Equal contributions of feline immunodeficiency virus and coinfections to morbidity in African lions

Feline immunodeficiency virus (FIV) is a pathogenic lentivirus related to human and simian immunodeficiency viruses that has been associated with AIDS-like pathologies in domestic and wild cats, as well as in hyenas. Despite known pathologies, progressive immunosuppression and ill health effects driven by these lentiviruses in association with other secondary infections remain understudied in free-ranging species. Here, the role of coinfections by gastrointestinal parasites and tick-borne hemoparasites for FIV disease progression was explored in 195 free-ranging African lions (Panthera leo) living in Kruger National Park (KNP), South Africa. Using statistical methodology, we evaluated the effects of FIV on a range of health indicators to explore how direct and indirect effects of FIV and associated coinfections align to determine lion health outcomes. Findings show direct negative effects of FIV on host immunity and nutritional status, and exacerbation of aggressive behaviors, conditions which may increase exposure/susceptibility to other secondary infections. When taken together, the contribution of coinfecting parasites to morbidity in lions is of similar magnitude as direct effects of FIV infection alone, suggesting that the particular coinfection assemblage may play a role in mediating disease progression within natural lion populations

Hidden Consequences of Living in a Wormy World: Nematode‐Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co-occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T-helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune-mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown.We used cross-sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free-ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode-induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild

Serum biochemistry panels in African buffalo: Defining reference intervals and assessing variability across season, age and sex

Serum biochemical parameters can be utilized to evaluate the physiological status of an animal, and relate it to the animal’s health. In order to accurately interpret individual animal biochemical results, species-specific reference intervals (RI) must be established. Reference intervals for biochemical parameters differ between species, and physiological differences including reproductive status, nutritional resource availability, disease status, and age affect parameters within the same species. The objectives of this study were to (1) establish RI for biochemical parameters in managed African buffalo (Syncerus caffer), (2) assess the effects of age, sex, pregnancy, and season on serum biochemistry values, and (3) compare serum biochemistry values from a managed herd to a free-ranging buffalo herd and to values previously published for captive (zoo) buffalo. Season profoundly affected all biochemistry parameters, possibly due to changes in nutrition and disease exposure. Age also affected all biochemical parameters except gamma glutamyl transferase and magnesium, consistent with patterns seen in cattle. Sex and reproductive status had no detectable effects on the parameters that were measured. The biochemical profiles of managed buffalo were distinct from those observed in the free-ranging herd and captive buffalo. Biochemical differences between buffalo from captive, managed, and free-ranging populations may be related to nutritional restriction or lack of predation in the context of management or captivity. The reference intervals provided in this study, in addition to the seasonal and age-related patterns observed, provide a foundation for health investigations that may inform management strategies in this ecologically and economically important species

Does intensive forest management affect innate immunity of wild deer mice (Peromyscus maniculatus)?

To examine the influence of forest management on wildlife immunity, the innate immune system of wild deer mice (Peromyscus maniculatus) inhabiting forest plots of different management intensities in the Oregon coast range was measured by bactericidal assay. Bactericidal activity was compared across three management levels, including 40-50 year old forest stands without recent intervention, areas clear-cut within the past 12 months but not managed further, and finally, plots clear-cut within the past 12 months that were also intensively treated with herbicides. Our results show a trend whereby bactericidal activity increases with management intensity, indicating that innate immunity in animals inhabiting more disturbed environments is better or upregulated. Although unexpected, this pattern may result from stress associated with poor habitat quality and could ultimately could change the dynamics of pathogens harbored in these communities

Rainfall-driven sex-ratio genes in African buffalo suggested by correlations between Y-chromosomal haplotype frequencies and foetal sex ratio

Background - The Y-chromosomal diversity in the African buffalo (Syncerus caffer) population of Kruger National Park (KNP) is characterized by rainfall-driven haplotype frequency shifts between year cohorts. Stable Y-chromosomal polymorphism is difficult to reconcile with haplotype frequency variations without assuming frequency-dependent selection or specific interactions in the population dynamics of X- and Y-chromosomal genes, since otherwise the fittest haplotype would inevitably sweep to fixation. Stable Y-chromosomal polymorphism due one of these factors only seems possible when there are Y-chromosomal distorters of an equal sex ratio, which act by negatively affecting X-gametes, or Y-chromosomal suppressors of a female-biased sex ratio. These sex-ratio (SR) genes modify (suppress) gamete transmission in their own favour at a fitness cost, allowing for stable polymorphism. Results - Here we show temporal correlations between Y-chromosomal haplotype frequencies and foetal sex ratios in the KNP buffalo population, suggesting SR genes. Frequencies varied by a factor of five; too high to be alternatively explained by Y-chromosomal effects on pregnancy loss. Sex ratios were male-biased during wet and female-biased during dry periods (male proportion: 0.47-0.53), seasonally and annually. Both wet and dry periods were associated with a specific haplotype indicating a SR distorter and SR suppressor, respectively. Conclusions - The distinctive properties suggested for explaining Y-chromosomal polymorphism in African buffalo may not be restricted to this species alone. SR genes may play a broader and largely overlooked role in mammalian sex-ratio variatio

Hidden Consequences of Living in a Wormy World:Nematode-Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co-occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T-helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune-mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown.We used cross-sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free-ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode-induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild

Evaluation of the Sensitivity and Specificity of an Enzyme-Linked Immunosorbent Assay for Diagnosing Brucellosis in African Buffalo (Syncerus caffer)

Brucellosis is a disease of veterinary and public health importance worldwide. In sub- Saharan Africa, where this disease has been detected in several free-ranging wildlife species, successful disease control may be dependent on accurate detection in wildlife reservoirs, including African buffalo (Syncerus caffer). This study estimates the sensitivity and specificity of a commercial enzyme-linked immunosorbent assay (IDEXX, Brucellosis Serum Ab Test) for brucellosis based on a dataset of 571 serum samples from 258 buffalo located within the Kruger National Park, South Africa. We defined a pseudo-gold standard test result as those buffalo that were consistently positive or negative on two additional serological tests, namely the rose bengal test (RBT) and the complement fixation test (CFT). The ELISA’s cut-off value was selected using receiver operating characteristics (ROC) analysis, the pseudo-gold standard, and a threshold criterion that maximizes the total sensitivity and specificity. Then, we estimated the sensitivity and specificity of all three tests using Bayesian inference and latent class analysis. We estimated the ELISA to have a sensitivity of 0.928 (95% BCI from 0.869-0.974) and specificity of 0.870 (95% BCI from 0.836-0.900). Compared to the ELISA, the RBT had a higher estimated sensitivity of 0.986 (95% BCI from 0.928- 0.999), and both the RBT and CFT had higher specificities, estimated to be 0.992 (95% BCI from 0.971 to 0.996) and 0.998 (95% BCI from 0.992 to 0.999), respectively. Therefore, this study shows that no single serological test perfectly diagnosed infection. However, after adjustment of cut-off values for South African conditions, the IDEXX Brucellosis Serum Ab Test may be a valuable additional screening test for brucellosis in Kruger National Park’s African buffalo.This is an author's peer-reviewed final manuscript, as accepted by the publisher. The published article is copyrighted by the Wildlife Disease Association and can be found at: http://www.jwildlifedis.org/,This research was approved by Kruger National Park’s Scientific Services committee and by Oregon State University and University of Georgia IACUC (Protocol numbers OSU: 3822; UGA: A201010-190-A1).Keywords: Bayesian, Sensitivity, Enzyme linked immunosorbent assay, Brucellosis, Latent data, African buffalo, Specificit

Context-dependent costs and benefits of tuberculosis resistance traits in a wild mammalian host

Disease acts as a powerful driver of evolution in natural host populations, yet individuals in a population often vary in their susceptibility to infection. Energetic trade-offs between immune and reproductive investment lead to the evolution of distinct life history strategies, driven by the relative fitness costs and benefits of resisting infection. However, examples quantifying the cost of resistance outside of the laboratory are rare. Here, we observe two distinct forms of resistance to bovine tuberculosis (bTB), an important zoonotic pathogen, in a free-ranging African buffalo (Syncerus caffer) population. We characterize these phenotypes as “infection resistance,” in which hosts delay or prevent infection, and “proliferation resistance,” in which the host limits the spread of lesions caused by the pathogen after infection has occurred. We found weak evidence that infection resistance to bTB may be heritable in this buffalo population (h2 = 0.10) and comes at the cost of reduced body condition and marginally reduced survival once infected, but also associates with an overall higher reproductive rate. Infection-resistant animals thus appear to follow a “fast” pace-of-life syndrome, in that they reproduce more quickly but die upon infection. In contrast, proliferation resistance had no apparent costs and was associated with measures of positive host health—such as having a higher body condition and reproductive rate. This study quantifies striking phenotypic variation in pathogen resistance and provides evidence for a link between life history variation and a disease resistance trait in a wild mammalian host population