Across the Arctic: Mitogenomic Phylogeny of Arctic Foxes (Vulpes lagopus) Reveals Several New Matrilines and Illuminates the Colonization History of the Icelandic Population

Background/Objectives: Arctic foxes (Vulpes lagopus) exemplify the vulnerability of Arctic species to global warming and anthropogenic impacts, including habitat loss, interspecific competition with temperate species, pollution (chemical and biological), and declining prey abundance. Despite their ecological importance, the evolutionary and demographic history of the species is still incompletely understood, and the colonization history of isolated island populations, such as the one on Iceland, remains unresolved. Methods: We analyzed 80 mitochondrial genomes from across the Holarctic, including 22 Icelandic individuals. We combined phylogenetic reconstruction, coalescence-dating, haplotype network analysis, and diversity metrics to infer matrilineal relationships and colonization history. Results: Seven distinct haplogroups (Hg.1–Hg.7) were identified, which diverged ≥65 thousand years ago (kya). Two haplogroups were broadly distributed across Fennoscandia, Russia, Iceland, and Canada, while others were region-specific: two in eastern Russia (respectively diverging ~171 kya and ~89 kya), one in central Russia (~66 kya), and two in Iceland (~95 kya and ~66 kya). Three haplogroups were detected in Iceland, and at least four unrelated founding females are required to explain the current matrilineal diversity. One haplogroup contained sufficient representatives for molecular dating, yielding a minimum colonization age of ~5600 years, assuming in situ diversification. Observed matrilineal diversity in Iceland does not uniquely identify a single geographic source. Conclusions: Arctic foxes’ distribution and diversity reflect repeated cycles of isolation and expansion as circumpolar environments shifted. Broader sampling across the Nearctic is critical to clarify the timing, sources, and routes of Iceland’s colonization, as Nearctic sampling was limited to a single Canadian mitogenome.