extended parenting and the evolution of cognition...evolution, neuroscience keywords: parenting,...

royalsocietypublishing.org/journal/rstb

ReviewCite this article: Uomini N, Fairlie J, Gray RD,Griesser M. 2020 Extended parenting and theevolution of cognition. Phil. Trans. R. Soc. B20190495.http://dx.doi.org/10.1098/rstb.2019.0495

Accepted: 8 February 2020

One contribution of 15 to a theme issue ‘Lifehistory and learning: how childhood,caregiving and old age shape cognition andculture in humans and other animals’.

Subject Areas:behaviour, cognition, developmental biology,evolution, neuroscience

Keywords:parenting, corvidae, Siberian jays,new Caledonian crows, cognitive evolution,social learning

Authors for correspondence:Natalie Uominie-mail: [email protected] Griessere-mail: [email protected]

†These authors contributed equally to thiswork.

Electronic supplementary material is availableonline at rs.figshare.com.

Extended parenting and the evolutionof cognitionNatalie Uomini1,†, Joanna Fairlie2, Russell D. Gray1,3 and Michael Griesser4,†

1Department of Linguistic and Cultural Evolution, Max Planck Institute for the Science of Human History,Kahlaische Strasse 10, Jena, Germany2Independent Researcher, UK3School of Psychology, University of Auckland, 23 Symonds Street, Auckland 1010, New Zealand4State Key Laboratory of Biocontrol, Department of Ecology and School of Life Sciences, Sun Yat-sen University,Guangzhou 510275, People’s Republic of China

NU, 0000-0002-9898-6415; JF, 0000-0001-9900-6098; RDG, 0000-7 0002-9858-0191;MG, 0000-0002-2220-2637

Traditional attempts to understand the evolution of human cognitioncompare humans with other primates. This research showed that relativebrain size covaries with cognitive skills, while adaptations that buffer thedevelopmental and energetic costs of large brains (e.g. allomaternal care),and ecological or social benefits of cognitive abilities, are critical for theirevolution. To understand the drivers of cognitive adaptations, it is profitableto consider distant lineages with convergently evolved cognitions. Here, weexamine the facilitators of cognitive evolution in corvid birds, where somespecies display cultural learning, with an emphasis on family life. We pro-pose that extended parenting (protracted parent–offspring association) ispivotal in the evolution of cognition: it combines critical life history, socialand ecological conditions allowing for the development and maintenanceof cognitive skillsets that confer fitness benefits to individuals. This novelhypothesis complements the extended childhood idea by considering theparents’ role in juvenile development. Using phylogenetic comparativeanalyses, we show that corvids have larger body sizes, longer developmenttimes, extended parenting and larger relative brain sizes than other passer-ines. Case studies from two corvid species with different ecologies andsocial systems highlight the critical role of life-history features on juveniles’cognitive development: extended parenting provides a safe haven, access totolerant role models, reliable learning opportunities and food, resultingin higher survival. The benefits of extended juvenile learning periods,over evolutionary time, lead to selection for expanded cognitive skillsets.Similarly, in our ancestors, cooperative breeding and increased group sizesfacilitated learning and teaching. Our analyses highlight the critical roleof life history, ecological and social factors that underlie both extendedparenting and expanded cognitive skillsets.

This article is part of the theme issue ‘Life history and learning: howchildhood, caregiving and old age shape cognition and culture in humansand other animals’.

1. IntroductionThe diverse and flexible cognitive abilities of our species are considered pivotalfor our evolutionary history [1]. Our extended childhood is a key life-historytrait that impacts on human cognition, giving humans a period of cognitiveflexibility (changeability) to explore more options during learning [1–6]. Lifehistory describes the age-specific patterns that are central to an organism’slife, including the reproductive allocation strategies, development and ageingpatterns [7]. However, extended developmental periods evolved not only inhumans and other primates, but also in bats, cetaceans, elephants and severalbird families [7]. Thus, we ask here two questions: (i) Are the effects of extendedchildhood on cognition specific to humans, or can they be generalized to other

© 2020 The Author(s) Published by the Royal Society. All rights reserved.

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RSTB20190495—5/5/20—22:24–Copy Edited by: Not Mentioned

, [email protected]

and Department of Biology, University of Konstanz, Universitätsstrasse 10, 78457 Konstanz, Germany

New

for human evolutionary history An

species with relatively expanded cognitive skillsets? (ii) Whatis the particular role of parenting on the development ofcognition in individuals?

While the term ‘cognition’ has no agreed definition [8], wefollowhereAllen [9], defining it as ‘the brain’s synthesis of infor-mation from diverse sensory and memory sources to produceappropriate responses’. We refer to skillsets as the combinationof cognitive abilities possessed by a species or an individual.Evolutionary cognitive studies investigate cognitive changesover time in species. The ‘embodied cognition’ approach,which views cognition as a result of interactions between anindividual’s bodyand its environment [10,11], is an increasinglyinfluential view in cognitive science [11–13]. However, the inter-actions between life history, ecology and learning have rarelybeen considered in cognitive evolution research. Thus, we usehere an integrative approach to propose a new model of cogni-tive evolution based on extended childhoods and extendedparenting typical of family-living species.

Many scholars consider brain size as a useful proxy for cog-nitive abilities because species with larger brains tend to showmore diverse and flexible behaviours [13], but the validity ofthis proxy is debated [11,14–16]. Since brain morphology candiffer between lineages [14,17], it is recommended to relatebrain sizes to cognitive abilities only within lineages, and toconsider behaviour when inferring cognitive abilities in indi-viduals or species [14]. Work focusing on brains showed thatthey are paradoxical adaptations for two reasons. First, braintissue is energetically very expensive to grow and maintain[18], and thus, large brains can only evolve if their costs are buf-fered through prolonged developmental periods and/orallomaternal energy inputs (expensive brain framework [19]).Second, it takes time for an individual’s brain to develop thecognitive abilities that make this adaptation worthwhile.Thus, cognitive adaptations are constructed developmentally,and their development relies on access to learning opportu-nities [20–22]. The combination of these factors stresses theimportance of ontogeny, and a constant, reliable access toresources during development to offset the cost of largebrains [23]. Thus, selection on brain size and learning abilityis associated with extended developmental periods [24,25].Relevant for models of cognitive evolution is that individualswith extended learning periods are predicted to developlarger cognitive skillsets, allowing them to more successfullyreproduce and avoid extrinsic mortality [24].

Here, we focus on the coevolutionary links of life-historytraits with extended skill-learning periods. While learning iscostly, including increased parental investment and highervulnerability of naive juveniles [26], several studies showedfitness benefits of faster learning ability [27,28]. Previouswork assessed particular drivers of cognitive abilities (usuallyusing brain size as a proxy), including ecological, social andcultural drivers, or assessed very specific aspects of cognition,such as innovations [3,16,22,23,29–31], but rarely consideredthe evolutionary interplay between developmental trajecto-ries, sociality, cognition and brain evolution [4,19,30,32,33].Previous work showed that enlarged brain size evolved inspecies with a larger body size, larger group sizes, longerreproductive lifespan, more reliance on social learning andmore variable environments [34]. These data are largely inline with the cognitive buffer hypothesis, which proposesthat larger brains provide more abilities that help to surviveunfavourable conditions [30]. Nevertheless, what remains tobe clarified is the fitness benefit of extended parenting for the

evolution of cognitive abilities.We develop below the extendedparenting hypothesis, which extends and complements the‘extended childhood’ hypothesis [2,3,35–38] based on a phylo-genetic comparison of corvids with other passerines, andinsights from two long-term field studies on corvids.

2. The extended parenting hypothesisWe will argue that the ontogenetic development of expandedandmore flexible cognitive skillsets requires (i) a fitness benefit,(ii) ample and reliable social learning opportunities (facilitatedby extended childhood and extended parenting), (iii) thebuffering of the costs of developing and maintaining a largebrain, and (iv) ecological conditions that facilitate extendedparenting (figure 1). The comparative data below show thatextended parenting is critical for the evolution of large brainsand large cognitive skillsets in most cases. Previous modelsand comparative work identified a set of ecological, socialand life-history parameters that are associated with largerbrains: (i) ecological and social challenges that favour certaincognitive abilities [30], (ii) a life history that provides the oppor-tunity to develop more cognitive and sensory–motor abilitiesand covers their developmental and maintenance costs[23,32], and (iii) a fitness benefit from having these abilities[39]. These requirements are found not only in species withincreased levels of alloparental care [40], but also in specieswith extended parenting. In birds, extended parentingprovides an evolutionary steppingstone for transitions to coop-erative breeding, where others than parents provide parentalcare [41], alleviating the development and maintenance costsof large brains. Comparative work showed that family livingis associated with a larger body size, an increased lifespanand productive, mild environments [41]. Thus, buildingupon the cultural intelligence idea [22], we propose here thatparenting itself is pivotal for the social environment thatfavours the evolution of cognitive adaptations through learn-ing, and that it links to environmental conditions thatsupport the costs of large brains and provide a benefit fromincreased skillsets [39] (figure 1).

For extended parenting to evolve, it must confer benefitsthat offset the costs of delayed maturation [7,42], for example,increased survival [43]. Increased flexibility and innovative-ness, such as rates of novel feeding behaviours in naturalpopulations, can also facilitate survival in changing environ-ments [39,44]. An extended developmental and childhoodphase provides more time to learn difficult skills, supportingthe evolution of socioecological niches with specializedforaging techniques [45–47]. In humans, cognitive flexibilityis greatest in preschool-aged children but decreases sub-sequently, which suggests that the evolution of an extendedchildhood favoured the variable use of a more exploratorylearning strategy early on and fixed learned strategies lateron in life, creating a fruitful balance between innovationand imitation in cultural learning [2]. An extended childhoodhas been an integral part of human life-history patterns for atleast 600 000 years, as shown by fossil evidence for bodymass, brain size and dental development of human ancestorsand related extinct species [48]. Our ancestors’ technologicalskills included the most difficult to learn technologies docu-mented until that time (i.e. involving the most elementsand hierarchical levels of action sequencing, and demandingthe longest learning times), as evidenced by archaeological

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such as or

tool analyses and transmission experiments [49–53]. Learninga skill, including stone tool-making that demands extensivetime investment, is costly to the individual and the group.In humans, apprenticeship strategies evolved to reducethese costs [49,50,54]. Because offspring must be fed untilthey have acquired a self-sustaining level of foraging skills[24], a lengthening of provisioning time increases the coststo the feeders. Taken together, these data illustrate the criticalrole of costs in our model for both parents and learners.

3. Corvid life histories: comparison withother passerines

Research on human cognitive evolution benefits from consider-ation of non-primate species [23,30,55]. Birds, which have a 300million-year-long evolutionary history independent of mam-mals, provide an excellent outgroup to untangle the factorsinvolved in cognitive evolution. We focus on corvids becausethey show convergent cognitive abilities that rival apes inmany domains, such as in tool manufacture, planning andinsight [56]. These abilities have been linked to an increase inneuron density in their neocortex, particularly the telencepha-lon [17]. Thus, corvids provide us with a comparison to earlyhuman ancestors as they present an intriguing example of con-vergent evolution in innovative problem-solving, increasedmanipulative dexterity, technical skills and socioculturaltransmission of skills that lead to cultural variation [57].

Corvids are a globally distributed passerine family thatincludes 127 species. Corvids and 30 related bird familiesform the super-clade of Corvides, which includes other birdspecies with large brain sizes (e.g. drongos, currawongs,

Australian magpies). Corvids originated in the Australo-Papuan region around 14 Ma in rainforest habitats [58], andinterestingly, they differ in a large number of traits from otherpasserines (table 1). Corvids are among the largest passerines,and have much larger relative brain sizes. The incubationtime is longer than the passerine mean, and the time spent inthe nest is almost double the mean for other passerines. Impor-tantly for learning, offspring have extended periods beyondfledging where they remain associated with their parents com-pared to other passerines. Finally, a high number of corvidspecies breed cooperatively.

Although we lack detailed data on the brain structure ofmany species, phylogenetic analyses show that bird specieswith extended family life have larger telencephalons, and alarger proportion of neurons located in their telencephalon[17] (table 2). Thus, corvids stand out from other passerinesnot only in terms of their cognitive abilities, but also inhaving a set of life-history features linked to extended parent-ing. But how does extended parenting affect learning, andimportantly, survival? Two case studies that directly addressedlearning in corvids are presented below. Crucially, the datafrom these species are not confounded by potential effects ofcooperative breeding, which has been previously identifiedto facilitate the evolution of large brains [30,40].

4. Siberian jays: learning opportunities matterSiberian jays (Perisoreus infaustus; electronic supplementarymaterial, video S1) are sedentary corvids that occur through-out the northern Palearctic [63]. Their social system has twounique facets that provide insights into the benefits of

extrinsicmortality

developmentperiods

extendedparenting

learningopportunities

role models

paying costs of skilllearning and large brain

cognitiveskillset

cognitive bufferhypothesis

expensive brainhypothesis

ª self-domestication

hypothesis

culturalintelligencehypothesis

elaboratedniche

cooperativebreeding

lifespan

productiveenvironments

variableenvironments

Figure 1. The extended parenting hypothesis. Grey box: aspects related to living in family groups. Green boxes: ecological aspects; purple boxes: life-history aspects;blue boxes: extended parenting and social aspects; orange boxes: cognitive aspects; brown: costs of learning and brains; black squared boxes: links to otherhypotheses.


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many corvid

our phylogenetic

[55,57].

Green stippled boxes: ecological aspects; purple checkered

boxes: life-history aspects; blue boxes: extended parenting and social aspects; orange box: cognitive aspects; brown dashed box: costs of learning and brains;

black squared boxes: links to other hypotheses.

Table 1. Basic life-history characteristics of corvids compared to other passerines. Data were compiled from published datasets [16,18,41,59,60], the onlineversion of the Handbook of the Birds of the World [61], unpublished data on brain size compiled by K. Isler (personal communication Q6), and a recent phylogeny[62]. Parenting time: time offspring remain associated with their parents beyond independence. Residual brain size: log(brain mass (g))/log(body mass (g)).Phylogenetic controlled comparisons (corvids versus other passerines) using PGLSs in the R-package Geiger for continuous parameters (providing t-values),respectively phylogenetic logistic regressions in the R-package phylolm (providing z-values). Bold denotes traits with statistically significant differences.

traitN corvidspecies

N otherpasserinespecies

trait mean ± s.e.

λ estimate s.e.t-value/z-value p-valuecorvids

otherpasserines

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

Table 2. Phylogenetic regression models using PGLSs in the R-package Geiger, assessing the effect of family system (non-family living versus family living, [41];this information is available for all N = 26 species included) and the post-fledging association time of offspring with their parents (data available for N = 17species [61]; data for Kea: A. Bond, personal communication) on relative size (a,b) and relative number of neurons (c,d) in the telencephalon of birds. Bodymass is included to control for its effects on brain parameters. Telencephalon data from [17] on N = 26 altricial bird species; models including post-fledgingassociation time. Bold denotes traits with statistically significant differences.

estimate s.e. t-value p-value

(a) telencephalon size in relation total brain mass (%)

intercept 60.44 3.95 15.29 <0.001

non-family versus family living −12.23 3.96 −3.09 0.005

body weight 0.01 0.01 2.04 0.053

(b)

intercept 45.23 3.94 11.48 <0.001

post-fledging association time 0.06 0.02 2.75 0.016

body weight 0.01 0.01 1.63 0.12

(c) number of neurons in telencephalon in relation to all neurons (%)

intercept 75.01 2.28 32.93 <0.001

non-family versus family living −6.53 2.36 −2.76 0.011

body weight 0.01 0.00 2.06 0.051

(d)

intercept 66.44 2.28 29.08 <0.001

post-fledging association time 0.03 0.01 2.43 0.029

body weight 0.01 0.01 1.73 0.1


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(p<0.05).

adult body weight (g)

(pers. comm. 2014),

A. Bond, pers. comm. 2019)

Basic life-history characteristics of corvids (127 total species) compared to other passerines (4796 total species). Table 1. Data were compiled from unpublished data on corvid social characteristics compiled by Andria Kroner and Anne Clark (pers. comm., 2019), published datasets

(p<0.05).

trait

in relation to total brain mass (%)

190

family living. First, the species does not breed cooperatively(i.e. only parents incubate and feed young), despite the factthat offspring can remain with their parents for years afterfledging, which is associated with cooperative breeding inmost species [41]. Second, Siberian jay groups consist of abreeding pair, retained offspring and/or unrelated non-breeders. The latter are forced by the socially dominantretained offspring to disperse from the natal territory one totwo months after fledging and settle in another group [64].Retained offspring can remain up to an age of 4 years withtheir parents, which is well beyond the mean lifespan of 2.2years [63].

Parents differ in their behaviour towards kin and non-kin(electronic supplementary material, figures S1 and S2) as theyare nepotistic and only provide access to resources and pred-ator protection to kin [63], resulting in a higher survival ofkin compared to non-kin [43].

Field experiments on predator recognition and problem-solving in juveniles reveal how fitness-related proxies dependon kinship. Predation by goshawks is the main reason for mor-tality in Siberian jays, especially affecting juveniles [43,65].Juveniles do not respond to perched predators when encoun-tering them on their own, but when other group membersstart mobbing a perched predator, particularly retained off-spring immediately copy the behaviour of their parents [66].Natural mobbing events are very brief, as mobbed predatorsquickly move off, so that unrelated non-breeders havemuch fewer opportunities than retained offspring to observemobbing. However, in experimental settings where preda-tor models are presented, mobbing could last as long as4 min, providing also unrelated non-breeder with learningopportunities. Consequently, all juveniles survived their firstwinter of life [67]. Moreover, retained juveniles learn to accessa feeding device (electronic supplementary material, figureS3) faster than unrelated juveniles [68], as their learning is facili-tated by more tolerant role models (i.e. their parents; electronicsupplementary material, video S1). Thus, a life history invol-ving extended parenting is a critical support for learning:parents provide their offspring with a safe haven, access tofood and reliable learning opportunities, which togetherboost the long-term survival of retained offspring [67].

5. New Caledonian crows: tool manufacturematters

New Caledonian crows (Corvus moneduloides; electronic sup-plementary material, video S1) are endemic to the tropicalSouth Pacific island of New Caledonia, where they live infamily groups with extended dependency periods: offspringcan be fed by their parents for up to 2 years [69], whichmight explain why this species does not breed cooperatively[69]. During this extended developmental period, juvenileshave access to tolerant role models (both related andunrelated [70]), from whom they can learn tool-use and tool-making skills [70,71] (electronic supplementary material,figure S4 and video S1). Social learning experiments showedthat adults and juveniles learn about the appropriate contextfor certain actions from each other, demonstrating the potentialfor lifelong learning ability [72]. In the wild, adults scaffoldlearning of juveniles by allowing them to be in physical contactduring foraging (electronic supplementarymaterial, figure S5),and by sometimes leaving a tool in a tree hole that juveniles can

then use with success (electronic supplementary material,video S1). However, this extended tool-making learningperiod comes with a high cost: juveniles are unable to makefunctional tools until they are at least six months old. Adult-level proficiency is reached at 10–12 months of age [70], requir-ing that parents provision their offspring through their firstyear of life. Thus, wild juveniles grow up in a safe haven,surrounded by tolerant role models that constantly make anduse tools (electronic supplementary material, figure S6), andjuveniles have ample occasions to borrow and use otherbirds’ tools (electronic supplementary material, video S1).

New Caledonian crows have the largest relative brain sizeamong corvids [73], suggesting selective pressures on someaspects of cognitive performance [17]. Compared to othercorvids, they have significantly larger brain areas subservinglearning, action sequencing and fine motor control functions[74], all of which support the tool-making and tool-use beha-viours enacted by New Caledonian crows. In experimentalsettings, New Caledonian crows have been shown to excelat problem-solving, physical cognition and causal reasoningin tests such as the trap-tube, string pulling and Aesop’sfable tasks (in which suitable objects must be dropped intoa beaker of water to raise the water level to obtain a floatingreward) [75].

Several evolutionary adaptations were crucial for theemergence of tool-making skills in New Caledonian crowsand representative human ancestors [76], including increasesin brain size and brain networking potential, stable groupswith a high social tolerance providing opportunities forsocial learning, and extended parenting and developmentperiods. Increased social learning opportunities allow indi-viduals to acquire more skills and to become more effectiveindividual learners [20,22].

6. Cognitive consequences of extended parentingIn the corvid case studies we presented, Siberian jays tolerateretained offspring more than unrelated non-breeders, whichincreases the learning opportunities and survival prospectsof retained offspring [43]. New Caledonian crows are highlytolerant to juveniles independent of their kinship [70], andadults scaffold the learning process of juveniles acquiringtool-making skills (‘education by master–apprenticeship’[77]). In addition, juveniles of both species are highly proactivein ways that foster opportunities to observe others and topractice skills. In Siberian jays, retained juveniles pay moreattention to the behaviour of the adults in their group thanunrelated juveniles do [66]. Juvenile New Caledonian crowsactively follow group members, direct begging behaviourstowards them, steal foraged food from them and also stealready-made tools that they can use to get food. These beha-viours are tolerated by the adults and ensure survival ofjuvenile corvids that are not yet nutritionally independent.Thus, learning opportunities arise from the interplay betweenextended childhood and extended parenting. The safe havenprovided by extended parenting is critical for learning oppor-tunities, and creates extended developmental periods thatfeed back into the extended childhood.

Centred on extended parenting, our model (illustrated infigure 1) extends and complements the ‘extended childhood’model [2,3,35–38], while highlighting the active nature ofboth adults and juveniles. Our model integrates previous


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non-breeders

(see electronic supplementary material, figures S4, S5, S6, and video S1)

,76].

[55],

models of cognitive and brain evolution [4,16,19,29–32,78] butadds crucial details on the interactions with ecological traits,life-history traits and fitness benefits.More productive environ-ments facilitate low extrinsic mortality, leading to a longerlifespan and an associated reduction in reproductive allocation[7,42]. These conditions facilitate extended family time [41,79],and a safe haven through access to food and protection frompredators [41], which in turn facilitate extended developmentalperiods with ample learning opportunities provided by toler-ant role models [20] (i.e. the ‘playful protected learningenvironment’ of humans [2]). These conditions are likely tofavour the evolution of larger cognitive skillsets [32,80].The costs of extended learning periods are paid by extendedprovisioning, which is enabled by productive environments.Moreover, extended family time also facilitates the evolutionof cooperative breeding, which additionally can enable theevolution of larger brains (table 2) that sustain larger skillsets[40]. Extended learning time, more role models to learn fromand a release from the costs of large brains allow the develop-ment of larger ormore flexible cognitive skillsets, which in turngive species chances tomove into newecological niches [39,81],or allows them to cope with environmental degradation lead-ing to variable environments [41]. This later factor is alsoassociated with the evolution of cooperative breeding [41].Together, these adaptations can incur fitness benefits throughthe safe haven, an expansion of the cognitive skillset and coop-erative breeding.

The life-history filter model [32] proposes that survivalchallenges only result in cognitive adaptations if the lifehistory of species include a low extrinsic mortality, which inturn allows to reallocate resources into the development

and maintenance of a larger brain. Drawing upon this idea,we propose that integrating the family filter into this modelcan explain the absence of large brains in long-lived speciesdue to short family times, or the occurrence of large brainsin short-lived species due to extended parenting (figure 2).Thus, not only extrinsic mortality and size constraints [32],but also extended parenting can explain the occurrence ofgrade-shifts (i.e. deviations from body sized-based expectedbrain sizes) of animals.

7. Discussion and conclusionThe comparative data on corvids support the fundamentalrole of extended parenting for the evolution of cognitive skill-sets through learning, and family living links to critical lifehistory and ecology features that have been previously ident-ified to facilitate cognitive evolution. Extended parenting isonly possible if (i) the life-history pace is slow enough sothat the optimal onset of independent reproduction is notat the first opportunity [42], (ii) parents can afford extendedoffspring association [79], and (iii) the ecological setting pro-vides productive environments or adaptations that bufferpossible ecological costs. Particularly, the access to tolerantrole models is a key variable that affects between-individualvariability in learning within and between species. Extendedparenting allows these high-quality relationships to develop,and has a direct impact on fitness, as shown by the restrictedlearning opportunities of unrelated juveniles in Siberian jays,and their lower survival [66,68]. Similarly, adult New Caledo-nian crows are highly tolerant to their own but also unrelated

life-history filter:

lifes

pan

pare

ntin

gtim

eco

gniti

vead

apta

tions

L1 L2 L3 L4 L5 L6 L7 L8

L1 L2 L3 L4 L5 L6 L7 L8

family filter:

variation in extrinsic mortalitysets cognitive potential

extended parentingprovides more learning

opportunities

achieved cognition:

cognitive challenges

level of extrinsic mortality× learning opportunites

Figure 2. The life history and family filter explaining cognitive adaptations (modified after [32]), illustrated with eight altricial hypothetical bird lineages. Cognitivechallenges can only lead to cognitive adaptations in long-lived species (allowing to compensate the energetic costs of increased brains and larger skillsets), whichare exposed to ample learning opportunities in a safe environment (provided by extended parenting). (Online version in colour.)


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compensating for

interacts withlearning opportunities

a species includes a low

,

in

juveniles, scaffolding the sensory–motor and embodiedlearning process of juveniles.

This special issue examines whether and how the life his-tory of different species is connected with their cognitiveabilities. Cognitive flexibility throughout the lifetime is centralto our cognitive abilities [2], and might also underlie thoseobserved in corvids and other species, allowing individualsto adjust their behaviour in response to varying inputs. Experi-ence continues to shape the phenotype through adulthood alsobeyond sensitive developmental periods, just to a lesser extent[2,35]. In experimental studies, adult New Caledonian crowscan adapt their tool-use skills on a daily basis according tochanging local conditions [82]. Adult Siberian jays must learnnew skills, such as recognizing a rare predator species, or acces-sing new food sources [68]. Cognitive flexibility in humans andcorvids is based on plastic alteration of brain networks, whichare highly interconnected and self-organize by interactingdynamically to adapt to changing conditions [17,83–86].Variation in the cultural environment affects brain growth inhumans [87], and impacts on birds’ cognitive developmentthrough the enhancement of neural plasticity mechanisms[33]. Our analysis shows that prolonged parenting is associatedwith a higher neuron density in the telencephalon of theirneocortex across species (table 2), which underlies some ofthe cognitive skills that characterize corvids or parrots. Thus,extended parenting fosters an expansion of the cognitive skill-set via an increase in neuron density of critical brain regions.At the individual level, we speculate that inter-individualvariation in brain growth patterns could cause socioculturaldiversification at the group level thanks to the socioculturalsetting of tolerant group members (safe haven), combinedwith extended developmental periods.

In the context of this article, we need to know howdevelop-mental changes in each individual might affect evolutionarychange in a whole species. For example, epigenetic changesthat increase neuronal plasticity (metaplasticity) in responseto new environmental and social triggers [88,89] in offspringare heritable via both biological and cultural routes [88].These epigenetic changes might allow for increased learningability in juveniles [90]. We also need to understand muchbetter how learning varies through individual life stages,between species, comparatively across multiple species, andevolutionarily through time [13,91]. Most fundamentally, weare in need of more developmental studies that examine howthe social environment impacts on brain development, andconsequently on the skills expressed by juveniles [92].

To summarize, we presented an integrative model of cog-nitive evolution that incorporates life history, ecology,

sociality and learning. We have discussed the evolutionarytrade-offs of a life history involving extended development(including the brain) that on the one hand offers individualslonger learning periods to acquire necessary survival skills,but on the other hand is energy-expensive, often requiringelaborate food processing skills that take time to learn.Adopting a comparative approach based on life history andlearning in corvids, we find notable similarities with the unu-sual life history of humans, with its extended childhoodthat has characterized our lineage for the last 600 000 years.Corvids have key characteristics that make them a relevantcomparison family to understand human evolution. Enlargedbrains and reliance on sociocultural learning of skills, enabledby extended development periods in species with prolongedparenting and access to tolerant role models in a safe haven,are likely to result in expanded cognitive skillsets. Theseconditions were also present in our ancestors, for whomcooperative breeding led to a safe haven where juvenilescould learn skills from extended family, including grand-parents [36–38,46,93], and increased group sizes openedmore learning opportunities for individuals [91,94]. Thecase studies on Siberian jays and New Caledonian crowsshow that extended family life is crucial to provide thesocial learning opportunities where juveniles acquire vitalskills. We propose that extended parenting could well haveled to the extended, lifelong learning found in humans,given its life history, ecological and social links that previouswork identified to facilitate the evolution of flexible andexpanded cognitive skillsets across species.

Data accessibility. Data were compiled from the published sources listedin the table caption.Authors’ contributions. N.U. and M.G. wrote the paper, with inputs fromJ.F. and R.D.G. All authors approved the final version.Competing interests. We declare we have no competing interests.Funding. N.U.’s fieldwork and thewriting of this paperweremade poss-ible by support from theMax Planck Society and the support of a grantfrom TempletonWorld Charity Foundation (https://www.templeton-worldcharity.org/) #0271. The opinions expressed in this publicationare those of the authors and do not necessarily reflect the views ofTempleton World Charity Foundation, Inc. M.G.’s Siberian jay field-work was funded by the Swiss National Research Foundation (grantnos PPOOP3_123520, PPOOP3_150752).Acknowledgements. Weare indebted toAlisonGopnik,Michael TomaselloandWillem Frankenhuis for the invitation to participate in this specialissue and the inspiring conference that preceded it. We thank twoanonymous reviewers for their constructive feedback. Thanks toAnne Clark and Andria Kroner for sharing their unpublished corviddata. We thank Michael Haslam, Gavin Hunt, Christian Rutz, MartinaSchiestl, Neil Smith, Alex Taylor and the landowners for their supportto N.U.’s New Caledonian crow fieldwork.

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1

Extended parenting and the evolution of cognition

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

Supplementary,material,

Video S1 (see Uomini.Fairlie.Gray.Griesser.2020_ExtendedParenting_VIDEO_S1.mp4). 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. Video by Charlotte Wrobleski.

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.

Video by Natalie Uomini and Neil Smith.

Figure S1. A wild Siberian jay parent (left) and its retained offspring (right) foraging

together. Photo by Michael Griesser.

*Authors for correspondence ([email protected] and [email protected]).


2

Figure S2. The same jay parent (foreground) as in Figure S1, this time displacing an

immigrant juvenile (background). Photo by Michael Griesser.

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. Photo by Michael Griesser.


3

Figure S4. An adult wild New Caledonian crow (right) with a tool in its beak and two

begging juveniles. Photo by Natalie Uomini and Neil Smith.

Figure S5. A juvenile wild New Caledonian crow (right) using a tool to probe together

with a tolerant adult (left). Photo by Natalie Uomini.

Figure S6. Up in the canopy, a wild juvenile New Caledonian crow begs at an adult

that holds a tool in its beak. Photo by Neil Smith.

extended parenting and the evolution of cognition...evolution, neuroscience keywords: parenting,...

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