Review
Explaining brain size variation: from social to cultural brain

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Although the social brain hypothesis has found near-universal acceptance as the best explanation for the evolution of extensive variation in brain size among mammals, it faces two problems. First, it cannot account for grade shifts, where species or complete lineages have a very different brain size than expected based on their social organization. Second, it cannot account for the observation that species with high socio-cognitive abilities also excel in general cognition. These problems may be related. For birds and mammals, we propose to integrate the social brain hypothesis into a broader framework we call cultural intelligence, which stresses the importance of the high costs of brain tissue, general behavioral flexibility and the role of social learning in acquiring cognitive skills.

Section snippets

The social brain

It has long been known that various mammalian and bird lineages differ in brain size, relative to body size 1, 2. The most widely accepted explanation is known as the Machiavellian intelligence [3] or social brain hypothesis [4]. Developed to explain variation order in relative brain size among mammalian orders and within primates, the hypothesis argues that large brains are adaptations for dealing with the complexities of social life. Several studies have documented the remarkably

Grade shifts and the social brain

For some species or lineages, the social brain hypothesis does a poor job of predicting their brain size. On the one hand, orangutans (Pongo spp.) or aye-ayes (Daubentonia madagascariensis) live in socially simple societies but nonetheless have larger brains than related primates living in far more complex societies [19]. On the other hand, some relatively small-brained taxonomic groups have better socio-cognitive abilities than expected on the basis of their brain size, a phenomenon known as

Domain-specific or domain-general cognitive abilities?

The second problem with the social brain hypothesis is the growing evidence for a non-modular, general intelligence: an overarching ability to respond flexibly to new or complex situations, to learn and to innovate. Studies reviewed in Box 2 support the idea that general intelligence is not a uniquely derived human trait but instead a phylogenetically old phenomenon, found among primates, rodents and birds.

Parallel emergence of abilities in multiple domains is not explained by the social brain

A cultural rather than just social brain

The existence of domain-general cognitive abilities in larger-brained birds and primates is incompatible with the social brain hypothesis. However, it is entirely consistent with Reader and Laland's [32] proposal that general behavioral flexibility, not tied to any domain in particular (i.e. content-neutral), is the adaptation underlying cognitive performance in primates. For some reason, however, this idea did not become as popular as the social brain hypothesis, despite its strong explanatory

Concluding remarks

In conclusion, we noted two weaknesses in the social brain hypothesis: it cannot account for the presence of domain-general cognitive abilities in birds and mammals, and it leaves grade shifts in brain size unexplained.

Unexplained grade shifts can have thee causes. First, some filter (e.g., due to small body size or high unavoidable mortality) may prevent the evolution of a larger brain, even though selection would in principle favor improved socio-cognitive abilities. Second, the taxon's high

Acknowledgments

The research reported here was supported by the Swiss National Fund (SNF-grant nos 105312-114107, 31003A-111915, 31003A-117789 and 310030-13083). We thank Sonja Koski, Caroline Schuppli, Michèle Schubiger and three anonymous reviewers for valuable comments.

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