Abstract
The polygamous mating system of free-ranging domestic dogs (FRDs) contrasts with the social monogamy typical of gray wolves and all other wild canids. The transition to polygamy in dogs could have been initiated by a shift from apex predator to human commensal during the early domestication stages. Here, we test this hypothesis by investigating the characteristics of the FRD mating system that could have been important for domestication. This inference is based on genome-wide Single Nucleotide Polymorphism (SNP) data from three geographically distinct populations, including behavioral data for one of them. The reconstructed genealogies form a wide network of kinship relationships resulting from the frequent occurrence of maternal and paternal half-siblings, reflecting male and female polygamy. Reproductive success is positively correlated with the strength of social interactions and the number of connections with opposite-sex individuals, implying a preference toward familiar mates and the importance of social relationships in determining mating patterns. This is supported by a nonrandom distribution of reproductive partners and a reproductive skew in males and females. Multiple paternity within litters points to female polygamy within a single estrus, and sexual size dimorphism implies sexual selection favoring larger males. Physiological changes resulting from polygamy, including increased male fertility and reduced breeding seasonality, could have facilitated the natural spread of novel adaptive traits and limited the introgression from wolves. The change in reproductive patterns, typically considered a consequence of selective breeding, could instead have occurred naturally in response to the dietary niche change, triggering further changes that facilitated the domestication process.