Inter-Island Whole-Genome Comparison Reveals Micro-Evolutionary Dynamics of the Red Fox, Stimulated Through Post-Glacial Sea-Level Alterations

Continental islands provide a system for understanding the mechanisms behind allopatric evolution. The red fox (Vulpes vulpes) is characterized by its remarkable dispersibility and adaptability, covering the widest distributional range among the Carnivora. The Hondo red fox (V. v. japonica) is a distinctive subspecies that evolved within the Japanese Archipelago, which has an intricate geohistory. Their genomic evolution process among islands offers valuable insights into the relationships between diversification of terrestrial organisms and geographic dynamics associated with climate changes, and conservation of these unique populations. We constructed novel ∼2.4 Gbp whole-genome assemblies with high coverage depth of four wild Hondo red foxes across three predominant islands and estimated the genomic distance, phylogeny, diversity, demography, and split time to reconstruct their biogeographic history at a spatiotemporally fine scale. Despite having a large geographic distance between one another, the pairwise genomic distance was closest between two individuals on the same island. Phylogenetic divergence pattern and runs of homozygosity supported disparate genetic characteristics per island. Historical demographic dynamics exhibited independent trajectories on each island following the Last Glacial, and sudden demographic differentiation was detected during the Hypsithermal. These findings indicate that post-glacial marine transgression degenerated land bridges between islands and strongly contributed to allopatric evolution, even for the highly dispersive generalist. Modern three-island populations are likely considered as respective evolutionarily significant units. This study expands our knowledge regarding the evolutionary history of the red fox and offers crucial insights into the formation process of biodiversity and endemism in terrestrial animals on continental islands.