Population connectivity patterns of genetic diversity, immune responses and exposure to infectious pneumonia in a metapopulation of desert bighorn sheep.

Habitat fragmentation is an important driver of biodiversity loss and can be remediated through management actions aimed at maintenance of natural connectivity in metapopulations. Connectivity may protect populations from infectious diseases by preserving immunogenetic diversity and disease resistance. However, connectivity could exacerbate the risk of infectious disease spread across vulnerable populations. We tracked the spread of a novel strain of Mycoplasma ovipneumoniae in a metapopulation of desert bighorn sheep Ovis canadensis nelsoni in the Mojave Desert to investigate how variation in connectivity among populations influenced disease outcomes. M. ovipneumoniae was detected throughout the metapopulation, indicating that the relative isolation of many of these populations did not protect them from pathogen invasion. However, we show that connectivity among bighorn sheep populations was correlated with higher immunogenetic diversity, a protective immune response and lower disease prevalence. Variation in protective immunity predicted infection risk in individual bighorn sheep and was associated with heterozygosity at genetic loci linked to adaptive and innate immune signalling. Together, these findings may indicate that population connectivity maintains immunogenetic diversity in bighorn sheep populations in this system and has direct effects on immune responses in individual bighorn sheep and their susceptibility to infection by a deadly pathogen. Our study suggests that the genetic benefits of population connectivity could outweigh the risk of infectious disease spread and supports conservation management that maintains natural connectivity in metapopulations.

Correction: Multiple innate antibacterial immune defense elements are correlated in diverse ungulate species.

[This corrects the article DOI: 10.1371/journal.pone.0225579.].

Multiple innate antibacterial immune defense elements are correlated in diverse ungulate species.

In this study, we aimed to evaluate to what extent different assays of innate immunity reveal similar patterns of variation across ungulate species. We compared several measures of innate antibacterial immune function across seven different ungulate species using blood samples obtained from captive animals maintained in a zoological park. We measured mRNA expression of two receptors involved in innate pathogen detection, toll-like receptors 2 and 5 (TLR2 and 5), the bactericidal capacity of plasma, as well as the number of neutrophils and lymphocytes. Species examined included aoudad (Ammotragus lervia), American bison (Bison bison bison), yak (Bos grunniens), Roosevelt elk (Cervus canadensis roosevelti), fallow deer (Dama dama), sika deer (Cervus nippon), and Damara zebra (Equus quagga burchellii). Innate immunity varied among ungulate species. However, we detected strong, positive correlations between the different measures of innate immunity-specifically, TLR2 and TLR5 were correlated, and the neutrophil to lymphocyte ratio was positively associated with TLR2, TLR5, and bacterial killing ability. Our results suggest that ecoimmunological study results may be quite robust to the choice of assays, at least for antibacterial innate immunity; and that, despite the complexity of the immune system, important sources of variation in immunity in natural populations may be discoverable with comparatively simple tools.

Detection of bacterial-reactive natural IgM antibodies in desert bighorn sheep populations.

Ecoimmunology is a burgeoning field of ecology which studies immune responses in wildlife by utilizing general immune assays such as the detection of natural antibody. Unlike adaptive antibodies, natural antibodies are important in innate immune responses and often recognized conserved epitopes present in pathogens. Here, we describe a procedure for measuring natural antibodies reactive to bacterial antigens that may be applicable to a variety of organisms. IgM from desert bighorn sheep plasma samples was tested for reactivity to outer membrane proteins from Vibrio coralliilyticus, a marine bacterium to which sheep would have not been exposed. Immunoblotting demonstrated bighorn sheep IgM could bind to a variety of bacterial cell envelope proteins while ELISA analysis allowed for rapid determination of natural antibody levels in hundreds of individual animals. Natural antibody levels were correlated with the ability of plasma to kill laboratory strains of E. coli bacteria. Finally, we demonstrate that natural antibody levels varied in two distinct populations of desert bighorn sheep. These data demonstrate a novel and specific measure of natural antibody function and show that this varies in ecologically relevant ways.