skip to main content

Explore Research Products in the NSF-PAR

  • NSF Public Access
  • Search Results
  • Coalescence modeling of intrainfection Bacillus anthracis populations allows estimation of infection parameters in wild populations
Title: Coalescence modeling of intrainfection Bacillus anthracis populations allows estimation of infection parameters in wild populations
Bacillus anthracis , the etiological agent of anthrax, is a well-established model organism. For B. anthracis and most other infectious diseases, knowledge regarding transmission and infection parameters in natural systems, in large part, comprises data gathered from closely controlled laboratory experiments. Fatal, natural anthrax infections transmit the bacterium through new host−pathogen contacts at carcass sites, which can occur years after death of the previous host. For the period between contact and death, all of our knowledge is based upon experimental data from domestic livestock and laboratory animals. Here we use a noninvasive method to explore the dynamics of anthrax infections, by evaluating the terminal diversity of B. anthracis in anthrax carcasses. We present an application of population genetics theory, specifically, coalescence modeling, to intrainfection populations of B. anthracis to derive estimates for the duration of the acute phase of the infection and effective population size converted to the number of colony-forming units establishing infection in wild plains zebra ( Equus quagga ). Founding populations are small, a few colony-forming units, and infections are rapid, lasting roughly between 1 d and 3 d in the wild. Our results closely reflect experimental data, showing that small founding populations progress acutely, killing the host within days. We believe this method is amendable to other bacterial diseases from wild, domestic, and human systems.  more » « less
Award ID(s):
1816161 1103054
NSF-PAR ID:
10174143
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
117
Issue:
8
ISSN:
0027-8424
Page Range / eLocation ID:
4273 to 4280
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ( , Parasites & Vectors)
    Abstract

    Domestic dogs are susceptible to numerous vector-borne pathogens that are of significant importance for their health. In addition to being of veterinary importance, many of these pathogens are zoonotic and thus may pose a risk to human health. In the USA, owned dogs are commonly screened for exposure to or infection with several canine vector-borne pathogens. Although the screening data are widely available to show areas where infections are being diagnosed, testing of owned dogs is expected to underestimate the actual prevalence in dogs that have no access to veterinary care. The goal of this study was to measure the association between the widely available data from a perceived low-risk population with temporally and spatially collected data from shelter-housed dog populations. These data were then used to extrapolate the prevalence in dogs that generally lack veterinary care. The focus pathogens includedDirofilaria immitis,Ehrlichiaspp.,Anaplasmaspp., andBorrelia burgdorferi.There was a linear association between the prevalence of selected vector-borne pathogens in shelter-housed and owned dog populations and, generally, the data suggested that prevalence of heartworm (D. immitis) infection and seroprevalence ofEhrlichiaspp. andB. burgdorferiare higher in shelter-housed dogs, regardless of their location, compared with the owned population. The seroprevalence ofAnaplasmaspp. was predicted to be higher in areas that have very low to low seroprevalence, but unexpectedly, in areas of higher seroprevalence within the owned population, the seroprevalence was expected to be lower in the shelter-housed dog population. If shelters and veterinarians make decisions to not screen dogs based on the known seroprevalence of the owned group, they are likely underestimating the risk of exposure. This is especially true for heartworm. With this new estimate of the seroprevalence in shelter-housed dogs throughout the USA, shelters and veterinarians can make evidence-based informed decisions on whether testing and screening for these pathogens is appropriate for their local dog population. This work represents an important step in understanding the relationships in the seroprevalences of vector-borne pathogens between shelter-housed and owned dogs, and provides valuable data on the risk of vector-borne diseases in dogs.

    Graphical abstract

     
    more » « less
  2. ( , mSystems)
    ABSTRACT A central challenge in the fields of evolutionary immunology and disease ecology is to understand the causes and consequences of natural variation in host susceptibility to infectious diseases. As hosts progress from birth to death in the wild, they are exposed to a wide variety of microorganisms that influence their physical condition, immune system maturation, and susceptibility to concurrent and future infection. Thus, multiple exposures to the same or different microbes can be important environmental drivers of host immunological variation and immune priming. In this perspective, I discuss parasite infracommunity interactions and their imprint on host immunity in space and time. I further consider feedbacks from parasite community dynamics within individual hosts on the transmission of disease at higher levels of biological organization and highlight the promise of systems biology approaches, using flour beetles as an example, for studying the role of multiple infections on immunological variation in wild populations. 
    more » « less
  3. ; ; ; ( , Journal of Animal Ecology)
    Abstract

    World‐wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease‐induced mortality is likely even greater, but remains notoriously difficult to estimate—especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature.

    Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population‐ and landscape‐level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species.

    We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations.

    Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population‐level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape.

    The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite‐induced mortality can be applied to other host–parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts.

     
    more » « less
  4. ; ; ; ; ; ; ; ( , Ecology and Evolution)
    Abstract

    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.

     
    more » « less
  5. ; ; ; ; ; ; ; ; ; ; et al ( , Frontiers in Immunology)
    Exposure and immunity to generalist pathogens differ among host species and vary across spatial scales. Anthrax, caused by a multi-host bacterial pathogen, Bacillus anthracis , is enzootic in Kruger National Park (KNP), South Africa and Etosha National Park (ENP), Namibia. These parks share many of the same potential host species, yet the main anthrax host in one (greater kudu ( Tragelaphus strepsiceros ) in KNP and plains zebra ( Equus quagga ) in ENP) is only a minor host in the other. We investigated species and spatial patterns in anthrax mortalities, B. anthracis exposure, and the ability to neutralize the anthrax lethal toxin to determine if observed host mortality differences between locations could be attributed to population-level variation in pathogen exposure and/or immune response. Using serum collected from zebra and kudu in high and low incidence areas of each park (18- 20 samples/species/area), we estimated pathogen exposure from anti-protective antigen (PA) antibody response using enzyme-linked immunosorbent assay (ELISA) and lethal toxin neutralization with a toxin neutralization assay (TNA). Serological evidence of pathogen exposure followed mortality patterns within each system (kudus: 95% positive in KNP versus 40% in ENP; zebras: 83% positive in ENP versus 63% in KNP). Animals in the high-incidence area of KNP had higher anti-PA responses than those in the low-incidence area, but there were no significant differences in exposure by area within ENP. Toxin neutralizing ability was higher for host populations with lower exposure prevalence, i.e., higher in ENP kudus and KNP zebras than their conspecifics in the other park. These results indicate that host species differ in their exposure to and adaptive immunity against B. anthracis in the two parks. These patterns may be due to environmental differences such as vegetation, rainfall patterns, landscape or forage availability between these systems and their interplay with host behavior (foraging or other risky behaviors), resulting in differences in exposure frequency and dose, and hence immune response. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email