Phil. Trans. R. Soc. B. article template

Phil. Trans. R. Soc. B.

doi:10.1098/rstb.2019.0495

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Extended parenting and the evolution of cognition 1

Natalie'Uomini'*1^,'Joanna'Fairlie2,'Russell'D.'Gray1,3,'Michael'Griesser'*4^'2 1"Department"of"Linguistic"and"Cultural"Evolution,"Max"Planck"Institute"for"the"Science"of"Human"History,"3

Kahlaische"Str."10,"Jena,"Germany,"ORCID:"0000J0002J9898J6415""4 2"Independent"researcher,"UK,"ORCID:"0000J0001J9900J6098""5

3"School"of"Psychology,"University"of"Auckland,"23"Symonds"St.,"Auckland"1010,"New"Zealand,"ORCID:"0000J6 0002J9858J0191"7

4"State"Key"Laboratory"of"Biocontrol,"Department"of"Ecology"and"School"of"Life"Sciences,"Sun"YatJsen"8 University,"Guangzhou,"510275,"China,"ORCID:"0000J0002J2220J2637""9

"10 ^"these"authors"contributed"equally"11

"12 Keywords:"parenting,"Corvidae,"Siberian"jays,"New"Caledonian"crows,"cognitive"evolution,"social"learning"13

!14 15

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Main!Text!17

Summary!!18 Traditional!attempts!to!understand!the!evolution!of!human!cognition!compare!humans!with!other!primates.!This!19 research!showed!that!relative!brain!size!co=varies!with!cognitive!skills,!while!adaptations!that!buffer!the!developmental!20 and!energetic!costs!of!large!brains!(e.g.,!allomaternal!care),!and!ecological!or!social!benefits!of!cognitive!abilities,!are!21 critical!for!their!evolution.!To!understand!the!drivers!of!cognitive!adaptations,!it!is!profitable!to!consider!distant!lineages!22 with!convergently!evolved!cognitions.!Here,!we!examine!the!facilitators!of!cognitive!evolution!in!corvid!birds,!where!23 some!species!display!cultural!learning,!with!an!emphasis!on!family!life.!We!propose!that!extended!parenting!(protracted!24 parent=offspring!association)!is!pivotal!in!the!evolution!of!cognition:!it!combines!critical!life=history,!social,!and!25 ecological!conditions!allowing!for!the!development!and!maintenance!of!cognitive!skillsets!that!confer!fitness!benefits!to!26 individuals.!This!novel!hypothesis!complements!the!extended!childhood!idea!by!considering!the!parents'!role!in!juvenile!27 development.!Using!phylogenetic!comparative!analyses,!we!show!that!corvids!have!larger!body!sizes,!longer!28 development!times,!extended!parenting,!and!larger!relative!brain!sizes!than!other!passerines.!Case!studies!from!two!29 corvid!species!with!different!ecologies!and!social!systems!highlight!the!critical!role!of!life=history!features!on!juveniles'!30 cognitive!development:!extended!parenting!provides!a!safe!haven,!access!to!tolerant!role!models,!reliable!learning!31 opportunities,!and!food,!resulting!in!higher!survival.!The!benefits!of!extended!juvenile!learning!periods,!over!32 evolutionary!time,!lead!to!selection!for!expanded!cognitive!skillsets.!Similarly,!in!our!ancestors,!cooperative!breeding!33 and!increased!group!sizes!facilitated!learning!and!teaching.!Our!analyses!highlight!the!critical!role!of!life=history,!34 ecological,!and!social!factors!that!underlie!both!extended!parenting!and!expanded!cognitive!skillsets.!35 !36 Introduction!!37 The!diverse!and!flexible!cognitive!abilities!of!our!species!are!considered!pivotal!for!our!evolutionary!history![1].!Our!38 extended!childhood!is!a!key!life!history!trait!that!impacts!on!human!cognition,!giving!humans!a!period!of!cognitive!39 flexibility!(changeability)!to!explore!more!options!during!learning![1=6].!Life!history!describes!the!age=specific!patterns!40 that!are!central!to!an!organism's!life,!including!the!reproductive!allocation!strategies,!development!and!ageing!patterns!41 [7].!However,!extended!developmental!periods!evolved!not!only!in!humans!and!other!primates,!but!also!in!bats,!42 cetaceans,!elephants,!and!several!bird!families![7].!Thus,!we!ask!here!two!questions:!(1)!Are!the!effects!of!extended!43 childhood!on!cognition!specific!to!humans,!or!can!they!be!generalised!to!other!species!with!relatively!expanded!44 cognitive!skillsets?!(2)!What!is!the!particular!role!of!parenting!on!the!development!of!cognition!in!individuals?!!45 !46 While!the!term!"cognition"!has!no!agreed!definition![8],!we!follow!here!Allen![9],!defining!it!as!"the!brain's!synthesis!of!47 information!from!diverse!sensory!and!memory!sources!to!produce!appropriate!responses".!We!refer!to!skillsets!as!the!48

*Authors!for!correspondence!(traduck@gmail.com!and!michael.griesser@gmail.com).!

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combination!of!cognitive!abilities!possessed!by!a!species!or!an!individual.!Evolutionary!cognitive!studies!investigate!49 cognitive!changes!over!time!in!species.!The!"embodied!cognition"!approach,!which!views!cognition!as!a!result!of!50 interactions!between!an!individual's!body!and!its!environment![10,!11],!is!an!increasingly!influential!view!in!cognitive!51 science![11=13].!However,!the!interactions!between!life=history,!ecology,!and!learning!have!rarely!been!considered!in!52 cognitive!evolution!research.!Thus,!we!use!here!an!integrative!approach!to!propose!a!new!model!of!cognitive!evolution!53 based!on!extended!childhoods!and!extended!parenting!typical!of!family!living!species.!!54 !55 Many!scholars!consider!brain!size!as!a!useful!proxy!for!cognitive!abilities!because!species!with!larger!brains!tend!to!56 show!more!diverse!and!flexible!behaviours![13],!but!the!validity!of!this!proxy!is!debated![11,!14=16].!Since!brain!57 morphology!can!differ!between!lineages![14,!17],!it!is!recommended!to!relate!brain!sizes!to!cognitive!abilities!only!58 within!lineages,!and!to!consider!behaviour!when!inferring!cognitive!abilities!in!individuals!or!species![14].!Work!59 focussing!on!brains!showed!that!they!are!paradoxical!adaptations!for!two!reasons.!First,!brain!tissue!is!energetically!60 very!expensive!to!grow!and!maintain![18],!and!thus,!large!brains!can!only!evolve!if!their!costs!are!buffered!through!61 prolonged!developmental!periods!and/or!allomaternal!energy!inputs!(expensive!brain!framework![19]).!Second,!it!takes!62 time!for!an!individual's!brain!to!develop!the!cognitive!abilities!that!make!this!adaptation!worthwhile.!Thus,!cognitive!63 adaptations!are!constructed!developmentally,!and!their!development!relies!on!access!to!learning!opportunities![20=22].!64 The!combination!of!these!factors!stresses!the!importance!of!ontogeny,!and!a!constant,!reliable!access!to!resources!65 during!development!to!offset!the!cost!of!large!brains![23].!Thus,!selection!on!brain!size!and!learning!ability!is!associated!66 with!extended!developmental!periods![24,!25].!Relevant!for!models!of!cognitive!evolution!is!that!individuals!with!67 extended!learning!periods!are!predicted!to!develop!larger!cognitive!skillsets,!allowing!them!to!more!successfully!68 reproduce!and!avoid!extrinsic!mortality![24].!!69 !70 Here,!we!focus!on!the!co=evolutionary!links!of!life!history!traits!with!extended!skill=learning!periods.!While!learning!is!71 costly,!including!increased!parental!investment!and!higher!vulnerability!of!naïve!juveniles![26],!several!studies!showed!72 fitness!benefits!of!faster!learning!ability![27,!28].!Previous!work!assessed!particular!drivers!of!cognitive!abilities!(usually!73 using!brain!size!as!a!proxy),!including!ecological,!social,!and!cultural!drivers,!or!assessed!very!specific!aspects!of!74 cognition,!such!as!innovations![3,!16,!22,!23,!29=31],!but!rarely!considered!the!evolutionary!interplay!between!75 developmental!trajectories,!sociality,!cognition,!and!brain!evolution![4,!19,!30,!32,!33].!Previous!work!showed!that!76 enlarged!brain!size!evolved!in!species!with!a!larger!body!size,!larger!group!sizes,!longer!reproductive!lifespan,!more!77 reliance!on!social!learning,!and!more!variable!environments![34].!These!data!are!largely!in!line!with!the!cognitive!buffer!78 hypothesis,!which!proposes!that!larger!brains!provide!more!abilities!that!help!to!survive!unfavourable!conditions![30].!79 Nevertheless,!what!remains!to!be!clarified!is!the!fitness!benefit!of!extended!parenting!for!the!evolution!of!cognitive!80 abilities.!We!develop!below!the!extended!parenting!hypothesis,!which!extends!and!complements!the!"extended!81 childhood"!hypothesis![2,!3,!35=38]!based!on!a!phylogenetic!comparison!of!corvids!with!other!passerines,!and!insights!82 from!two!long=term!field!studies!on!corvids.!!83 !84 The!extended!parenting!hypothesis!85 We!will!argue!that!the!ontogenetic!development!of!expanded!and!more!flexible!cognitive!skillsets!requires!(1)!a!fitness!86 benefit,!(2)!ample!and!reliable!social!learning!opportunities!(facilitated!by!extended!childhood!and!extended!parenting),!87 (3)!the!buffering!of!the!costs!of!developing!and!maintaining!a!large!brain,!and!(4)!ecological!conditions!that!facilitate!88 extended!parenting!(Fig.!1).!The!comparative!data!below!show!that!extended!parenting!is!critical!for!the!evolution!of!89 large!brains!and!large!cognitive!skillsets!in!most!cases.!Previous!models!and!comparative!work!identified!a!set!of!90 ecological,!social!and!life=history!parameters!that!are!associated!with!larger!brains:!(i)!ecological!and!social!challenges!91 that!favour!certain!cognitive!abilities![30],!(ii)!a!life=history!that!provides!the!opportunity!to!develop!more!cognitive!and!92 sensory=motor!abilities!and!covers!their!developmental!and!maintenance!costs![23,!32],!and!(iii)!a!fitness!benefit!from!93 having!these!abilities![39].!These!requirements!are!found!not!only!in!species!with!increased!levels!of!alloparental!care!94 [40],!but!also!in!species!with!extended!parenting.!In!birds,!extended!parenting!provides!an!evolutionary!steppingstone!95 for!transitions!to!cooperative!breeding,!where!others!than!parents!provide!parental!care![41],!alleviating!the!96 development!and!maintenance!costs!of!large!brains.!Comparative!work!showed!that!family!living!is!associated!with!a!97 larger!body!size,!an!increased!lifespan,!and!productive,!mild!environments![41].!Thus,!building!upon!the!cultural!98 intelligence!idea![22],!we!propose!here!that!parenting!itself!is!pivotal!for!the!social!environment!that!favours!the!99 evolution!of!cognitive!adaptations!through!learning,!and!that!it!links!to!environmental!conditions!that!support!the!costs!100 of!large!brains!and!provide!a!benefit!from!increased!skillsets![39]!(Fig.!1).!!101 !102 For!extended!parenting!to!evolve,!it!must!confer!benefits!that!offset!the!costs!of!delayed!maturation![7,!42],!for!103 example!increased!survival![43].!Increased!flexibility!and!innovativeness,!such!as!rates!of!novel!feeding!behaviours!in!104 natural!populations,!can!also!facilitate!survival!in!changing!environments![39,!44].!An!extended!developmental!and!105 childhood!phase!provides!more!time!to!learn!difficult!skills,!supporting!the!evolution!of!socioecological!niches!with!106 specialized!foraging!techniques![45=47].!In!humans,!cognitive!flexibility!is!greatest!in!preschool=aged!children!but!107 decreases!subsequently,!which!suggests!that!the!evolution!of!an!extended!childhood!favoured!the!variable!use!of!a!108 more!exploratory!learning!strategy!early!on!and!fixed!learned!strategies!later!on!in!life,!creating!a!fruitful!balance!109

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between!innovation!and!imitation!in!cultural!learning![2].!An!extended!childhood!has!been!an!integral!part!of!human!110 life!history!patterns!for!at!least!600,000!years,!as!shown!by!fossil!evidence!for!body!mass,!brain!size,!and!dental!111 development!of!human!ancestors!and!related!extinct!species![48].!Our!ancestors'!technological!skills!included!the!most!112 difficult!to!learn!technologies!documented!until!that!time!(i.e.,!involving!the!most!elements!and!hierarchical!levels!of!113 action!sequencing,!and!demanding!the!longest!learning!times),!as!evidenced!by!archaeological!tool!analyses!and!114 transmission!experiments![49=53].!Learning!a!skill,!including!stone!tool=making!that!demands!extensive!time!115 investment,!is!costly!to!the!individual!and!the!group.!In!humans,!apprenticeship!strategies!evolved!to!reduce!these!costs!116 [49,!50,!54].!Because!offspring!must!be!fed!until!they!have!acquired!a!self=sustaining!level!of!foraging!skills![24],!a!117 lengthening!of!provisioning!time!increases!the!costs!to!the!feeders.!Taken!together,!these!data!illustrate!the!critical!role!118 of!costs!in!our!model!for!both!parents!and!learners.!!119 !120 Corvid!life!histories:!comparison!with!other!passerines!!121 Research!on!human!cognitive!evolution!benefits!from!consideration!of!non=primate!species![23,!30,!55].!Birds,!which!122 have!a!300!million=year!long!evolutionary!history!independent!of!mammals,!provide!an!excellent!outgroup!to!untangle!123 the!factors!involved!in!cognitive!evolution.!We!focus!on!corvids!because!they!show!convergent!cognitive!abilities!that!124 rival!apes!in!many!domains,!such!as!in!tool=manufacture,!planning,!and!insight![56].!These!abilities!have!been!linked!to!125 an!increase!in!neuron!density!in!their!neocortex,!particularly!the!telencephalon![17].!Thus,!corvids!provide!us!with!a!126 comparison!to!early!human!ancestors!as!they!present!an!intriguing!example!of!convergent!evolution!in!innovative!127 problem=solving,!increased!manipulative!dexterity,!technical!skills,!and!sociocultural!transmission!of!skills!that!lead!to!128 cultural!variation![57].!!129 !130 Corvids!are!a!globally!distributed!passerine!family!that!includes!127!species.!Corvids!and!30!related!bird!families!form!131 the!super=clade!of!Corvides,!which!includes!other!bird!species!with!large!brain!sizes!(e.g.,!drongos,!currawongs,!132 Australian!magpies).!Corvids!originated!in!the!Australo=Papuan!region!around!14!million!years!ago!in!rainforest!habitats!133 [58],!and!interestingly,!they!differ!in!a!large!number!of!traits!from!other!passerines!(Table!1).!Corvids!are!among!the!134 largest!passerines,!and!have!much!larger!relative!brain!sizes.!The!incubation!time!is!longer!than!the!passerine!mean,!135 and!the!time!spent!in!the!nest!is!almost!double!the!mean!for!other!passerines.!Importantly!for!learning,!offspring!have!136 extended!periods!beyond!fledging!where!they!remain!associated!with!their!parents!compared!to!other!passerines.!137 Finally,!a!high!number!of!corvid!species!breed!cooperatively.!!138 !139

Table!1!about!here!140 !141 Although!we!lack!detailed!data!on!the!brain!structure!of!many!species,!phylogenetic!analyses!show!that!bird!species!142 with!extended!family!life!have!larger!telencephalons,!and!a!larger!proportion!of!neurons!located!in!their!telencephalon!143 [17]!(Table!2).!Thus,!corvids!stand!out!from!other!passerines!not!only!in!terms!of!their!cognitive!abilities,!but!also!in!144 having!a!set!of!life=history!features!linked!to!extended!parenting.!But!how!does!extended!parenting!affect!learning,!and!145 importantly,!survival?!Two!case!studies!that!directly!addressed!learning!in!corvids!are!presented!below.!Crucially,!the!146 data!from!these!species!are!not!confounded!by!potential!effects!of!cooperative!breeding,!which!has!been!previously!147 identified!to!facilitate!the!evolution!of!large!brains![30,!40].!148 !149

Table!2!about!here!150 !151 Siberian!jays:!learning!opportunities!matter!!152 Siberian!jays!(Perisoreus"infaustus;!Video!S1)!are!sedentary!corvids!that!occur!throughout!the!northern!Palearctic![59].!153 Their!social!system!has!two!unique!facets!that!provide!insights!into!the!benefits!of!family!living.!First,!the!species!does!154 not!breed!cooperatively!(i.e.,!only!parents!incubate!and!feed!young),!despite!the!fact!that!offspring!can!remain!with!155 their!parents!for!years!after!fledging,!which!is!associated!with!cooperative!breeding!in!most!species![41].!Second,!156 Siberian!jay!groups!consist!of!a!breeding!pair,!retained!offspring!and/or!unrelated!non=breeders.!The!latter!are!forced!157 by!the!socially!dominant!retained!offspring!to!disperse!from!the!natal!territory!1=2!months!after!fledging!and!settle!in!158 another!group![60].!Retained!offspring!can!remain!up!to!an!age!of!4!years!with!their!parents,!which!is!well!beyond!the!159 mean!lifespan!of!2.2!years![59].!!!160 !161 Parents!differ!in!their!behaviour!towards!kin!and!non=kin!(Figure!S1,!Figure!S2)!as!they!are!nepotistic!and!only!provide!162 access!to!resources!and!predator!protection!to!kin![59],!resulting!in!a!higher!survival!of!kin!compared!to!non=kin![43].!!163 Field!experiments!on!predator!recognition!and!problem=solving!in!juveniles!reveal!how!fitness!related!proxies!depend!164 on!kinship.!Predation!by!goshawks!is!the!main!reason!for!mortality!in!Siberian!jays,!especially!affecting!juveniles![43,!165 61].!Juveniles!do!not!respond!to!perched!predators!when!encountering!them!on!their!own,!but!when!other!group!166 members!start!mobbing!a!perched!predator,!particularly!retained!offspring!immediately!copy!the!behaviour!of!their!167 parents![62].!Natural!mobbing!events!are!very!brief,!as!mobbed!predators!quickly!move!off,!so!that!unrelated!non=168 breeders!have!much!fewer!opportunities!than!retained!offspring!to!observe!mobbing.!However,!in!experimental!169

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settings!where!predator!models!are!presented,!mobbing!could!last!as!long!as!4!minutes,!providing!also!unrelated!non=170 breeder!with!learning!opportunities.!Consequently,!all!juveniles!survived!their!first!winter!of!life![63].!Moreover,!171 retained!juveniles!learn!to!access!a!feeding!device!(Figure!S3)!faster!than!unrelated!juveniles![64],!as!their!learning!is!172 facilitated!by!more!tolerant!role!models!(i.e.,!their!parents;!Video!S1).!Thus,!a!life!history!involving!extended!parenting!is!173 a!critical!support!for!learning:!parents!provide!their!offspring!with!a!safe!haven,!access!to!food!and!reliable!learning!174 opportunities,!which!together!boost!the!long=term!survival!of!retained!offspring![63].!!175

!176 New!Caledonian!crows:!tool!manufacture!matters!!177 New!Caledonian!crows!(Corvus"moneduloides;!Video!S1)!are!endemic!to!the!tropical!South!Pacific!island!of!New!178 Caledonia,!where!they!live!in!family!groups!with!extended!dependency!periods:!offspring!can!be!fed!by!their!parents!for!179 up!to!2!years![65],!which!might!explain!why!this!species!does!not!breed!cooperatively![65].'During'this!extended!180 developmental!period,!juveniles!have!access!to!tolerant!role!models!(both!related!and!unrelated![66]),!from!whom!they!181 can!learn!tool=use!and!tool=making!skills![66,!67]!(Figure!S4;!Video!S1).!Social!learning!experiments!showed!that!adults!182 and!juveniles!learn!about!the!appropriate!context!for!certain!actions!from!each!other,!demonstrating!the!potential!for!!183 lifelong!learning!ability![68].!In!the!wild,!adults!scaffold!learning!of!juveniles!by!allowing!them!to!be!in!physical!contact!184 during!foraging!(Figure!S5),!and!by!sometimes!leaving!a!tool!in!a!tree!hole!that!juveniles!can!then!use!with!success!185 (Video!S1).!However,!this!extended!toolmaking!learning!period!comes!with!a!high!cost:!juveniles!are!unable!to!make!186 functional!tools!until!they!are!at!least!6!months!old.!Adult=level!proficiency!is!reached!at!10!to!12!months!of!age![66],!187 requiring!that!parents!provision!their!offspring!through!their!first!year!of!life.!Thus,!wild!juveniles!grow!up!in!a!safe!188 haven,!surrounded!by!tolerant!role!models!that!constantly!make!and!use!tools!(Figure!S6),!and!juveniles!have!ample!189 occasions!to!borrow!and!use!other!birds'!tools!(Video!S1).!!190 !191 New!Caledonian!crows!have!the!largest!relative!brain!size!amongst!corvids![69],!suggesting!selective!pressures!on!some!192 aspects!of!cognitive!performance![17].!Compared!to!other!corvids,!they!have!significantly!larger!brain!areas!subserving!193 learning,!action!sequencing,!and!fine!motor!control!functions![70],!all!of!which!support!the!tool=making!and!tool=use!194 behaviours!enacted!by!New!Caledonian!crows.!In!experimental!settings,!New!Caledonian!crows!have!been!shown!to!195 excel!at!problem=solving,!physical!cognition,!and!causal!reasoning!in!tests!such!as!the!trap=tube,!string!pulling,!and!196 Aesop's!fable!tasks!(in!which!suitable!objects!must!be!dropped!into!a!beaker!of!water!to!raise!the!water!level!to!obtain!a!197 floating!reward)![71].!!198 !199 Several!evolutionary!adaptations!were!crucial!for!the!emergence!of!toolmaking!skills!in!New!Caledonian!crows!and!200 representative!human!ancestors![72],!including!increases!in!brain!size!and!brain!networking!potential,!stable!groups!201 with!a!high!social!tolerance!providing!opportunities!for!social!learning,!and!extended!parenting!and!development!202 periods.!Increased!social!learning!opportunities!allow!individuals!to!acquire!more!skills!and!to!become!more!effective!203 individual!learners![20,!22].!!204 !205 Cognitive!consequences!of!extended!parenting!206 In!the!corvid!case!studies!we!presented,!Siberian!jays!tolerate!retained!offspring!more!than!unrelated!non=breeders,!207 which!increases!the!learning!opportunities!and!survival!prospects!of!retained!offspring![43].!New!Caledonian!crows!are!208 highly!tolerant!to!juveniles!independent!of!their!kinship![66],!and!adults!scaffold!the!learning!process!of!juveniles!209 acquiring!tool=making!skills!("education!by!master=apprenticeship"![73]).!In!addition,!juveniles!of!both!species!are!highly!210 proactive!in!ways!that!foster!opportunities!to!observe!others!and!to!practice!skills.!In!Siberian!jays,!retained!juveniles!211 pay!more!attention!to!the!behaviour!of!the!adults!in!their!group!than!unrelated!juveniles!do![62].!Juvenile!New!212 Caledonian!crows!actively!follow!group!members,!direct!begging!behaviours!towards!them,!steal!foraged!food!from!213 them,!and!also!steal!ready=made!tools!that!they!can!use!to!get!food.!These!behaviours!are!tolerated!by!the!adults!and!214 ensure!survival!of!juvenile!corvids!that!are!not!yet!nutritionally!independent.!Thus,!learning!opportunities!arise!from!the!215 interplay!between!extended!childhood!and!extended!parenting.!The!safe!haven!provided!by!extended!parenting!is!216 critical!for!learning!opportunities,!and!creates!extended!developmental!periods!that!feed!back!into!the!extended!217 childhood.!!218 !219 Centred!on!extended!parenting,!our!model!(illustrated!in!Fig.!1)!extends!and!complements!the!"extended!childhood"!220 model![2,!3,!35=38],!while!highlighting!the!active!nature!of!both!adults!and!juveniles.!Our!model!integrates!previous!221 models!of!cognitive!and!brain!evolution![4,!16,!19,!29=32,!74]!but!adds!crucial!details!on!the!interactions!with!ecological!222 traits,!life!history!traits,!and!fitness!benefits.!More!productive!environments!facilitate!low!extrinsic!mortality,!leading!to!223 a!longer!lifespan!and!an!associated!reduction!in!reproductive!allocation![7,!42].!These!conditions!facilitate!extended!224 family!time![41,!75],!and!a!safe!haven!through!access!to!food!and!protection!from!predators![41],!which!in!turn!facilitate!225 extended!developmental!periods!with!ample!learning!opportunities!provided!by!tolerant!role!models![20]!(i.e.,!the!226 "playful!protected!learning!environment"!of!humans![2]).!These!conditions!are!likely!to!favour!the!evolution!of!larger!227 cognitive!skillsets![32,!76].!The!costs!of!extended!learning!periods!are!paid!by!extended!provisioning,!which!is!enabled!228 by!productive!environments.!Moreover,!extended!family!time!also!facilitates!the!evolution!of!cooperative!breeding,!229

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which!additionally!can!enable!the!evolution!of!larger!brains!(Table!2)!that!sustain!larger!skillsets![40].!Extended!learning!230 time,!more!role!models!to!learn!from,!and!a!release!from!the!costs!of!large!brains!allow!the!development!of!larger!or!231 more!flexible!cognitive!skillsets,!which!in!turn!give!species!chances!to!move!into!new!ecological!niches![39,!77],!or!232 allows!them!to!cope!with!environmental!degradation!leading!to!variable!environments![41].!This!later!factor!is!also!233 associated!with!the!evolution!of!cooperative!breeding![41].!Together,!these!adaptations!can!incur!fitness!benefits!234 through!the!safe!haven,!an!expansion!of!the!cognitive!skillset,!and!cooperative!breeding.!!235 !236

Figure!1!about!here!237 !!238 The!life=history!filter!model![32]!proposes!that!survival!challenges!only!result!in!cognitive!adaptations!if!the!life=history!239 of!species!include!a!low!extrinsic!mortality,!which!in!turn!allows!to!reallocate!resources!into!the!development!and!240 maintenance!of!a!larger!brain.!Drawing!upon!this!idea,!we!propose!that!integrating!the!family=filter!into!this!model!can!241 explain!the!absence!of!large!brains!in!long=lived!species!due!to!short!family!times,!or!the!occurrence!of!large!brains!in!242 short=lived!species!due!to!extended!parenting!(Fig.!2).!Thus,!not!only!extrinsic!mortality!and!size!constraints![32],!but!243 also!extended!parenting!can!explain!the!occurrence!of!grade=shifts!(i.e.,!deviations!from!body!sized!based!expected!244 brain!sizes)!of!animals.!!245 !246

Figure!2!about!here!247 !248 Discussion!and!conclusions!!249 !250 The!comparative!data!on!corvids!support!the!fundamental!role!of!extended!parenting!for!the!evolution!of!cognitive!251 skillsets!through!learning,!and!family!living!links!to!critical!life!history!and!ecology!features!that!have!been!previously!252 identified!to!facilitate!cognitive!evolution.!Extended!parenting!is!only!possible!if!(i)!the!life!history!pace!is!slow!enough!253 so!that!the!optimal!onset!of!independent!reproduction!is!not!at!the!first!opportunity![42],!(ii)!parents!can!afford!254 extended!offspring!association![75],!and!(iii)!the!ecological!setting!provides!productive!environments!or!adaptations!255 that!buffer!possible!ecological!costs.'Particularly,!the!access!to!tolerant!role!models!is!a!key!variable!that!affects!256 between=individual!variability!in!learning!within!and!between!species.!Extended!parenting!allows!these!high=quality!257 relationships!to!develop,!and!has!a!direct!impact!on!fitness,!as!shown!by!the!restricted!learning!opportunities!of!258 unrelated!juveniles!in!Siberian!jays,!and!their!lower!survival![62,!64].!Similarly,!adult!New!Caledonian!crows!are!highly!259 tolerant!to!their!own!but!also!unrelated!juveniles,!scaffolding!the!sensory=motor!and!embodied!learning!process!of!260 juveniles.!!261 !262 This!special!issue!examines!whether!and!how!the!life!history!of!different!species!is!connected!with!their!cognitive!263 abilities.!Cognitive!flexibility!throughout!the!lifetime!is!central!to!our!cognitive!abilities![2],!and!might!also!underlie!264 those!observed!in!corvids!and!other!species,!allowing!individuals!to!adjust!their!behaviour!in!response!to!varying!inputs.!265 Experience!continues!to!shape!the!phenotype!through!adulthood!also!beyond!sensitive!developmental!periods,!just!to!a!266 lesser!extent![2,!35].!In!experimental!studies,!adult!New!Caledonian!crows!can!adapt!their!tool=use!skills!on!a!daily!basis!267 according!to!changing!local!conditions![78].!Adult!Siberian!jays!must!learn!new!skills,!such!as!recognizing!a!rare!predator!268 species,!or!accessing!new!food!sources![64].!Cognitive!flexibility!in!humans!and!corvids!is!based!on!plastic!alteration!of!269 brain!networks,!which!are!highly!interconnected!and!self=organise!by!interacting!dynamically!to!adapt!to!changing!270 conditions![17,!79,!80,!81,!82].!Variation!in!the!cultural!environment!affects!brain!growth!in!humans![83],!and!impacts!271 on!birds'!cognitive!development!through!the!enhancement!of!neural!plasticity!mechanisms![33].!Our!analysis!shows!272 that!prolonged!parenting!is!associated!with!a!higher!neuron!density!in!the!telencephalon!of!their!neocortex!across!273 species!(Table!2),!which!underlies!some!of!the!cognitive!skills!that!characterise!corvids!or!parrots.!Thus,!extended!274 parenting!fosters!an!expansion!of!the!cognitive!skill=set!via!an!increase!in!neuron!density!of!critical!brain!regions.!At!the!275 individual!level,!we!speculate!that!inter=individual!variation!in!brain!growth!patterns!could!cause!sociocultural!276 diversification!at!the!group!level!thanks!to!the!sociocultural!setting!of!tolerant!group!members!(safe!haven),!combined!277 with!extended!developmental!periods.!!278 !279 In!the!context!of!this!article,!we!need!to!know!how!developmental!changes!in!each!individual!might!affect!evolutionary!280 change!in!a!whole!species.!For!example,!epigenetic!changes!that!increase!neuronal!plasticity!(metaplasticity)!in!281 response!to!new!environmental!and!social!triggers![84,!85]!in!offspring!are!heritable!via!both!biological!and!cultural!282 routes![84].!These!epigenetic!changes!might!allow!for!increased!learning!ability!in!juveniles![86].!We!also!need!to!283 understand!much!better!how!learning!varies!through!individual!life!stages,!between!species,!comparatively!across!284 multiple!species,!and!evolutionarily!through!time![13,!87].!Most!fundamentally,!we!are!in!need!of!more!developmental!285 studies!that!examine!how!the!social!environment!impacts!on!brain!development,!and!consequently!on!the!skills!286 expressed!by!juveniles![88].!!287 !288 !289

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To!summarise,!we!presented!an!integrative!model!of!cognitive!evolution!that!incorporates!life!history,!ecology,!290 sociality,!and!learning.!We!have!discussed!the!evolutionary!trade=offs!of!a!life!history!involving!extended!development!291 (including!the!brain)!that!on!the!one!hand!offers!individuals!longer!learning!periods!to!acquire!necessary!survival!skills,!292 but!on!the!other!hand!is!energy=expensive,!often!requiring!elaborate!food!processing!skills!that!take!time!to!learn.!293 Adopting!a!comparative!approach!based!on!life!history!and!learning!in!corvids,!we!find!notable!similarities!with!the!294 unusual!life!history!of!humans,!with!its!extended!childhood!that!has!characterised!our!lineage!for!the!last!600,000!years.!295 Corvids!have!key!characteristics!that!make!them!a!relevant!comparison!family!to!understand!human!evolution.!Enlarged!296 brains!and!reliance!on!sociocultural!learning!of!skills,!enabled!by!extended!development!periods!in!species!with!297 prolonged!parenting!and!access!to!tolerant!role!models!in!a!safe!haven,!are!likely!to!result!in!expanded!cognitive!298 skillsets.!These!conditions!were!also!present!in!our!ancestors,!for!whom!cooperative!breeding!led!to!a!safe!haven!where!299 juveniles!could!learn!skills!from!extended!family,!including!grandparents![36=38,!46,!89],!and!increased!group!sizes!300 opened!more!learning!opportunities!for!individuals![87,!90].!The!case!studies!on!Siberian!jays!and!New!Caledonian!301 crows!show!that!extended!family!life!is!crucial!to!provide!the!social!learning!opportunities!where!juveniles!acquire!vital!302 skills.!We!propose!that!extended!parenting!could!well!have!led!to!the!extended,!lifelong!learning!found!in!humans,!303 given!its!life=history,!ecological!and!social!links!that!previous!work!identified!to!facilitate!the!evolution!of!flexible!and!304 expanded!cognitive!skillsets!across!species.!!305 !306 Acknowledgments!307 We!are!indebted!to!Alison!Gopnik,!Michael!Tomasello,!and!Willem!Frankenhuis!for!the!invitation!to!participate!in!this!308 special!issue!and!the!inspiring!conference!that!preceded!it.!We!thank!two!anonymous!reviewers!for!their!constructive!309 feedback.!Thanks!to!Anne!Clark!and!Andria!Kroner!for!sharing!their!unpublished!corvid!data.!We!thank!Michael!Haslam,!310 Gavin!Hunt,!Christian!Rutz,!Martina!Schiestl,!Neil!Smith,!Alex!Taylor,!and!the!landowners!for!their!support!to!NU's!New!311 Caledonian!crow!fieldwork.!NU's!fieldwork!and!the!writing!of!this!paper!were!made!possible!by!support!from!the!Max!312 Planck!Society!and!the!support!of!a!grant!from!Templeton!World!Charity!Foundation!313 (https://www.templetonworldcharity.org/)!#0271.!The!opinions!expressed!in!this!publication!are!those!of!the!authors!314 and!do!not!necessarily!reflect!the!views!of!Templeton!World!Charity!Foundation,!Inc.!MG's!Siberian!jay!fieldwork!was!315 funded!by!the!Swiss!National!Research!Foundation!(grant!numbers!PPOOP3_123520,!PPOOP3_150752).!316 !317

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[87] Richerson, P. J. & Boyd, R. 2000 Climate, culture and the evolution of cognition. The evolution 505 of cognition, 329-345. 506 [88] Morand-Ferron, J. this issue. 507 [89] Gurven, M. this issue. 508 [90] Tomasello, M. this issue. 509 [91] Drobniak, S. M., Wagner, G., Mourocq, E. & Griesser, M. 2015 Family living: an overlooked 510 but pivotal social system to understand the evolution of cooperative breeding. Behavioral Ecology 511 26, 805-811. (DOI: 10.1093/beheco/arv015). 512 [92] Valcu, M., Dale, J., Griesser, M., Nakagawa, S. & Kempenaers, B. 2014 Global gradients of 513 avian longevity support the classic evolutionary theory of ageing. Ecography 37, 930-938. 514 (DOI:10.1111/ecog.00929). 515 [93] Del Hoyo, J., Elliot, A., Sargatal, J. & Christie, D. A. 2011 Handbook of the Birds of the World. 516 Barcelona, Lynx Editions. 517 [94] Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. 2012 The global diversity of 518 birds in space and time. Nature 491, 444-448. (DOI:10.1038/nature11631). 519 !520 !521 !522 !523 !524

11

Tables''525

'526 Table'1.'Basic'life'history'characteristics'of'corvids'compared'to'other'passerines.'Data'were'compiled'from'published'527 data;sets'[16,'18,'41,'91,'92],'the'online'version'of'the'Handbook'of'the'Birds'of'the'World'[93],'unpublished'data'on'528 brain'size'compiled'by'Karin'Isler'(personal'communication),'and'a'recent'phylogeny'[94].'Parenting'time:'time'529 offspring'remain'associated'with'their'parents'beyond'independence.'Residual'brain'size:'log(brain'mass'(g))/log(body'530 mass'(g)).'Phylogenetic'controlled'comparisons'(corvids'vs'other'passerines)'using'PGLSs'in'the'R;package'Geiger'for'531 continuous'parameters'(providing't;values),'respectively'phylogenetic'logistic'regressions'in'the'R;package'phylolm'532 (providing'z;values).'Bold'denotes'traits'with'statistically'significant'differences.'533 '534 trait'

'

N'corvid'

species'

N'other'passerine'

species'

trait'mean±SE' λ'

'

estimate'

'

SE'

'

t;value/'

z;value'

p;value'

'corvids'

'

other'

passerines'

weight'(g)' 70' 1999' 267.8±23.83' 37.9±3.14' 1' ;89.58' 163.18' ;0.55' 0.58'

median*clutch*size* 64* 1577* 4.2±0.11* 3.2±0.03* 0.85* <1.20* 0.59* <2.04* 0.041*incubation'time'(days)' 42' 1019' 18.3±.0.21' 14.5±0.10' 0.92' ;1.17' 1.42' ;0.83' 0.41'

nestling*time*(days)* 41* 997* 28.±91.29* 16.0±0.16* 0.93* <8.28* 2.46* <3.37* 0.0008*parenting*time*(days)* 32* 557* 300.8±70.4* 98.1±6.16* 0.74* <181.21* 86.49* <2.10* 0.036*lifespan*(years)* 30* 701* 17.7±0.97* 9.8±0.16* 0.70* <7.66* 2.21* <3.46* 0.0006*family*living*(%)* 62* 1820* 81±0.05* 48±0.01* 0.70* <1.49* 0.59* <2.51* 0.012*cooperative'breeding'(%)' 63' 1819' 48±0.06' 16±0.01' 0.69' ;1.00' 0.59' ;1.71' 0.087'

residual*brain*size* 28* 426* 0.31±0.01* <0.09±0.01* 0.95* <0.26* 0.1* <2.61* 0.009*'535 '536 '537

12

Table&2.&Phylogenetic&regression&models&using&PGLSs&in&the&R;package&Geiger,&assessing&the&effect&of&family&system&(non;538 family&living&vs&family&living,&[41];&this&information&is&available&for&all&N=26&species&included)&and&the&post;fledging&539 association&time&of&offspring&with&their&parents&(data&available&for&N&=&17&species&[93];&data&for&Kea:&personal&540 communication&Alan&Bond)&on&relative&size&(a,b)&and&relative&number&of&neurons&(c,d)&in&the&telencephalon&of&birds.&541 Body&mass&is&included&to&control&for&its&effects&on&brain&parameters.&Telencephalon&data&from&[17]&on&N=26&altricial&bird&542 species;&models&including&post;fledging&association&time.&Bold&denotes&traits&with&statistically&significant&differences.&&543 &544 telencephalon*size*in*relation*total*brain*mass*(%)*(a)& Estimate& SE& t&value& p;value& &

intercept, 60.44, 3.95, 15.29, <0.001,&non7family,vs,family,living, 712.23, 3.96, 73.09, 0.005,&body&weight& 0.01& 0.01& 2.04& 0.053&

&

& & & & & &(b)& Estimate& SE& t&value& p;value&

&intercept, 45.23, 3.94, 11.48, <0.001,&post7fledging,association,time, 0.06, 0.02, 2.75, 0.016,&body&weight& 0.01& 0.01& 1.63& 0.12&

&

& & & & & &number*of*neurons*in*telencephalon*in*relation*to*all*neurons*(%)*(c)& Estimate& SE& t&value& p;value&

&intercept, 75.01, 2.28, 32.93, <0.001,&non7family,vs,family,living, 76.53, 2.36, 72.76, 0.011,&body&weight& 0.01& 0.00& 2.06& 0.051&

&

& & & & & &(d)& Estimate& SE& t&value& p;value&

&intercept, 66.44, 2.28, 29.08, <0.001,&post7fledging,association,time, 0.03, 0.01, 2.43, 0.029,&body&weight& 0.01& 0.01& 1.73& 0.1&

&&545 & &546

13

Figures&547

&548 Figure&1.&The&extended&parenting&hypothesis.&Grey&box:&aspects&related&to&living&in&family&groups.&Green&boxes:&549 ecological&aspects;&purple&boxes:&life;history&aspects;&blue&boxes:&extended&parenting&and&social&aspects;&orange&boxes:&550 cognitive&aspects;&brown:&costs&of&learning&and&brains;&black&squared&boxes:&links&to&other&hypotheses.&&551 &552

&553 & &554

14

Figure&2:&The&life;history&and&family&filter&explaining&cognitive&adaptations&(modified&after&[32]),&illustrated&with&8&555 altricial&hypothetical&bird&lineages.&Cognitive&challenges&can&only&lead&to&cognitive&adaptations&in&long;lived&species&556 (allowing&to&compensate&the&energetic&costs&of&increased&brains&and&larger&skillsets),&which&are&exposed&to&ample&557 learning&opportunities&in&a&safe&environment&(provided&by&extended&parenting).&558 &559

&560 &561 & &562

15

&563

Supplementary&material&564

Please&see&attached&PDF&and&Video&S1.&565 &566

Additional&Information&567

During,the,submission,process,you,will,be,asked,to,provide,the,following,information.,You,do,not,need,to,include,this,in,your,568 manuscript.,These,statements,will,be,available,to,reviewers,and,included,in,the,published,paper.,569 &570 Ethics,7,not,applicable,571 &572 Data,Accessibility,7,not,applicable,573 Data&were&compiled&from&the&published&sources&listed&in&the&Table&caption.&&574 &&575 Authors',Contributions&576 NU&and&MG&wrote&the&paper,&with&inputs&from&JF&and&RG.&All&authors&approved&the&final&version.&&577 &578 Competing,Interests,579 We&have&no&competing&interests.&580 &581 &582

Phil. Trans. R. Soc. B. doi:10.1098/rstb.2019.0495

1

Extended parenting and the evolution of cognition

Natalie Uomini*, Joanna Fairlie, Russell D. Gray, Michael Griesser*

!

Supplementary,material, Video S1. Part 1: Wild Siberian jays at the feeding board during the social learning experiments. The first three birds seen are adults, then the juvenile appears alone. Part 2: Adult and juvenile wild New Caledonian crows interacting with tools. The juvenile is seen begging and has a red gape. The other two birds are adults.

Figure S1. A wild Siberian jay parent and its retained offspring foraging together.

*Authors for correspondence (traduck@gmail.com and michael.griesser@gmail.com).

Phil. Trans. R. Soc. B. doi:10.1098/rstb.2019.0495

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Figure S2. The same jay parent as in Figure S1, this time displacing an immigrant juvenile.

Figure S3. Setup of the social learning experiment with Siberian jays. A breeder waits at the feeding board until its offspring has taken food. Parents are tolerant of kin juveniles even in an experimental setting.

Phil. Trans. R. Soc. B. doi:10.1098/rstb.2019.0495

3

Figure S4. An adult wild New Caledonian crow with a tool in its beak and two begging juveniles.

Figure S5. A juvenile wild New Caledonian crow using a tool to probe together with an adult.

Figure S6. Up in the canopy, a wild juvenile New Caledonian crow begs at an adult that holds a tool in its beak.