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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.
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