Genetics of Cerebellar and Neocortical Expansion in Anthropoid Primates: A Comparative Approach

Abstract

What adaptive changes in brain structure and function underpin the evolution of increased cognitive performance in humans and our close relatives? Identifying the genetic basis of brain evolution has become a major tool in answering this question. Numerous cases of positive selection, altered gene expression or gene duplication have been identified that may contribute to the evolution of the neocortex, which is widely assumed to play a predominant role in cognitive evolution. However, the components of the neocortex co-evolve with other functionally interdependent regions of the brain, most notably in the cerebellum. The cerebellum is linked to a range of cognitive tasks and expanded rapidly during hominoid evolution. Here we present data that suggest that, across anthropoid primates, protein-coding genes with known roles in cerebellum development were just as likely to be targeted by selection as genes linked to cortical development. Indeed, based on currently available gene ontology data, protein-coding genes with known roles in cerebellum development are more likely to have evolved adaptively during hominoid evolution. This is consistent with phenotypic data suggesting an accelerated rate of cerebellar expansion in apes that is beyond that predicted from scaling with the neocortex in other primates. Finally, we present evidence that the strength of selection on specific genes is associated with variation in the volume of either the neocortex or the cerebellum, but not both. This result provides preliminary evidence that co-variation between these brain components during anthropoid evolution may be at least partly regulated by selection on independent loci, a conclusion that is consistent with recent intraspecific genetic analyses and a mosaic model of brain evolution that predicts adaptive evolution of brain structure.

Co‐evolution of cerebral and cerebellar expansion in cetaceans

“…Our results are therefore consistent with a “mosaic” model of brain evolution (Barton & Harvey, ), and data from molecular studies in other vertebrates that suggest selection may act on independent sets of genes and developmental pathways that control the size of each brain component (e.g. Noreikiene et al, ; Harrison & Montgomery, ; Montgomery et al, ).…”

Maternal investment, life histories, and the evolution of brain structure in primates

“…However, the brain is composed of functionally and anatomically heterogeneous structures which show heterochronicity in their development (5)(6)(7)(8). It has also been demonstrated that structures' developmental scheduling is influenced by structure-specific genes (12). It is therefore possible that different brain structures have different life history correlates.…”

Relative Cerebellum Size Is Not Sexually Dimorphic across Primates

“…This region is even larger in apes relative to monkeys [Rilling and Insel, 1998], which may reflect increased technical intelligence related to the complex tool use abilities observed in great apes [Barton and Venditti, 2014]. In fact, the cerebellum underwent rapid evolutionary expansion during ape evolution [Barton and Venditti, 2014;Smaers et al, 2018;Miller et al, 2019], and genes involved in cerebellum development are more likely to have evolved adaptively during hominoid evolution than those involved in cortical development [Harrison and Montgomery, 2017]. Thus far, sex differences in the relative cerebellum size have only been investigated in humans, with studies showing mixed results [e.g., female-biased: Hutchinson et al, 2003; male-biased: Raz et al, 1998Raz et al, , 2001; no difference: Filipek et al, 1994;Luft et al, 1998, Nopoulos et al, 2000Szabó et al, 2003;Leonard et al, 2008;Fan et al, 2010].…”