Explaining patterns of infection in free‐living populations using laboratory immune experiments

Murphy, Lisa; Nalpas, Nicolas C.; Stear, M. J.; Cattadori, Isabella M.

doi:10.1111/j.1365-3024.2011.01281.x

Cited by 31 publications

(133 citation statements)

References 51 publications

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“…This is based on the findings that the helminths used in this study cause subclinical disease and although they can induce tissue pathology and morbidity, these conditions rarely lead to mortality at intensities comparable to field observations (28,40). Rabbit mortality can occur in concurrent infections with virulent strains of myxoma virus (41) or of rabbit hemorrhagic disease virus (42).…”

Section: Significancementioning

confidence: 82%

“…These contrasting dynamics can be captured within the rabbit-helminth system. We have shown experimentally that T. retortaeformis is reduced or cleared in older hosts by a strong type 1-type 2-acquired immune response, whereas G. strigosum persists with high abundances despite a type 2 immune reaction typical to helminths (28,29,38). Our model framework assumes that host susceptibility and helminth establishment are affected by immunity and/or parasite intensity dependence.…”

Section: Significancementioning

confidence: 99%

“…and yet the parasites show contrasting infection dynamics (26,27) and a distinct response to host immunity (28,29). Additionally, the system is under the influence of climate warming (30,31) and a strong seasonal regime (26,27,32) (Fig.…”

Section: Significancementioning

confidence: 99%

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Host immunity shapes the impact of climate changes on the dynamics of parasite infections

Mignatti

Boag

Cattadori

2016

Proc. Natl. Acad. Sci. U.S.A.

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Global climate change is predicted to alter the distribution and dynamics of soil-transmitted helminth infections, and yet host immunity can also influence the impact of warming on host-parasite interactions and mitigate the long-term effects. We used time-series data from two helminth species of a natural herbivore and investigated the contribution of climate change and immunity on the longterm and seasonal dynamics of infection. We provide evidence that climate warming increases the availability of infective stages of both helminth species and the proportional increase in the intensity of infection for the helminth not regulated by immunity. In contrast, there is no significant long-term positive trend in the intensity for the immune-controlled helminth, as immunity reduces the net outcome of climate on parasite dynamics. Even so, hosts experienced higher infections of this helminth at an earlier age during critical months in the warmer years. Immunity can alleviate the expected long-term effect of climate on parasite infections but can also shift the seasonal peak of infection toward the younger individuals.long-term climate warming | seasonality | host-parasite interaction | gastrointestinal helminths | European rabbit T he marked progression of climate warming and intensification of extreme climatic events have been implicated in the increased prevalence of infections, epidemic outbreaks, and the geographical shifting of endemic foci of infections (1-3). Experimental manipulations of vectors and infective stages have shown that warming, coupled with increased variability in temperature, can influence the vital rates of the parasite and the immunophysiological characteristics of the host (4-9). Predictive models of infection dynamics have reinforced the importance of these findings by showing that the risk of infection and transmission are likely to increase with the projected temperature changes (10-15) and synchronous, unpredicted weather events (16), although exceptions have been reported (17)(18)(19). Despite these findings, the extent to which climate disruption is in fact having an effect on parasite infections in natural systems is far from clear, as nonlinear effects in the parasite-host relationship and confounding variables can be difficult to disentangle.The way climate change modifies the development and survival of vectors and infective stages, and the consequences for the contact rate between infective and susceptible individuals, has been the central focus of many of the predictions and trials. However, this approach ignores the contribution of variability in the response of the hosts, which we expect to be critical in regulating the parasite abundance and the changes in the transmission rate. Given that immunity to infections is an important source of variation among individuals (20-23), if climate increases exposure to parasites, do we expect a proportional increase in the intensity of infection in hosts that mount an immune response against these parasites? In other words, how does variatio...

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Section: Significancementioning

confidence: 82%

Section: Significancementioning

confidence: 99%

See 1 more Smart Citation

Host immunity shapes the impact of climate changes on the dynamics of parasite infections

Mignatti

Boag

Cattadori

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…In the laboratory they may do so via a diverse cascade of effector mechanisms [15]. However, not all effectors necessarily produce resistance to all species [15],[27], and vigorous effector responses have been observed without efficient resistance [27],[28]. Recently, moreover, Th2 responses have also been linked [25] with tolerance to macroparasites.…”

Section: Discussionmentioning

confidence: 99%

An Immunological Marker of Tolerance to Infection in Wild Rodents

et al. 2014

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“…A model of the seasonal dynamics of the T. retortaeformis -rabbit interaction suggested that acquired immunity develops proportionally to the accumulated exposure to infection and successfully reduces helminth intensity in older hosts [21], [30]. These results were recently confirmed by challenging laboratory rabbits with a primary infection of T. retortaeformis where the quick production of antibodies and eosinophils was associated with the consistent reduction but not complete clearance of the helminth by 120 days post challenge [31].…”

Section: Introductionmentioning

confidence: 92%

Network Model of Immune Responses Reveals Key Effectors to Single and Co-infection Dynamics by a Respiratory Bacterium and a Gastrointestinal Helminth

et al. 2012

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Co-infections alter the host immune response but how the systemic and local processes at the site of infection interact is still unclear. The majority of studies on co-infections concentrate on one of the infecting species, an immune function or group of cells and often focus on the initial phase of the infection. Here, we used a combination of experiments and mathematical modelling to investigate the network of immune responses against single and co-infections with the respiratory bacterium Bordetella bronchiseptica and the gastrointestinal helminth Trichostrongylus retortaeformis. Our goal was to identify representative mediators and functions that could capture the essence of the host immune response as a whole, and to assess how their relative contribution dynamically changed over time and between single and co-infected individuals. Network-based discrete dynamic models of single infections were built using current knowledge of bacterial and helminth immunology; the two single infection models were combined into a co-infection model that was then verified by our empirical findings. Simulations showed that a T helper cell mediated antibody and neutrophil response led to phagocytosis and clearance of B. bronchiseptica from the lungs. This was consistent in single and co-infection with no significant delay induced by the helminth. In contrast, T. retortaeformis intensity decreased faster when co-infected with the bacterium. Simulations suggested that the robust recruitment of neutrophils in the co-infection, added to the activation of IgG and eosinophil driven reduction of larvae, which also played an important role in single infection, contributed to this fast clearance. Perturbation analysis of the models, through the knockout of individual nodes (immune cells), identified the cells critical to parasite persistence and clearance both in single and co-infections. Our integrated approach captured the within-host immuno-dynamics of bacteria-helminth infection and identified key components that can be crucial for explaining individual variability between single and co-infections in natural populations.

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Explaining patterns of infection in free‐living populations using laboratory immune experiments

Cited by 31 publications

References 51 publications

Host immunity shapes the impact of climate changes on the dynamics of parasite infections

Host immunity shapes the impact of climate changes on the dynamics of parasite infections

An Immunological Marker of Tolerance to Infection in Wild Rodents

Network Model of Immune Responses Reveals Key Effectors to Single and Co-infection Dynamics by a Respiratory Bacterium and a Gastrointestinal Helminth

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