Range‐wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange and distinct demographic histories

Abstract

Widely distributed taxa provide an opportunity to compare biogeographic responses to climatic fluctuations on multiple continents and to investigate speciation. We conducted the most geographically and genomically comprehensive study to date of the red fox (Vulpes vulpes), the world's most widely distributed wild terrestrial carnivore. Analyses of 697 bp of mitochondrial sequence in ~1000 individuals suggested an ancient Middle Eastern origin for all extant red foxes and a 400 kya (SD = 139 kya) origin of the primary North American (Nearctic) clade. Demographic analyses indicated a major expansion in Eurasia during the last glaciation (~50 kya), coinciding with a previously described secondary transfer of a single matriline (Holarctic) to North America. In contrast, North American matrilines (including the transferred portion of Holarctic clade) exhibited no signatures of expansion until the end of the Pleistocene (~12 kya). Analyses of 11 autosomal loci from a subset of foxes supported the colonization time frame suggested by mtDNA (and the fossil record) but, in contrast, reflected no detectable secondary transfer, resulting in the most fundamental genomic division of red foxes at the Bering Strait. Endemic continental Y-chromosome clades further supported this pattern. Thus, intercontinental genomic exchange was overall very limited, consistent with long-term reproductive isolation since the initial colonization of North America. Based on continental divergence times in other carnivoran species pairs, our findings support a model of peripatric speciation and are consistent with the previous classification of the North American red fox as a distinct species, V. fulva.

Red foxes colonizing the tundra: genetic analysis as a tool for population management

“…The overall aim of this paper was to elucidate the fine-scaled genetic relationship between Swedish red foxes in recently colonized tundra areas and red foxes in the boreal and nemoral zones with specific emphasis on identifying the invasive pathways. Based on the mitochondrial DNA, the historical origin of tundra red foxes could not be elucidated since there was little divergence and all documented haplotypes (except the novel Swedish ones) are common and widespread across Eurasia (Statham et al 2014). These results were in agreement with a general pattern of low mitochondrial structuring across large parts of the European mainland (Statham et al 2014).…”

“…Based on the mitochondrial DNA, the historical origin of tundra red foxes could not be elucidated since there was little divergence and all documented haplotypes (except the novel Swedish ones) are common and widespread across Eurasia (Statham et al 2014). These results were in agreement with a general pattern of low mitochondrial structuring across large parts of the European mainland (Statham et al 2014). The U and U4 haplotypes belong to the Holarctic clade whereas the U66 haplotype only has been identified in Sweden (Statham et al 2014).…”

“…Among these, four were present in the tundra region and all nine in the boreo-nemoral region (Table 1). The previously documented haplotypes, U and U4 has a Eurasian distribution whereas haplotype U66 only has been documented in Sweden (Table 1, Statham et al 2014). The remaining six haplotypes were previously unpublished (GenBank Accession nos KX768845-KX768850) and were closely related (separated by single substitutions) to the U, U4 or U66 haplotypes (Table 1; Fig.…”

“…We used the same software to calculate a minimum spanning network that was visualized in HapStar 0.7 (Teacher and Griffiths 2011). For reference and alignment, we used 53 cytochrome-b haplotypes previously published by Statham et al (2014) and references therein.…”

“…For all individuals, we sequenced the 5 0 portion of the cytochrome-b fragment at the commercial lab Macrogen Inc. (www.macrogen.com). Sequences were verified for accurate species origin using BLAST, controlled visually and aligned in BioEdit 7.2.5 and haplotypes were determined against previously published data ( Statham et al 2014). Novel haplotypes (n = 6) were deposited on GenBank (Accession No KX768845-50).…”