A co‐infection with two gastrointestinal nematodes alters host immune responses and only partially parasite dynamics

Murphy, Lisa; Pathak, Ashutosh K.; Cattadori, Isabella M.

doi:10.1111/pim.12045

Cited by 30 publications

(65 citation statements)

References 30 publications

(74 reference statements)

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“…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%

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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: 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%

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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“…While there is some variability in the immune response between rabbits (Murphy et al, 2011(Murphy et al, , 2013Cattadori et al, 2013), the effect of this variability on egg hatchability will be addressed in a different study. To address our aims, we infected a single rabbit for each species and followed the hatching success of eggs produced by a cohort of parasites of the same age exposed to an immune response that changed over the course of the trial.…”

Section: Experimental Designmentioning

confidence: 99%

“…Trichostrongylus retortaeformis and G. strigosum are directly transmitted nematodes that colonize the small intestine and stomach, respectively, of the European rabbit (Oryctolagus cuniculus). We recently showed that rabbits mount a strong immune response to both nematodes by targeting third-stage larvae, adult worms and adult excretory/secretory compounds (Murphy et al, 2011(Murphy et al, , 2013Pathak et al, 2012;Cattadori et al, 2013). What determined this different pattern is unclear, since eggs of both parasites were exposed to identical environmental conditions in the laboratory and the field.…”

Section: Introductionmentioning

confidence: 99%

Does host immunity influence helminth egg hatchability in the environment?

2014

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Transmission success for helminths with free-living stages depends on the ability of eggs and larvae to develop and survive once in the environment. While environmental conditions are often suggested to influence egg phenology and hatching rate, immunity against parasite eggs might also play a role. We examined this hypothesis using the gastrointestinal helminths Trichostrongylus retortaeformis and Graphidium strigosum, two common infections of the European rabbit. Changes in egg hatching rate and volume were examined in relation to specific antibodies in the serum and bound to eggshells, using eggs shed in host faeces over a 15-week period. Hatching rate was consistently higher for T. retortaeformis than G. strigosum and no changes were observed between weeks. Egg volume increased for G. strigosum but decreased for T. retortaeformis. We did find evidence of egg-specific antibody responses and fewer antibodies were bound to eggs of T. retortaeformis compared to G. strigosum. Little to no association was found between antibodies and hatchability, or volume, for both helminths. We suggest that host antibodies play a relatively minor role in the egg hatching rate of these gastrointestinal helminths.

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“…As data on within-host community dynamics of parasites are beginning to emerge (Murphy et al 2013; Telfer et al 2010), models are needed to explore both the within-host assembly process and how this process affects host population dynamics. Earlier work on population dynamics of parasite communities (e.g., Dobson and Roberts 1994) emphasized the importance of aggregated distributions of parasite species within different host individuals in determining population-level parasite coexistence.…”

Section: Introductionmentioning

confidence: 99%

Eight challenges in modelling disease ecology in multi-host, multi-agent systems

et al. 2015

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Many disease systems exhibit complexities not captured by current theoretical and empirical work. In particular, systems with multiple host species and multiple infectious agents (i.e., multi-host, multi-agent systems) require novel methods to extend the wealth of knowledge acquired studying primarily single-host, single-agent systems. We outline eight challenges in multi-host, multi-agent systems that could substantively increase our knowledge of the drivers and broader ecosystem effects of infectious disease dynamics.

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A co‐infection with two gastrointestinal nematodes alters host immune responses and only partially parasite dynamics

Cited by 30 publications

References 30 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

Does host immunity influence helminth egg hatchability in the environment?

Eight challenges in modelling disease ecology in multi-host, multi-agent systems

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