Joint dog and wolf genealogies reveal the evolution of the canine genome

Dogs and their closest extant relative, the grey wolf, diverged around 30k years ago, but have since experienced complex histories of gene flow involving other canids, adaptive pressures due to close association with humans, and changing climates. We infer joint genealogies of dogs, grey wolves, and a coyote using available whole genomes to reconstruct the evolutionary forces shaping the dog genome. These genealogies reveal multiple strong mutation-rate pulses unique to dogs, including signals detectable across ancient dogs from the past 10,000 years. We further detect pervasive genealogical signatures of purifying selection and find that GC-biased gene conversion is a major driver of diversity patterns around gene promoters in dogs. We introduce a new genealogy-based selection scan, TwigScan, that computes time-stratified differentiation, increasing power over traditional FST-based approaches. Applying this framework, alongside a second single-population test for detecting more recent selection within dogs, we identify multiple known and novel loci with signatures of positive selection. Among these, the region surrounding the amylase 2B locus shows evidence of introgression from a deeply divergent, unsampled canid lineage with divergence comparable to that of dholes. AMY2B duplications appear to occur exclusively on this introgressed haplotype which increased in frequency approximately 7,000-8,000 years ago, coinciding with increased reliance on starch-rich diets in human populations. Together, these results show how mutation-rate variation, gene conversion, selection, and inter-species gene flow have jointly shaped the dog genome, highlighting the power of genealogical approaches for resolving complex evolutionary histories. Significance StatementDogs were likely the first animal domesticated by humans, yet the evolutionary processes shaping the modern dog genome remain unresolved. Recent advances now enable reconstruction of genome-wide genealogies from genetic variation, enabling evolutionary histories to be traced along ancestral lineages through time. Applied to dogs, grey wolves, and coyotes, we investigate how mutation, selection, and interspecies gene flow shaped canine evolution. We identify mutation-rate pulses unique to dogs--only the second clear example of such a phenomenon in mammals--and quantify pervasive effects of purifying selection and GC-biased gene conversion. We identify regions of excess dog-wolf divergence and show that the selected AMY2B starch-digestion locus in dogs likely originated through introgression from a deeply divergent ghost canid lineage.