Yasmin Emery, Letizia Pessina, Redouan Bshary

The factors shaping brain evolution and cognition are broadly categorized as being either social or environmental. However, the relative importance of these factors is heavily debated, partly due to the limitations from the standard interspecific evolutionary comparative approach. Here, we adopt a complementary strategy leveraging the high degree of brain plasticity that evolved in fishes to ask how variation in social and environmental factors affect individual brain development. We investigated how overall brain size and brain part sizes varied between demes of the same population in the coral reef associated batu coris Coris batuensis. This wrasse species is ideal for our approach because its local population densities (a correlate of intraspecific social complexity) are dissociated from both densities of other species (reflecting interspecific complexity, including competitors and predators) and habitat complexity (represented by the three-dimensional structure of the coral reefs and adjacent areas). We found that individuals from demes with higher intraspecific population density possess larger overall brain volumes than those from lower population density environment, caused by an enlargement of all five main brain regions. Brain anatomical measures did not correlate with measures of interspecific or habitat complexity. Our results suggest that brain plasticity in the batu coris evolved to allow individuals to adapt specifically to variation in intraspecific social challenges. The results support a broader version of the social brain hypothesis, emphasizing the entire brain over specific regions like the neocortex in mammals or the telencephalon in fishes.