ABSTRACT
Owing to a complex history of host-parasite coevolution, lentiviruses exhibit a high degree of species specificity. Given the well-documented viral archeology of human immunodeficiency virus (HIV) emergence following human exposures to simian immunodeficiency virus (SIV), an understanding of processes that promote successful cross-species lentiviral transmissions is highly relevant. We previously reported natural cross-species transmission of a subtype of feline immunodeficiency virus, puma lentivirus A (PLVA), between bobcats (Lynx rufus) and mountain lions (Puma concolor) for a small number of animals in California and Florida. In this study, we investigate host-specific selection pressures, within-host viral fitness, and inter- versus intraspecies transmission patterns among a larger collection of PLV isolates from free-ranging bobcats and mountain lions. Analyses of proviral and viral RNA levels demonstrate that PLVA fitness is severely restricted in mountain lions compared to that in bobcats. We document evidence of diversifying selection in three of six PLVA genomes from mountain lions, but we did not detect selection among 20 PLVA isolates from bobcats. These findings support the hypothesis that PLVA is a bobcat-adapted virus which is less fit in mountain lions and under intense selection pressure in the novel host. Ancestral reconstruction of transmission events reveals that intraspecific PLVA transmission has occurred among panthers (Puma concolor coryi) in Florida following the initial cross-species infection from bobcats. In contrast, interspecific transmission from bobcats to mountain lions predominates in California. These findings document outcomes of cross-species lentiviral transmission events among felids that compare to the emergence of HIV from nonhuman primates.IMPORTANCE Cross-species transmission episodes can be singular, dead-end events or can result in viral replication and spread in the new species. The factors that determine which outcome will occur are complex, and the risk of new virus emergence is therefore difficult to predict. We used molecular techniques to evaluate the transmission, fitness, and adaptation of puma lentivirus A (PLVA) between bobcats and mountain lions in two geographic regions. Our findings illustrate that mountain lion exposure to PLVA is relatively common but does not routinely result in communicable infections in the new host. This is attributed to efficient species barriers that largely prevent lentiviral adaptation. However, the evolutionary capacity for lentiviruses to adapt to novel environments may ultimately overcome host restriction mechanisms over time and under certain ecological circumstances. This phenomenon provides a unique opportunity to examine cross-species transmission events leading to new lentiviral emergence.
Subject(s)
Cat Diseases/virology , Immunodeficiency Virus, Feline/physiology , Lynx/virology , Puma/virology , Animals , California/epidemiology , Cat Diseases/epidemiology , Cat Diseases/transmission , Cats , Female , Florida/epidemiology , Male , Phylogeny , Polymorphism, Genetic , Selection, Genetic , Species Specificity , Viral TropismABSTRACT
Mountain lions (Puma concolor) throughout North and South America are infected with puma lentivirus clade B (PLVB). A second, highly divergent lentiviral clade, PLVA, infects mountain lions in southern California and Florida. Bobcats (Lynx rufus) in these two geographic regions are also infected with PLVA, and to date, this is the only strain of lentivirus identified in bobcats. We sequenced full-length PLV genomes in order to characterize the molecular evolution of PLV in bobcats and mountain lions. Low sequence homology (88% average pairwise identity) and frequent recombination (1 recombination breakpoint per 3 isolates analyzed) were observed in both clades. Viral proteins have markedly different patterns of evolution; sequence homology and negative selection were highest in Gag and Pol and lowest in Vif and Env. A total of 1.7% of sites across the PLV genome evolve under positive selection, indicating that host-imposed selection pressure is an important force shaping PLV evolution. PLVA strains are highly spatially structured, reflecting the population dynamics of their primary host, the bobcat. In contrast, the phylogeography of PLVB reflects the highly mobile mountain lion, with diverse PLVB isolates cocirculating in some areas and genetically related viruses being present in populations separated by thousands of kilometers. We conclude that PLVA and PLVB are two different viral species with distinct feline hosts and evolutionary histories. Importance: An understanding of viral evolution in natural host populations is a fundamental goal of virology, molecular biology, and disease ecology. Here we provide a detailed analysis of puma lentivirus (PLV) evolution in two natural carnivore hosts, the bobcat and mountain lion. Our results illustrate that PLV evolution is a dynamic process that results from high rates of viral mutation/recombination and host-imposed selection pressure.
Subject(s)
Genome, Viral , Immunodeficiency Virus, Feline/isolation & purification , Lynx/virology , Puma/virology , RNA, Viral/genetics , Sequence Analysis, DNA , Animals , Cluster Analysis , Evolution, Molecular , Genetic Variation , Immunodeficiency Virus, Feline/classification , Immunodeficiency Virus, Feline/genetics , Molecular Sequence Data , North America , Phylogeography , Recombination, Genetic , Selection, Genetic , Viral Proteins/geneticsABSTRACT
Outbreaks of infectious disease represent serious threats to the viability of many vertebrate populations, but few studies have included quantitative evaluations of alternative approaches to the management of disease. The most prevalent management approach is monitoring for and rapid response to an epizootic. An alternative is vaccination of a subset of the free-living population (i.e., a "vaccinated core") such that some individuals are partially or fully immune in the event of an epizootic. We developed a simulation model describing epizootic dynamics, which we then embedded in a demographic simulation to assess these alternative approaches to managing rabies epizootics in the island fox (Urocyon littoralis), a species composed of only 6 small populations on the California Channel Islands. Although the monitor and respond approach was superior to the vaccinated-core approach for some transmission models and parameter values, this type of reactive management did not protect the population from rabies under many disease-transmission assumptions. In contrast, a logistically feasible program of prophylactic vaccination for part of the wild population yielded low extinction probabilities across all likely disease-transmission scenarios, even with recurrent disease introductions. Our use of a single metric of successful management-probability of extreme endangerment (i.e., quasi extinction)-to compare very different management approaches allowed an objective assessment of alternative strategies for controlling the threats posed by infectious disease outbreaks.
Subject(s)
Conservation of Natural Resources/methods , Disease Outbreaks/veterinary , Endangered Species , Foxes , Rabies Vaccines/administration & dosage , Rabies virus/physiology , Rabies/veterinary , Animals , California , Disease Outbreaks/prevention & control , Foxes/physiology , Models, Biological , Population Dynamics , Rabies/epidemiology , Rabies/prevention & controlABSTRACT
Artificial light at night (ALAN) is increasing in extent and intensity across the globe. It has been shown to interfere with animal sensory systems, orientation and distribution, with the potential to cause significant ecological impacts. We analysed the locations of 102 mountain lions (Puma concolor) in a light-polluted region in California. We modelled their distribution relative to environmental and human-disturbance variables, including upward radiance (nearby lights), zenith brightness (sky glow) and natural illumination from moonlight. We found that mountain lion probability of presence was highly related to upward radiance, that is, related to lights within approximately 500 m. Despite a general pattern of avoidance of locations with high upward radiance, there were large differences in degree of avoidance among individuals. The amount of light from artificial sky glow was not influential when included together with upward radiance in the models, and illumination from moonlight was not influential at all. Our results suggest that changes in visibility associated with lunar cycles and sky glow are less important for mountain lions in their selection of light landscapes than avoiding potential interactions with humans represented by the presence of nearby lights on the ground. This article is part of the theme issue 'Light pollution in complex ecological systems'.
Subject(s)
Puma , Animals , Humans , Lighting , Environmental Pollution , Ecosystem , EnvironmentABSTRACT
Small effective population sizes raise the probability of extinction by increasing the frequency of potentially deleterious alleles and reducing fitness. However, the extent to which cancers play a role in the fitness reduction of genetically depauperate wildlife populations is unknown. Santa Catalina island foxes (Urocyon littoralis catalinae) sampled in 2007-2008 have a high prevalence of ceruminous gland tumors, which was not detected in the population prior to a recent bottleneck caused by a canine distemper epidemic. The disease appears to be associated with inflammation from chronic ear mite (Otodectes) infections and secondary elevated levels of Staphyloccus pseudointermedius bacterial infections. However, no other environmental factors to date have been found to be associated with elevated cancer risk in this population. Here, we used whole genome sequencing of the case and control individuals from two islands to identify candidate loci associated with cancer based on genetic divergence, nucleotide diversity, allele frequency spectrum, and runs of homozygosity. We identified several candidate loci based on genomic signatures and putative gene functions, suggesting that cancer susceptibility in this population may be polygenic. Due to the efforts of a recovery program and weak fitness effects of late-onset disease, the population size has increased, which may allow selection to be more effective in removing these presumably slightly deleterious alleles. Long-term monitoring of the disease alleles, as well as overall genetic diversity, will provide crucial information for the long-term persistence of this threatened population.
Subject(s)
Foxes , Neoplasms , Animals , Animals, Wild , Foxes/genetics , Genetic Drift , Genomics , Neoplasms/genetics , Neoplasms/veterinaryABSTRACT
Plague seroprevalence was estimated in populations of pumas and bobcats in the western United States. High levels of exposure in plague-endemic regions indicate the need to consider the ecology and pathobiology of plague in nondomestic felid hosts to better understand the role of these species in disease persistence and transmission.
Subject(s)
Lynx/microbiology , Plague/transmission , Puma/microbiology , Yersinia pestis/isolation & purification , Animals , Antibodies, Bacterial/blood , Colorado , Disease Reservoirs , Humans , Seroepidemiologic Studies , Yersinia pestis/immunologyABSTRACT
Determining parameters that govern pathogen transmission (such as the force of infection, FOI), and pathogen impacts on morbidity and mortality, is exceptionally challenging for wildlife. Vital parameters can vary, for example across host populations, between sexes and within an individual's lifetime.Feline immunodeficiency virus (FIV) is a lentivirus affecting domestic and wild cat species, forming species-specific viral-host associations. FIV infection is common in populations of puma (Puma concolor), yet uncertainty remains over transmission parameters and the significance of FIV infection for puma mortality. In this study, the age-specific FOI of FIV in pumas was estimated from prevalence data, and the evidence for disease-associated mortality was assessed.We fitted candidate models to FIV prevalence data and adopted a maximum likelihood method to estimate parameter values in each model. The models with the best fit were determined to infer the most likely FOI curves. We applied this strategy for female and male pumas from California, Colorado, and Florida.When splitting the data by sex and area, our FOI modeling revealed no evidence of disease-associated mortality in any population. Both sex and location were found to influence the FOI, which was generally higher for male pumas than for females. For female pumas at all sites, and male pumas from California and Colorado, the FOI did not vary with puma age, implying FIV transmission can happen throughout life; this result supports the idea that transmission can occur from mothers to cubs and also throughout adult life. For Florida males, the FOI was a decreasing function of puma age, indicating an increased risk of infection in the early years, and a decreased risk at older ages.This research provides critical insight into pathogen transmission and impact in a secretive and solitary carnivore. Our findings shed light on the debate on whether FIV causes mortality in wild felids like puma, and our approach may be adopted for other diseases and species. The methodology we present can be used for identifying likely transmission routes of a pathogen and also estimating any disease-associated mortality, both of which can be difficult to establish for wildlife diseases in particular.
ABSTRACT
Feline foamy virus (FFV) is a retrovirus that has been detected in multiple feline species, including domestic cats (Felis catus) and pumas (Puma concolor). FFV results in persistent infection but is generally thought to be apathogenic. Sero-prevalence in domestic cat populations has been documented in several countries, but the extent of viral infections in nondomestic felids has not been reported. In this study, we screened sera from 348 individual pumas from Colorado, Southern California and Florida for FFV exposure by assessing sero-reactivity using an FFV anti-Gag ELISA. We documented a sero-prevalence of 78.6% across all sampled subpopulations, representing 69.1% in Southern California, 77.3% in Colorado, and 83.5% in Florida. Age was a significant risk factor for FFV infection when analyzing the combined populations. This high prevalence in geographically distinct populations reveals widespread exposure of puma to FFV and suggests efficient shedding and transmission in wild populations.
Subject(s)
Cat Diseases/epidemiology , Puma/virology , Retroviridae Infections/veterinary , Spumavirus/isolation & purification , Animals , Antibodies, Viral/blood , California/epidemiology , Cat Diseases/virology , Cats , Colorado/epidemiology , Female , Florida/epidemiology , Male , Prevalence , Retroviridae Infections/epidemiology , Seroepidemiologic Studies , Species SpecificityABSTRACT
We report two complete foamy retrovirus (FV) genomes isolated from Puma concolor, a large cat native to the Americas. Due to high overall genetic relatedness to known feline foamy viruses (FFVs), we propose the name Puma concolor FFV (FFVPc). The data confirm that felines are infected with distinct but closely related FVs.
ABSTRACT
Canine peritoneal larval cestodiasis (CPLC) is a poorly understood disease of dogs caused by asexual multiplication of larval Mesocestoides spp. tapeworms. In this study, we examined the descriptive statistics and survival characteristics of 60 dogs diagnosed with CPLC from 1989 to 2009. Clinically affected dogs presented with ascites (60%), anorexia/weight loss (42%), vomiting (23%), diarrhea (9%) and tachypnea (9%), while subclinical infections (22%) were incidentally detected, typically during ovariohysterectomy or neuter. Survival at 6 months and 1 year post-diagnosis were 72.3% and 60.5%, respectively, and survival was not affected by sex or age. Using Cox proportional hazard analyses, we determined that the most significant factors influencing survival were the severity of clinical signs at the time of diagnosis and application of an aggressive treatment strategy after diagnosis. Dogs that were not treated aggressively were >5 times more likely to die than dogs that were treated with a combination of surgery/lavage and high doses of fenbendazole.
Subject(s)
Cestode Infections/veterinary , Dog Diseases/parasitology , Mesocestoides , Peritoneal Diseases/veterinary , Animals , Anthelmintics/therapeutic use , Cestode Infections/mortality , Cestode Infections/therapy , Dog Diseases/mortality , Dog Diseases/therapy , Dogs , Female , Fenbendazole/therapeutic use , Logistic Models , Male , Peritoneal Diseases/mortality , Peritoneal Diseases/parasitology , Peritoneal Diseases/therapy , Praziquantel/therapeutic use , Retrospective Studies , Survival AnalysisABSTRACT
The devastating effect of West Nile virus (WNV) on the avifauna of North America has led zoo managers and conservationists to attempt to protect vulnerable species through vaccination. The Island Scrub-Jay (Aphelocoma insularis) is one such species, being a corvid with a highly restricted insular range. Herein, we used congeneric Western Scrub-Jays (Aphelocoma californica) to test the efficacy of three WNV vaccines in protecting jays from an experimental challenge with WNV: (1) the Fort Dodge West Nile-Innovator(®) DNA equine vaccine, (2) an experimental DNA plasmid vaccine, pCBWN, and (3) the Merial Recombitek(®) equine vaccine. Vaccine efficacy after challenge was compared with naïve and nonvaccinated positive controls and a group of naturally immune jays. Overall, vaccination lowered peak viremia compared with nonvaccinated positive controls, but some WNV-related pathology persisted and the viremia was sufficient to possibly infect susceptible vector mosquitoes. The Fort Dodge West Nile-Innovator DNA equine vaccine and the pCBWN vaccine provided humoral immune priming and limited side effects. Five of the six birds vaccinated with the Merial Recombitek vaccine, including a vaccinated, non-WNV challenged control, developed extensive necrotic lesions in the pectoral muscle at the vaccine inoculation sites, which were attributed to the Merial vaccine. In light of the well-documented devastating effects of high morbidity and mortality associated with WNV infection in corvids, vaccination of Island Scrub-Jays with either the Fort Dodge West Nile-Innovator DNA vaccine or the pCBWN vaccine may increase the numbers of birds that would survive an epizootic should WNV become established on Santa Cruz Island.
Subject(s)
Bird Diseases/prevention & control , Bird Diseases/virology , Vaccination/methods , West Nile Fever/prevention & control , West Nile Virus Vaccines/standards , West Nile virus/immunology , Animals , Antibodies, Viral/blood , Autopsy , Bird Diseases/pathology , Birds , California , Disease Models, Animal , Immunohistochemistry , Vaccination/standards , West Nile Fever/pathology , West Nile Virus Vaccines/immunologyABSTRACT
Transmission of West Nile virus (WNV) on mainland California poses an ongoing threat to the island scrub-jay (ISSJ, Aphelocoma insularis), a species that occurs only on Santa Cruz Island, California, and whose total population numbers <5000. Our report describes the surveillance and management efforts conducted since 2006 that are designed to understand and mitigate for the consequences of WNV introduction into the ISSJ population. We suspect that WNV would most likely be introduced to the island via the movement of infected birds from the mainland. However, antibody testing of >750 migrating and resident birds on the island from 2006 to 2009 indicated that WNV had not become established by the end of 2009. Several species of competent mosquito vectors were collected at very low abundance on the island, including the important mainland vectors Culex tarsalis and Culex quinquefasciatus. However, the island was generally cooler than areas of mainland California that experienced intense WNV transmission, and these lower temperatures may have reduced the likelihood of WNV becoming established because they do not support efficient virus replication in mosquitoes. A vaccination program was initiated in 2008 to create a rescue population of ISSJ that would be more likely to survive a catastrophic outbreak. To further that goal, we recommend managers vaccinate >100 ISSJ each year as part of ongoing research and monitoring efforts.