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

Mark J. Statham, James Murdoch, Jan Janecka, Keith B. Aubry, Ceiridwen J. Edwards, Carl D. Soulsbury, Oliver Berry, Zhenghuan Wang, David Harrison, Malcolm Pearch, Louise Tomsett, Judith Chupasko, Benjamin N. Sacks

Research output: Contribution to journalArticle

43 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)4813-4830
Number of pages18
JournalMolecular Ecology
Volume23
Issue number19
Early online date25 Sep 2014
DOIs
Publication statusPublished - Oct 2014
Externally publishedYes

Fingerprint

Phylogeography
demographic history
Vulpes vulpes
phylogeography
genomics
demographic statistics
colonization
divergence
Demography
history
last glaciation
reproductive isolation
carnivore
fossil record
strait
chromosome
Pleistocene
North America
Eurasia
Y chromosome

Cite this

Statham, Mark J. ; Murdoch, James ; Janecka, Jan ; Aubry, Keith B. ; Edwards, Ceiridwen J. ; Soulsbury, Carl D. ; Berry, Oliver ; Wang, Zhenghuan ; Harrison, David ; Pearch, Malcolm ; Tomsett, Louise ; Chupasko, Judith ; Sacks, Benjamin N. / Range-wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange and distinct demographic histories. In: Molecular Ecology. 2014 ; Vol. 23, No. 19. pp. 4813-4830.
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Statham, MJ, Murdoch, J, Janecka, J, Aubry, KB, Edwards, CJ, Soulsbury, CD, Berry, O, Wang, Z, Harrison, D, Pearch, M, Tomsett, L, Chupasko, J & Sacks, BN 2014, 'Range-wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange and distinct demographic histories', Molecular Ecology, vol. 23, no. 19, pp. 4813-4830. https://doi.org/10.1111/mec.12898

Range-wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange and distinct demographic histories. / Statham, Mark J.; Murdoch, James; Janecka, Jan; Aubry, Keith B.; Edwards, Ceiridwen J.; Soulsbury, Carl D.; Berry, Oliver; Wang, Zhenghuan; Harrison, David; Pearch, Malcolm; Tomsett, Louise; Chupasko, Judith; Sacks, Benjamin N.

In: Molecular Ecology, Vol. 23, No. 19, 10.2014, p. 4813-4830.

Research output: Contribution to journalArticle

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T1 - Range-wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange and distinct demographic histories

AU - Statham, Mark J.

AU - Murdoch, James

AU - Janecka, Jan

AU - Aubry, Keith B.

AU - Edwards, Ceiridwen J.

AU - Soulsbury, Carl D.

AU - Berry, Oliver

AU - Wang, Zhenghuan

AU - Harrison, David

AU - Pearch, Malcolm

AU - Tomsett, Louise

AU - Chupasko, Judith

AU - Sacks, Benjamin N.

N1 - No full text in Eprints. HN 17/11/2017

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N2 - 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.

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KW - nuclear DNA

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KW - speciation

KW - Vulpes fulva

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KW - Y-chromosome

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