skip to main content

Title: Reactivation of latent infections with migration shapes population-level disease dynamics
Annual migration is common across animal taxa and can dramatically shape the spatial and temporal patterns of infectious disease. Although migration can decrease infection prevalence in some contexts, these energetically costly long-distance movements can also have immunosuppressive effects that may interact with transmission processes in complex ways. Here, we develop a mechanistic model for the reactivation of latent infections driven by physiological changes or energetic costs associated with migration (i.e. ‘migratory relapse’) and its effects on disease dynamics. We determine conditions under which migratory relapse can amplify or reduce infection prevalence across pathogen and host traits (e.g. infectious periods, virulence, overwinter survival, timing of relapse) and transmission phenologies. We show that relapse at either the start or end of migration can dramatically increase prevalence across the annual cycle and may be crucial for maintaining pathogens with low transmissibility and short infectious periods in migratory populations. Conversely, relapse at the start of migration can reduce the prevalence of highly virulent pathogens by amplifying culling of infected hosts during costly migration, especially for highly transmissible pathogens and those transmitted during migration or the breeding season. Our study provides a mechanistic foundation for understanding the spatio-temporal patterns of relapsing infections in migratory hosts, more » with implications for zoonotic surveillance and understanding how infection patterns will respond to shifts in migratory propensity associated with environmental change. Further, our work suggests incorporating within-host processes into population-level models of pathogen transmission may be crucial for reconciling the range of migration–infection relationships observed across migratory species. « less
; ;
Award ID(s):
1911925 1754392
Publication Date:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Page Range or eLocation-ID:
Sponsoring Org:
National Science Foundation
More Like this
  1. Co-infections of hosts by multiple pathogen species are ubiquitous, but predicting their impact on disease remains challenging. Interactions between co-infecting pathogens within hosts can alter pathogen transmission, with the impact on transmission typically dependent on the relative arrival order of pathogens within hosts (within-host priority effects). However, it is unclear how these within-host priority effects influence multi-pathogen epidemics, particularly when the arrival order of pathogens at the host-population scale varies. Here, we combined models and experiments with zooplankton and their naturally co-occurring fungal and bacterial pathogens to examine how within-host priority effects influence multi-pathogen epidemics. Epidemiological models parametrized with within-host priority effects measured at the single-host scale predicted that advancing the start date of bacterial epidemics relative to fungal epidemics would decrease the mean bacterial prevalence in a multi-pathogen setting, while models without within-host priority effects predicted the opposite effect. We tested these predictions with experimental multi-pathogen epidemics. Empirical dynamics matched predictions from the model including within-host priority effects, providing evidence that within-host priority effects influenced epidemic dynamics. Overall, within-host priority effects may be a key element of predicting multi-pathogen epidemic dynamics in the future, particularly as shifting disease phenology alters the order of infection within hosts.
  2. Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans , the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experiencedmore »severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.« less
  3. Abstract

    Host competence, or how well an individual transmits pathogens, varies substantially within and among animal populations. As this variation can alter the course of epidemics and epizootics, revealing its underlying causes will help predict and control the spread of disease. One host trait that could drive heterogeneity in competence is host tolerance, which minimizes fitness losses during infection without decreasing pathogen load. In many cases, tolerance should increase competence by extending infectious periods and enabling behaviors that facilitate contact among hosts. However, we argue that the links between tolerance and competence are more varied. Specifically, the different physiological and behavioral mechanisms by which hosts achieve tolerance should have a range of effects on competence, enhancing the ability to transmit pathogens in some circumstances and impeding it in others. Because tissue-based pathology (damage) that reduces host fitness is often critical for pathogen transmission, we focus on two mechanisms that can underlie tolerance at the tissue level: damage-avoidance and damage-repair. As damage-avoidance reduces transmission-enhancing pathology, this mechanism is likely to decrease host competence and pathogen transmission. In contrast, damage-repair does not prevent transmission-relevant pathology from occurring. Rather, damage-repair provides new, healthy tissues that pathogens can exploit, likely extending the infectious periodmore »and increasing host competence. We explore these concepts through graphical models and present three disease systems in which damage-avoidance and damage-repair alter host competence in the predicted directions. Finally, we suggest that by incorporating these links, future theoretical studies could provide new insights into infectious disease dynamics and host–pathogen coevolution.

    « less
  4. Transmission is the fundamental process whereby pathogens infect their hosts and spread through populations, and can be characterized using mathematical functions. The functional form of transmission for emerging pathogens can determine pathogen impacts on host populations and can inform the efficacy of disease management strategies. By directly measuring transmission between infected and susceptible adult eastern newts (Notophthalmus viridescens) in aquatic mesocosms, we identified the most plausible transmission function for the emerging amphibian fungal pathogen Batrachochytrium salamandrivorans (Bsal). Although we considered a range of possible transmission functions, we found that Bsal transmission was best explained by pure frequency dependence. We observed that >90% of susceptible newts became infected within 17 days post-exposure to an infected newt across a range of host densities and initial infection prevalence treatments. Under these conditions, we estimated R_0 = 4.9 for Bsal in an eastern newt population. Our results suggest that Bsal has the capability of driving eastern newt populations to extinction and that managing host density may not be an effective management strategy. Intervention strategies that prevent Bsal introduction or increase host resistance or tolerance to infection may be more effective. Our results add to the growing empirical evidence that transmission of wildlife pathogens canmore »saturate and be functionally frequency-dependent.« less
  5. Reguera, Gemma (Ed.)
    ABSTRACT Mucosal defenses are crucial in animals for protection against pathogens and predators. Host defense peptides (antimicrobial peptides, AMPs) as well as skin-associated microbes are key components of mucosal immunity, particularly in amphibians. We integrate microbiology, molecular biology, network-thinking, and proteomics to understand how host and microbially derived products on amphibian skin (referred to as the mucosome) serve as pathogen defenses. We studied defense mechanisms against chytrid pathogens, Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), in four salamander species with different Batrachochytrium susceptibilities. Bd infection was quantified using qPCR, mucosome function (i.e., ability to kill Bd or Bsal zoospores in vitro ), skin bacterial communities using 16S rRNA gene amplicon sequencing, and the role of Bd-inhibitory bacteria in microbial networks across all species. We explored the presence of candidate-AMPs in eastern newts and red-backed salamanders. Eastern newts had the highest Bd prevalence and mucosome function, while red-back salamanders had the lowest Bd prevalence and mucosome function, and two-lined salamanders and seal salamanders were intermediates. Salamanders with highest Bd infection intensity showed greater mucosome function. Bd infection prevalence significantly decreased as putative Bd-inhibitory bacterial richness and relative abundance increased on hosts. In co-occurrence networks, some putative Bd-inhibitory bacteria were found asmore »hub-taxa, with red-backs having the highest proportion of protective hubs and positive associations related to putative Bd-inhibitory hub bacteria. We found more AMP candidates on salamanders with lower Bd susceptibility. These findings suggest that salamanders possess distinct innate mechanisms that affect chytrid fungi. IMPORTANCE How host mucosal defenses interact, and influence disease outcome is critical in understanding host defenses against pathogens. A more detailed understanding is needed of the interactions between the host and the functioning of its mucosal defenses in pathogen defense. This study investigates the variability of chytrid susceptibility in salamanders and the innate defenses each species possesses to mediate pathogens, thus advancing the knowledge toward a deeper understanding of the microbial ecology of skin-associated bacteria and contributing to the development of bioaugmentation strategies to mediate pathogen infection and disease. This study improves the understanding of complex immune defense mechanisms in salamanders and highlights the potential role of the mucosome to reduce the probability of Bd disease development and that putative protective bacteria may reduce likelihood of Bd infecting skin.« less