Beyond the mosaic model of brain evolution: Rearing environment defines local and global plasticity

Abstract

Comparative animal studies have identified a trend toward a more global structural organization as brains become larger, suggesting that brain regions grow in sync as predicted by the concerted model of brain evolution. At the same time, brain plasticity studies have identified a boost in local brain structure triggered by the environment, suggesting that brain regions grow independently, as predicted by the mosaic model. Nevertheless, it is unclear whether the environment can also trigger shifts toward a more global brain structure, that is, whether phenotypic plasticity proceeds in a concerted fashion. Here, we examined the impact of radically different rearing environments on brain organization in a teleost fish, the three-spined stickleback (Gasterosteus aculeatus). We computed novel indices of local and global brain structure across groups reared in the two environments and entered them as predictors of differences in brain and body sizes. Changes in local brain structure predicted differences in both body and brain sizes, whereas changes in global brain structure only predicted differences in brain size. Our findings highlight the emergence of brain plasticity in a population as local and global changes that are both compatible with the concerted model.