Genomic Flatlining in the Endangered Island Fox

Abstract

Genetic studies of rare and endangered species often focus on defining and preserving genetically distinct populations, especially those having unique adaptations [1, 2]. Much less attention is directed at understanding the landscape of deleterious variation, an insidious consequence of geographic isolation and the inefficiency of natural selection to eliminate harmful variants in small populations [3-5]. With population sizes of many vertebrates decreasing and isolation increasing through habitat fragmentation and loss, understanding the extent and nature of deleterious variation in small populations is essential for predicting and enhancing population persistence. The Channel Island fox (Urocyon littoralis) is a dwarfed species that inhabits six of California's Channel Islands and is derived from the mainland gray fox (U. cinereoargenteus). These isolated island populations have persisted for thousands of years at extremely small population sizes [6, 7] and, consequently, are a model for testing ideas about the accumulation of deleterious variation in small populations under natural conditions. Analysis of complete genome sequence data from island foxes shows a dramatic decrease in genome-wide variation and a sharp increase in the homozygosity of deleterious variants. The San Nicolas Island population has a near absence of variation, demonstrating a unique genetic flatlining that is punctuated by heterozygosity hotspots, enriched for olfactory receptor genes and other genes with high levels of ancestral variation. These findings question the generality of the small-population paradigm that maintains substantial genetic variation is necessary for short- and long-term persistence.

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

“…Our results thus support the view that, even in small populations, the random loss of variation does not affect all sites in the same way, and we further contribute to the general debate about the relative role of drift and selection when the effective population size is very small (9)(10)(11)58).…”

“…Despite the difficulty in assessing the role of genetic factors in past extinctions of small populations, the causative link between low genetic and genomic variation, fitness reduction, and high extinction risk is supported by theoretical arguments and empirical evidence (24,(62)(63)(64)(65). Still, the long-term persistence of species at extremely low levels of genomic variation has also been documented (11,66). We believe that our study, even if based on a limited number of whole genomes, can help explaining this apparent contradiction between expectation and observation.…”

“…This conservation paradigm, strictly related to the extinction vortex metaphor (5), is supported by empirical evidence (6)(7)(8), but it is challenged by studies showing that selection can be powerful also at small population sizes (9,10) and that survival and even demographic expansion can occur with almost no genomic variation (11). Interestingly, if extinction does not occur, drift in small isolated groups can produce, or contribute to, genetic and phenotypic divergence, possibly leading to speciation (12,13).…”

Purging of Strongly Deleterious Mutations Explains Long-Term Persistence and Absence of Inbreeding Depression in Island Foxes

“…Previous analysis of whole genome sequences from island foxes sampled in 1988 revealed dramatically reduced levels of diversity and increased levels of putatively deleterious alleles relative to the mainland gray fox [5]. On the smallest island, San Nicolas, the population is nearly monomorphic across its entire genome [5].…”

Maximising evolutionary potential in functional proxies for extinct species: a conservation genetic perspective on de‐extinction

“…Furthermore, assuming relevant adaptive loci can be identified and altered, it may still prove difficult to find and subsequently resurrect a sufficient number of genetic variants to achieve adequate levels of genomic diversity for two reasons (see also Box 4). First, many extinct species with phenotypic traits of interest are likely to have experienced a 'pre-extinction genetic bottleneck' that reduced genome-wide diversity and resulted in individuals with similar genomes Palkopoulou et al 2015;Park et al 2015;Robinson et al 2016;but see Bouzat 2010). Second, our ability to describe what once existed will depend on the temporal and spatial distributions of archival samples at time of collection.…”