High genetic distinctiveness of wild and farm fox ( Vulpes vulpes L.) populations in Poland: evidence from mitochondrial DNA analysis

High genetic distinctiveness of wild and farm fox ( Vulpes vulpes L.) populations in Poland: evidence from mitochondrial DNA analysis

In Poland, the number of wild red foxes ( Vulpes vulpesL.) and the size of the fur-farming industry are growing. Thereis concern that the gene pool of the wild foxes is being infiltrated by that of the farm animals. We analyzed three groups Polishfarm foxes and wild-living animals from Poland and North America to investigate the gene flow or introgression between farm andwild red foxes. We took into account the breeding history of the species and the evolutionary relationships between fox populationson different continents. We compared the haplotypes based on the concatenated nucleotide sequences ofMT-CO1(mitochondriallyencoded cytochrome c oxidase I) andMT-ATP6(mitochondrially encoded ATP synthase 6) genes. It was confirmed that investigatedfur-farm animals originated from wild individuals living in North America. We found a haplotype common to wild foxes from Europe(Poland) and wild North American individuals. The common haplotype shared by both investigated wild-living groups could indicatesome degree of introgression between Polish farm and wild-living populations. Haplotypes characteristic of North American foxes weretransferred to the Polish wild population and have been established. However, the pairwise Φ STvalues make it clear that North Americanwild and Polish wild foxes are genetically distinct evolutionary groups.

___

  • Aubry KB, Statham MJ, Sacks BN, Perrine JD, Wisely SM (2009). Phylogeography of the North American red fox: vicariance in Pleistocene forest refugia. Mol Ecol 18: 2668-2686.
  • Balcom A (1916). Fox farming in Prince Edward Island: a chapter in the history of speculation. Q J Econ 30: 665-681.
  • Berteaux D, Gallant D, Sacks BN, Statham MJ (2015). Red foxes ( Vulpes vulpes ) at their expanding front in the Canadian Arctic have indigenous maternal ancestry. Polar Biol 38: 913-917.
  • Clement M, Posada D, Crandall KA (2000). TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657-1659.
  • Edwards CJ, Soulsbury CD, Statham MJ, Ho SYW, Wall D, Dolf G, Iossa G, Baker PJ, Harris S, Sacks BN et al. (2012). Temporal genetic variation of the red fox, Vulpes vulpes , across western Europe and the British Isles. Quaternary Sci Rev 57: 95-104.
  • Excoffier L, Lischer HEL (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564-567.
  • Galov A, Sindičić M, Andreanszkyc T, Čurković S, Dězđek D, Slavica A, Hartl GB, Krueger B (2014). High genetic diversity and low population structure in red foxes ( Vulpes vulpes ) from Croatia. Mamm Biol 79: 77-80.
  • Huson DH, Bryant D (2006). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
  • İbiş O, Tez C, Özcan S (2014). Phylogenetic status of the Turkish red fox ( Vulpes vulpes ), based on partial sequences of the mitochondrial cytochrome b gene. Vertebr Zool 64: 273-284.
  • Inoue T, Nonaka N, Mizuno A, Morishima Y, Sato H, Katakura K, Oku Y (2007). Mitochondrial DNA phylogeography of the red fox ( Vulpes vulpes ) in northern Japan. Zool Sci 24: 1178-1186.
  • Jeżewska-Witkowska G, Horecka B, Jakubczak A, Kasperek K, Ślaska B, Bugno-Poniewierska M, Piórkowska M (2012). Genetic variability of farmed and free-living populations of red foxes (Vulpes vulpes ). Ann Anim Sci 12: 501-512.
  • Kamler JF, Ballard WB (2002). A review of native and nonnative red foxes in North America. Wildl Soc Bull 30: 370-379.
  • Kutschera VE, Lecomte N, Janke A, Selva N, Sokolov AA, Haun T, Steyer K, Nowak C, Hailer F (2013). A range-wide synthesis and timeline for phylogeographic events in the red fox ( Vu lp es vulpes ). BMC Evol Biol 13: 114. doi: 10.1186/1471-2148-13- 114.
  • Langille BL, O’Leary KE, Whitney HG, Marshall HD (2014). Mitochondrial DNA diversity and phylogeography of insular Newfoundland red foxes ( Vulpes vulpes deletrix ). J Mammal 95: 772-780.
  • Laut AC (1921). The Fur Trade of America. New York, NY, USA: Macmillan.
  • Leite JV, Álvares F, Velo-Antón G, Brito JC, Godinho R (2015). Differentiation of North African foxes and population genetic dynamics in the desert: insights into the evolutionary history of two sister taxa, Vulpes rueppellii and Vulpes vulpes . Org Divers Evol 15: 731. doi:10.1007/s13127-015-0232-8.
  • Lounsberry ZT, Quinn CB, Angulo C, Kalani T, Tiller E, Sacks BN (2016). Investigating genetic introgression from farmed red foxes into the wild population in Newfoundland, Canada. Conserv Genet doi:10.1007/s10592-016-0914-6.
  • McDevitt A, Zub K, Kawałko A, Oliver MK, Herman JS, Wójcik JM (2012). Climate and refugial origin influence the mitochondrial lineage distribution of weasels ( Mustela nivalis ) in a phylogeographic suture zone . Biol J Linn Soc 106: 57-69.
  • Perrine JD, Pollinger JP, Sacks BN, Barrett RH, Wayne RK (2007). Genetic evidence for the persistence of the critically endangered Sierra Nevada red fox in California. Conserv Genet 8: 1083- 1095.
  • Petersen M (1914). The Fur Traders and Fur Bearing Animals. Pittsburgh, PA, USA: Hammond Press. P é w é TL, Hopkins OM (1967). Malmnal remains of pre-Wisconsin age in Alaska. In: Hopkins DM, editor. The Bering Land Bridge. Palo Alto, CA, USA: Stanford University Press, pp. 266-287.
  • Piórkowska M (2013). Common fox farming yesterday and today. Wiadomości Zootechniczne 51: 65-76 (article in Polish with an abstract in English).
  • Sacks BN, Brazeal JL, Lewis JC (2016). Landscape genetics of the nonnative red fox of California. Ecol Evol 6: 4775-4791.
  • Sacks BN, Moore M, Statham MJ, Wittmer HU (2011). A restricted hybrid zone between native and introduced red fox ( Vu lp es vulpes ) populations suggests reproductive barriers and competitive exclusion. Mol Ecol 20: 326-341.
  • Sacks BN, Statham MJ, Perrine JD, Wisely SM, Aubry KB (2010). North American montane red foxes: expansion, fragmentation, and the origin of the Sacramento Valley red fox. Conserv Genet11: 1523-1539.
  • Ślaska B, Grzybowska-Szatkowska L (2011). Analysis of the mitochondrial haplogroups of farm and wild-living raccoon dogs in Poland. Mitochondr DNA 22: 105-110.
  • Ślaska B, Zięba G, Rozempolska-Rucińska I, Jeżewska-Witkowska G, Nisztuk S, Horecka B, Zoń A (2016). Mitochondrial DNA haplotypes are associated with performance traits in raccoon dogs. Anim Sci Pap Rep 34: 293-302.
  • Statham MJ, Murdoch J, Janecka J, Aubry KB, Edwards CJ, Soulsbury CD, Berry O, Wang Z, Harrison D, Pearch M et al. (2014). Range-wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange, and distinct demographic histories. Mol Ecol 23: 4813-4830.
  • Statham MJ, Sacks BN, Aubry KB, Perrine JD, Wisely SM (2012). The origin of recently established red fox populations in the United States: translocations or natural range expansions? J Mammal 93: 52-65.
  • Statham MJ, Trut LN, Sacks BN, Kharlamova AV, Oskina IN, Gulevich RG, Johnson JL, Temnykh SV, Acland GM, Kukekova AV (2011). On the origin of a domesticated species: identifying the parent population of Russian silver foxes ( Vulpes vulpes). Biol J Linn Soc 103: 168-175.
  • Tamura K, Dudley J, Nei M, Kumar S (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
  • Teacher AGF, Thomas JA, Barnes I (2011). Modern and ancient red fox ( Vulpes vulpes ) in Europe show an unusual lack of geographical and temporal structuring, and differing responses within the carnivores to historical climatic change. Evol Biol 11: 214. doi: 10.1186/1471-2148-11-214.
  • Wandeler P, Hoeck PEA, Keller LF (2007). Back to the future: museum specimens in population genetics. Trends Ecol Evol 22: 634-642.
  • Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marshall CR (1997). Molecular systematics of the Canidae . Syst Biol 46: 622- 653.
  • Yu JN, Han SH, Kim BH, Kryukov AP, Kim S, Lee BY, Kwak M (2012). Insights into Korean red fox ( Vulpes vulpes ) based on mitochondrial cytochrome b sequence variation in east Asia. Zool Sci 29: 753-760.