Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (<i>Urocyon littoralis</i>)

Funk, W. Chris; Lovich, Robert E.; Hohenlohe, Paul A.; Hofman, Courtney A.; Morrison, Scott; Sillett, T. Scott; Ghalambor, Cameron K.; Maldonado, Jesús E.; Rick, Torben C.; Day, Mitch D.; Polato, Nicholas R.; Fitzpatrick, Sarah W.; Coonan, Timothy J.; Crooks, Kevin R.; Dillon, Adam; Garcelon, David K.; King, Julie L.; Boser, Christina L.; Gould, Nicholas P.; Andelt, William F.

doi:10.1111/mec.13605

Cited by 124 publications

(125 citation statements)

References 116 publications

(239 reference statements)

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“…All sequences were aligned to the domestic dog ( Canis familiaris ) reference genome, canFam3.1. Phylogenetic analyses show that island fox genomes cluster by population, and southern and northern island populations define distinct clusters, consistent with prior studies (Figures 1A, B, S1) [4, 5, 8, 9]. …”

Section: Resultssupporting

confidence: 89%

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

et al. 2018

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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]. Island foxes (Urocyon littoralis), the dwarfed descendants of mainland gray foxes (U. cinereoargenteus), have inhabited California’s Channel Islands for >9,000 years [2-4]. Previous genomic analyses revealed 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 following recent severe bottlenecks [6, 7]. Here, we combine morphological and genomic data with population genetic simulations to determine the mechanism underlying the enigmatic persistence of these foxes. First, through analysis of genomes from 1929-2009, 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 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.

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Section: Resultssupporting

confidence: 89%

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

et al. 2018

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“…Many studies have provided strong empirical evidence that genetic drift is a powerful driver of genetic differentiation (Slatkin ; Funk et al . ), especially in small and insular populations (Strand et al . ).…”

Section: Discussionmentioning

confidence: 99%

Archipelagos of the Anthropocene: rapid and extensive differentiation of native terrestrial vertebrates in a single metropolis

et al. 2017

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Some of the best evidence for rapid evolutionary change comes from studies of archipelagos and oceanic islands. City parks are analogous systems as they create geographically isolated green spaces that differ in size, structure and complexity. Very little, however, is known about whether city parks within a single urban centre drive selection and result in the diversification of native species. Here, we provide evidence for the rapid genetic and morphological differentiation of a native lizard (Intellagama lesueurii) at four geographically close yet unconnected parks within one city. Year of establishment of each city park varied from 1855 (oldest) to 2001 (youngest) equating to a generation time range of 32 to three generations. Genetic divergence among city park populations was large despite the small pairwise geographic distances (<5 km) and found to be two to three times higher for microsatellites and three to 33 times higher for mtDNA relative to nonurban populations. Patterns of morphological differentiation were also found to be most extensive among the four city park populations. In contrast to nonurban populations, city park populations showed significant differentiation in relative body size, relative head and limb morphology and relative forelimb and hindlimb length. Crucially, we show that these patterns of differentiation are unlikely to have been caused by founder events and/or drift alone. Our results suggest that city park 'archipelagos' could represent theatres for rapid evolution that may, in time, favour adaptive diversification.

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“…To test this hypothesis, we conducted linear regressions between pairwise estimates of genetic differentiation ( F ST and Jost's D) within our 4 genetic clusters, and average measures of within‐population genetic diversity ( H O , H E , and AR) at our 14 neutral microsatellite markers. As gene flow with mainland populations is unlikely to have significantly contributed to within‐population genetic diversity of the islands (Funk et al., ), estimates of within‐population genetic diversity are an ideal index of historical genetic drift for this analysis.…”

Section: Methodsmentioning

confidence: 99%

Selection and drift influence genetic differentiation of insular Canada lynx (Lynx canadensis) on Newfoundland and Cape Breton Island

Prentice

Bowman

Khidas

et al. 2017

Ecology and Evolution

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Island populations have long been important for understanding the dynamics and mechanisms of evolution in natural systems. While genetic drift is often strong on islands due to founder events and population bottlenecks, the strength of selection can also be strong enough to counteract the effects of drift. Here, we used several analyses to identify the roles of genetic drift and selection on genetic differentiation and diversity of Canada lynx (Lynx canadensis) across eastern Canada, including the islands of Cape Breton and Newfoundland. Specifically, we assessed whether we could identify a genetic component to the observed morphological differentiation that has been reported across insular and mainland lynx. We used a dinucleotide repeat within the promoter region of a functional gene that has been linked to mammalian body size, insulin‐like growth factor‐1 (IGF‐1). We found high genetic differentiation at neutral molecular markers but convergence of allele frequencies at the IGF‐1 locus. Thus, we showed that while genetic drift has influenced the observed genetic structure of lynx at neutral molecular markers, natural selection has also played a role in the observed patterns of genetic diversity at the IGF‐1 locus of insular lynx.

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Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

Cited by 124 publications

References 116 publications

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

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

Archipelagos of the Anthropocene: rapid and extensive differentiation of native terrestrial vertebrates in a single metropolis

Selection and drift influence genetic differentiation of insular Canada lynx (Lynx canadensis) on Newfoundland and Cape Breton Island

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