The evolution of the social brain: anthropoid primates contrast with other vertebrates

Abstract

The social brain hypothesis argues that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living. We test predictions arising from the hypothesis using comparative data from birds and four mammalian orders (Carnivora, Artiodactyla, Chiroptera and Primates) and show that, across all non-primate taxa, relative brain size is principally related to pairbonding, but with enduring stable relationships in primates. We argue that this reflects the cognitive demands of the behavioural coordination and synchrony that is necessary to maintain stable pairbonded relationships. However, primates differ from the other taxa in that they also exhibit a strong effect of group size on brain size. We use data from two behavioural indices of social intensity (enduring bonds between group members and time devoted to social activities) to show that primate relationships differ significantly from those of other taxa. We suggest that, among vertebrates in general, pairbonding represents a qualitative shift from loose aggregations of individuals to complex negotiated relationships, and that these bonded relationships have been generalized to all social partners in only a few taxa (such as anthropoid primates).

Figure 1

Mean relative brain size (±s.e.m.) as a function of social system in (a) carnivores and (b) ungulates. For comparison, the relationship between relative brain size and social system are presented for two additional vertebrate taxa: (c) bats and (d) birds, based on data provided by S. Shultz & R. Dunbar 2007 (unpublished data) and Pitnick et al. (2006).

Figure 2

Mean relative brain size (±s.e.m.) as a function of social system in primates.

Figure 3

Relationship between pairbond duration and type and relative brain size across bird species (mean±s.e.m.; data from Shultz & Dunbar, unpublished data).

Figure 4

Differences in percentage of genera that are bonded in individual ungulate (artiodactyl), carnivore, prosimian and anthropoid genera (for details and definitions, see §2). Bondedness in ungulates is heavily influenced by the suids (5 out of 9 suid genera are female bonded). Sample sizes are: 49 ungulate species, 54 carnivores, 23 prosimians and 38 anthropoid primates (data from Nowak 1999).

Figure 5

(a) Mean±SE total social time, and (b) corrected for number of other individuals in the group for monogamous (grey bars), harem (black bars) and multimale (white bars) ungulates and primates. Sample sizes are: 38 primate species and 6 ungulates (for sources: see §2).