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

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.

支撑人类及其近缘类群认知能力提升演化的脑结构与功能适应性改变究竟为何？阐明脑演化的遗传基础，已成为解答该问题的核心研究手段。学界已发现诸多可能推动新皮层（neocortex）演化的事件，包括正向选择、基因表达改变或基因复制，而新皮层普遍被认为在认知演化中发挥主导作用。然而，新皮层的各组成部分会与脑内其他功能互作区域协同演化，其中尤以小脑（cerebellum）最为显著。小脑与多种认知任务相关，且在人猿总科（hominoid）的演化历程中发生了快速扩张。本研究展示的数据表明，在类人猿灵长类动物中，已知参与小脑发育的编码蛋白基因，与皮层发育相关基因一样，均有可能受到选择作用的靶向修饰。事实上，基于当前可用的基因本体（Gene Ontology）数据，已知参与小脑发育的编码蛋白基因，在人猿总科演化过程中更易发生适应性演化。这与表型研究结果一致：类人猿的小脑扩张速率超出了其他灵长类基于新皮层缩放比例所预测的水平。最后，本研究提供的证据显示，特定基因所受选择的强度，与新皮层或小脑的体积变异存在关联，但并非同时与两者相关。该结果为类人猿灵长类演化过程中脑各组成部分的协同变异，至少部分由独立位点的选择所调控提供了初步依据；这一结论与近期的种内遗传分析结果，以及预测脑结构可发生适应性演化的脑演化镶嵌模型相符。