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Before Europeans colonized North America, a uniquely American wolf roamed the eastern forests of southern Canada to Florida and west to the Great Plains. Known today as "red wolf" (Canis rufus) in the south and "eastern wolf" (Canis lycaon) in the north, evidence suggests that these indigenous forest wolves shared a common evolutionary history until only a few centuries ago when they were extirpated from the intervening majority of their historical range. While the eastern wolf persists today primarily as a small population in Algonquin Provincial Park, Canada, the red wolf was ostensibly driven from its last stronghold in gulf-coastal Louisiana and Texas by 1980. The last-known red wolves were taken captive for propagation and reintroduction. Today, the red wolf exists as ~250 descendants of 12 founders and are distributed among 42 captive breeding facilities and one reintroduced population in coastal North Carolina. As red and eastern wolves declined in the 20th century, coyotes expanded from the west into the eastern forests, replacing them. Along with human persecution, coyote hybridization has been blamed for the late 20th century demise of the red wolf. However, rather than helping to drive the red wolf to extinction, coyote hybridization may have instead helped to preserve it. In this issue of Molecular Ecology, vonHoldt and colleagues provide the most comprehensive description yet of the substantial quantity and distribution of red wolf ancestry sequestered in southeastern coyote populations. They find the highest frequency of red wolf genes in coyotes from the gulf-coastal sites where the last known wild red wolves occurred, but also present evidence for a high prevalence of red wolf genes in coyotes throughout the southeastern expansion zone. Given the significant reduction in genetic diversity in extant red wolves owing to their late 20th century population bottleneck, this coyote-sequestered reservoir of red wolf genes could prove an important resource for red wolf conservation.

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Poaching is the major cause of death for large carnivores in several regions, contributing to their global endangerment. The traditional hypothesis used in wildlife management (killing for tolerance) suggests reducing protections for a species will decrease poaching. However, recent studies suggest reducing protections will instead increase poaching (facilitated illegal killing) and its concealment (facilitated cryptic poaching). Here, we build survival and competing risk models for mortality and disappearances of adult collared red wolves (Canis rufus) released in North Carolina, USA from 1987 to 2020 (n = 526). We evaluated how changes in federal and state policies protecting red wolves influenced the hazard and incidence of mortality and disappearance. We observed substantial increases in the hazard and incidence of red wolf reported poaching, and smaller increases in disappearances, during periods of reduced federal and state protections (including liberalizing hunting of coyotes, C. latrans); white-tailed deer (Odocoileus virginianus) and American black bear (Ursus americanus) hunting seasons; and management phases. Observed increases in hazard (85-256%) and incidence of reported poaching (56-243%) support the 'facilitated illegal killing' hypothesis. We suggest improving protective policies intended to conserve endangered species generally and large carnivores in particular, to mitigate environmental crimes and generally improve the protection of wild animals.

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BACKGROUND: Gloger's rule postulates that animals should be darker colored in warm and humid regions where dense vegetation and dark environments are common. Although rare in Canis populations, melanism in wolves is more common in North America than other regions globally and is believed to follow Gloger's rule. In the temperate forests of the southeastern United States, historical records of red wolf (Canis rufus) and coyote (Canis latrans) populations document a consistent presence of melanism. Today, the melanistic phenotype is extinct in red wolves while occurring in coyotes and red wolf-coyote hybrids who occupy the red wolf's historical range. To assess if Gloger's rule could explain the occurrence and maintenance of melanistic phenotypes in Canis taxa, we investigated differences in morphology, habitat selection, and survival associated with pelage color using body measurements, GPS tracking data, and long-term capture-mark-recapture and radio-telemetry data collected on coyotes and hybrids across the southeastern United States. RESULTS: We found no correlation between morphometrics and pelage color for Canis taxa. However, we observed that melanistic coyotes and hybrids experienced greater annual survival than did their gray conspecifics. Furthermore, we observed that melanistic coyotes maintained larger home ranges and exhibited greater selection for areas with dense canopy cover and wetlands than did gray coyotes. CONCLUSIONS: In the southeastern United States, pelage color influenced habitat selection by coyotes and annual survival of coyotes and hybrids providing evidence that Gloger's rule is applicable to canids inhabiting regions with dense canopy cover and wetlands. Greater annual survival rates observed in melanistic Canis may be attributed to better concealment in areas with dense canopy cover such as coastal bottomland forests. We suggest that the larger home range sizes of melanistic coyotes may reflect the trade-off of reduced foraging efficiency in lower quality wetland habitat for improved survival. Larger home ranges and differential use of land cover by melanistic coyotes may facilitate weak assortative mating in eastern coyote populations, in which melanistic animals may have lower success of finding compatible mates in comparison to gray conspecifics. We offer that our observations provide a partial explanation for why melanism is relatively low (< 10%) but consistent within coyote populations throughout southeastern parts of their range.

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Captive management of many wildlife species can be challenging, with individuals displaying health disorders that are not generally described in the wild population. Retrospective studies have identified gastrointestinal (GI) diseases, in particular inflammatory bowel disease (IBD), as the second leading cause of captive adult red wolf (Canis rufus) mortality. Recent molecular studies show that imbalanced gut microbial composition is tightly linked to IBD in the domestic dog. The goal of the present study was to address two main questions: (1) how do red wolf gut microbiomes differ between animals with loose stool consistency, indicative of GI issues, and those with normal stool consistency and (2) how does dietary type relate to stool consistency and red wolf gut microbiomes? Fresh fecal samples were collected from 48 captive wolves housed in eight facilities in the United States and from two wild wolves living in Alligator River National Wildlife Refuge, NC, United States. For each individual, the stool consistency was categorized as loose or normal using a standardized protocol and their diet was categorized as either wild, whole meat, a mix of whole meat and kibble or kibble. We characterized gut microbiome structure using 16S rRNA gene amplicon sequencing. We found that red wolves with a loose stool consistency differed in composition than wolves with normal stool consistency, suggesting a link between GI health and microbiome composition. Diet was not related to stool consistency but did significantly impact gut microbiome composition; gut microbiome composition of wolves fed a kibble diet were significantly different than the gut microbiome composition of wolves fed a mixed, whole meat and wild diet. Findings from this study increase the understanding of the interplay between diet and GI health in the red wolf, a critical piece of information needed to maintain a healthy red wolf population ex situ.

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Anthropogenic hybridization of historically isolated taxa has become a primary conservation challenge for many imperiled species. Indeed, hybridization between red wolves (Canis rufus) and coyotes (Canis latrans) poses a significant challenge to red wolf recovery. We considered seven hypotheses to assess factors influencing hybridization between red wolves and coyotes via pair-bonding between the two species. Because long-term monogamy and defense of all-purpose territories are core characteristics of both species, mate choice has long-term consequences. Therefore, red wolves may choose similar-sized mates to acquire partners that behave similarly to themselves in the use of space and diet. We observed multiple factors influencing breeding pair formation by red wolves and found that most wolves paired with similar-sized conspecifics and wolves that formed congeneric pairs with nonwolves (coyotes and hybrids) were mostly female wolves, the smaller of the two sexes. Additionally, we observed that lower red wolf abundance relative to nonwolves and the absence of helpers increased the probability that wolves consorted with nonwolves. However, successful pairings between red wolves and nonwolves were associated with wolves that maintained small home ranges. Behaviors associated with territoriality are energetically demanding and behaviors (e.g., aggressive interactions, foraging, and space use) involved in maintaining territories are influenced by body size. Consequently, we propose the hypothesis that size disparities between consorting red wolves and coyotes influence positive assortative mating and may represent a reproductive barrier between the two species. We offer that it may be possible to maintain wild populations of red wolves in the presence of coyotes if management strategies increase red wolf abundance on the landscape by mitigating key threats, such as human-caused mortality and hybridization with coyotes. Increasing red wolf abundance would likely restore selection pressures that increase mean body and home-range sizes of red wolves and decrease hybridization rates via reduced occurrence of congeneric pairs.

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Cryopreserving genetic resources is becoming increasingly important for species management. In the zoo-based red wolf (Canis rufus) population, inbreeding continues to increase in the absence of new founders. Through banking sperm, we preserve genetic diversity and create the ability to decrease inbreeding accumulation in the future. The quality and quantity of banked sperm can be affected by cryopreservation media and semen collection methods. This study's objectives were to further optimize semen extender used for red wolf sperm cryopreservation, investigate effects of post-thaw holding temperature, and to determine if urethral catheterization is an effective method for semen collection in this species. Semen collection via electroejaculation (EE) was performed on 39 adult red wolf males (ages 1 to 11) from 15 institutions. Urethral catheterization (UC) was attempted on a subset (n = 14) of those males, prior to EE. Thirteen different semen extenders were used for cryopreservation, which varied in osmolarity (HI or NORM), sugar source (glucose, fructose, or a combination), and cryoprotectant (glycerol or DMSO). Significant decreases in percent motility, forward progressive status (FPS), and acrosomal integrity were observed over time across all extenders (P < 0.0001). Among the extender components examined, post-thaw sperm motility and FPS were lower in DMSO versus glycerol based treatments (P < 0.005). Therefore, DMSO should be considered unsuitable as a cryoprotectant when freezing red wolf sperm. Effects of osmolarity and sugar source were minimal and temporally variable, however notably, a higher percentage of morphologically normal sperm were observed in the fructose-based extenders compared to glucose-based extenders post-thaw (P < 0.05). Additionally, post-thaw sperm motility and FPS declined more rapidly in samples maintained at 37 °C compared to samples held at room temperature (P < 0.05). Greater volumes of semen were collected using EE compared to UC (P = 0.041), and sperm samples collected using EE also had greater motility and FPS (P < 0.05). Additionally, though no gross morphological differences were observed, there were fewer sperm with intact acrosomes in the samples collected via UC (P = 0.0443). Thus, UC should not be considered sufficient for semen collection in red wolves when the desired fate of sperm is cryopreservation and/or AI. However, UC does provide an opportunity for a basic reproductive evaluation of a red wolf male.

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Conservation efforts to preserve the red wolf (Canis rufus) have been in progress since the 1970s through the U.S. Fish and Wildlife Service Red Wolf Recovery Program and the Association of Zoos and Aquarium's Red Wolf Species Survival Plan. An ongoing part of this project has been to monitor mortality trends, particularly to look for potential genetic conditions resulting from inbreeding given the small founding population of only 14 individuals. An initial survey was conducted in the 1990s but a comprehensive assessment of the population has not been done since then. This retrospective review evaluates mortality in the population from 1997 to 2012 through analysis of gross necropsy and histology records provided by cooperating institutions that housed red wolves during the time period of interest. Of the 378 red wolves that died during this 15-yr period, 259 animals had gross necropsy records, histology records, or both that were evaluated. The major causes of neonatal death were parental trauma, stillbirth, or pneumonia. Overall, juveniles had very low mortality rates with only 12 wolves aged 30 days to 6 mo dying during the study period. The most common cause of death within the adult populations was neoplasia, with epithelial neoplasms, carcinomas, and adenocarcinomas being the most common types reported. Gastrointestinal disease was the second most common cause of death, particularly gastric dilation and volvulus, inflammatory bowel disease, and gastrointestinal perforations. These findings are in stark contrast to causes of mortality in the wild population, which are primarily due to human-related activities such as vehicular trauma, gunshot, or poisoning. Overall, the captive population has few health problems, but an increase in inflammatory bowel disease in particular warrants further investigation.

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The taxonomic status of the red wolf (Canis rufus) is heavily debated, but could be clarified by examining historic specimens from the southeastern United States. We analyzed mitochondrial DNA (mtDNA) from 3 ancient (350-1900 year olds) putative wolf samples excavated from middens and sinkholes within the historic red wolf range. We detected 3 unique mtDNA haplotypes, which grouped with the coyote mtDNA clade, suggesting that the canids inhabiting southeastern North America prior to human colonization from Europe were either coyotes, which would vastly expand historic coyote distributions, an ancient coyote-wolf hybrid, or a North American evolved red wolf lineage related to coyotes. Should the red wolf prove to be a distinct species, our results support the idea of either an ancient hybrid origin for red wolves or a shared common ancestor between coyotes and red wolves.

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A 2-yr-old female red wolf (Canis rufus gregoryi) sustained a degloving injury to the left thoracic limb while in a display habitat. Initial attempts to resolve the extensive wound by using conservative measures were unsuccessful. Subsequent treatment using a free skin graft consisted first of establishment of an adequate granulation bed via cortical bone fenestration. After establishment of a healthy granulation bed was achieved, free skin graft was harvested and transposed over the bed. To monitor viability and incorporation of the graft, serial thermographic imaging was performed. Thermography noninvasively detects radiant heat patterns and can be used to assess vascularization of tissue, potentially allowing early detection of graft failure. In this case, thermography documented successful graft attachment.

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Infectious diseases pose a significant threat to global biodiversity and may contribute to extinction. As such, establishing baseline disease prevalence in vulnerable species where disease could affect persistence is important to conservation. We assessed potential disease threats to endangered red wolves (Canis rufus) by evaluating regional (southeastern United States) disease occurrences in mammals and parasite prevalence in red wolves and sympatric coyotes (Canis latrans) in North Carolina. Common viral pathogens in the southeast region, such as canine distemper and canine parvovirus, and numerous widespread endoparasites could pose a threat to the red wolf population. The most prevalent parasites in red wolves and sympatric coyotes were heartworm (Dirofilaria immitis), hookworm (Ancylostoma caninum), and Ehrlichia spp.; several red wolves and coyotes were also positive for bacteria causing Lyme disease (Borrelia burgdorferi). Coyotes had a more species-rich parasite community than red wolves, suggesting they could harbor more parasites and act as a disease reservoir. Species identity and sex did not significantly affect parasite loads, but young canids were less likely to have heartworm and more likely to have high levels of endoparasites. Continued disease monitoring is important for red wolf recovery because low levels of genetic variability may compromise the wolves' abilities to combat novel pathogens from closely related species, such as domestic dogs and coyotes.

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In natural populations, the expression and severity of inbreeding depression can vary widely across taxa. Describing processes that influence the extent of inbreeding and inbreeding depression aid in our understanding of the evolutionary history of mating systems such as cooperative breeding and nonrandom mate selection. Such findings also help shape wildlife conservation theory because inbreeding depression reduces the viability of small populations. We evaluated the extent of inbreeding and inbreeding depression in a small, re-introduced population of red wolves (Canis rufus) in North Carolina. Since red wolves were first re-introduced in 1987, pedigree inbreeding coefficients (f) increased considerably and almost every wild born wolf was inbred (average f = 0.154 and max f = 0.383). The large inbreeding coefficients were due to both background relatedness associated with few founders and numerous close relative matings. Inbreeding depression was most evident for adult body size and generally absent for direct fitness measures such as reproductive success and survival; no lethal equivalents (LE = 0.00) were detected in juvenile survival. The lack of strong inbreeding depression in direct measures of fitness could be due to a founder effect or because there were no outbred individuals for comparison. Our results highlight the variable expression of inbreeding depression across traits and the need to measure a number of different traits when evaluating inbreeding depression in a wild population.

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By the 1970s, government-supported eradication campaigns reduced red wolves to a remnant population of less than 100 individuals on the southern border of Texas and Louisiana. Restoration efforts in the region were deemed unpromising because of predator-control programs and hybridization with coyotes. The U.S. Fish and Wildlife Service (USFWS) removed the last remaining red wolves from the wild and placed them in a captive-breeding program. In 1980, the USFWS declared red wolves extinct in the wild. During 1987, the USFWS, through the Red Wolf Recovery Program, reintroduced red wolves into northeastern North Carolina. Although restoration efforts have established a population of approximately 70-80 red wolves in the wild, issues of hybridization with coyotes, inbreeding, and human-caused mortality continue to hamper red wolf recovery. We explore these three challenges and, within each challenge, we illustrate how research can be used to resolve problems associated with red wolf-coyote interactions, effects of inbreeding, and demographic responses to human-caused mortality. We hope this illustrates the utility of research to advance restoration of red wolves.