university of zurich zurich open ......for review only 2 31 32 key words: social learning,...

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Year: 2011

Social learning and evolution: the cultural intelligencehypothesis

van Schaik, C P; Burkart, J M

http://dx.doi.org/10.1098/rstb.2010.0304.Postprint available at:http://www.zora.uzh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich.http://www.zora.uzh.ch

Originally published at:van Schaik, C P; Burkart, J M (2011). Social learning and evolution: the cultural intelligence hypothesis.Philosophical Transactions of the Royal Society. Series B, Biological Sciences, 366(1567):1008-1016.

http://dx.doi.org/10.1098/rstb.2010.0304.Postprint available at:http://www.zora.uzh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich.http://www.zora.uzh.ch

Originally published at:van Schaik, C P; Burkart, J M (2011). Social learning and evolution: the cultural intelligence hypothesis.Philosophical Transactions of the Royal Society. Series B, Biological Sciences, 366(1567):1008-1016.

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Social learning and evolution: The cultural intelligence hypothesis 1

2

Carel P. van Schaik1*

3

Judith M. Burkart1 4

5

1 Anthropologisches Institut & Museum, Universität Zürich, Winterthurerstrasse 190, 6

8057 Zürich, Switzerland 7

* Corresponding author’s e-mail: [email protected] 8

9

Short title: The cultural intelligence hypothesis 10

Abstract 11

If social learning is more efficient than independent individual exploration, animals 12

should learn vital cultural skills exclusively, and routine skills faster, through social 13

learning, provided they actually use social learning preferentially. Animals with 14

opportunities for social learning indeed do so. Moreover, more frequent 15

opportunities for social learning should boost an individual’s repertoire of learned 16

skills. This prediction is confirmed by comparisons among wild great ape populations 17

and by social deprivation and enculturation experiments. These findings shaped the 18

cultural intelligence hypothesis, which complements the traditional benefit 19

hypotheses for the evolution of intelligence by specifying the conditions in which 20

these benefits can be reaped. The evolutionary version of the hypothesis argues that 21

species with frequent opportunities for social learning should more readily respond 22

to selection for a greater number of learned skills. Because improved social learning 23

also improves asocial learning, the hypothesis predicts a positive interspecific 24

correlation between social learning performance and individual learning ability. 25

Variation among primates supports this prediction. The hypothesis also predicts that 26

more heavily cultural species should be more intelligent. Preliminary tests involving 27

birds and mammals support this prediction too. The cultural intelligence hypothesis 28

can also account for the unusual cognitive abilities of humans, as well as our unique 29

mechanisms of skill transfer. 30

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31

Key words: Social learning, intelligence, brain size, enculturation, cross-fostering, 32

social deprivation 33

34

1. INTRODUCTION 35

Intelligence is the ability to respond flexibly to new or complex situations, to learn, 36

and to innovate [1]. This ability is anchored in genetic predispositions towards faster 37

reaction times, greater working memory, inhibitory control and greater response to 38

novelty [2]. However, intelligence poses an evolutionary puzzle. What is heritable, 39

and therefore malleable by natural selection, is the ability to invent effective 40

solutions. But what contributes to fitness is not the ability to learn per se but rather 41

these innovative solutions: the learned skills. Rare, serendipitous inventions may 42

make major contributions to fitness, yet they are not heritable because their 43

acquisition depends on many additional factors, such as the constellation of 44

environmental conditions and sheer serendipity. Thus, selection to favour increased 45

cognitive abilities beyond mere conditioning, towards innovative solutions to 46

problems, i.e. true intelligence, must face a high threshold. 47

Nonetheless, many species are intelligent. Here we argue this is largely 48

because socially mediated learning (henceforth: social learning, for short) by 49

offspring or other relatives makes inventions heritable, thus lowering the threshold 50

for selection on intelligence. Opportunities for social learning allow an individual to 51

acquire many learned skills during development that it could not acquire on its own. 52

If the social system is such that such opportunities are frequent over many 53

generations, selection may favour increased individual learning ability, i.e. 54

intelligence, but it should certainly favour improved social-learning ability, which, as 55

an inevitable by-product will improve intelligence. 56

The ‘Vygotskian intelligence hypothesis’ [3] considers cultural effects on 57

cognitive development, and assumes them to be unique to humans [4, 5]. However, 58

several scholars have highlighted the presence of similar developmental effects in 59

apes [e.g. 6, 7, 8]. Allan Wilson [9] went further and suggested that these cultural 60

effects could also have affected the evolution of intelligence in our lineage and 61

others [see also 10, 11], an idea called the cultural intelligence hypothesis by Whiten 62

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and van Schaik [12]. This hypothesis builds on a long tradition suggesting that social 63

learning, and thus culture, may affect evolution [e.g., 13], and can also be linked to 64

Reader & Laland’s [14] hypothesis that general behavioural flexibility, which includes 65

social learning, may have favoured the evolution of intelligence. Here we examine 66

both the developmental and evolutionary aspects of the cultural intelligence 67

hypothesis. 68

This hypothesis was motivated by observations on great ape cultures. 69

Maturing chimpanzees and orang-utans would not have acquired these cultural 70

variants, which are complex learned skills, on their own if it were not for social 71

learning [15-18]. This is evident for tool-assisted nut cracking in chimpanzees [19] or 72

seed extraction from Neesia fruits in orang-utans, that improve fitness by bringing 73

unusual energetic benefits, but which are rarely invented, and hence patchily 74

distributed [20]. However, numerous less spectacular examples [21, 22] may also 75

contribute to fitness and may also be difficult to invent, as suggested by their patchy 76

geographic distribution [23]. Their acquisition should therefore also be dependent 77

on social learning. Comparisons across populations indicated that the set of learned 78

(cultural) skills, in particular difficult tool-using skills, is larger where opportunities 79

for social learning are more abundant [11, 24]. But the importance of social learning 80

may extend beyond the acquisition of cultural skills and also include non-culturally-81

varying (i.e. universal), learned skills [18, 25]. Indeed, there is little exploration and 82

learning by maturing apes in nature that is not socially guided, suggesting they prefer 83

social learning when possible [18]. All this suggests that they acquire their repertoire 84

of learned skills less through individual exploration and invention (arrow labelled 1 in 85

Figure 1) than through social learning (arrow 2) [see also 26]. Similar processes may 86

occur in capuchin monkeys [27, 28], and possibly to some extent in other non-87

primate lineages [cf. 29]. After having reviewed this developmental evidence in more 88

detail, we will examine the evolutionary consequences of this reliance on social 89

inputs for skill acquisition. 90

91

2. THE CULTURAL INTELLIGENCE HYPOTHESIS 92

Social learning can be defined as learning influenced by observation of, or 93

interaction with, another animal [30]. It thus encompasses two rather different 94

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processes. Learning through social interaction, including social play and agonistic 95

interactions, generally involves the acquisition of social skills. Learning via social 96

information is essential for the acquisition of non-social skills, although it may also 97

be used in the acquisition of social skills [e.g. through eavesdropping: 31]. This 98

second kind of social learning can take different forms of varying complexity, ranging 99

from mechanisms as simple as local or stimulus enhancement to complex forms of 100

imitation [e.g. summarized in 32]. It must be pointed out, however, that most social 101

learning in animals is not direct copying. Indeed, along with a variable involvement 102

of dedicated cognitive mechanisms [33-35], social learning almost invariably includes 103

an important element of individual evaluation [36], and may indeed largely rely on 104

existing asocial learning mechanisms [37]. 105

Social learning is not necessarily adaptive [38]. However, whereas horizontal 106

social learning (i.e. from peers) to acquire perishable information about the state of 107

the biotic or social environment can sometimes be maladaptive, vertical and oblique 108

social learning (i.e. from parents or others in that generation) of cognitively 109

demanding skills by naïve immatures is most likely to be adaptive [cf. 39]. 110

Throughout, we will focus on these adaptive forms. 111

The cultural intelligence hypothesis assumes that social learning is more 112

efficient than individual, or asocial, exploration and learning, and that individuals in 113

practice tend to rely on social learning to acquire these skills, i.e. prefer it to asocial 114

learning. We expect higher efficiency for social learning because asocial learners face 115

the fundamental problem of identifying which environmental stimuli they should 116

attend to, forcing them to explore in a less directed fashion. Thus, the signal-to-noise 117

(relevant versus irrelevant) ratio of stimuli encountered by immatures is higher for 118

those relying on social learning, making it more likely that they acquire a skill 119

through either socially directed trial-and-error learning (enhancement effects) or 120

observational forms of social learning (i.e. copying of actions, goals or results). 121

Asocial learners, on the other hand, have a far lower signal-to-noise ratio since social 122

inputs do not help them to filter out irrelevant stimuli [cf. 40]. Thus, at constant 123

cognitive abilities, they will on average be less likely or take longer to find a solution 124

to a problem than social learners. 125

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A test of the assumption that social learning is more efficient requires that 126

social learning be operationalised. A commonly used definition is that subjects 127

acquire particular behaviours or skills faster when exposed to skilled role models 128

than they do in a control situation, in which they can independently explore and 129

eventually learn the skill individually. This assumption has been validated in many 130

taxa, and especially in primates [34], although success rates vary across lineages 131

[41], as do known mechanisms [35]. It is also supported by experiments in humans 132

[39]. Thus, social learning acts to speed up the acquisition of behaviour patterns that 133

are universal in the species concerned and thus probably have an innate component 134

[42-44], such as nest building in great apes. It also improves their adult deployment, 135

as shown for nest building in chimpanzees [45, 46]. However, social learning also 136

allows acquisition of novel behaviours (innovations) that the animals would not learn 137

at all otherwise: In many experiments, the control animals fail to find the solution 138

[e.g. 47, 48], a finding supported by the patchy geographic incidence of learned skills 139

in wild populations [21, 22]. 140

A second critical assumption is that animals able to learn socially do so 141

preferentially rather than rely on individual exploration to acquire skills [as humans 142

should do: 39]. Field observations show that infants in several primate species show 143

relatively little independent exploration, but strongly increase selective exploration 144

of potential food items after mothers fed on them [25], to the point that among 145

orang-utans their diets have become identical with those of their mothers by 146

weaning [18], which cannot be attributed to genetic predispositions, because 147

mothers from the same population differ with regard to their feeding repertoires 148

from each other. Vertical inheritance of foraging specializations in dolphins suggests 149

the same process [49]. Experiments similarly show that infants of some species avoid 150

novel foods until their mothers or others have tried them [e.g. Daubentonia: 44]. 151

Rats likewise avoid foods not eaten by others, focusing instead on those eaten by 152

others [50]. 153

Interspecific cross-fostering experiments are the most powerful tool to 154

demonstrate a preference for social learning, if they produce a bias toward the 155

behaviour of the adopting species. Although most examples in rodents and birds 156

refer to sexual imprinting [51], a few experiments have examined the effects of more 157

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long-term exposure to heterospecific parents. They found powerful effects on diet, 158

foraging, movement and even styles of social behaviour, in birds [52-54] and 159

mammals [55, 56], suggesting that social learning (through social information and 160

social interaction) prevails over asocial learning in these domains. Enculturation 161

studies, reviewed below, show equally powerful effects. Overall, these findings 162

support the assumption that especially the young and naïve of various species 163

actually show a preference for social learning over individual exploration, although 164

the exceptions [e.g. 57] might provide a useful testing ground for the cultural 165

intelligence hypothesis. 166

167

3. TESTING THE DEVELOPMENTAL PREDICTION 168

The main prediction of the developmental version of the cultural intelligence 169

hypothesis is that the number of learned skills acquired by a maturing individual 170

depends on its opportunities for social learning during this period. While we already 171

noted that observational data from wild apes support this prediction, we now 172

discuss experiments that artificially reduce access to role models for social learning 173

(deprivation) or provide better role models with larger skill repertoires 174

(enculturation). 175

176

(a) Deprivation effects 177

For several decades following World War II, many deprivation experiments 178

were conducted in which infant monkeys or apes were reared without access to 179

their mothers or other adult conspecifics. Monkeys and apes reared in partial social 180

deprivation (i.e. with peers only) tend to have near-normal sexual and social 181

competence, which can largely be learned through social interaction, but clearly 182

reduced maternal competence [58-61]. For physical skills, learned through social 183

information, the effects are stronger. Infant chimpanzees reared without adult role 184

models show much reduced competence in many physical skills, such as nest 185

building [45, 46] and tool use [62], or fail to develop them altogether, despite 186

showing otherwise normal behaviour. Thus, primates, especially apes, deprived of 187

adult role models acquire a smaller set of learned skills (see ESM for more details). 188

189

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(b) Enculturation studies 190

Enculturation is interspecific cross-fostering, in which an animal is reared by 191

humans and treated more or less like a human child, thus exposed to human 192

artefacts and rules through joint attention and active teaching. Enculturation thus 193

provides increased opportunities for socially guided learning, including in domains 194

not present in normal conspecific individuals (e.g. complex artefacts, language). 195

Usually, the cross-fostered individuals were apes, but where monkeys were studied 196

the results were in the same direction [e.g. 63]. Enculturation brings about more 197

rapid behavioural and motor development [8] and an increased number of learned 198

skills [reviewed in e.g. 64, 65, 66], including more interest in objects and more 199

sophisticated object manipulation [66, 67] and more skilful tool use [63, 68]. Perhaps 200

most strikingly, some great apes developed unusually elaborate comprehension and 201

some use of human language systems despite the complete absence of such 202

symbolic signalling in the wild [6]. Further details are provided in the ESM. Thus, 203

enculturation studies not only show the strong preference for socially guided 204

learning and interest in role models’ actions of infant primates, but also the 205

remarkable potential for apes to acquire learned skills well outside the range of 206

acquisition during normal development if appropriate role models are available. 207

208

(c) A stronger version of cultural intelligence 209

A stronger version of the cultural intelligence hypothesis is that social 210

learning not merely increases the set of learned skills, as examined so far, but also 211

affects the asocial learning ability (intelligence) itself. Where an individual has a 212

greater set of learned skills, it may become a better asocial learner through the 213

experience it has gathered in learning the other skills, either because affordance 214

learning has increased its scope of possible innovations or because learning has 215

produced transfer of experience and abilities to new situations. This experience 216

effect is ubiquitous in humans [69] and has long been known for captive primates 217

[70], but also explains why wild primates generally show poor performance on 218

cognitive tasks requiring familiarity with human artefacts or tasks [71-73]. Thus, 219

where the population has a large pool of skills and social learning is possible, this 220

should allow the individual not only to increase its set of learned skills but also, 221

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through experience, to improve its asocial learning ability (arrow labelled 3 in Figure 222

1). 223

The critical prediction of this stronger version is that the frequency of 224

opportunities for social learning during development affects asocial learning ability, 225

i.e. intelligence. Indeed, social deprivation reduces learning ability in rodents [74] 226

and probably primates [75, 76]. On the other hand, enculturation effects improve it 227

[67, 77, 78]. For instance, only enculturated individuals master delayed imitation. 228

However, because the exact nature of enculturation effects remains unclear (see 229

detailed discussion in ESM) and systematic cognitive tests of primates deprived only 230

of adult role models have not yet been conducted, this conclusion is preliminary. If 231

further, systematic tests support this prediction, the evolutionary effects envisaged 232

by the cultural intelligence hypotheses, reviewed below, are even stronger. 233

234

4. THE EVOLUTIONARY VERSION OF THE CULTURAL INTELLIGENCE HYPOTHESIS 235

The observations and experiments reviewed above show that individuals with 236

more opportunities for social learning systematically acquire a larger set of learned 237

skills and also become better asocial learners. This effect of social learning may have 238

two opposing evolutionary consequences. If individuals in lineages with 239

systematically increased opportunities for social learning can more efficiently 240

acquire the minimum number of skills to survive and reproduce, but derive no 241

fitness benefit from enlarging the set of learned skills, then selection would favour 242

smaller brains in these lineages than in less sociable ones. However, given that 243

relative brain size has consistently increased over evolutionary time [79], the 244

opposite outcome is more likely. Thus, if the number and complexity of skills 245

acquired through social learning positively impact survival and/or reproduction, 246

lineages with more opportunities for social learning can more readily respond to 247

selection for an increased set of learned skills than lineages with limited contact 248

between the generations or tolerant independent animals. 249

The increased set of learned skills is actually achieved through selection on 250

improved social-learning ability. However, this can lead to improved asocial-learning 251

ability, i.e. intelligence, in two distinct ways (Figure 2). First, better social learning 252

performance automatically improves asocial learning processes [26], due to the high 253

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overlap of the cognitive processes involved in social and asocial learning [37]. For 254

instance, at the simplest level, selection on enhancement learning favours the causal 255

understanding of agent-object relations. All forms of observational social learning 256

benefit from increased inhibitory control, attention and memory – components of 257

executive functions that enhance individual learning [2]. Emulation critically requires 258

goal understanding; production imitation requires inhibitory control and working 259

memory. In the extreme case, social learning abilities may merely function as input 260

channels for the asocial learning mechanisms [37]. Thus, selection for more effective 261

social learning indirectly or directly improves asocial learning abilities. A second way 262

in which improved social-learning ability can improve asocial-learning ability is direct. 263

It arises whenever the experience effect operates and the increased set of learned 264

skills leads to a direct improvement of the asocial-learning ability. 265

In lineages with opportunities for social learning, a positive co-evolutionary 266

process between social-learning ability and brain size may ensue, until increases in 267

brain size no longer provide sufficient additional payoff in survival or reproduction in 268

the current environment. Different lineages are expected to go different distances in 269

this eco-evolutionary process, with the position of the equilibrium depending on 270

where the fitness costs of continued investment in neural structures begin to 271

balance the benefits. 272

The cultural intelligence hypothesis therefore makes two evolutionary 273

predictions, which can be tested comparatively. The first prediction is that social-274

learning abilities and asocial-learning abilities show correlated evolution. The second 275

is that intelligence and frequency of opportunities for social learning show correlated 276

evolution. 277

278

(a) Co-evolution of social and asocial learning 279

The prediction of a positive interspecific relationship between the abilities for 280

social and asocial learning is a strong one because under other hypotheses for the 281

evolution of intelligence (see discussion), greater individual intelligence is not 282

necessarily accompanied by greater ability for social learning. 283

Reader and Laland [14] and Reader et al. [80] provided comparative support 284

for this prediction by showing that among primates, reports of social learning, 285

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regardless of mechanism, show a significant positive correlation with reports of 286

innovation, and both show significant positive correlations with the executive brain 287

ratio, i.e. (neocortex + striatum / brainstem). Similarly, Lefebvre [81] reviewed 288

evidence for a positive interspecific correlation between performance in social 289

learning and individual learning experiments among birds. 290

A more detailed test compares the asocial learning ability with the cognitive 291

complexity of social learning across a set of taxa. We compared four primate grades: 292

prosimians (lemurs, galagos and lorises, and in principle tarsiers), monkeys (i.e. both 293

Old and New World monkeys, great apes (i.e. leaving out the gibbons and humans), 294

and humans. While these grades do not correspond to actual clades, they are fairly 295

homogeneous with respect to life style and relative brain size [e.g. 82]. The summary 296

of table 1 shows that the performance in both social and asocial learning increases 297

systematically from prosimians, to monkeys, to great apes and finally humans. It is 298

generally assumed that observational forms of social learning, including all forms of 299

emulation and imitation, involve more complex cognitive mechanisms than the non-300

observational forms, such as facilitation and enhancement. There is no evidence for 301

observational learning in prosimians [34]. Almost all the observational forms of social 302

learning documented so far among monkeys refer to contextual imitation [33] or 303

imitation of species-typical actions [11], whereas among great apes we see evidence 304

for copying of novel actions, complex action sequences (also: production imitation), 305

or deferred imitation (see also ESM). Subiaul [35] argues that this distinction is 306

supported by neurobiological differences between these latter two lineages, with 307

production imitation requiring neural adaptations that mediate the planning and 308

coordination of gross and fine motor patterns. In support, human children can copy 309

known motor acts before they can copy novel actions or action sequences [83]. 310

311

(b) Opportunities for social learning and brain size 312

The second prediction is that selection would be most likely to favour the 313

evolution of improved domain-general cognitive abilities where opportunities for 314

social learning are present, and should do so more when such opportunities are 315

systematically more abundant. This is a ceteris paribus prediction. Thus, not all 316

lineages satisfying the condition need to have evolved greater intelligence, but 317

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conversely all highly intelligent species should have excellent opportunities for social 318

learning. In short, prediction two is that the most intelligent species should all be 319

highly cultural species. 320

A proper test of the second prediction requires knowledge of the distribution 321

and extent of culture among taxa in the wild. This information is woefully 322

incomplete, forcing us to use indirect estimates of the amount of social learning in 323

the wild as a first approach to testing this prediction. Opportunities for social 324

learning correlate with a number of non-exclusive variables that can therefore be 325

used as proxies for it: presence of stable social units containing overlapping 326

generations, a long period of close association with one or more parents, the 327

presence of cooperative breeding, and extent of social tolerance in social units [24, 328

84]. Because the effect of social tolerance outweighs that of group size, in both 329

theoretical [26] and empirical studies [14], group size is not a relevant variable, 330

although group living per se probably is. 331

Intelligence must likewise be assayed indirectly, using neuro-anatomical 332

measures, although theoretically there is no obvious best measure [85]. Results 333

obtained with different measures are often the same [e.g. 86] or similar [e.g. 14], but 334

not always [87]. 335

As yet, no systematic analyses have been done for mammals, but among 336

birds, several patterns are consistent with the cultural intelligence hypothesis. First, 337

young of altricial species generally have far longer and more intensive contact with 338

parents than precocial ones, and thus more opportunities for social learning. 339

Accordingly, altricial birds have far larger average relative brain size than precocial 340

ones [88]. Second, among altricial birds, the duration of post-fledging parental care, 341

a period during which various skills improve [89], is positively correlated with relative 342

brain size [90], as predicted. Third, among bowerbirds, learning of bower building 343

has been argued to be socially mediated [91], and the species that build bowers are 344

larger-brained than either non-bower-building relatives or ecologically similar but 345

unrelated species [92]. Finally, among precocial birds, post-hatching care consists 346

largely of protecting and less of provisioning, allowing a test of the effect of 347

opportunities for social learning without being confounded by that of direct energy 348

inputs to the young. This care is highly variable, but largely homogeneous within 349

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families (because most variation is at the higher taxonomic levels, we therefore 350

consider patterns at the level of family]. As predicted, the number of caretakers in a 351

family strongly predicts relative brain size (K. Isler & CvS, unpublished). 352

353

5. DISCUSSION 354

(a) The evolution of intelligence 355

The cultural intelligence hypothesis makes plausible assumptions that were 356

empirically supported: (i) social learning is more efficient than individual learning, 357

and (ii) animals appear to rely on it preferentially. The developmental effects on skill 358

repertoires it predicts were found as well, whereas we also found preliminary 359

support for the predicted evolutionary effects: interspecific correlation between 360

individual and social learning abilities and a relationship between opportunities for 361

social learning and cognitive abilities across taxa. Future tests should focus on 362

aspects not yet sufficiently evaluated. For instance, species with high social 363

tolerance, as well as species with demonstrated traditions in natural conditions, 364

should have larger relative brain size than sister taxa lacking these features. If future 365

tests remain favourable, then cultural intelligence should be part of the explanation 366

for variation in intelligence and brain size across species. 367

Unlike the cultural intelligence hypothesis, currently popular hypotheses for 368

the evolution of intelligence emphasize specific benefits. For the lineage that gave 369

rise to humans, the primates, the most popular idea is that the challenges and 370

opportunities of living in individualized, stable social groups have provided the 371

strongest selective pressure toward increased cognitive abilities (social brain 372

hypothesis), but ecological pressures, such as foraging demands, have probably 373

contributed as well [93]. More specific benefits may have applied in particular 374

lineages [e.g. acoustic foraging in aye-ayes: 94]. All of these hypotheses enjoy some 375

support from comparative tests using brain size as a proxy for cognitive performance 376

[e.g. 95], although all hypotheses positing domain-specific benefits must explain how 377

more generalized cognitive abilities, i.e. intelligence, subsequently arose from these 378

specific cognitive adaptations. An alternative approach assumes domain-general 379

benefits in the form of general problem-solving abilities, bringing fitness-enhancing 380

behavioural flexibility [14, 80]. This idea is supported by the high correlations among 381

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performance measures on various and sundry cognitive tasks, suggesting the 382

existence of general intelligence in animals, at least primates [96, 97]. There is also a 383

good relationship between this general intelligence and aspects of brain size [80, 87]. 384

Such benefits alone may not be sufficient to explain patterns in the evolution 385

of brain size and intelligence. Brain tissue is metabolically more costly than many 386

other tissues in the body, and consequently larger brains lead to developmental 387

delays in precocial species [98] or require species to have higher metabolic turnover 388

[99]. Therefore, benefits due to increased brain size must be greater than those due 389

to equal changes in the size of most other tissues. Indeed, variation in the strength 390

of these costs or ability to bear them explains much interspecific variation in brain 391

size [98, 100]. By arguing that social learning leads to a more efficient use of brain 392

tissue than individual exploration, the cultural intelligence hypothesis explicitly 393

acknowledges these costs. 394

The efficiency argument holds regardless of the exact nature of the benefits 395

or whether the benefits are domain-general or domain-specific, provided learning of 396

skills is involved. Thus, the cultural intelligence hypothesis complements the benefit 397

hypotheses mentioned above by specifying the conditions in which these benefits 398

are likely to be cost-effective enough to be favoured by natural selection. The 399

cultural intelligence hypothesis is therefore not meant to replace the benefit 400

hypotheses because intelligence will not be favoured by natural selection merely 401

because the costs are low, but only if it also provides clear improvements in survival 402

or reproductive success. Rather, the cultural intelligence hypothesis specifies the 403

conditions in which these potential benefits can be realized, namely whenever the 404

social conditions allow sufficient social learning. 405

The complementarity with the benefits hypotheses makes it difficult to 406

independently test the cultural intelligence hypothesis, at least until information on 407

the taxonomic incidence of the expression of culture and oblique and vertical social 408

learning is available. However, the cultural intelligence hypothesis correctly predicts 409

the interspecific correlation between asocial and social learning, which is not 410

predicted by the benefit hypotheses. It can also account for correlated evolution 411

between opportunities for social learning and relative brain size, independent of 412

living in stable groups. 413

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414

(b) Cultural intelligence and human evolution 415

Species vary dramatically in cognitive abilities. Much of this variation should 416

be linked to the extent to which social learning is possible and improves survival 417

and/or reproductive success. The equilibrium reached in a particular taxon will 418

depend on (i) its social system and life history, i.e. its aggregate measure of 419

opportunities for social learning, and (ii) on the degree to which the possession of 420

any skills or knowledge will improve survival or reproductive success. The latter need 421

not be true for organisms in habitats with high unavoidable mortality. Some species 422

will therefore end up relying more on social learning and on more sophisticated 423

forms of it than others, even if opportunities for social learning are similar. Evidently, 424

taxa with highly tolerant social systems, slow development and low rates of 425

unavoidable mortality are expected to have evolved the most extensive forms of 426

social learning. Great apes, capuchin monkeys, dolphins and toothed whales, 427

elephants, corvids and parrots, all lineages with known social-learning abilities [101, 428

102], fit these conditions. 429

The evolution of uniquely human cognitive abilities is entirely consistent with 430

the cultural intelligence hypothesis. Although the term cultural intelligence had been 431

proposed earlier [11] to apply to animals generally, Herrmann et al. [5] soon 432

thereafter used the term cultural intelligence to specifically refer to humans (i.e. the 433

Vygotskian intelligence hypothesis [3]). Their comparison of adult chimpanzees and 434

orang-utans with human toddlers showed that human infants outperformed apes in 435

the social, but not the physical domains of cognition, suggesting that socio-cognitive 436

abilities (including social learning) and physical cognition have become dissociated in 437

humans. This may seem inconsistent with the broader cultural intelligence 438

hypothesis, but note that human adults clearly outperform all great apes in both 439

social and physical cognition, indicating the social cognitive abilities simply mature 440

earlier than the physical cognitive abilities. Herrmann et al. [5] version of the cultural 441

intelligence hypothesis thus is that humans show specific adaptations fostering social 442

learning that become apparent early in ontogeny and enable a further, socially 443

constructed amplification of cognitive skills. This position is paralleled by the concept 444

of pedagogy proposed as a specifically human adaptation by Gergely et al. [103], 445

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which encompasses specialised communicative acts on the part of the role model 446

and specific sensitivity to these acts on the part of the infant. These human-specific 447

adaptations are entirely consistent with the broad cultural intelligence hypothesis 448

developed here [cf. 104], and probably arose after humans adopted cooperative 449

breeding [105, 106]. 450

451

Acknowledgements 452

We thank Stephan Lehner for help in literature searches, and Christine 453

Hrubesch, Adrian Jaeggi, Claudia Rudolf von Rohr, Andrea Strasser, Maria van 454

Noordwijk and Andrew Whiten for discussion, and several reviewers, as well as Kevin 455

Laland and Andy Whiten for comments on the manuscript. Supported by SNF 456

3100A0-111915 and SNF 105312-114107. 457

458

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Figure Captions 723

Figure 1

The sources of an individual’s set of learned skills as acquired during development:

(1) the skills learned through social learning from the population’s pool of learned

skills, and (2) the skills acquired through innovation from its own asocial (individual)

learning ability. The dashed arrow 3 reflects the effect of experience on asocial

learning ability.

Figure 2

The evolution of intelligence through cultural feedback. Selection on an increased set

of learned skills is achieved by improved social learning. Due to the high cognitive

overlap, social learning improves the asocial (individual) learning ability (i.e.

intelligence; shown by arrow 1). More learned skills also improve the latter through

stronger experience effects (arrow 2).

724

725

726

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university of zurich zurich open ......for review only 2 31 32 key words: social learning,...

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