Why are there so many explanations for primate brain evolution?

Abstract

The question as to why primates have evolved unusually large brains has received much attention, with many alternative proposals all supported by evidence. We review the main hypotheses, the assumptions they make and the evidence for and against them. Taking as our starting point the fact that every hypothesis has sound empirical evidence to support it, we argue that the hypotheses are best interpreted in terms of a framework of evolutionary causes (selection factors), consequences (evolutionary windows of opportunity) and constraints (usually physiological limitations requiring resolution if large brains are to evolve). Explanations for brain evolution in birds and mammals generally, and primates in particular, have to be seen against the backdrop of the challenges involved with the evolution of coordinated, cohesive, bonded social groups that require novel social behaviours for their resolution, together with the specialized cognition and neural substrates that underpin this. A crucial, but frequently overlooked, issue is that fact that the evolution of large brains required energetic, physiological and time budget constraints to be overcome. In some cases, this was reflected in the evolution of 'smart foraging' and technical intelligence, but in many cases required the evolution of behavioural competences (such as coalition formation) that required novel cognitive skills. These may all have been supported by a domain-general form of cognition that can be used in many different contexts.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Keywords: coalitions; energetics; foraging innovations; multilevel sociality; social brain hypothesis; social complexity.

Figure 1.

Alternative explanations for the evolution of large brains in primates. Explanations differ in whether their central claim is (a) about ontogenetic or energetic constraints, versus ecological or social processes, (b) whether they view food, mating or predation as the rate-limiting process for fitness, and (c) whether they view the fitness benefits from large brains as being direct (individual-level benefits) or indirect (arising out of social processes). Principal references: ^a[–24], ^b[20,21], ^c[,–27], ^d[–33], ^e[25], ^f[34], ^g[17,18,35], ^h[17,36,37], ⁱ[38], ^j[39], ^k[40] and ^l[5,6,8,41,42].

Figure 2.

(a) Path model of Dunbar & Shultz [6] defining the relationships between key variables in primate social, ecological and brain evolution. Solid lines indicate statistically confirmed relationships based on the phylogenetically controlled path analysis given by Dunbar & Shultz [6]; dotted lines indicate additional relationships not included in the original path analysis but for which there is confirmatory statistical evidence. Boxes with dashed outlines indicate variables not included in the original path analysis of [6]. Shaded boxes indicate major environmental drivers. (b) Path model of Navarette et al. [52]. Lines indicate phylogenetically controlled statistically significant relationships. Technical intelligence here refers to a combination of foraging innovations and extractive foraging. In some (but not all) models, social learning correlates with social group size (dashed line). Dashed boxes enclose variables that covary together. The graph is redrawn to a similar orientation to that in (a).