Abstract
The recovery and persistence of rare and endangered species are often threatened by genetic factors, such as the accumulation of deleterious mutations, loss of adaptive potential, and inbreeding depression [1]. Island foxes (Urocyon littoralis), thedwarfed descendants of mainland gray foxes (Urocyon cinereoargenteus), have inhabited California's Channel Islands for >9,000 years [2-4]. Previous genomic analyses revealed that island foxes have exceptionally low levels of diversity and elevated levels of putatively deleterious variation [5]. Nonetheless, all six populations have persisted for thousands of generations, and several populations rebounded rapidly after recent severe bottlenecks [6, 7]. Here,we combine morphological and genomic data withpopulation-genetic simulations to determine the mechanism underlying the enigmatic persistence of these foxes. First, through analysis of genomes from 1929 to 2009, we show that island foxes have remained at small population sizes with low diversity for many generations. Second, we present morphological data indicating an absence of inbreeding depression in island foxes, confirming that they are not afflicted with congenital defects common to other small and inbred populations. Lastly, our population-genetic simulations suggest that long-term small population size results in a reduced burden of strongly deleterious recessive alleles, providing a mechanism for the absence of inbreeding depression in island foxes. Importantly, the island fox illustrates a scenario in which genetic restoration through human-assisted gene flow could be a counterproductive or even harmful conservation strategy. Our study sheds light on the puzzle of island fox persistence, a unique success story that provides a model for the preservation of small populations.
Highlights
We found that the empirical numbers of peaks, average peak widths, and proportions of shared peaks all fell within the middle 95% of values obtained through simulation (Table S2), suggesting that demographic processes alone can account for empirical patterns of variation in peaks of heterozygosity within and between San Nicolas fox genomes
We found that purging of recessive deleterious alleles became weaker and the accumulation of additive deleterious alleles became more severe as population size declined (Table S6)
Our genomic analyses show that recent catastrophic bottlenecks had limited impact on island fox genomes, indicating that exceptionally low heterozygosity and higher levels of putatively deleterious alleles are caused by historically small population size
Summary
The recovery and persistence of rare and endangered species are often threatened by genetic factors, such as the accumulation of deleterious mutations, loss of adaptive potential, and inbreeding depression [1]. Predicted Genetic Variation in Large Mainland versus Small Island Populations We hypothesized that the absence of inbreeding depression in island foxes may be attributed to purging of strongly deleterious recessive mutations in island populations relative to the mainland, despite the overall accumulation of deleterious variants observed in island genomes. To test this hypothesis, we conducted forward-in-time simulations [20] under a range of demographic models (Figure 4A), each consisting of a mainland population of 10,000 diploids giving rise to an island population with a final size of 1,000 diploids. These findings suggest that individuals derived from historically small populations carry a reduced burden of strongly deleterious recessive alleles relative to individuals from a large outbred population, reducing the former’s risk of inbreeding depression
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