Think big: Allometry as a driver of rates, trajectories and scaling in the evolution of primate brain shape

Abstract

Variability in brain shape is a prominent feature in primate evolution. To date, however, investigations have largely focused on variation in brain size rather than shape. This is because shape data has been difficult to access at sufficiently broad scales and computational complexity. The role of allometry, in particular, remains an open question. Here, we employ three-dimensional (3D) geometric morphometrics, phylogenetic comparative methods and new methodology to determine the factors influencing evolutionary rates, phenotypic trajectories and scaling of primate brain shape, using a large sample of 386 endocasts, representing 151 species and all 16 primate families. We found a tight relationship between brain shape and size on rates of evolution in the morphology of the primate brain. Hominoidea and Cercopithecinae showed significant evolutionary allometry after controlling for phylogeny, whereas Strepsirrhini, Colobinae and Platyrrhini did not. Hominoidea and Papionini showed markedly high rates of brain shape evolution, whereas Strepsirrhini and Platyrrhini experienced a significant slowdown. In humans, apes and lesser apes the brain evolved a globular shape with expanded frontal lobes. Our results suggest that changes in allometry favoured shape changes at large scales promoting the rapid evolution of hominoids and papionins brains. On the other hand, the smaller scale effect of size on the brain shape of strepsirrhines and platyrrhines played a key role in their low evolutionary rates. Our study demonstrates that most brain shape variability in primates was driven by evolving brains of different size. We conclude that although the order Primates is typically characterised as being large-brained, such strong allometric effects are largely confined to the cognitively most advanced papionins and hominoids.