Polygenic adaptation signals reveal selection on key behavioral traits early in dog domestication history

Dogs, the first domesticated animals, show behavioral and morphological changes shaped by artificial selection, but when and where these traits were selected remains unclear. Analyzing two independent canine genomic datasets comprising 1,987 and 722 individuals, we found that polygenic shifts in key behavioral traits associated with domestication were more consistently shared across dog lineages than those in morphological traits. Specifically, we first grouped breeds into three major genetic lineages-Asian Spitz, African-Middle Eastern, and European Modern-and integrated genomic variation with breed-level measures of 36 behavioral and four morphological traits. We then tested for polygenic adaptation using pairwise population comparisons and PolyGraph. Across both datasets, pro-social behavioral shifts, particularly reduced owner-directed aggression and non-social fear, showed the most consistent selection signals. PolyGraph detected shifts toward lower values for both traits on branches ancestral to the major dog lineages. Trainability showed an ancestral increase, whereas attachment/attention seeking increased in specific lineages, based on dog-only analyses designed to minimize rearing-related confounding in wolves. Hunting-related behaviors also showed lineage-specific shifts, while morphological traits varied substantially across datasets and lineages. Ancient genetic trait scores mirrored these patterns: prehistoric dogs already differed from wolves in shared pro-social behavioral traits and displayed lineage-specific shifts in hunting-related behaviors, whereas morphological scores remained heterogeneous. Together, these findings indicate that both shared behavioral changes and functional differentiation among dog lineages began early in domestication.