Evidence for Concerted and Mosaic Brain Evolution in Dragon Lizards

The brain plays a critical role in a wide variety of functions including behaviour, perception, motor control, and homeostatic maintenance. Each function can undergo different selective pressures over the course of evolution, and as selection acts on the outputs of brain function, it necessarily alters the structure of the brain. Two models have been proposed to explain the evolutionary patterns observed in brain morphology. The concerted brain evolution model posits that the brain evolves as a single unit and the evolution of different brain regions are coordinated. The mosaic brain evolution model posits that brain regions evolve independently of each other. It is now understood that both models are responsible for driving changes in brain morphology; however, which factors favour concerted or mosaic brain evolution is unclear. Here, we examined the volumes of the 6 major neural subdivisions across 14 species of the agamid lizard genus Ctenophorus (dragons). These species have diverged multiple times in behaviour, ecology, and body morphology, affording a unique opportunity to test neuroevolutionary models across species. We assigned each species to an ecomorph based on habitat use and refuge type, then used MRI to measure total and regional brain volume. We found evidence for both mosaic and concerted brain evolution in dragons: concerted brain evolution with respect to body size, and mosaic brain evolution with respect to ecomorph. Specifically, all brain subdivisions increase in volume relative to body size, yet the tectum and rhombencephalon also show opposite patterns of evolution with respect to ecomorph. Therefore, we find that both models of evolution are occurring simultaneously in the same structures in dragons, but are only detectable when examining particular drivers of selection. We show that the answer to the question of whether concerted or mosaic brain evolution is detected in a system can depend more on the type of selection measured than on the clade of animals studied.