True Colors: Commercially-acquired morphological genotypes reveal hidden allele variation among dog breeds, informing both trait ancestry and breed potential

Direct-to-consumer canine genetic testing is becoming increasingly popular among dog owners. The data collected therein provides intriguing insight into the current status of morphological variation present within purebred populations. Mars WISDOM PANELTM data from 11,790 anonymized dogs, representing 212 breeds and 4 wild canine species, were evaluated at genes associated with 7 coat color traits and 5 physical characteristics. Frequencies for all tested alleles at these 12 genes were determined by breed and by phylogenetic grouping. A sub-set of the data, consisting of 30 breeds, was divided into separate same-breed populations based on country of collection, body size, coat variation, or lineages selected for working or conformation traits. Significantly different (p ≤ 0.00167) allele frequencies were observed between populations for at least one of the tested genes in 26 of the 30 breeds. Next, standard breed descriptions from major American and international registries were used to determine colors and tail lengths (e.g. genetic bobtail) accepted within each breed. Alleles capable of producing traits incongruous with breed descriptions were observed in 143 breeds, such that random mating within breeds has probabilities of between 4.9e−7 and 0.25 of creating undesirable phenotypes. Finally, the presence of rare alleles within breeds, such as those for the recessive black coloration and natural bobtail, was combined with previously published identity-by-decent haplotype sharing levels to propose pathways by which the alleles may have spread throughout dog breeds. Taken together, this work demonstrates that: 1) the occurrence of low frequency alleles within breeds can reveal the influence of regional or functional selection practices; 2) it is possible to trace the mode by which characteristics have spread across breeds during historical breed formation; and 3) the necessity of addressing conflicting ideals in breed descriptions relative to actual genetic potential is crucial. Author Summary From the sleek Doberman Pinscher to the coifed Poodle, the sunny Golden Retriever to the aristocratic Pekingese, the world of purebred dogs offers options that appeal to nearly all aesthetics. Pure dog breeds, of which there are over 400 worldwide, are created through selective breeding over multiple generations, toward an ideal goal of temperament, behavior, and physical appearance. Written descriptions of these breed-specific ideals are produced and maintained by dedicated breed enthusiasts, and provide guidelines that direct breeders in their selection choices. However, the genetic mechanisms that produce the spectrum of canine colors and patterns, sculpt the small triangular ears of a Siberian Husky or the long soft ears of a Basset Hound, are complicated and intertwined. This means that some breeds can carry rare, hidden traits for many generations, hampering selection efforts toward uniformity. We have determined the genotypes of >11,000 dogs, representing >200 breeds, at 12 genes that impact coat color and physical characteristics. In doing so, we can now present realistic trait frequencies within each breed, report occurrences of gene variants that can produce undesirable traits, and draw conclusions about the historic spread of characteristics across modern related breeds and those with distant shared ancestry.