title: Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis).
abstract: The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction-site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small Ne (range = 2.1-89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome-wide divergence. Nonetheless, outlier tests identified 3.6-6.6% of loci as high FST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high FST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small Ne in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.
authors.affiliation: Department of Biology, Graduate Degree Program in Ecology, Colorado State University, 1878 Campus Delivery, Fort Collins, CO, 80523, USA.
authors.forename: W Chris
authors.initials: WC
authors.lastname: Funk
authors.affiliation: Naval Facilities Engineering Command Southwest, 1220 Pacific Highway, San Diego, CA, 92132, USA.
authors.forename: Robert E
authors.initials: RE
authors.lastname: Lovich
authors.affiliation: Department of Biological Sciences, Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID, 83844, USA.
authors.forename: Paul A
authors.initials: PA
authors.lastname: Hohenlohe
authors.affiliation: Department of Anthropology, University of Maryland, College Park, MD, 20742, USA.|Program in Human Ecology and Archaeobiology, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA.|Center for Conservation and Evolutionary Genetics, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, 20008, USA.
authors.forename: Courtney A
authors.initials: CA
authors.lastname: Hofman
authors.affiliation: The Nature Conservancy, San Francisco, CA, 94105, USA.
authors.forename: Scott A
authors.initials: SA
authors.lastname: Morrison
authors.affiliation: Migratory Bird Center, Smithsonian Conservation Biology Institute, National Zoological Park, MRC 5503, Washington, DC, 20013-7012, USA.
authors.forename: T Scott
authors.initials: TS
authors.lastname: Sillett
authors.affiliation: Department of Biology, Graduate Degree Program in Ecology, Colorado State University, 1878 Campus Delivery, Fort Collins, CO, 80523, USA.
authors.forename: Cameron K
authors.initials: CK
authors.lastname: Ghalambor
authors.affiliation: Center for Conservation and Evolutionary Genetics, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, 20008, USA.|Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA.
authors.forename: Jesus E
authors.initials: JE
authors.lastname: Maldonado
authors.affiliation: Program in Human Ecology and Archaeobiology, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA.
authors.forename: Torben C
authors.initials: TC
authors.lastname: Rick
authors.affiliation: Department of Biological Sciences, Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID, 83844, USA.
authors.forename: Mitch D
authors.initials: MD
authors.lastname: Day
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14850, USA.
authors.forename: Nicholas R
authors.initials: NR
authors.lastname: Polato
authors.affiliation: Kellogg Biological Station, Department of Integrative Biology, Michigan State University, Hickory Corners, MI, 49060, USA.
authors.forename: Sarah W
authors.initials: SW
authors.lastname: Fitzpatrick
authors.affiliation: National Park Service, Channel Islands National Park, 1901 Spinnaker Drive, Ventura, CA, 93001, USA.
authors.forename: Timothy J
authors.initials: TJ
authors.lastname: Coonan
authors.affiliation: Department of Fish, Wildlife and Conservation Biology, Colorado State University, 1474 Campus Delivery, Fort Collins, CO, 80523, USA.
authors.forename: Kevin R
authors.initials: KR
authors.lastname: Crooks
authors.affiliation: Department of Fish, Wildlife and Conservation Biology, Colorado State University, 1474 Campus Delivery, Fort Collins, CO, 80523, USA.
authors.forename: Adam
authors.initials: A
authors.lastname: Dillon
authors.affiliation: Institute for Wildlife Studies, P.O. Box 1104, Arcata, CA, 95518, USA.
authors.forename: David K
authors.initials: DK
authors.lastname: Garcelon
authors.affiliation: Catalina Island Conservancy, P.O. Box 2739, Avalon, CA, 90704, USA.
authors.forename: Julie L
authors.initials: JL
authors.lastname: King
authors.affiliation: The Nature Conservancy, San Francisco, CA, 94105, USA.
authors.forename: Christina L
authors.initials: CL
authors.lastname: Boser
authors.affiliation: Fisheries, Wildlife and Conservation Biology, North Carolina State University, Turner House, Box 7646, Raleigh, NC, 27695-7646, USA.
authors.forename: Nicholas
authors.initials: N
authors.lastname: Gould
authors.affiliation: Department of Fish, Wildlife and Conservation Biology, Colorado State University, 1474 Campus Delivery, Fort Collins, CO, 80523, USA.
authors.forename: William F
authors.initials: WF
authors.lastname: Andelt
mesh_terms: D000818:Animals; D002140:California; D019143:Evolution, Molecular; D005589:Foxes / Q000235:genetics*; D040961:Genetic Drift; D014644:Genetic Variation; D005828:Genetics, Population; D060005:Genotyping Techniques; D062312:Islands; D020641:Polymorphism, Single Nucleotide; D017422:Sequence Analysis, DNA
keywords: conservation genomics; divergent selection; effective population size; genetic drift; population divergence