Body size, inbreeding, and lifespan in domestic dogs

Inbreeding poses a real or potential threat to nearly every species of conservation concern. Inbreeding leads to loss of diversity at the individual level, which can cause inbreeding depression, and at the population level, which can hinder ability to respond to a changing environment. In closed populations such as endangered species and ex situ breeding programs, some degree of inbreeding is inevitable. It is therefore vital to understand how different patterns of breeding and inbreeding can affect fitness in real animals. Domestic dogs provide an excellent model, showing dramatic variation in degree of inbreeding and in lifespan, an important aspect of fitness that is known to be impacted by inbreeding in other species. There is a strong negative correlation between body size and lifespan in dogs, but it is unknown whether the higher rate of aging in large dogs is due to body size per se or some other factor associated with large size. We used dense genome-wide SNP array data to calculate average inbreeding for over 100 dog breeds based on autozygous segment length and found that large breeds tend to have higher coefficients of inbreeding than small breeds. We then used data from the Veterinary medical Database and other published sources to estimate life expectancies for pure and mixed breed dogs. When controlling for size, variation in inbreeding was not associated with life expectancy across breeds. When comparing mixed versus purebred dogs, however, mixed breed dogs lived about 1.2 years longer on average than size-matched purebred dogs. Furthermore, individual pedigree coefficients of inbreeding and lifespans for over 9000 golden retrievers showed that inbreeding does negatively impact lifespan at the individual level. Registration data from the American Kennel Club suggest that the molecular inbreeding patterns observed in purebred dogs result from specific breeding practices and/or founder effects and not the current population size. Our results suggest that recent inbreeding, as reflected in variation within a breed, is more likely to affect fitness than historic inbreeding, as reflected in variation among breeds. Our results also indicate that occasional outcrosses, as in mixed breed dogs, can have a substantial positive effect on fitness.