skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Dead or alive: carbon as a currency to integrate disease and ecosystem ecology theory
Death is a common outcome of infection, but most disease models do not track hosts after death. Instead, these hosts disappear into a void. This assumption lacks critical realism, because dead hosts can alter host–pathogen dynamics. Here, we develop a theoretical framework of carbon‐based models combining disease and ecosystem perspectives to investigate the consequences of feedbacks between living and dead hosts on disease dynamics and carbon cycling. Because autotrophs (i.e. plants and phytoplankton) are critical regulators of carbon cycling, we developed general model structures and parameter combinations to broadly reflect disease of autotrophic hosts across ecosystems. Analytical model solutions highlight the importance of disease–ecosystem coupling. For example, decomposition rates of dead hosts mediate pathogen spread, and carbon flux between live and dead biomass pools are sensitive to pathogen effects on host growth and death rates. Variation in dynamics arising from biologically realistic parameter combinations largely fell along a single gradient from slow to fast carbon turnover rates, and models predicted higher disease impacts in fast turnover systems (e.g. lakes and oceans) than slow turnover systems (e.g. boreal forests). Our results demonstrate that a unified framework, including the effects of pathogens on carbon cycling, provides novel hypotheses and insights at the nexus of disease and ecosystem ecology.  more » « less
Award ID(s):
1831944
PAR ID:
10478468
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
John Wiley & Sons Ltd
Date Published:
Journal Name:
Oikos
Volume:
2023
Issue:
7
ISSN:
0030-1299
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; (, Journal of Animal Ecology)
    Abstract Heterogeneities in infections among host populations may arise through differences in environmental conditions through two mechanisms. First, environmental conditions may alter host exposure to pathogens via effects on survival. Second, environmental conditions may alter host susceptibility, making infection more or less likely if contact between a host and pathogen occurs. Further, host susceptibility might be altered through acquired resistance, which hosts can develop, in some systems, through exposure to dead or decaying pathogens and their metabolites. Environmental conditions may alter the rates of pathogen decomposition, influencing the likelihood of hosts developing acquired resistance.The present study primarily tests how environmental context influences the relative contributions of pathogen survival and per capita transmission on host infection prevalence using the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) as a model system. Secondarily, we evaluate how environmental context influences the decomposition of Bd because previous studies have shown that dead Bd and its metabolites can illicit acquired resistance in hosts. We conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition and per capita transmission rates vary among water sources [e.g. artificial spring water (ASW) or water from three ponds].We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd, rather than differences in per capita transmission rates. Bd mortality rates varied among pond water treatments and were lower in ASW compared to pond water.These results suggest that variation in Bd infection dynamics could be a function of environmental factors in waterbodies that result in differences in exposure of hosts to live Bd. In contrast to the persistence of live Bd, we found that the rates of decomposition of dead Bd did not vary among water sources, which may suggest that exposure of hosts to dead Bd or its metabolites might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the environmental dependence of free‐living pathogens could lead to a deeper understanding of the patterns of outbreak heterogeneity, which could inform surveillance and management strategies. 
    more » « less
  2. ; ; ; (, mSphere)
    Buchler, Nicolas E (Ed.)
    ABSTRACT Infectious diseases remain a major cause of global mortality, yet basic questions concerning the relationship between within-host processes governing pathogen burden (pathogen replication, immune responses) and population-scale (epidemiological) patterns of mortality remain obscure. We use a structured literature review to leverage the extensive biomedical data generated by controlled host infections to address the epidemiological question of whether infection-induced mortality is constant, accelerating, or follows some other pattern of change and to infer the within-host mechanistic basis of this pattern. We show that across diverse lethal infection models, the risk of death increases approximately exponentially in time since infection, in a manner phenomenologically similar to the dynamics of all-cause death. We further show that this pattern of accelerating risk is consistent with multiple alternate mechanisms of pathogen growth and host-pathogen interaction, underlining the limitations of current experimental approaches to connect within-host processes to epidemiological patterns. We review critical experimental questions that our work highlights, requiring additional non-invasive data on pathogen burden throughout the course of infection.IMPORTANCEHere, we ask a simple question: what are the dynamics of pathogen-induced death? Death is a central phenotype in both biomedical and epidemiological infectious disease biology, yet very little work has attempted to link the biomedical focus on pathogen dynamics within a host and the epidemiological focus on populations of infected hosts. To systematically characterize the dynamics of death in controlled animal infections, we analyzed 209 data sets spanning diverse lethal animal infection models. Across experimental models, we find robust support for an accelerating risk of death since the time of infection, contrasting with conventional epidemiological models that assume a constant elevated risk of death. Using math models, we show that multiple processes of growth and virulence are consistent with accelerating risk of death, and we end with a discussion of critical experiments to resolve how within-host biomedical processes map onto epidemiological patterns of disease. 
    more » « less
  3. ; ; (, Proceedings of the Royal Society B: Biological Sciences)
    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. 
    more » « less
  4. ; (, Proceedings of the Royal Society B: Biological Sciences)
    To make more informed predictions of host–pathogen interactions under climate change, studies have incorporated the thermal performance of host, vector and pathogen traits into disease models to quantify effects on average transmission rates. However, this body of work has omitted the fact that variation in susceptibility among individual hosts affects disease spread and long-term patterns of host population dynamics. Furthermore, and especially for ectothermic host species, variation in susceptibility is likely to be plastic, influenced by variables such as environmental temperature. For example, as host individuals respond idiosyncratically to temperature, this could affect the population-level variation in susceptibility, such that there may be predictable functional relationships between variation in susceptibility and temperature. Quantifying the relationship between temperature and among-host trait variation will therefore be critical for predicting how climate change and disease will interact to influence host–pathogen population dynamics. Here, we use a model to demonstrate how short-term effects of temperature on the distribution of host susceptibility can drive epidemic characteristics, fluctuations in host population sizes and probabilities of host extinction. Our results emphasize that more research is needed in disease ecology and climate biology to understand the mechanisms that shape individual trait variation, not just trait averages. 
    more » « less
  5. ; (, Integrative and Comparative Biology)
    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 period 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. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email