Embracing covariation in brain evolution: large brains, extended development, and flexible primate social systems

Abstract

Brain size, body size, developmental length, life span, costs of raising offspring, behavioral complexity, and social structures are correlated in mammals due to intrinsic life-history requirements. Dissecting variation and direction of causation in this web of relationships often draw attention away from the factors that correlate with basic life parameters. We consider the "social brain hypothesis," which postulates that overall brain and the isocortex are selectively enlarged to confer social abilities in primates, as an example of this enterprise and pitfalls. We consider patterns of brain scaling, modularity, flexibility of brain organization, the "leverage," and direction of selection on proposed dimensions. We conclude that the evidence supporting selective changes in isocortex or brain size for the isolated ability to manage social relationships is poor. Strong covariation in size and developmental duration coupled with flexible brains allow organisms to adapt in variable social and ecological environments across the life span and in evolution.

Fig. 1

Body weight (a), brain volume (b), isocortex volume (c), and the size of the isocortex relative to the rest of the brain (d) are regressed against group size in primates. Open diamonds are averages of species. Data are from Dunbar (1992); isocortex volume is gray matter with a white matter component as detailed in Stephan et al. (1981).

Fig. 2

Brain volume as a function of body weight (a) and isocortex volume as a function of the rest of the brain (b) in primates and other mammals. These data show that the overall brain and isocortex size is disproportionately expanded in primates relative to many other mammals, but that the size of the brain and isocortex strongly covaries within taxonomic groups. Data are from Stephan et al. (1981).

Fig. 3

Isocortical regions are plotted against the overall isocortex volume (a) or the rest of the isocortex volume (b–d) in several mammalian species. The frontal gray matter and the primary visual cortex (V1) expand faster than the size of the primary auditory cortex (A1) as overall brain size increases. These observations suggest that various isocortical regions expand with a distinct allometry. Data are from [Kaskan et al., 2005] and [Smaers et al., 2010].

Fig. 4

Isocortex volume (a) and isocortex volume relative to the rest of the brain (b) are plotted against the rest of the brain (i.e., brain–isocortex) in haplorhine and strepsirhine primates. As brains expand, the isocortex becomes disproportionately enlarged in strepsirhine and haplorhine primates. This is evident from the observation that the relative size of the isocortex increases as the rest of the brain expands. Data are from Stephan et al. (1981).

Fig. 5

Residuals derived from a linear regression through the brain size and body size are correlated against group size in primates. In one scenario, residuals are derived from a linear regression through the brain and body size of both haplorhine and strepsirhine primates (red line). In another scenario, residuals are derived from two separate linear regressions derived for haplorhine and strepsirhine primates (blue line). The correlation coefficient between group size and brain versus body size residual values derived from both haplorhine and strepsirhine primates is higher than the correlation coefficient between group size and brain versus body size residuals obtained for strepsirhine and haplorhine primates. Data are from Pérez-Barbería et al. (2007). Although the authors examined the geometric means rather than the arithmetic means of primate group size, the low correlation coefficients between group size and brain versus body size residuals in primates do not support the claim that group size correlates with brain size in primates.

Fig. 6

The range of reported group size within primates is plotted against the relative size of the isocortex. These data show that group size varies extensively within primate species. Data on group size ranges are from [Izawa, 1976] and [Smuts et al., 1986], [Koenig, 1995] and [Higham et al., 2009].

Fig. 7

The Biaka and Aeta are taller than Turkana, Massai, Ache, and !Kung. (a) Biaka and Aeta reach adult height later than Turkana and Massai. (b) Biaka and Aeta have a reduced survival probability at birth than Biaka and Aeta do. Data are from Migliano et al. (2007).