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Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.

Comparative studies have identified a wide range of behavioural and ecological correlates of relative brain size, with results differing between taxonomic groups, and even within them. In primates for example, recent studies contradict one another over whether social or ecological factors are critical. A basic assumption of such studies is that with sufficiently large samples and appropriate analysis, robust correlations indicative of selection pressures on cognition will emerge. We carried out a comprehensive re-examination of correlates of primate brain size using two large comparative datasets and phylogenetic comparative methods. We found evidence in both datasets for associations between brain size and ecological variables (home range size, diet and activity period), but little evidence for an effect of social group size, a correlation which has previously formed the empirical basis of the Social Brain Hypothesis. However, reflecting divergent results in the literature, our results exhibited instability across datasets, even when they were matched for species composition and predictor variables. We identify several potential empirical and theoretical difficulties underlying this instability and suggest that these issues raise doubts about inferring cognitive selection pressures from behavioural correlates of brain size., (© 2017 The Author(s).)