Inverse covariation between the neocortex and the limbic system is concentrated at deep evolutionary divergences

Abstract

The macroscale architecture of mammalian brains consists of a broadly conserved set of structures, but the relative sizes of these structures vary substantially across species. Much of this variation follows conserved scaling relationships, but particular systems can expand or contract relative to the rest of the brain, providing targets for adaptive selection. One prominent example is a volumetric tradeoff between the neocortex and the limbic system, in which expansion of one is associated with reduction of the other, a feature apparent when brain structure volumes are examined across living species. However, whether this relationship has operated throughout mammalian evolution or arose during particular periods of diversification is unknown. Using phylogenetic comparative methods, we here show that the tradeoff between the neocortex and the limbic system is concentrated at deep evolutionary divergences separating major mammalian groups. After accounting for shared ancestry and brain size, the tradeoff strengthens progressively among deeper branches of the mammalian phylogeny, extending broadly across limbic structures, with the strongest signal involving olfactory components. Recent divergences show no consistent relationship. Our analyses indicate that the neocortex-limbic tradeoff emerged during the early diversification of mammals, highlighting how present-day variation in brain organization retains signatures of ancient evolutionary transitions.