Host-parasite Model Research Articles

Diversity and Host Specificity of Avian Haemosporidians in an Afrotropical Conservation Region.

Afrotropical regions have high bird diversity, yet few studies have attempted to unravel the prevalence of avian haemosporidia in conservation areas. The diversity and host specificity of parasites in biodiversity hotspots is crucial to understanding parasite distribution and potential disease emergence. We test the hypothesis that biodiverse regions are associated with highly diverse parasites. By targeting the cytochrome b (Cytb) gene, we molecularly screened 1035 blood samples from 55 bird species for avian haemosporidia infections to determine its prevalence and diversity on sites inside and adjacent to the Kruger National Park. Overall infection prevalence was 28.41%. Haemoproteus, Leucocytozoon, and Plasmodium presented prevalences of 17.39%, 9.24%, and 4.64%, respectively. One hundred distinct parasite lineages were detected, of which 56 were new lineages. Haemoproteus also presented the highest diversity compared to Leucocytozoon and Plasmodium with varying levels of specificity. Haemoproteus lineages were found to be specialists while Plasmodium and Leucocytozoon lineages were generalists. We also found a positive relationship between avian host diversity and parasite diversity, supporting an amplification effect. These findings provide insight data for host-parasite and co-evolutionary relationship models.

A Parasite Plant Promotes the Coexistence of Two Annual Plants.

Consumers can influence the competitive outcomes of prey species in various ways. Modern coexistence theory predicts that consumers can promote prey coexistence by preferably targeting a competitively superior one, thereby reducing fitness differences. However, previous studies yielded mixed conclusions. In this study, we tested the hypothesis that a parasitic annual plant, Cuscuta campestris, facilitates the coexistence of two common annual plants. We performed field surveys and parasitism experiments to parameterize a plant competition dynamics model. The model suggested a competition-defence tradeoff: the legume Lespedeza striata was a better competitor than the grass Setaria faberi, while it was more susceptible to the parasite. Moreover, an empirical host-parasite dynamics model, extended from the plant competition model, predicted their coexistence within broad, biologically reasonable ranges of parameters. This work provides field evidence of the coexisting-promoting role of a parasitic plant, as caused by stabilising feedback between host and parasite densities.

The impacts of synthetic and cellulose-based fibres and their associated dyes on fish hosts and parasite health

Plastic pollution is now a ubiquitous feature of freshwater systems and the majority of this is fibrous. Here, we test the effects of plastic and cellulose-based fibres (polyester, cotton, and bamboo from commercial clothing) on fish host-parasite interactions using a freshwater fish host-parasite model system (guppy Poecilia reticulata-Gyrodactylus turnbulli). For uninfected fish, polyester exposure was associated with significantly higher mortality rates compared with the other two fibre types. For infected fish, whilst polyester and cotton exposure were not associated with any significant changes to parasite burdens, fish exposed to bamboo fibres had significantly reduced maximum parasite burdens compared with fish not exposed to any fibres, indicating that the bamboo fibres and/or associated dyes conferred some degree of resistance or tolerance. Whilst unable to determine the exact nature of the chemical dyes, when testing off-host parasite survival on exposure to the fibre dyes, cotton and particularly polyester dyes were associated with higher parasite mortality compared to bamboo. Overall, we add to the growing body of evidence which shows that polyester microplastic fibres and their associated dyes can be detrimental for both fish and parasite survival, and we highlight the need for increased transparency from textile industries on the chemical identity of fabric dyes.

Local thermal adaptation and local temperature regimes drive the performance of a parasitic helminth under climate change: The case of Marshallagia marshalli from wild ungulates.

Across a species' range, populations are exposed to their local thermal environments, which on an evolutionary scale, may cause adaptative differences among populations. Helminths often have broad geographic ranges and temperature-sensitive life stages but little is known about whether and how local thermal adaptation can influence their response to climate change. We studied the thermal responses of the free-living stages of Marshallagia marshalli, a parasitic nematode of wild ungulates, along a latitudinal gradient. We first determine its distribution in wild sheep species in North America. Then we cultured M. marshalli eggs from different locations at temperatures from 5 to 38°C. We fit performance curves based on the metabolic theory of ecology to determine whether development and mortality showed evidence of local thermal adaptation. We used parameter estimates in life-cycle-based host-parasite models to understand how local thermal responses may influence parasite performance under general and location-specific climate-change projections. We found that M. marshalli has a wide latitudinal and host range, infecting wild sheep species from New Mexico to Yukon. Increases in mortality and development time at higher temperatures were most evident for isolates from northern locations. Accounting for location-specific parasite parameters primarily influenced the magnitude of climate change parasite performance, while accounting for location-specific climates primarily influenced the phenology of parasite performance. Despite differences in development and mortality among M. marshalli populations, when using site-specific climate change projections, there was a similar magnitude of impact on the relative performance of M. marshalli among populations. Climate change is predicted to decrease the expected lifetime reproductive output of M. marshalli in all populations while delaying its seasonal peak by approximately 1 month. Our research suggests that accurate projections of the impacts of climate change on broadly distributed species need to consider local adaptations of organisms together with local temperature profiles and climate projections.

Study of the cross-talk between Fasciola hepatica juveniles and the intestinal epithelial cells of the host by transcriptomics in an in vitro model

Fasciolosis is a globally widespread trematodiasis with a major economic and veterinary impact. Therefore, this disease is responsible for millions of dollars in losses to the livestock industry, and also constitutes an emerging human health problem in endemic areas. The ubiquitous nature of Fasciola hepatica, the main causative agent, is one of the key factors for the success of fasciolosis. Accordingly, this parasite is able to subsist in a wide variety of ecosystems and hosts, thanks to the development of a plethora of strategies for adaption and immune evasion. Fasciolosis comprises a growing concern due to its high prevalence rates, together with the emergence of strains of the parasite resistant to the treatment of choice (triclabendazole). These facts highlight the importance of developing novel control measures which allow for an effective protection against the disease before F. hepatica settles in a niche inaccessible to the immune system. However, knowledge about the initial phases of the infection, including the migration mechanisms of the parasite and the early innate host response, is still scarce. Recently, our group developed an in vitro host-parasite interaction model that allowed the early events to be unveiled after the first contact between the both actors. This occurs shortly upon ingestion of F. hepatica metacercariae and the emergence of the newly excysted juveniles (FhNEJ) in the host duodenum. Here, we present a transcriptomic analysis of such model using an approach based on RNA sequencing (RNA-Seq), which reveals changes in gene expression related to proteolysis and uptake of metabolites in FhNEJ. Additionally, contact with the parasite triggered changes in host intestinal cells related to pseudogenes expression and host defence mechanisms, including immune response, among others. In sum, these results provide a better understanding of the early stages of fasciolosis at molecular level, and a pool of targets that could be used in future therapeutic strategies against the disease.

Effects of forest loss and fragmentation on bat-ectoparasite interactions

Human land use causes habitat loss and fragmentation, influencing host-parasite associations through changes in infestation rates, host mortality and possibly local extinction. Bat-ectoparasite interactions are an important host-parasite model possibly affected by such changes, as this system acts as both reservoirs and vectors of several pathogens that can infect different wild and domestic species. This study aimed to assess how the prevalence and abundance of bat ectoparasites respond to forest loss, fragmentation, and edge length. Bats and ectoparasites were sampled at twenty sites, forming a gradient of forest cover, in southwestern Brazil during two wet (2015 and 2016) and two dry (2016 and 2017) seasons. Effects of landscape metrics on host abundance as well as parasite prevalence and abundance were assessed through structural equation models. Nine host-parasite associations provided sufficient data for analyses, including one tick and eight flies on four bat species. Forest cover positively influenced the prevalence or abundance of three fly species, but negatively influenced one fly and the tick species. Prevalence or abundance responded positively to edge length for three fly species, and negatively for the tick. In turn, number of fragments influenced the prevalence or abundance of four fly species, two positively and two negatively. Our results support species-specific responses of ectoparasites to landscape features, and a tendency of host-generalist ticks to benefit from deforestation while most host-specialist flies are disadvantaged. Differences in host traits and abundance, along with parasite life cycles and environmental conditions, are possible explanations to our findings.

Features of Engorgement of Ixodes ricinus Ticks Infesting the Northern White-Breasted Hedgehog in an Urban Park.

In this work we exploited the parallel dense tick and hedgehog populations of an urban park in Budapest, Hungary as a good host-parasite model to obtain detailed data about this physiological relationship. Over a 27-week period from April to October, 57 hedgehogs were captured in an urban park and kept for 10-14 days in animal house. All dropped off ticks were sampled, which allowed us to draw more a detailed picture of Ixodes ricinus-hedgehog relationships. The results indicated that the hedgehog is an effective host for ticks (prevalence: 100%) and the mean intensity of infestation was 83.25. Of the male ticks, 68.42% dropped off dead; 1.56% of the dropped off nymphs and 11.4% of the larvae finished their bloodmeal with red cuticles, while 5.79% of the females could not finish their blood meal, and dropped off dried, dead, or shrunken. We applied novel statistical methods of survival analysis of prevalent cohorts to estimate the whole attachment times of ticks from the observed attachment times, having no information about when the ticks attached to their hosts. Mean attachment times were 4 days for larvae, 5 days for nymphs, 10 days for females, and 8 days for males. On the first day after capture of the hosts, fewer females, nymphs, and larvae detached engorged than had been predicted, but this was not true for males. Mean intensity of infestation per host was 1.4 for males, 6.7 for females, 45.0 for nymphs, and 29.3 for larvae. As regards seasonality, the activity of all stages of ticks consisted of several smaller peaks and considerably differed by season. Studies of the dense tick-host populations of this natural habitat could provide further valuable data about tick-host relations, the data of which cannot be drawn from most other hedgehog habitats.

Qualitative Analysis of a Nicholson-Bailey Model in Patchy Environment

We studied a host-parasite model qualitatively. The host-parasitoid model is obtained by modifying the Nicholson-Bailey model so that the number of hosts that parasitoids can't attack is fixed. Topological classification of equilibria is achieved with the implementation of linearization. Furthermore, Neimark-Sacker bifurcation is explored using the bifurcation theory of normal forms at interior steady-state. The bifurcation in the model is controlled by implementing two control strategies. The theoretical studies are backed up by numerical simulations, which show the conclusions and their importance.

Complex effects of chytrid parasites on the growth of the cyanobacterium Planktothrix rubescens across interacting temperature and light gradients

Chytrids are important drivers of aquatic ecosystems as phytoplankton parasites. The interaction between these parasites and their hosts are shaped by abiotic factors such as temperature and light. Here, we performed a full-factorial experiment to study how temperature and light interact to affect the dynamics of the bloom-forming toxic cyanobacterium Planktothrix rubescens and its chytrid parasite. We used a dynamic host-parasite model to explore how temperature and light affect long term dynamics. At low temperatures, chytrids do not survive. Higher light and temperature levels stimulated both phytoplankton and chytrid growth, with complex effects on their dynamics. Model exploration indicates that increasing temperature and light shifts equilibrium outcomes from P. rubescens persisting alone to stable coexistence and then to limit cycles. This provides an alternative biological explanation for why P. rubescens is mainly found in the relatively cold and dark lake metalimnion – it may enable avoidance of its parasite. Our study emphasizes the importance of investigating how abiotic factors interact with biotic interactions to drive complex outcomes.

Behaviour is more important than thermal performance for an Arctic host-parasite system under climate change.

Climate change is affecting Arctic ecosystems, including parasites. Predicting outcomes for host–parasite systems is challenging due to the complexity of multi-species interactions and the numerous, interacting pathways by which climate change can alter dynamics. Increasing temperatures may lead to faster development of free-living parasite stages but also higher mortality. Interactions between behavioural plasticity of hosts and parasites will also influence transmission processes. We combined laboratory experiments and population modelling to understand the impacts of changing temperatures on barren-ground caribou (Rangifer tarandus) and their common helminth (Ostertagia gruehneri). We experimentally determined the thermal performance curves for mortality and development of free-living parasite stages and applied them in a spatial host–parasite model that also included behaviour of the parasite (propensity for arrested development in the host) and host (long-distance migration). Sensitivity analyses showed that thermal responses had less of an impact on simulated parasite burdens than expected, and the effect differed depending on parasite behaviour. The propensity for arrested development and host migration led to distinct spatio-temporal patterns in infection. These results emphasize the importance of considering behaviour—and behavioural plasticity—when projecting climate-change impacts on host–parasite systems.

Parasite‐driven cascades or hydra effects: Susceptibility and foraging depression shape parasite–host–resource interactions

Abstract Parasites kill hosts but also can indirectly increase the abundance of their resources. Given this resource feedback, how much will parasites decrease host density? Can they increase host density? Seeking answers, we integrate trait measurements, a resource–host–parasite model and experimental epidemics with plankton. This combination reveals how parasites may decrease or increase host density. This spectrum of outcomes reflects tension between parasite‐driven mortality (a density‐mediated effect) and foraging depression upon contact with parasite propagules (a trait‐mediated one). In the model, mortality rises when higher susceptibility to infection increases infection prevalence. These large epidemics release resources while suppressing hosts (creating a trophic cascade). In contrast, when hosts are less susceptible and parasites depress host foraging, a resource feedback can elevate host density during epidemics (creating a hydra effect), particularly at higher carrying capacity of resources. This combination creates the hydra effect because it elevates primary production relative to per‐host consumption of resources (two key determinants of host density). We test these predictions qualitatively with trait measurements and a mesocosm experiment. Clonal lines of zooplankton hosts differed in their foraging depression and susceptibility. Then, with these different host genotypes, we created epidemics in mesocosms supplied with either low or high nutrients (to manipulate carrying capacity). Hydra effects and trophic cascades both arose and in the trait–nutrient combinations predicted by the model. Hence, we show how tension between trait‐ and density‐mediated effects of parasites can govern the fate of host density during epidemics—from trophic cascades to hydra effects. Read the free Plain Language Summary for this article on the Journal blog.

Agrochemicals as a Threat to Freshwater Ecosystems: Antiparasitic Potential of Fungicides on a Non-Target Host-Parasite Model

Agrochemicals as a Threat to Freshwater Ecosystems: Antiparasitic Potential of Fungicides on a Non-Target Host-Parasite Model

Integrating Infection Intensity into Within- and Between-Host Pathogen Dynamics: Implications for Invasion and Virulence Evolution.

AbstractInfection intensity can dictate disease outcomes but is typically ignored when modeling infection dynamics of microparasites (e.g., bacteria, virus, and fungi). However, for a number of pathogens of wildlife typically categorized as microparasites, accounting for infection intensity and within-host infection processes is critical for predicting population-level responses to pathogen invasion. Here, we develop a modeling framework we refer to as reduced-dimension host-parasite integral projection models (reduced IPMs) that we use to explore how within-host infection processes affect the dynamics of pathogen invasion and virulence evolution. We find that individual-level heterogeneity in pathogen load-a nearly ubiquitous characteristic of host-parasite interactions that is rarely considered in models of microparasites-generally reduces pathogen invasion probability and dampens virulence-transmission trade-offs in host-parasite systems. The latter effect likely contributes to widely predicted virulence-transmission trade-offs being difficult to observe empirically. Moreover, our analyses show that intensity-dependent host mortality does not always induce a virulence-transmission trade-off, and systems with steeper than linear relationships between pathogen intensity and host mortality rate are significantly more likely to exhibit these trade-offs. Overall, reduced IPMs provide a useful framework to expand our theoretical and data-driven understanding of how within-host processes affect population-level disease dynamics.

SPEMS: A sustainable parasitic energy management system for smart homes

The amount of electricity consumed grows exponentially with each passing year. Energy management (EM) has the potential to help satisfy electricity demands more efficiently. It implements strategies to reduce energy consumption during peak time or shift its usage to off-peak hours. This research introduces SPEMS (Sustainable Parasitic EM System), a competitive yet cooperative Multi-agent System (MAS) based framework that optimizes energy cost, consumption, Peak-to-Average Ratio (PAR), and user’s discomfort unobtrusively. The framework devises an optimized load scheduling plan for smart appliances using the Host-Parasite Model where the agents with conflicting objectives need to have a symbiotic relationship. Our work follows a quantitative approach towards evaluating user comfort. It takes into account environmental aspects like user presence and weather elements including user temperature, apparent temperature, and visibility. SPEMS adapts itself to user’s behavior patterns without requiring the user to enter their everyday feedback. The concept of sampled Hall of Fame is incorporated to preserve and use the best schedules from previous days ensuring progress towards finding optimal schedules. Experiments have been performed on real-time data collected from a real home for about one and a half years. Results show that our model is computationally inexpensive, sustainable, and minimizes cost, consumption, and PAR with reduced discomfort of the user.

Experimental Horizontal Transmission of Enterospora nucleophila (Microsporea: Enterocytozoonidae) in Gilthead Sea Bream (Sparus aurata).

Simple SummaryEnterospora nucleophila is a microsporidian parasite infecting gilthead sea bream (Sparus aurata) that has been associated with increased mortality, growth arrestment and emaciation in aquaculture settings. The investigations on this parasite depend on material from spontaneous outbreaks in fish farms, which hampers advancements in infection research and control. In the present study, different ways of horizontal transmission were performed in order to establish an in vivo transmission model. Parasite transmission was achieved with all the assayed routes, but with milder clinical signs than in natural infections.Enterospora nucleophila is a microsporidian enteroparasite that infects mainly the intestine of gilthead sea bream (Sparus aurata), leading to an emaciative syndrome. Thus far, the only available information about this infection comes from natural outbreaks in farmed fish. The aim of the present study was to determine whether E. nucleophila could be transmitted horizontally using naturally infected fish as donors, and to establish an experimental in vivo procedure to study this host–parasite model without depending on natural infections. Naïve fish were exposed to the infection by cohabitation, effluent, or intubated either orally or anally with intestinal scrapings of donor fish in four different trials. We succeeded in detecting parasite in naïve fish in all the challenges, but the infection level and the disease signs were always milder than in donor fish. The parasite was found in peripheral blood of naïve fish at 4 weeks post-challenge (wpc) in oral and effluent routes, and up to 12 wpc in the anal transmission trial. Molecular diagnosis detected E. nucleophila in other organs besides intestine, such as gills, liver, stomach or heart, although the intensity was not as high as in the target tissue. The infection tended to disappear through time in all the challenge routes assayed, except in the anal infection route.

Chemical detection triggers honey bee defense against a destructive parasitic threat.

Invasive species events related to globalization are increasing, resulting in parasitic outbreaks. Understanding of host defense mechanisms is needed to predict and mitigate against the consequences of parasite invasion. Using the honey bee Apis mellifera and the mite Varroa destructor, as a host-parasite model, we provide a comprehensive study of a mechanism of parasite detection that triggers a behavioral defense associated with social immunity. Six Varroa-parasitization-specific (VPS) compounds are identified that (1) trigger Varroa-sensitive hygiene (VSH, bees' key defense against Varroa sp.), (2) enable the selective recognition of a parasitized brood and (3) induce responses that mimic intrinsic VSH activity in bee colonies. We also show that individuals engaged in VSH exhibit a unique ability to discriminate VPS compounds from healthy brood signals. These findings enhance our understanding of a critical mechanism of host defense against parasites, and have the potential to apply the integration of pest management in the beekeeping sector.

Coevolution fails to maintain genetic variation in a host–parasite model with constant finite population size

Coevolutionary negative frequency-dependent selection has been hypothesized to maintain genetic variation in host and parasites. Despite the extensive literature pertaining to host–parasite coevolution, the temporal dynamics of genetic variation have not been examined in a matching-alleles model (MAM) with a finite population size relative to the expectation under neutral genetic drift alone. The dynamics of the MA coevolution in an infinite population, in fact, suggests that genetic variation in these coevolving populations behaves neutrally. By comparing host heterozygosity to the expectation in a single-species model of neutral genetic drift we find that while this is also largely true in finite populations two additional phenomena arise. First, reciprocal natural selection acting on stochastic perturbations in host and pathogen allele frequencies results in a slight increase or decrease in genetic variation depending on the parameter conditions. Second, following the fixation of an allele in the parasite, selection in the MAM becomes directional, which then rapidly erodes genetic variation in the host. Hence, rather than maintain it, we find that, on average, matching-alleles coevolution depletes genetic variation.

The Role of Small Extracellular Vesicles in Viral-Protozoan Symbiosis: Lessons From Trichomonasvirus in an Isogenic Host Parasite Model.

The protozoan parasite Trichomonas vaginalis (TV), exclusively adapted to the human genital tract, is one of the most common sexually transmitted pathogens. Adding to the complexity of the host-pathogen interactions, the parasite harbors TV-specific endosymbiont viruses (Trichomonasvirus, TVV). It was reported that small extracellular vesicles (sEVs) released by TV play a role in host immunity; however, the role of the viral endosymbiosis in this process remained unknown. We hypothesized that the virus may offer evolutionary benefit to its protozoan host at least in part by altering the immunomodulatory properties of sEVs spreading from the site of infection to non-infected immune effector cells. We infected human vaginal epithelial cells, the natural host of the parasite, with TV natively harboring TVV and an isogenic derivative of the parasite cured from the viral infection. sEVs were isolated from vaginal cell culture 24 h post TV infection and from medium where the isogenic TV strains were cultured in the absence of the human host. sEVs from TVV-negative but not TVV-positive parasites cultured alone caused NF-κB activation and increase of IL-8 and RANTES expression by uterine endocervical cells, which provide innate immune defense at the gate to the upper reproductive tract. Similarly, mononuclear leukocytes increased their IL-8, IL-6 and TNF-α output in response to sEVs from virus-negative, but not isogenic virus-positive parasites, the latter exosomes being immunosuppressive in comparison to TV medium control. The same phenomenon of suppressed immunity induced by the TVV-positive compared to TVV-negative phenotype was seen when stimulating the leukocytes with sEVs originating from infected vaginal cultures. In addition, the sEVs from the TVV-positive infection phenotype suppressed immune signaling of a toll-like receptor ligand derived from mycoplasma, another frequent TV symbiont. Quantitative comparative proteome analysis of the secreted sEVs from virus-positive versus virus-negative TV revealed differential expression of two functionally uncharacterized proteins and five proteins involved in Zn binding, protein binding, electron transfer, transferase and catalytic activities. These data support the concept that symbiosis with viruses may provide benefit to the protozoan parasite by exploiting sEVs as a vehicle for inter-cellular communications and modifying their protein cargo to suppress host immune activation.

Parasite Assemblages in a Bivalve Host Associated with Changes in Hydrodynamics

Studies on marine community structure and their modulation by horizontal and vertical abiotic gradients have focused on free-living species, neglecting parasites despite their important role in ecosystems. Field observations, a laboratory flume experiment and modelling were used to examine parasite infection patterns related to host tidal and spatial position along a Portuguese coastal lagoon (Ria de Aveiro). Cockles (Cerastoderma edule) and trematodes were used as a host-parasite model to test the hypotheses: (1) higher infection levels in subtidal cockles, positioned downstream and (2) higher current velocity in downstream areas with consequent higher cockle infection. Cockles were collected from two spatial and tidal positions in two seasons. The relationship between current velocity and cockle infection was examined experimentally by exposing cockles to cercariae of Himasthla elongata at two current velocities. Intertidal cockles displayed higher infection, highlighting vertical position as an important driver of infection possibly due to first host proximity and/or trematode life cycle facilitation (higher cockle exposure to final host predation). The hydrodynamic model showed that the Ria de Aveiro was abiotically heterogenous with cockles displaying higher infection levels in the downstream area. Multiple regression analysis demonstrated a positive correlation between salinity, dissolved oxygen, current velocity and trematode abundance. The influence of current velocity on infection success was corroborated experimentally. The present study demonstrated the importance of host vertical and horizontal position on trematode infection, highlighting the positive influence of current velocity by supporting settlement and promoting favourable abiotic conditions.

A general mathematical method for predicting spatio-temporal correlations emerging from agent-based models.

Agent-based models are used to study complex phenomena in many fields of science. While simulating agent-based models is often straightforward, predicting their behaviour mathematically has remained a key challenge. Recently developed mathematical methods allow the prediction of the emerging spatial patterns for a general class of agent-based models, whereas the prediction of spatio-temporal pattern has been thus far achieved only for special cases. We present a general and mathematically rigorous methodology that allows deriving the spatio-temporal correlation structure for a general class of individual-based models. To do so, we define an auxiliary model, in which each agent type of the primary model expands to three types, called the original, the past and the new agents. In this way, the auxiliary model keeps track of both the initial and current state of the primary model, and hence the spatio-temporal correlations of the primary model can be derived from the spatial correlations of the auxiliary model. We illustrate the agreement between analytical predictions and agent-based simulations using two example models from theoretical ecology. In particular, we show that the methodology is able to correctly predict the dynamical behaviour of a host–parasite model that shows spatially localized oscillations.