Red Fox Ancestry and Connectivity Assessments Reveal Minimal Fur Farm Introgression in Greater Yellowstone Ecosystem

Abstract

Rocky Mountain red foxes Vulpes vulpes macroura potentially encounter other red fox Vulpes vulpes lineages at lower elevations, which may include nonindigenous red foxes derived from fur farms. Introgression from nonindigenous red foxes could have negative evolutionary consequences for the rare Rocky Mountain red fox subspecies. Red foxes at high elevations in the Greater Yellowstone Ecosystem exhibit lighter coat colors than those at lower elevations, potentially indicating that they represent the indigenous subspecies and that gene flow across the elevational gradient is restricted. We collected tissue samples across a 1,750-m elevation range and examined mitochondrial DNA sequences and nuclear DNA microsatellite genotypes to assess the ancestry and genetic population structure of red foxes in the northern Greater Yellowstone Ecosystem. We also used reference samples from fur farm red foxes and indigenous red foxes of the western United States to assess the extent of nonindigenous introgression across the ecosystem. We found little overlap in the elevational distribution of maternally inherited mitochondrial DNA haplotypes: above 1,600 m, we only found indigenous Rocky Mountain haplotypes (n = 4), whereas below 1,600 m, we found haplotypes not indigenous to the Rocky Mountains (n = 5) that were associated with fur farms or indigenous to the Great Plains. In contrast, biparentally inherited microsatellite variation showed little population structure across the elevational gradient. Despite this evidence of nuclear gene flow across the elevational gradient, we found little fur farm introgression in the microsatellite genotypes. It is possible that long-standing nuclear (but apparently not mitochondrial) gene flow between Rocky Mountain red foxes and indigenous red foxes on the Great Plains explained the low nuclear differentiation of these populations. Importantly, our results suggested that high elevations of the northern Greater Yellowstone Ecosystem remained free of significant fur farm introgression. Mitonuclear discordance could reflect sex-biased dispersal, which we hypothesize could be the effect of elevational differences in reproductive phenology.

Contrasting genetic trajectories of endangered and expanding red fox populations in the western U.S

“…Multiple previous studies have described mitochondrial variation in red foxes in wild North American populations and globally distributed fur farms (e.g., Aubry et al 2009 ; Sacks et al 2010 ; Statham et al 2011 , 2012 , 2014 ; Kasprowicz et al 2016 ; Lounsberry et al 2017 ; Merson et al 2017 ; Black et al 2018 ; Cross et al 2018 ). Using all known published homologous mtDNA haplotypes sampled in wild populations in North America or fur farms, we recreated a median joining network in PopART (Leigh and Bryant 2015 ) and identified haplotypes as belonging to one of four previously described matrilineal groups: the Holarctic clade corresponding to Alaska and northwestern Canada, the Eastern subclade corresponding to eastern North America, the Mountain subclade corresponding to the western contiguous U.S., and the Widespread subclade that is ancestral to both the Mountain and Eastern subclades (i.e., member haplotypes occur in either eastern North America or the western U.S. but not in both; Aubry et al 2009 ; Sacks et al 2010 ).…”

“…Although recognized as four distinct subspecies, indigenous western red foxes form a single lineage that is >20,000 years diverged from red foxes in the remainder of the continent (see Supplementary Text SI for details on taxonomy). Available information on phenotype suggests that montane members of the lineage are also smaller, have proportionally larger foot surfaces, and breed considerably later in the year, all of which have been suggested to represent local adaptations to the subalpine environment (Grinnell et al 1937 ; Roest 1977 ; Fuhrmann 1998 ; Cross et al 2018 ; SCAT, 2022 ). Following European colonization of North America, native western red foxes declined in portions of their range presumably due to a combination of unregulated harvest and poisoning associated with predator control programs (Perrine et al 2010 ; Sacks et al 2010 ).…”

“…Both the departure from historical montane habitat and apparent rapid increase have led some to posit that red foxes in the Intermountain basins are not members of native western montane subspecies, but rather descendants of nonnative red foxes that escaped or were released from fur farms (e.g., Fichter and Williams 1967 ; Mace 1970 ), similar to feral populations documented in western Washington and California (Aubry 1984 ; Lewis et al 1999 ). Alternatively, these lower elevation red foxes may have also originated from a continental-scale expansion from eastern or northwestern North America (hereafter referred to as midcontinent) (e.g., Hoffmann et al 1969 ; Kamler and Ballard 2002 ; Cross et al 2018 ).…”

Insight into the Genetic Population Structure of Wild Red Foxes in Poland Reveals Low Risk of Genetic Introgression from Escaped Farm Red Foxes

“…Many wild animal populations are endangered by genetic introgression from domesticated animals that have escaped from farms [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 ]. Genetic introgression can be defined as the incorporation of alleles from one species into the gene pool of a second, divergent species [ 9 ].…”

“…There have been few studies of genetic introgression between farm red foxes and their wild counterparts. As the main research aim, genetic introgression was investigated in North America by Sacks et al [ 28 ], Lounsberry et al [ 5 ], Akins et al [ 29 ] and Cross et al [ 2 ]. It was also examined and discussed as a secondary aim in research that focused on other objectives [ 22 , 23 , 30 ].…”