Sophie Preckler-Quisquater’s research while affiliated with University of California, Davis and other places

A few iconic examples have proven the value of facilitated gene flow for counteracting inbreeding depression and staving off extinction, yet the practice is often not implemented for fear of causing outbreeding depression. Using genomic sequencing, climatic niche modeling, and demographic reconstruction, we sought to assess the risks and benefits of using translocations as a tool for recovery of endangered montane red fox (Vulpes vulpes) populations in the western United States. We demonstrated elevated inbreeding and homozygosity of deleterious alleles across all populations, but especially those isolated in the Cascade and Sierra Nevada ranges. Consequently, translocations would be expected to increase population growth by masking deleterious recessive alleles. Demographic reconstructions further indicated shallow divergences of less than a few thousand years among montane populations, suggesting low risk of outbreeding depression. These genomic-guided findings set the stage for future management, the documentation of which will provide a roadmap for recovery of other data-deficient taxa.

Spatial mark-recapture abundance estimates obtained from fecal genotyping are becoming an essential component of conservation of carnivores. The bobcat (Lynx rufus) is a widespread carnivore in California, USA, that until recently lacked robust demographic data. To facilitate a statewide abundance study, we created a single nucleotide polymorphism (SNP) genotyping panel for individual identification. For SNP discovery, we performed restriction site-associated DNA sequencing (RADseq) on 78 samples collected throughout California and subsequently designed a panel of 96 SNPs for sequencing on a microfluidic platform. This panel includes loci to identify sex and differentiate bobcats from other common carnivores. The panel reliably differentiates individuals when using DNA extracted from feces, with 89% of samples amplifying at > 90% of SNPs. Importantly, we found autosomal SNPs were monomorphic in the closely related Canada lynx (L. canadensis) suggesting the panel would still be effective for bobcat study in areas of sympatry. Fecal genotyping provides a cost-effective, noninvasive method for population monitoring and detecting individual movement. Our panel generates standardized genotypes that can be analyzed across laboratories and used for continued bobcat monitoring in California and other western states.

Human‐facilitated introductions of nonnative populations can lead to secondary contact between allopatric lineages, resulting in lineage homogenisation or the formation of stable hybrid zones maintained by reproductive barriers. We investigated patterns of gene flow between the native Sacramento Valley red fox ( Vulpes vulpes patwin ) and introduced conspecifics of captive‐bred origin in California's Central Valley. Considering their recent divergence (20–70 kya), we hypothesised that any observed barriers to gene flow were primarily driven by pre‐zygotic (e.g. behavioural differences) rather than post‐zygotic (e.g. reduced hybrid fitness) barriers. We also explored whether nonnative genes could confer higher fitness in the human‐dominated landscape resulting in selective introgression into the native population. Genetic analysis of red foxes ( n = 682) at both mitochondrial (cytochrome b + D‐loop) and nuclear (19,051 SNPs) loci revealed narrower cline widths than expected under a simulated model of unrestricted gene flow, consistent with the existence of reproductive barriers. We identified several loci with reduced introgression that were previously linked to behavioural divergence in captive‐bred and domestic canids, supporting pre‐zygotic, yet possibly hereditary, barriers as a mechanism driving the narrowness and stability of the hybrid zone. Several loci with elevated gene flow from the nonnative into the native population were linked to genes associated with domestication and adaptation to human‐dominated landscapes. This study contributes to our understanding of hybridisation dynamics in vertebrates, particularly in the context of species introductions and landscape changes, underscoring the importance of considering how multiple mechanisms may be maintaining lineages at the species and subspecies level.

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- versus intra-farm genetic diversity alongside the historical record is critical to understanding of the origins of this emerging domesticate and the relationships between wild and farm-bred fox populations.

Secondary contact zones between deeply divergent, yet interfertile, lineages provide windows into the speciation process. North American grey foxes ( Urocyon cinereoargenteus ) are divided into western and eastern lineages that diverged approximately 1 million years ago. These ancient lineages currently hybridize in a relatively narrow zone of contact in the southern Great Plains, a pattern more commonly observed in smaller‐bodied taxa, which suggests relatively recent contact after a long period of allopatry. Based on local ancestry inference with whole‐genome sequencing ( n = 43), we identified two distinct Holocene pulses of admixture. The older pulse (500–3500 YBP) reflected unidirectional gene flow from east to west, whereas the more recent pulse (70–200 YBP) of admixture was bi‐directional. Augmented with genotyping‐by‐sequencing data from 216 additional foxes, demographic analyses indicated that the eastern lineage declined precipitously after divergence, remaining small throughout most of the late Pleistocene, and expanding only during the Holocene. Genetic diversity in the eastern lineage was highest in the southeast and lowest near the contact zone, consistent with a westward expansion. Concordantly, distribution modelling indicated that during their isolation, the most suitable habitat occurred far east of today's contact zone or west of the Great Plains. Thus, long‐term isolation was likely caused by the small, distant location of the eastern refugium, with recent contact reflecting a large increase in suitable habitat and corresponding demographic expansion from the eastern refugium. Ultimately, long‐term isolation in grey foxes may reflect their specialized bio‐climatic niche. This system presents an opportunity for future investigation of potential pre‐ and post‐zygotic isolating mechanisms.

The gray fox (Urocyon cinereoargenteus) lineage diverged from all other extant canids at their most basal node and is restricted to the Americas. Previous mitochondrial analysis from coastal populations identified deeply divergent (up to 1 Mya) eastern and western lineages that predate most intraspecific splits in carnivores. We conducted genotyping by sequencing (GBS) and mitochondrial analysis on gray foxes sampled across North America to determine geographic concordance between nuclear and mitochondrial contact zones and divergence times. We also estimated the admixture within the contact zone between eastern and western gray foxes based on nuclear DNA. Both datasets confirmed that eastern and western lineages met in the southern Great Plains (i.e, Texas and Oklahoma), where they maintained high differentiation. Admixture was generally low, with the majority of admixed individuals carrying <10% ancestry from the other lineage. Divergence times confirmed a mid-Pleistocene split, similar to the mitochondrial estimates. Taken together, findings suggest gray fox lineages represent an ancient divergence event, far older than most intraspecific divergences in North American carnivores. Low admixture may reflect a relatively recent time since secondary contact (e.g., post-Pleistocene) or, alternatively, ecological or reproductive barriers between lineages. Though further research is needed to disentangle these factors, our genomic investigation suggests species-level divergence exists between eastern and western gray fox lineages.

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.

The red wolf (Canis rufus) of the eastern US was driven to near‐extinction by colonial‐era persecution and habitat conversion, which facilitated coyote (C. latrans) range expansion and widespread hybridization with red wolves. The observation of some gray wolf (C. lupus) ancestry within red wolves sparked controversy over whether it was historically a subspecies of gray wolf with its predominant “coyote‐like” ancestry obtained from post‐colonial coyote hybridization (2‐species hypothesis) versus a distinct species closely related to the coyote that hybridized with gray wolf (3‐species hypothesis). We analyzed mitogenomes sourced from before the 20th century bottleneck and coyote invasion, along with hundreds of modern amplicons, which led us to reject the 2‐species model and to investigate a broader phylogeographic 3‐species model suggested by the fossil record. Our findings broadly support this model, in which red wolves ranged the width of the American continent prior to arrival of the gray wolf to the mid‐continent 60–80 ka; red wolves subsequently disappeared from the mid‐continent, relegated to California and the eastern forests, which ushered in emergence of the coyote in their place (50–30 ka); by the early Holocene (12–10 ka), coyotes had expanded into California, where they admixed with and phenotypically replaced western red wolves in a process analogous to the 20th century coyote invasion of the eastern forests. Findings indicate that the red wolf pre‐dated not only European colonization but human, and possibly coyote, presence in North America . These findings highlight the urgency of expanding conservation efforts for the red wolf.

The Sacramento Valley red fox (Vulpes vulpes patwin) is a native subspecies of conservation need endemic to the northern portion of California's Central Valley, USA. We conducted an occupancy survey to investigate habitat use and obtain a crude, range‐wide estimate of abundance. We used 2 previously developed red fox distribution models based on presence‐only data to stratify sampling of 107 sites with baited cameras for ≥90 days during March 2013–June 2016, resulting in red fox detections at 30 sites. All detections occurred in 1 of the 93 sites where 1 or both previous presence‐only models predicted occurrence. Red fox occurrence was positively associated with dry agriculture, human development, and proximity to grassland, and negatively associated with wetlands and flooded agriculture. The models predicted that 34.21% of the 12,000‐km² Sacramento Valley landscape contained red foxes, which we estimate corresponded to approximately 1,600 breeding individuals. This estimate is comparable to that of the federally endangered California San Joaquin kit fox (Vulpes macrotis mutica), underscoring its potential vulnerability and conservation need. Targeted efforts to enhance its habitat, such as juxtaposition of grassland patches with agricultural and rural residential structures through conservation easements, could benefit conservation of the Sacramento Valley red fox. © 2018 The Wildlife Society.