Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution

Abstract

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.

Figure 1.

Phylogenetic mapping of the three principal components that distinguish great apes from other anthropoids ((a) PC2 prefrontal white matter, (b) PC4 prefronto-striatal, and (c) PC7 cortico-cerebellar) in relation to absolute brain size. Darker shades (red in colour version) indicate a joint increase in respective PCs and absolute brain size, medium shades (yellow in colour version) an increase in PCs but not in absolute brain size and no shading no increase in either respective PCs or absolute brain size. More detailed figures, including full colour resolution, representing the phylogenetic mapping of each principal component are available in electronic supplementary material, S2. More information on the procedure used to visualize the inferred evolutionary patterns on the phylogeny is provided in electronic supplementary material, S3. (Online version in colour.)

Figure 2.

Phylogenetic mapping of the principal component that indicates high loadings of the relative size of the hippocampal–entorhinal formation in relation to brain size. Darker shades (red in colour version) indicate the magnitude of the variation in the relative size of the hippocampal–entorhinal formation in lineages that experienced brain size decrease. White indicates lineages where the relative size of the hippocampal–entorhinal formation undergoes little change. More detailed figures, figures representing analogous visualizations for other principal components, and full colour resolution for all figures are available in electronic supplementary material, S2. More information on the procedure used to visualize the inferred evolutionary patterns on the phylogeny is provided in electronic supplementary material, S3. (Online version in colour.)