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Abstract

Variation in neocortex size is one of the defining features of mammalian brain evolution. The paramount assumption has been that neocortex size indicates a monotonic allometric relationship with brain size. This assumption holds the concomitant neurodevelopmental assumption that the ontogenetic trajectory of neocortex size is so stable across species that it restrains changes in the direction of evolution. Here we test this fundamental assumption. Whereas previous research has focused exclusively on changes in mean size among groups (i.e., intercept), we additionally investigate changes in covariation (i.e., slope) and strength of allometric integration (i.e., residual variation). We further increase data resolution by investigating 350 species representing 11 mammalian orders. Results identify nine shifts in covariation between neocortex and brainstem in different mammalian groups, indicate that these shifts occur independently of shifts in size, and demonstrate that the strength of allometric integration across different neocortical regions in primates is inversely related to the neurodevelopmental gradient such that later developing regions underwent more evolutionary change. Although our results confirm that variation in brain organization is structured along a neurodevelopmental gradient, our results suggest two additional principles of size reorganization in brain evolution: (1) repatterning of growth allocation among brain regions may occur independently of size and (2) later developing regions indicate faster evolution, not necessarily directional evolution toward larger size. We conclude that the evolution of neocortex size in mammals is far more variable than previously assumed, in turn suggesting a higher degree of evolutionary flexibility in neurodevelopmental patterning than commonly suggested.