An official website of the United States government
Abstract While the negative effects that pathogens have on their hosts are well-documented in humans and agricultural systems, direct evidence of pathogen-driven impacts in wild host populations is scarce and mixed. Here, to determine how the strength of pathogen-imposed selection depends on spatial structure, we analyze growth rates across approximately 4000 host populations of a perennial plant through time coupled with data on pathogen presence-absence. We find that infection decreases growth more in the isolated than well-connected host populations. Our inoculation study reveals isolated populations to be highly susceptible to disease while connected host populations support the highest levels of resistance diversity, regardless of their disease history. A spatial eco-evolutionary model predicts that non-linearity in the costs to resistance may be critical in determining this pattern. Overall, evolutionary feedbacks define the ecological impacts of disease in spatially structured systems with host gene flow being more important than disease history in determining the outcome.
more »
« less
Pathogens stabilize or destabilize depending on host stage structure
A common assumption is that pathogens more readily destabilize their host populations, leading to an elevated risk of driving both the host and pathogen to extinction. This logic underlies many strategies in conservation biology and pest and disease management. Yet, the interplay between pathogens and population stability likely varies across contexts, depending on the environment and traits of both the hosts and pathogens. This context-dependence may be particularly important in natural consumer-host populations where size- and stage-structured competition for resources strongly modulates population stability. Few studies, however, have examined how the interplay between size and stage structure and infectious disease shapes the stability of host populations. Here, we extend previously developed size-dependent theory for consumer-resource interactions to examine how pathogens influence the stability of host populations across a range of contexts. Specifically, we integrate a size- and stage-structured consumer-resource model and a standard epidemiological model of a directly transmitted pathogen. The model reveals surprisingly rich dynamics, including sustained oscillations, multiple steady states, biomass overcompensation, and hydra effects. Moreover, these results highlight how the stage structure and density of host populations interact to either enhance or constrain disease outbreaks. Our results suggest that accounting for these cross-scale and bidirectional feedbacks can provide key insight into the structuring role of pathogens in natural ecosystems while also improving our ability to understand how interventions targeting one may impact the other.
more »
« less
- Award ID(s):
- 2243076
- PAR ID:
- 10534197
- Publisher / Repository:
- AIMS press
- Date Published:
- Journal Name:
- Mathematical Biosciences and Engineering
- Volume:
- 20
- Issue:
- 12
- ISSN:
- 1551-0018
- Page Range / eLocation ID:
- 20378 to 20404
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Climate warming is altering life cycles of ectotherms by advancing phenology and decreasing generation times. Theoretical models provide powerful tools to investigate these effects of climate warming on consumer–resource population dynamics. Yet, existing theory primarily considers organisms with simplified life histories in constant temperature environments, making it difficult to predict how warming will affect organisms with complex life cycles in seasonal environments. We develop a size-structured consumer–resource model with seasonal temperature dependence, parameterized for a freshwater insect consuming zooplankton. We simulate how climate warming in a seasonal environment could alter a key life-history trait of the consumer, number of generations per year, mediating responses of consumer–resource population sizes and consumer persistence. We find that, with warming, consumer population sizes increase through multiple mechanisms. First, warming decreases generation times by increasing rates of resource ingestion and growth and/or lengthening the growing season. Second, these life-history changes shorten the juvenile stage, increasing the number of emerging adults and population-level reproduction. Unstructured models with similar assumptions found that warming destabilized consumer–resource dynamics. By contrast, our size-structured model predicts stability and consumer persistence. Our study suggests that, in seasonal environments experiencing climate warming, life-history changes that lead to shorter generation times could delay population extinctions.more » « less
-
Social and spatial structures of host populations play important roles in pathogen transmission. For environmentally transmitted pathogens, the host space use interacts with both the host social structure and the pathogen’s environmental persistence (which determines the time-lag across which two hosts can transmit). Together, these factors shape the epidemiological dynamics of environmentally transmitted pathogens. While the importance of both social and spatial structures and environmental pathogen persistence has long been recognized in epidemiology, they are often considered separately. A better understanding of how these factors interact to determine disease dynamics is required for developing robust surveillance and management strategies. Here, we use a simple agent-based model where we vary host mobility (spatial), host gregariousness (social) and pathogen decay (environmental persistence), each from low to high levels to uncover how they affect epidemiological dynamics. By comparing epidemic peak, time to epidemic peak and final epidemic size, we show that longer infectious periods, higher group mobility, larger group size and longer pathogen persistence lead to larger, faster growing outbreaks, and explore how these processes interact to determine epidemiological outcomes such as the epidemic peak and the final epidemic size. We identify general principles that can be used for planning surveillance and control for wildlife host–pathogen systems with environmental transmission across a range of spatial behaviour, social structure and pathogen decay rates. This article is part of the theme issue ‘The spatial–social interface: a theoretical and empirical integration’.more » « less
-
null (Ed.)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, 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.more » « less
-
Abstract Changes to migration routes and phenology create novel contact patterns among hosts and pathogens. These novel contact patterns can lead to pathogens spilling over between resident and migrant populations. Predicting the consequences of such pathogen spillover events requires understanding how pathogen evolution depends on host movement behaviour. Following spillover, pathogens may evolve changes in their transmission rate and virulence phenotypes because different strategies are favoured by resident and migrant host populations. There is conflict in current theoretical predictions about what those differences might be. Some theory predicts lower pathogen virulence and transmission rates in migrant populations because migrants have lower tolerance to infection. Other theoretical work predicts higher pathogen virulence and transmission rates in migrants because migrants have more contacts with susceptible hosts.We aim to understand how differences in tolerance to infection and host pace of life act together to determine the direction of pathogen evolution following pathogen spillover from a resident to a migrant population.We constructed a spatially implicit model in which we investigate how pathogen strategy changes following the addition of a migrant population. We investigate how differences in tolerance to infection and pace of life between residents and migrants determine the effect of spillover on pathogen evolution and host population size.When the paces of life of the migrant and resident hosts are equal, larger costs of infection in the migrants lead to lower pathogen transmission rate and virulence following spillover. When the tolerance to infection in migrant and resident populations is equal, faster migrant paces of life lead to increased transmission rate and virulence following spillover. However, the opposite can also occur: when the migrant population has lower tolerance to infection, faster migrant paces of life can lead to decreases in transmission rate and virulence.Predicting the outcomes of pathogen spillover requires accounting for both differences in tolerance to infection and pace of life between populations. It is also important to consider how movement patterns of populations affect host contact opportunities for pathogens. These results have implications for wildlife conservation, agriculture and human health.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3934/mbe.2023901
