Managing hybridization of a recovering endangered species: The red wolf Canis rufus as a case study

Abstract Hybridization presents a unique challenge for conservation biologists and managers. While hybridization is an important evolutionary process, hybridization is also a threat formany native species. The endangered species recovery effort for the red wolf Canis rufus is a classic system for understanding and addressing the challenges of hybridization. From 1987?1993, 63 red wolves were released from captivity in eastern North Carolina, USA, to establish a free-ranging, non-essential experimental population. By 1999, managers recognized hybridization with invasive coyotes Canis latrans was the single greatest threat to successful recovery, and an adaptive management plan was adopted with innovative approaches for managing the threat of hybridization. Here we review the application and results of the adaptive management efforts from 1993 to 2013 by comparing: (1) the numbers of wolves, coyotes, and hybrids captured, (2) the numbers of territorial social groups with presumed breeding capabilities, (3) the number of red wolf and hybrid litters documented each year and (4) the degree of coyote introgression into the wild red wolf gene pool. We documented substantial increases in the number of known red wolves and red wolf social groups from 1987–2004 followed by a plateau and slight decline by 2013.The number of red wolf litters exceeded hybrid litters each year and the proportion of hybrid litters per year averaged 21%. The genetic composition of the wild red wolf population is estimated to include < 4% coyote ancestry from recent introgression since reintroduction. We conclude that the adaptive management plan was effective at reducing the introgression of coyote genes into the red wolf population, but population recovery of red wolves will require continuation of the current management plan, or alternative approaches, for the foreseeable future. More broadly, we discuss the lessons learned from red wolf adaptive management that could assist other endangered species recovery efforts facing the challenge of minimizing hybridization.

Download Full-text

DNA profiles of the eastern Canadian wolf and the red wolf provide evidence for a common evolutionary history independent of the gray wolf

Canadian Journal of Zoology ◽

10.1139/z00-158 ◽

2000 ◽

Vol 78 (12) ◽

pp. 2156-2166 ◽

Cited By ~ 86

Author(s):

Paul J Wilson ◽

Sonya Grewal ◽

Ian D Lawford ◽

Jennifer NM Heal ◽

Angela G Granacki ◽

...

Keyword(s):

Genetic Material ◽

Gray Wolf ◽

Canis Rufus ◽

Red Wolf ◽

The Subject ◽

The 1960S ◽

Original Species ◽

Dna Profiles ◽

Microsatellite Alleles ◽

Red Wolves

The origin and taxonomy of the red wolf (Canis rufus) have been the subject of considerable debate and it has been suggested that this taxon was recently formed as a result of hybridization between the coyote and gray wolf. Like the red wolf, the eastern Canadian wolf has been characterized as a small "deer-eating" wolf that hybridizes with coyotes (Canis latrans). While studying the population of eastern Canadian wolves in Algonquin Provincial Park we recognized similarities to the red wolf, based on DNA profiles at 8 microsatellite loci. We examined whether this relationship was due to similar levels of introgressed coyote genetic material by comparing the microsatellite alleles with those of other North American populations of wolves and coyotes. These analyses indicated that it was not coyote genetic material which led to the close genetic affinity between red wolves and eastern Canadian wolves. We then examined the control region of the mitochondrial DNA (mtDNA) and confirmed the presence of coyote sequences in both. However, we also found sequences in both that diverged by 150 000 - 300 000 years from sequences found in coyotes. None of the red wolves or eastern Canadian wolf samples from the 1960s contained gray wolf (Canis lupus) mtDNA sequences. The data are not consistent with the hypothesis that the eastern Canadian wolf is a subspecies of gray wolf as it is presently designated. We suggest that both the red wolf and the eastern Canadian wolf evolved in North America sharing a common lineage with the coyote until 150 000 - 300 000 years ago. We propose that it retain its original species designation, Canis lycaon.

Download Full-text

Cross-fostering as a conservation tool to augment endangered carnivore populations

Journal of Mammalogy ◽

10.1093/jmammal/gyy087 ◽

2018 ◽

Vol 99 (5) ◽

pp. 1033-1041

Author(s):

Eric M Gese ◽

William T Waddell ◽

Patricia A Terletzky ◽

Chris F Lucash ◽

Scott R McLellan ◽

...

Keyword(s):

Life Span ◽

Litter Size ◽

Average Life ◽

Canis Rufus ◽

Average Life Span ◽

Red Wolf ◽

In The Wild ◽

Red Wolves ◽

Cross Fostering

Abstract Cross-fostering offspring with nonbiological parents could prove useful to augment populations of endangered carnivores. We used cross-fostering to augment captive-born and wild-born litters for the endangered red wolf (Canis rufus). Between 1987 and 2016, 23 cross-fostering events occurred involving captive-born pups fostered into captive litters (n = 8 events) and captive-born pups fostered into wild recipient litters (n = 15 events). Percentage of pups surviving 3 and 12 months was 91.7% for captive-born pups fostered into captive recipient litters. For pups fostered into wild litters, percentage of pups surviving 5 months was > 94% among fostered pups (pups fostered into a wild red wolf litter or replaced a hybrid litter), pups in recipient litters (wild-born litters receiving fostered pups), and pups in control litters (wild-born litters not in a fostering event) when using pups with known fates. Including pups with unknown fates as deaths, percentage of pups surviving 5 months was > 54% among fostered pups, pups in recipient litters, and pups in control litters. Among wild litters, percentage of pups surviving 12 months was > 82% among fostered pups, pups in recipient litters, and pups in control litters when using pups with known fates. Including pups with unknown fates as deaths, percentage of pups surviving 12 months was > 48% among fostered pups, pups in recipient litters, and pups in control litters. Although survival to 12 months was similar among the groups, average life span was different with pups in control litters living 3.3 years, pups in recipient litters living 4.6 years, and fostered pups living 5.6 years. Of fostered pups surviving > 12 months in the wild, 9 animals whelped or sired 26 litters. Cross-fostering was successful at augmenting litter size for red wolves without any deleterious effects on recipient litters, illustrating fostering as a tool for increasing populations of endangered carnivores.

Download Full-text

Pyospermia and spermophagy in semen of the red wolf

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100147508 ◽

1993 ◽

Vol 51 ◽

pp. 332-333

Author(s):

James K. Koehler ◽

Carrol C. Platz ◽

Will Waddell ◽

Michael H. Jones

Keyword(s):

United States ◽

Endangered Species ◽

Artificial Insemination ◽

Captive Breeding ◽

Southeastern United States ◽

Electron Microscopic Examination ◽

Electron Microscopic ◽

Canis Rufus ◽

Red Wolf ◽

In The Wild

The red wolf (Canis rufus) inhabited the Southeastern United States until the early 1900's when aggressive hunting and a shrinking primitive habitat virtually eradicated the species. C. rufus was certified as an endangered species in 1967 and was essentially extinct in the wild by 1980. About 200 animals are preserved in zoos and captive breeding facilities where efforts are underway to increase the stock. Since a shrinking gene pool and captive stress may reduce reproductive vigor, we undertook an electron microscopic examination of red wolf semen used for artificial insemination at the Graham, WA breeding facility of the Point Defiance Zoo.Animals were anesthetized with 175 mg. Telazol, IM before electroejaculation using a rectal probe Semen was washed in PBS prior to fixation in 1.25% glutaraldehyde in 0.1 M cacodylate, post fixed in OsO4, dehydrated in alcohol and propylene oxide and embedded in Epon 812. Some samples were incubated in capacitation or maintenance media for several hours before fixation as above.

Download Full-text

Effects of anthropogenic mortality on Critically Endangered red wolf Canis rufus breeding pairs: implications for red wolf recovery

Oryx ◽

10.1017/s0030605315000770 ◽

2015 ◽

Vol 51 (1) ◽

pp. 174-181 ◽

Cited By ~ 14

Author(s):

Joseph W. Hinton ◽

Kristin E. Brzeski ◽

David R. Rabon ◽

Michael J. Chamberlain

Keyword(s):

North Carolina ◽

Critically Endangered ◽

Population Declines ◽

Canis Rufus ◽

Red Wolf ◽

Management Actions ◽

Control Programmes ◽

Negative Effect ◽

Eastern North Carolina ◽

Red Wolves

AbstractFollowing precipitous population declines as a result of intensive hunting and 20th century predator-control programmes, hybridization of the Critically Endangered red wolf Canis rufus with coyotes Canis latrans posed a significant challenge for red wolf recovery efforts. Anthropogenic mortality and hybridization continue to pose challenges; the increasing number of wolf deaths caused by humans has limited wolf population growth, facilitated the encroachment of coyotes into eastern North Carolina, and affected the formation and disbandment of breeding pairs. We assessed the effects of anthropogenic mortality on Canis breeding units during a 22-year period (1991–2013). Our results show that deaths caused by people accounted for 40.6% of breeding pair disbandment, and gunshots were the primary cause of mortality. Red wolves replaced congeneric breeding pairs > 75% of the time when pairs disbanded under natural conditions or as a result of management actions. Since the mid 2000s anthropogenic mortality has caused annual preservation rates of red wolf breeding pairs to decline by 34%, and replacement of Canis breeders by red wolves to decline by 30%. Our results demonstrate that human-caused mortality, specifically by gunshots, had a strong negative effect on the longevity of red wolf pairs, which may benefit coyotes indirectly by removing their primary competitor. Coyotes are exacerbating the decline of red wolves by pair-bonding with resident wolves whose mates have been killed.

Download Full-text

Reviving ghost alleles: Genetically admixed coyotes along the American Gulf Coast are critical for saving the endangered red wolf

10.1101/2021.12.18.473316 ◽

2021 ◽

Author(s):

Bridgett vonHoldt ◽

Joseph Hinton ◽

Amy Shutt ◽

Jennifer Adams ◽

Lisette Waits ◽

...

Keyword(s):

Endangered Species ◽

Captive Breeding ◽

Gulf Coast ◽

Breeding Population ◽

New Paradigm ◽

Species Persistence ◽

Red Wolf ◽

Captive Breeding Program ◽

Innovative Solutions ◽

Red Wolves

The last red wolves were captured along the Gulf Coast in 1980, where they hybridized with coyote, to establish the captive breeding population. However, red wolf ancestry persists in local coyotes and could be leveraged by genomic innovations to support species persistence. We assessed genomic ancestry and morphology of coyotes in southwestern Louisiana, and find they carried 38-62% red wolf ancestry acquired in the last 30 years, which is enriched on land with minimal coyote hunting. These coyotes were also similar in ancestry to canids captured in the 1970s that initiated the red wolf captive breeding program. Further, we reported that coyotes with higher red wolf ancestry are larger in size. Our findings evidence the importance of hybrids as a reservoir of endangered species ancestry for contemporary conservation efforts. Admixed genomes are at the forefront of innovative solutions, with red wolf survival a prime candidate for this new paradigm.

Download Full-text

α1-Antitrypsin polymorphism and systematics of eastern North American wolves

Canadian Journal of Zoology ◽

10.1139/z02-066 ◽

2002 ◽

Vol 80 (5) ◽

pp. 961-963 ◽

Cited By ~ 12

Author(s):

L David Mech ◽

Nicholas E Federoff

Keyword(s):

North American ◽

Canis Lupus ◽

Canis Latrans ◽

Western Canada ◽

Gray Wolf ◽

Canis Rufus ◽

Red Wolf ◽

Relationship Of ◽

The Relationship ◽

Red Wolves

We used data on the polymorphic status of α1-antitrypsin (α1AT) to study the relationship of Minnesota wolves to the gray wolf (Canis lupus), which was thought to have evolved in Eurasia, and to red wolves (Canis rufus) and coyotes (Canis latrans), which putatively evolved in North America. Recent evidence had indicated that Minnesota wolves might be more closely related to red wolves and coyotes. Samples from wild-caught Minnesota wolves and from captive wolves, at least some of which originated in Alaska and western Canada, were similarly polymorphic for α1AT, whereas coyote and red wolf samples were all monomorphic. Our findings, in conjunction with earlier results, are consistent with the Minnesota wolf being a gray wolf of Eurasian origin or possibly a hybrid between the gray wolf of Eurasian origin and the proposed North American wolf.

Download Full-text

The Challenges of Red Wolf Conservation and the Fate of an Endangered Species Recovery Program

Conservation Letters ◽

10.1111/conl.12157 ◽

2015 ◽

Vol 8 (5) ◽

pp. 338-344 ◽

Cited By ~ 9

Author(s):

Dennis L. Murray ◽

Guillaume Bastille-Rousseau ◽

Jennifer R. Adams ◽

Lisette P. Waits

Keyword(s):

Endangered Species ◽

Species Recovery ◽

Red Wolf ◽

Recovery Program

Download Full-text

Wild red wolf Canis rufus poaching risk

10.1101/2020.12.08.416032 ◽

2020 ◽

Author(s):

Suzanne W. Agan ◽

Adrian Treves ◽

Lisabeth Willey

Keyword(s):

North Carolina ◽

Causes Of Death ◽

Hunting Season ◽

Canis Rufus ◽

Red Wolf ◽

In The Wild ◽

Endangered Population ◽

Red Wolves ◽

Mean Time ◽

Future Population

AbstractThe reintroduced red wolf population in northeastern North Carolina declined to 7 known wolves by October 2020. Poaching (illegal killing) is the major component of verified anthropogenic mortality in this and many other carnivore populations, but it is still not well understood. Poaching is often underestimated, partly as a result of cryptic poaching, when poachers conceal evidence. Cryptic poaching inhibits our understanding of the causes and consequences of anthropogenic mortality which is important to conservation as it can inform us about future population patterns within changing political and human landscapes. We estimate risk for marked adult red wolves of 5 causes of death (COD: legal, nonhuman, unknown, vehicle and poached) and disappearance, describe variation in COD in relation to hunting season, and compare time to disappearance or death. We include unknown fates in our risk estimates. We found that anthropogenic COD accounted for 0.724 – 0.787, including cryptic and reported poaching estimated at 0.510 – 0.635 of 508 marked animals. Risk of poaching and disappearance was significantly higher during hunting season. Mean time from collaring until nonhuman COD averaged 376 days longer than time until reported poached and 642 days longer than time until disappearance. Our estimates of risk differed from prior published estimates, as expected by accounting for unknown fates explicitly. We quantify the effects on risk for three scenarios for disappearances, which span conservative to most likely COD. Implementing proven practices that prevent poaching or hasten successful reintroduction may reverse the decline to extinction in the wild of this critically endangered population. Our findings add to a growing literature on endangered species protections and enhancing the science used to measure poaching worldwide.

Download Full-text

Rediscovery of Red Wolf Ghost Alleles in a Canid Population Along the American Gulf Coast

Genes ◽

10.3390/genes9120618 ◽

2018 ◽

Vol 9 (12) ◽

pp. 618 ◽

Cited By ~ 4

Author(s):

Elizabeth Heppenheimer ◽

Kristin Brzeski ◽

Ron Wooten ◽

William Waddell ◽

Linda Rutledge ◽

...

Keyword(s):

North Carolina ◽

Gulf Coast ◽

Nucleotide Polymorphisms ◽

Conservation Action ◽

Single Nucleotide ◽

Red Wolf ◽

Reintroduced Population ◽

Coastal Louisiana ◽

Red Wolves ◽

Bayesian Cluster

Rediscovering species once thought to be extinct or on the edge of extinction is rare. Red wolves have been extinct along the American Gulf Coast since 1980, with their last populations found in coastal Louisiana and Texas. We report the rediscovery of red wolf ghost alleles in a canid population on Galveston Island, Texas. We analyzed over 7000 single nucleotide polymorphisms (SNPs) in 60 canid representatives from all legally recognized North American Canis species and two phenotypically ambiguous canids from Galveston Island. We found notably high Bayesian cluster assignments of the Galveston canids to captive red wolves with extensive sharing of red wolf private alleles. Today, the only known extant wild red wolves persist in a reintroduced population in North Carolina, which is dwindling amongst political and taxonomic controversy. Our rediscovery of red wolf ancestry after almost 40 years introduces both positive opportunities for additional conservation action and difficult policy challenges.

Download Full-text