Genomic Diversity and Relatedness in the Founding Black-footed Ferret Population

Abstract

Black-footed ferrets (Mustela nigripes) are small obligate carnivores native to North American prairie ecosystems. They have the unfortunate but notable distinction of being assumed extinct twice in their history. Depending on healthy prairie dog (Cynomys spp.) colonies for both food and shelter, black-footed ferrets most likely declined in response to prairie habitat loss and fragmentation, prairie dog eradication programs, and non-native disease, most notably sylvatic plague (caused by the bacterium Yersinia pestis). After their rediscovery at a single site in Wyoming in 1981, a successful captive-breeding and reintroduction effort was established using the last 18 living individuals. Of these, only seven are considered to be genetic founders of all remaining black-footed ferrets. Coupled with the last wild population being isolated on the far western edge of the species range, the founding black-footed ferrets had likely experienced a severe genetic bottleneck. Genetic management of the captive breeding population has been largely achieved through pedigree analysis. Although studied prior to capture, the founders were assumed to be unrelated as they were all wild-caught, and paternity was assumed based upon proximity when captured. As they were all captured from the same dwindling source population, their relationships to each other are likely more complicated than studbook assumptions suggest. Fortunately, suitably preserved samples existed for 19 individuals of the source population, including the seven assumed founders. We used next generation sequencing data and bioinformatics focused on genomic variant discovery to characterize the amount of variation in the founders, estimate levels of relatedness among the sampled individuals, infer relationships, and compare to the current captive breeding population. We found low levels of genome-wide heterozygosity and high proportions of the genome in runs of homozygosity. Results confirmed some assumed relationships within the source population but contradicted others. Analysis also suggests that the founding population had a (not unexpected) higher level of background relatedness than initially assumed. This work will inform further genetic investigation and conservation of the species both in captive breeding and in establishing viable wild populations.