Genetic analysis of European red foxes reveals multiple distinct peripheral populations and central continental admixture

Abstract

Temperate terrestrial species in Europe were hypothesized to have been restricted to southern peninsular refugia (Iberia, Italy, Balkans) during the height of the last glacial period. However, recent analyses of fossil evidence indicate that some temperate species existed outside these areas during the last glacial maximum (LGM). Red foxes (Vulpes vulpes) in particular, could have been distributed across the southern half of the continent, potentially forming one continuous population. To investigate these hypotheses, we used 21 nuclear microsatellite loci and two fragments (768 bp) of mitochondrial DNA to characterize the population structure among a continent-wide sample of 288 European red foxes. We tested whether European red foxes clustered into discrete populations corresponding to the hypothetical peninsular refugia. Additionally, we sought to determine if distinct northern populations were formed after postglacial recolonization. Our results indicated that only the foxes of Iberia appeared to have remained distinct over a considerable period of time (32-104 kya). Spanish red foxes formed their own genotypic cluster; all mtDNA haplotypes were endemic and closely related, and together both the mitochondrial and nuclear datasets indicated this population contributed little to postglacial recolonization of Northern Europe. In contrast, red foxes from Italy and the Balkans contributed significantly to, or were part of, a wider, admixed population stretching across midlatitude Europe. In Northern Europe, we identified a Scandinavian population that had an ancestral relationship with red foxes to the south, and a more recent relationship with those to the east, in Russia. We also resolved two distinct populations on the islands of Ireland and Britain that had been separated from one another, and from those on the continent, since the late Pleistocene/mid Holocene (~4-24 kya).

Next-generation phylogeography resolves post-glacial colonization patterns in a widespread carnivore, the red fox (Vulpes vulpes), in Europe

“…3; Table S3). Although this conflicts with the current fossil evidence where the oldest known specimen in Ireland is from the Bronze Age (approximately 3.8 kyrs BP; (12)), this is congruent with previous studies demonstrating high haplotype diversity and the identification of many unique haplotypes at mitochondrial markers on the island (14,18). Another carnivore, the stoat (Mustela erminea) was proposed to be an early colonizer of Ireland over a post-glacial land bridge from Britain inferred from molecular dating and fossil data (50) and several potential prey species (e.g.…”

“…Following on from outstanding issues in relation to unresolved colonization scenarios (18) we first investigated the colonization history of red foxes in the British Isles. Two scenarios were incorporated between which the data and analysis presented by Statham et al (18) could not distinguish between. The first was that Ireland was colonized naturally overland from Britain after the end of the LGM (i.e.…”

“…It has existed as an island for approximately 15,000 years (almost twice as long as Britain; 49) and humans have been proposed as the primary mechanism of transport for its mammalian fauna in ancient and modern times (10,48). An estimate of 10.2 kyrs BP was estimated for a split between Irish and British red foxes using mtDNA data, but with a 95% CI range that incorporated the possibility of natural colonization before Ireland became an island (18). Both Irish and British populations are distinct from mainland European populations (Figs.…”

“…Alternatively, long-range gene flow between isolated refugia could explain the lack of phylogeographic structure in these species (8). More recent studies (17,18) identified mtDNA haplotypes that were unique to particular regions (e.g. Iberia) that potentially indicate long-term separation from other European populations.…”

Sequencing Red Fox Y Chromosome Fragments to Develop Phylogenetically Informative SNP Markers and Glimpse Male-Specific Trans-Pacific Phylogeography

“…The phylogeography of red fox ( Vulpes vulpes ) has been well-characterized in terms of mitochondrial and nuclear patterns of diversity over most of its global distribution [ 1 , 2 , 3 , 4 , 5 , 6 , 7 ]. For example, the most divergent mitochondrial split dates to approximately half a million years ago and separates a clade that evolved in North America south of the ice sheets prior to the last glaciation (Nearctic clade) and one that spans Eurasia and Alaska–western Canada, reflecting a secondary continental exchange event ~100 thousand years ago (ky) [ 2 , 4 ].…”