Missing history of a modern domesticate: Historical demographics and genetic diversity in farm-bred red fox populations

Abstract

The first record of captive-bred red foxes (Vulpes vulpes) dates to 1896 when a breeding enterprise emerged in the provinces of Atlantic Canada. Because its domestication happened during recent history, the red fox offers a unique opportunity to examine the genetic diversity of an emerging domesticated species in the context of documented historical and economic influences. In particular, the historical record suggests that North American and Eurasian farm-bred populations likely experienced different demographic trajectories. Here, we focus on the likely impacts of founder effects and genetic drift given historical trends in fox farming on North American and Eurasian farms. A total of 15 mitochondrial haplotypes were identified in 369 foxes from 10 farm populations that we genotyped (n = 161) or that were previously published. All haplotypes are endemic to North America. Although most haplotypes were consistent with eastern Canadian ancestry, a small number of foxes carried haplotypes typically found in Alaska and other regions of western North America. The presence of these haplotypes supports historical reports of wild foxes outside of Atlantic Canada being introduced into the breeding stock. These putative Alaskan and Western haplotypes were more frequently identified in Eurasian farms compared to North American farms, consistent with historical documentation suggesting that Eurasian economic and breeding practices were likely to maintain low-frequency haplotypes more effectively than in North America. Contextualizing inter- vs. intra-farm genetic diversity alongside the historical record is critical to understanding the origins of this emerging domesticate and the relationships between wild and farm-bred fox populations.

Graphical Abstract

Fig. 1.

Choropleths visualizing shifts in the fox farming industry in the United States between 1939 and 1973. The agricultural census surveyed fox farming twice (Sixteenth Census of the United States Agriculture 1940, Census of Agriculture 1974), and the data collected in each census is visualized. Only states belonging to the continental United States were included in the census.

Fig. 2.

mtDNA haplotype network of farm-bred foxes. Each node represents a haplotype identified in at least one farm-bred fox. Nodes are scaled according to the number of individuals carrying the haplotype and colored according to the relative frequency in each population. Step mutations are indicated by hatch marks. Areas of the network that fall outside of the Eastern subclade of the Nearctic clade are indicated with arrows, and the populations each haplotype was identified in are explicitly called out below each magnifier box. The ICG’s farm is subdivided into three populations, corresponding to individual lines: A = aggressive, T = tame, and C = conventional. This network includes both novel sequences and data published elsewhere (Statham et al. 2011; Lounsberry et al. 2017; Black et al. 2018; Zatoń‐Dobrowolska et al. 2019) (Supplementary Table 1).

Fig. 3.

Network of mtDNA haplotypes found in wild and farm-bred foxes. Each node represents a haplotype identified in at least one fox. Nodes are not scaled by frequency but are colored according to the relative frequency in each population. Step-mutations are indicated by hatch marks. Haplotypes from farm-bred foxes are aggregated at the continent level. Data from several external sources that sampled wild fox populations is included (Aubry et al. 2009; Kasprowicz et al. 2015; Lounsberry et al. 2017; Black et al. 2018; Quinn et al. 2019, 2022). Data from wild populations was not filtered to remove non-native haplotypes; this figure is intended to facilitate the comparison of data collected across multiple studies. As in Fig. 2, arrows call out the regions of the network corresponding to non-Eastern subclade haplotypes were identified on farms.

Fig. 4.

Haplotype frequency spectra from North American and Eurasian farms. Haplotype frequencies were compared based on the joint CytB and D-loop mtDNA haplotypes. North American farms had an excess of very rare and very common haplotypes relative to Eurasia (Supplementary Table 3). The bar furthest to the right corresponds to F-17, which was found in over 65% of North American farm-bred foxes.