A 120-y time series of genomes reveals the consequences of closed breeding in German Shepherd Dogs

Abstract

Many contemporary breed dogs display reduced genomic health compared to mixed-breed dogs, including reduced heterozygosity and increased genetic load, likely due to strong directed breeding. Lack of historical genomes, however, has made it difficult to disentangle the timing and drivers of these declines given complex and breed-specific demographic histories, artificial selection, and crossbreeding. Here, we sequenced genomes of nine 20th-century museum specimens (1906–1993) of pedigree German Shepherd Dogs (GSDs) to directly assess the consequences of contemporary breeding practices on genomic diversity and health over time. The GSD breed offers an excellent case study, given the breed’s fluctuations in global popularity, differing selective regimes, and the GSD’s use in the establishment of other breeds, including wolfdogs. Genome-wide heterozygosity showed significant reductions after the Second World War (WWII), coincident with an increase in both the frequency of runs of homozygosity and load. We also detected repeated population bottlenecks linked to the use of popular sires throughout the 20th century. Finally, although hybridization with wolves has led to genome-wide increases in heterozygosity in wolfdog breeds derived from the GSD, nonadmixed ancestry blocks (dog or wolf) were severely depleted in diversity due to the limited number of founders involved in their establishment. Combined, our results indicate that declines in the genomic health of GSDs and related breeds occurred not at the onset of breed formation but throughout the last century, as a result of population bottlenecks associated with WWII and the repeated use of popular sires.