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

Abstract

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 visualize the potential historic connections between breeds that share rare alleles; and 3) the necessity of addressing conflicting ideals in breed descriptions relative to actual genetic potential is crucial.

Fig 1. Allele frequencies for ASIP, MC1R, and CBD103 by phylogenetic breed relationship.

Breeds are grouped by phylogenetic clade, as described, and sorted within clade by frequency of e and then a^y to demonstrate patterns of phenotype expression across interacting genes. Thick black boxes highlight examples of color preference influencing interacting genes: a) Pointer/Setter breeds are commonly seen in solid colors, caused by the K^B allele of CBD103 or the e/e genotype of MC1R. Since the solid-color genotypes are epistatic to the dominant alleles of MC1R and all alleles of ASIP, variation at those genes does not follow a trend for color preference. b) Related breeds with high frequency of the k^y allele of CBD103 have a more structured pattern of ASIP allele preference. c) Breeds with a preference for the brindle pattern show heterogeneity for K^B/k^br (reflective of a k^br phenotype) and high frequency of a^y, required for the expression of brindle across the whole body.

Fig 2. Allele frequencies for MC1R, ASIP, TYRP1, and CBD103 across same-breed populations.

Horizontal black bars indicate within-breed allele distributions that are significantly different (p ≤ 0.00167).

Fig 3. Identity-by-decent (IBD) haplotype sharing breed relationships connect breeds carrying the T allele for tailless.

Solid black lines represent instances of significant haplotype sharing levels between breeds. The color of the breed names reflects the proposed carrier status of the tailless variant in the sampled members of those breeds, indicating not present (grey), present and permitted within the breed standard (green), and present and not permitted within the breed standard (red). The Dachshund breed shows no significant haplotype sharing with any other breed, however, its highest non-significant haplotype sharing value is with the Swedish Valhund (dashed line). Inset, the Australian Shepherd breed permits natural taillessness.

Fig 4. Identity-by-decent (IBD) haplotype sharing breed relationships connect breeds carrying the a allele of ASIP.

Solid black lines indicate instances of significant haplotype sharing between breeds. Breed names in purple indicate observed frequency of the a allele within the breed in the present study. Breed names in black indicate that the a allele was not detected within the sampled individuals of that breed. The dashed line connecting the Dalmatian to the Airedale Terrier indicates that no significant haplotype sharing was detected with the Dalmatian, however the highest non-significant level of haplotype sharing was measured with the Airedale Terrier. Inset images show examples of dogs with the recessive black phenotype, A) Shetland Sheepdog, B) Pumi.

Fig 5. Purebred dogs exhibiting color traits deemed inappropriate by one or more breed registries.

A) Bull Terrier with a brown nose and brown patch above its eye. B) Shetland Sheepdog with piebald white spotting. C) Great Dane with the harlequin pattern on a fawn base color.