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

Abstract

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...

Latitudinal gradients of parasite richness: a review and new insights from helminths of cricetid rodents

“…Final models were chosen based on lowest AICc scores using model selection functions in R. Significance codes: '*' ≤ 0.05, '**' ≤ 0.01, '***' ≤ 0.001. Disentangling these influences is the topic of previous and ongoing research (Møller et al 2013, Goedknegt et al 2015, Mignatti et al 2016, Gehman et al 2018. λ is an estimate of the phylogenetic signal in the analysis and ranges from 0 (no phylogenetic signal in data) to 1 (Brownian motion).…”

“…when eggs are deposited in the environment for transmission or during free-living larval or adult stages) and can independently affect the host species, which in turn can influence host exposure and susceptibility to infection by helminths. Disentangling these influences is the topic of previous and ongoing research (Møller et al 2013, Goedknegt et al 2015, Mignatti et al 2016, Gehman et al 2018.…”

Physical Cues Controlling Seasonal Immune Allocation in a Natural Piscine Model

“…Such results are of wider interest because seasonal patterns of immunity have been reported in many vertebrate systems ( 7 , 12 ), and yet their control is incompletely understood. Importantly, such seasonal responses likely influence the dynamics of infectious disease ( 2 – 4 ), and contribute to individual health and fitness. Understanding their origin may help to link individual heterogeneity in within-host disease progression and between-host disease transmission to predictive environmental measurements, increasing the possibility of projecting disease risk.…”

“…Disease risk, in humans and animals, is frequently seasonal and seasonal variation in host immune allocation ( 1 – 4 ) may contribute to this. Moreover, seasonal change in immune responses is often reported in vertebrates ( 5 – 9 ) and might constrain not just infectious disease, through effects on immuncompetence, but also autoimmune disease, through altering the tendency for immune autoreactivity.…”

Thermal Performance Curves and the Metabolic Theory of Ecology—A Practical Guide to Models and Experiments for Parasitologists

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