A brain-wide analysis maps structural evolution to distinct anatomical modules

Abstract

AbstractBrain anatomy is highly variable and it is widely accepted that anatomical variation impacts brain function and ultimately behavior. The structural complexity of the brain, including differences in volume and shape, presents an enormous barrier to define how variability underlies differences in function. In this study, we sought to investigate the evolution of brain anatomy in relation to brain region volume and shape across the brain of a single species with variable genetic and anatomical morphs. We generated a high-resolution brain atlas for the blind Mexican cavefish and coupled the atlas with automated computational tools to directly assess brain region shape and volume variability across all populations. We measured the volume and shape of every neuroanatomical region of the brain and assess correlations between anatomical regions in surface, cavefish and surface to cave F2 hybrids, whose phenotypes span the range of surface to cave. We find that dorsal regions of the brain are contracted in cavefish, while ventral regions have expanded. Interestingly, in hybrid fish the volume and shape of dorsal regions are inversely proportional to ventral regions. This trend is true for both volume and shape, suggesting that these two parameters share developmental mechanisms necessary for remodeling the entire brain. Given the high conservation of brain anatomy and function among vertebrate species, we expect these data to studies reveal generalized principles of brain evolution and show that Astyanax provides a system for functionally determining basic principles of brain evolution by utilizing the independent genetic diversity of different morphs, to test how genes influence early patterning events to drive brain-wide anatomical evolution.