Genomic Flatlining in the Endangered Island Fox (Urocyon littoralis)

With species declining worldwide due to exploitation and habitat loss, a vital element in mitigating future biodiversity loss will include understanding the genetic consequences of small population size and isolation. Population genetics theory holds that small populations in isolation will suffer from declining diversity, increasing genetic load, and eventual extirpation, in a process dubbed the “extinction vortex.” Island species therefore present an ideal system for empirically studying the impacts of small population size and isolation. Island foxes (Urocyon littoralis) are dwarfed descendants of the mainland gray fox (U. cinereoargenteus) that have persisted on California’s Channel Islands for thousands of generations. We sequenced complete genomes from each island population and the mainland to examine heterozygosity and deleterious variation within individual genomes. The genome of the San Nicolas Island fox (U. l. dickeyi) is almost entirely monomorphic, and retains the lowest observed genomic heterozygosity of any outbred species to date. Furthermore, genomes from all island populations exhibit reduced variation and an elevation in the proportion of deleterious alleles, resulting from strong genetic drift and reduced efficacy of selection. Through demographic simulations, we show that the observed patterns of heterozygosity within the island genomes can be attributed to severe bottlenecks and long-term small population size. The case of the island fox, with its persistence despite extreme lack of genetic variability and increased genetic load, raises questions about the generality of the small population paradigm.