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

As anthropogenic disturbances continue to drive habitat loss and range contractions, the maintenance of evolutionary processes will increasingly require targeting measures to the population level, even for common and widespread species. Doing so requires detailed knowledge of population genetic structure, both to identify populations of conservation need and value, as well as to evaluate suitability of potential donor populations. We conducted a range-wide analysis of the genetic structure of red foxes in the contiguous western U.S., including a federally endangered distinct population segment of the Sierra Nevada subspecies, with the objectives of contextualizing field observations of relative scarcity in the Pacific mountains and increasing abundance in the cold desert basins of the Intermountain West. Using 31 autosomal microsatellites, along with mitochondrial and Y-chromosome markers, we found that populations of the Pacific mountains were isolated from one another and genetically depauperate (e.g., estimated Ne range = 3-9). In contrast, red foxes in the Intermountain regions showed relatively high connectivity and genetic diversity. Although most Intermountain red foxes carried indigenous western matrilines (78%) and patrilines (85%), the presence of nonindigenous haplotypes at lower elevations indicated admixture with fur-farm foxes and possibly expanding midcontinent populations as well. Our findings suggest that some Pacific mountain populations could likely benefit from increased connectivity (i.e., genetic rescue) but that nonnative admixture makes expanding populations in the Intermountain basins a non-ideal source. However, our results also suggest contact between Pacific mountain and Intermountain basin populations is likely to increase regardless, warranting consideration of risks and benefits of proactive measures to mitigate against unwanted effects of Intermountain gene flow.

Noninvasive Sampling Reveals Short-Term Genetic Rescue in an Insular Red Fox Population.

Genetic factors in the decline of small populations are extremely difficult to study in nature. We leveraged a natural experiment to investigate evidence of inbreeding depression and genetic rescue in a remnant population of subalpine-specialized Sierra Nevada red foxes (Vulpes vulpes necator) using noninvasive genetic monitoring during 2010-2017. Only 7 individuals were detected in the first 2 years. These individuals assigned genetically to the historical population and exhibited genetic hallmarks of inbreeding and no evidence of reproduction. Two years into the study, we detected 2 first-generation immigrant males from a recently expanding population of red foxes in the Great Basin Desert. Through annual resampling of individuals (634 red fox DNA samples, 41 individuals) and molecular reconstruction of pedigrees, we documented 1-3 litters/year for 5 years, all descended directly or indirectly from matings involving immigrant foxes. The observed heterozygosity and allelic richness of the population nearly doubled in 2 years. Abundance increased, indicative of a rapidly expanding population. Throughout the study, adult survival was high. Restoration of gene flow apparently improved the demographic trajectory of this population in the short term. Whether these benefits continue in the longer term could depend on numerous factors, such as maintenance of any locally adapted alleles. This study highlights the value of noninvasive genetic monitoring to assess rapidly shifting conditions in small populations. Uncertainties about the longer-term trajectory of this population underscore the need to continue monitoring and to research potential for both negative and positive aspects of continued genetic infusion.