Brain-behavior differences in pre-modern and modern lineages of domestic dogs

Although domestic dogs were the first domesticated species, the nature of dog domestication remains a topic of ongoing debate. In particular, brain and behavior changes associated with different stages of the domestication process have been difficult to disambiguate. Most modern Western breed dogs possess highly derived physical and behavioral traits because of intense artificial selection for appearance and function within the past 200 years. In contrast, pre-modern dogs, including primitive/ancient breeds, village dogs, and New Guinea Singing Dogs, have undergone less intensive artificial selection and retain more ancestral characteristics. Consequently, comparisons between modern and pre-modern dogs can shed light on brain and behavior changes that have occurred recently in the domestication process. Here, we addressed this question using a voxel-based morphometry analysis of structural MRI images from 72 modern breed dogs and 13 pre-modern dogs (32 females). Modern breed dogs show widespread expansions of neocortex and reductions in the amygdala and other subcortical regions. Furthermore, cortical measurements significantly predicted individual variation in trainability, while amygdala measurements significantly predicted fear scores. These results contrast with the longstanding view that domestication consistently involves reduction in brain size and cognitive capacity. Rather, our results suggest that recent artificial selection has targeted higher-order brain regions in modern breed dogs, perhaps to facilitate behavioral flexibility and close interaction and cooperation with humans. Significance Statement This study provides novel insights into the neural changes associated with artificial selection during dog domestication by comparing brain morphology between modern breed dogs and a unique and rare sample of pre-modern dogs, including ancient breeds, village dogs, and New Guinea singing dogs. Our findings demonstrate that modern breed dogs exhibit significant cortical expansion linked to trainability and pre-modern dogs show amygdala enlargement associated with heightened fear, suggesting that brain evolution has happened rapidly in a species embedded in the anthropogenic environment.