Abstract Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions.
more »
« less
Community context for mechanisms of disease dilution: insights from linking epidemiology and plant–soil feedback theory
Abstract In many natural systems, diverse host communities can reduce disease risk, though less is known about the mechanisms driving this “dilution effect.” We relate feedback theory, which focuses on pathogen‐mediated coexistence, to mechanisms of dilution derived from epidemiological models, with the central goal of gaining insights into host–pathogen interactions in a community context. We first compare the origin, structure, and application of epidemiological and feedback models. We then explore the mechanisms of dilution, which are grounded in single‐pathogen, single‐host epidemiological models, from the perspective of feedback theory. We also draw on feedback theory to examine how coinfecting pathogens, and pathogens that vary along a host specialist–generalist continuum, apply to dilution theory. By identifying synergies among the feedback and epidemiological approaches, we reveal ways in which organisms occupying different trophic levels contribute to diversity–disease relationships. Additionally, using feedbacks to distinguish dilution in disease incidence from dilution in the net effect of disease on host fitness allows us to articulate conditions under which definitions of dilution may not align. After ascribing dilution mechanisms to macro‐ or microorganisms, we propose ways in which each contributes to diversity–disease and productivity–diversity relationships. Our analyses lead to predictions that can guide future research efforts.
more »
« less
- Award ID(s):
- 1738041
- PAR ID:
- 10457732
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Annals of the New York Academy of Sciences
- Volume:
- 1469
- Issue:
- 1
- ISSN:
- 0077-8923
- Page Range / eLocation ID:
- p. 65-85
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract For decades, people have reduced the transmission of pathogens by adding low‐quality hosts to managed environments like agricultural fields. More recently, there has been interest in whether similar ‘dilution effects’ occur in natural disease systems, and whether these effects are eroded as diversity declines. For some pathogens of plants, humans and other animals, the highest‐quality hosts persist when diversity is lost, so that high‐quality hosts dominate low‐diversity communities, resulting in greater pathogen transmission. Meta‐analyses reveal that these natural dilution effects are common. However, studying them remains challenging due to limitations on the ability of researchers to manipulate many disease systems experimentally, difficulties of acquiring data on host quality and confusion about what should and should not be considered a dilution effect. Because dilution effects are widely used in managed disease systems and have been documented in a variety of natural disease systems, their existence should not be considered controversial. Important questions remain about how frequently they occur and under what conditions to expect them. There is also ongoing confusion about their relationships to both pathogen spillover and general biogeographical correlations between diversity and disease, which has resulted in an inconsistent and confusing literature. Progress will require rigorous and creative research.more » « less
-
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
-
ABSTRACT To explain patterns between anthropogenic loss of species diversity and the rise in the number of novel zoonotic diseases, the “dilution effect” hypothesis predicts that with lower species diversity, infection risk will increase. The underlying mechanisms have been largely investigated in systems where pathogen transmission is vector‐borne or environmental. Relatively less research has been conducted in systems where transmission is direct, such as with orthohantaviruses (hereafter hantaviruses) and their rodent reservoir hosts. These systems are commonly cited as supporting a negative diversity‐disease pattern. To motivate empirical research on underlying mechanisms driving this pattern, we extend a mechanistic framework that links species diversity and infection prevalence of directly transmitted zoonotic pathogens by using rodent‐hantavirus systems in the Americas as models. Additionally, we summarize empirical studies, synthesize mechanistic evidence, and identify knowledge gaps. Our findings suggest that host regulation is a key mechanism likely to drive diversity‐disease patterns in rodent‐hantavirus systems of the Americas. Other mechanisms have received less empirical support but also less attention. Although host regulation likely functions via density‐dependent transmission, and can thus change contact rates among hosts, consequences to other mechanisms have been neglected. As observed in rodent‐hantavirus systems in the Americas, we propose that for a negative diversity‐disease pattern to manifest, the primary reservoir host species should be resilient to anthropogenic disturbance but also vulnerable to competition, predation, or both, and the “diversity” measure should be associated with host density.more » « less
-
Abstract Infectious diseases are a major threat for biodiversity conservation and can exert strong influence on wildlife population dynamics. Understanding the mechanisms driving infection rates and epidemic outcomes requires empirical data on the evolutionary trajectory of pathogens and host selective processes. Phylodynamics is a robust framework to understand the interaction of pathogen evolutionary processes with epidemiological dynamics, providing a powerful tool to evaluate disease control strategies. Tasmanian devils have been threatened by a fatal transmissible cancer, devil facial tumour disease (DFTD), for more than two decades. Here we employ a phylodynamic approach using tumour mitochondrial genomes to assess the role of tumour genetic diversity in epidemiological and population dynamics in a devil population subject to 12 years of intensive monitoring, since the beginning of the epidemic outbreak. DFTD molecular clock estimates of disease introduction mirrored observed estimates in the field, and DFTD genetic diversity was positively correlated with estimates of devil population size. However, prevalence and force of infection were the lowest when devil population size and tumour genetic diversity was the highest. This could be due to either differential virulence or transmissibility in tumour lineages or the development of host defence strategies against infection. Our results support the view that evolutionary processes and epidemiological trade‐offs can drive host‐pathogen coexistence, even when disease‐induced mortality is extremely high. We highlight the importance of integrating pathogen and population evolutionary interactions to better understand long‐term epidemic dynamics and evaluating disease control strategies.more » « less
An official website of the United States government
