&sex&ratio 0.186&(0.056) 11.05%(0.001) Body%mass 0.087%(0.135) 0.43%(0.524) Chick&development 0.084%(0.261) 0.12%(0.750) Climate((R =0.01,λ=0.90,df# =4,654) Temperature 0.041%(0.033) 1.60%(0.214) Rainfall 0.037%(0.031) 1.47%(0.233) Body%mass 0.019%(0.074) 0.09$(0.795) Chick&development 0.084%(0.145) 0.35%(0.564)

18 Full$model$(R =0.29,λ=0.82, df#=#7,72) Sexual'size%dimorphism 0.168&(0.098) 2.93%(0.093) Extrapair%paternity 0.230%(0.106) 4.70%(0.034) Adult&sex&ratio 0.234&(0.083) 7.88$(0.007) Temperature 0.027%(0.105) 0.08$(0.796) Rainfall 0.034%(0.087) 0.16%(0.696) Body%mass 0.334%(0.178) 3.54%(0.066) Chick&development 0.020$(0.223) 0.03$(0.900)

19 Crows, Vireos & allies Tits & Chickadees Australasian Robins Swallows & Martins Larks Old W Warblers & allies Wrens & allies Starlings, Thrashers & allies Thrushes & Flycatchers Sunbirds Waxbills & Weavers Sparrows Pipits & Wagtails Finches & Honeycreepers Cardinals & Tanagers Wood Warblers Austr. Babblers & Logrunners Honeyeaters & Thornbills NW Blackbirds Fairy wrens Bowerbirds & Austr. Treecreepers Tyrant flycatchers Buntings & NW Sparrows Antbirds, Cotingas & Manakins Plovers, Stilts & allies Ratites Parrots Falcons Woodpeckers Barbets & Toucans Bee eaters & Kingfishers Woodhoopoes & Hornbills Owls Vultures, Hawks & Eagles Snipes, Sandpipers & allies Jacanas & allies Gulls, Terns & allies Nightjars, Hummingbirds & allies Cranes & Rails Cuckoos & Bustards Sandgrouse & Grebes Storks, Herons & allies Gees & Swans Ducks Megapodes, Quail & allies Pheasants, Grouse & allies

20 Parental cooperation Parental cooperation Sexual size dimorphism Extra pair paternity Parental cooperation Adult sex ratio

21 Parental cooperation Relative male care Sexual size dimorphism Extra pair paternity Adult sex ratio Ambient temperature Rainfall Body mass Chick development Effect size

22 Supporting Information for: The evolution of parental cooperation in birds Authors Vladimír Remeš, Robert P. Freckleton, Jácint Tökölyi, András Liker, Tamás Székely Supplement S1. Full Materials and Methods. Fig. S1. Frequency distribution of parental cooperation and relative male care in birds. Fig. S2. Scatterplots of parental cooperation in relation to predictors as modeled by PGLS multiple regressions. Fig. S3. Scatterplots of relative male care in relation to predictors as modeled by PGLS multiple regressions. Fig. S4. Scatterplots of the durations of different phases of breeding cycle (nest building, egg incubation, chick care before and after fledging) in relation to adult body mass. Fig. S5. Estimates of semivariograms and Moran s I for residuals from i) the four PGLS models of parental cooperation with EPP, and ii) the three PGLS models of relative male care with EPP. Table S1. Full results of PGLS models of parental cooperation run across 500 phylogenies. Table S2. Summary of results of PGLS models of relative male care. Table S3. Full results of PGLS models of relative male care run across 500 phylogenies. Table S4. Factor loadings of climatic variables on the first two principal components.

23 Supporting Information for: The evolution of parental cooperation in birds Authors Vladimír Remeš, Robert P. Freckleton, Jácint Tökölyi, András Liker, Tamás Székely Supplement S1 Full Materials and Methods Data collection We quantified sex-specific contribution to care on an ordinal scale from 0 to 4 as follows: 0 - no male contribution, 1 - male contribution 1-33%, 2 - male contribution 34-66%, 3 - male contribution 67-99%, 4 - male contribution 100%. Thus, this score varied from female-only care (0) to approximately equal care by male and female, (2) to male-only care (4). Although this scoring system does not quantify absolute parental effort, it quantifies relative participation of sexes, which is the metric we were interested in here. Scores were gathered separately for nest building, incubation, nest guarding (i.e., guarding and defending the nest during incubation), chick brooding, chick feeding, chick guarding (i.e., guarding and defending the brood after hatching), post-fledging feeding of chicks, and post-fledging guarding of chicks (i.e., guarding and defending the brood after fledging, for details see (1)). Scoring was a necessity rather than preference, since quantitative data were not available for many species. This is a common practice in comparative studies; see (2 6) for similar approaches. Our scoring was significantly repeatable (sensu(7)) between two independent observers who scored a subset of species (intraclass correlation, repeatability of mean score of all care components: r ICC = 0.79, F = 8.6, p < 0.001, n = 31 species). These scores also correlate with an independent measure of care (i.e., sex differences in the length of care, see (8)). Data collection was designed to cover the broad phylogenetic diversity and full variability of breeding systems exhibited by birds. Our data set contained 659 species from 113 avian families. Sample size differed between individual analyses, because not all traits were available for all species (see below). There were too many missing values in some of the parental activities to allow data enhancement by imputation. To represent the extent of biparental care, the eight parental activities were re-coded on a 3 level scale so that 0 represented exclusive uniparental care by the male or female (original scores 0 or 4), 1 represented biparental care biased toward either the male or the female (original scores 1 or 3), and 2 represented approximately equal contribution by the male and female (original score 2). Finally, we calculated parental cooperation by averaging the extent of biparental care across the eight activities. However, not all activities

24 were available for all species (average number of activities = 4.83, SD = 1.56, n = 659 species; all activities were available only for 28 species). At the same time, means for different parental activities ranged from 0.58 for incubation to 1.69 for post-fledging feeding across species. Consequently, differences between activity-specific means could have introduced bias into the calculation of parental cooperation for every species depending on which activity happened to lack for a particular species. Therefore, before averaging across activities we centered the extent of biparental care for each activity by subtracting the mean from the original score. The resulting parental cooperation ranged from minimum parental cooperation to maximum parental cooperation (frequency distribution of parental cooperation across 659 species of birds is available in Fig. S1) and varied across the phylogeny (Fig. 1). Here, minimum cooperation is when all activities are carried out by one sex (the male or the female, ca. around the value of 1.5), whereas the maximum cooperation is when all parental care activities are shared approximately equally between the male and the female (ca. around the value of 1.5). To test specific hypotheses that predict effects on the scale from female-biased to male-biased care, we calculated in the same way as above centered values of the original scores of sex-specific engagement in parental care. Resulting values of this relative male care ranged from 2 (strongly female-biased care) to 3 (strongly male-biased care; frequency distribution of relative male care across 659 species of birds is available in Fig. S1). Note that for sake of simplifying the analyses, we worked with the ordinal scores as if they were continuous variables (for the necessity to work with ordinal scores see above). We used two proxies of sexual selection that are widely available: sexual size dimorphism and extra-pair paternity (9). We calculated size dimorphism index as SDI = body mass of the heavier sex divided by body mass of the lighter sex minus one and made the values positive for male-biased dimorphism and negative for female-biased dimorphism. We then also calculated absolute SDI by taking absolute values of the original SDI. Greater value of the absolute SDI thus means greater difference in body masses between sexes, suggesting differential selection acting on males and females that may indicate sexual selection (10, 11). Indeed, when we quantified percentage of polygamous pairings of males and females and calculated absolute difference between the sexes, this difference correlated positively with absolute SDI (r = 0.28, n = 496 species). This showed that extensive sexual size dimorphism was correlated with divergent mating strategies of the two sexes indicating strong sexual selection. Extra-pair paternity was expressed as % of broods containing at least one extra-pair offspring (EPP), in accordance with recent studies (12). However, to check the sensitivity of our analyses to this particular choice, we also repeated all analyses with % of extra-pair offspring in the population (EPY). Although this variable dramatically decreased sample size, results were robust to the choice of EPP vs. EPY (details of these sensitivity analyses are available in Tables S1 and S2). This is probably not surprising, as evolutionary correlation between EPP and EPY was 0.92.

25 Social environment was characterized by adult sex ratio (ASR), which was expressed as the proportion of males in the adult population (13, 14). We then calculated the absolute deviation from ASR of 0.5 to express the degree of bias in the frequency of males vs. females in the population. This value was always positive and increased with increasing deviation from ASR of 0.5 (ASR bias). To characterize ambient environment, first we recorded breeding season for each species from literature. Second, based on digitized ranges (15) and global climatic layers (CRU Dataset, we extracted climatic conditions in the breeding range of every species during its breeding season. We extracted i) the average monthly temperature ( C) and rainfall (mm); ii) within-year variation as SD of breeding season monthly averages for temperature and rainfall; and iii) among-year variation as SD across 49 years ( ) of monthly averages for temperature and rainfall during the species' breeding season. Rainfall was log-transformed prior to all calculations. We excluded seabirds from all the analyses, as climatic variables do not affect their food supply in the same way as in terrestrial birds (Procellariiformes, Sphenisciformes, Alcidae, Fregatidae, Sulidae, Pelecanidae, some Sternidae, Laridae, Stercorariidae, and Phalacrocoracidae). To control for potential confounds, we included the following life-history traits in the models. For every species in our dataset, we obtained estimates of body mass of males and females (g) and used their average, and chick development (altricial vs. precocial). Body mass captures many aspects of species life history, including adult mortality (16), and thus pair bond duration and divorce rate (17, 18). Demanding chicks (i.e. altricial) preclude the evolution of reduced parental care (19 21). In a previous study of shorebirds, species with less demanding (i.e. precocial) young exhibited uniparental care with higher probability than species with more demanding (i.e. semiprecocial) young (20). Thus, chick development could influence parental cooperation by setting overall offspring demand. Since the length of breeding cycle might influence parental cooperation (22), we also recorded durations of breeding cycle phases (nest building, incubation, chick feeding, post-fledging care). However, we were able to find durations of all four phases only for 214 out of our 659 species. All these durations correlated well with body mass (for the relationship of breeding cycle duration to adult body mass in our dataset see Fig. S4) and thus to avoid decreasing the sample size, we modeled only adult body mass. Phylogenetic analyses We used phylogenetic generalized least squares (PGLS) approach implemented in a fast likelihood algorithm (23) in the R language (24). In PGLS models, we estimated the phylogenetic signal by optimizing the λ parameter (25). We used 500 phylogenetic trees extracted from (Hackett constraint, (26)). We ran the PGLS analyses across all the trees and then summarized the resulting 500