Complex dynamics of a predator–prey–parasite system: An interplay among infection rate,predator's reproductive gain and preference

Parasites are considered as an important factor in regulating their host populations through trait-mediated effects. On the other hand, predation becomes particularly interesting in host–parasite systems because predation can significantly alter the abundance of parasites and their host population. The combined effects of parasites and predator on host population and community structure therefore may have larger effect. Different field experiments confirm that predators consume disproportionately large number of infected prey in comparison to their susceptible counterpart. There are also substantial evidences that predator has the ability to distinguish prey that have been infected by a parasite and avoid such prey to reduce fitness cost. In this paper we study the predator–prey dynamics, where the prey species is infected by some parasites and predators consume both the susceptible and infected prey with some preference. We demonstrate that complexity in such systems largely depends on the predator's selectivity, force of infection and predator's reproductive gain. If the force of infection and predator's reproductive gain are low, parasites and predators both go to extinction whatever be the predator's preference. The story may be totally different in the opposite case. Survival of species in stable, oscillatory or chaotic states, and their extinction largely depend on the predator's preference. The system may also show two coexistence equilibrium points for some parameter values. The equilibrium with lower susceptible prey density is always stable and the equilibrium with higher susceptible prey density is always unstable. These results suggest that understanding the consequences of predator's selectivity or preference may be crucial for community structure involving parasites.     

Persistence of host and parasite populations subject to experimental size-selective removal

Predators have the potential to limit the spread of pathogens not only by selecting infected prey but also by shaping prey demographics. We tested this idea with an epidemiological experiment in which we simulated variable levels of size-selective predation on zooplankton hosts and monitored the persistence of host and parasite populations. In the absence of simulated predation, the virulent protozoan Caullerya mesnili frequently drove its host Daphnia galeata to extinction. Uninfected control populations showed lower extinction rates and higher average densities than infected populations in the absence of simulated predation (all of the latter went extinct or remained infected). With a weak removal rate of the largest hosts, the proportion of populations in which the parasite drove the host to extinction decreased, while the number of populations in which the host persisted and the parasite went extinct increased. Host-parasite coexistence was also observed in some cases. With intermediate levels of removal, most of the parasite populations went extinct, while the host populations persisted. With an even higher removal rate, Daphnia were driven to extinction as well. Thus, variation in one factor, size-selective mortality, resulted in four different patterns of population dynamics. Our results highlight the potential role of predation in shaping the epidemiology and community structure of host-parasite systems.     

Population dynamics of plant-parasite interactions: thresholds for invasion

Thresholds are derived for the invasion of plant populations by parasites. The theory is developed for a generic model that takes into account two features characteristic of plant-parasite interactions: a dual source of inoculum (infection from primary or externally introduced inoculum and secondary infection from contact between susceptible and infected host tissue) and a host response to infection load. Each of the threshold criteria is shown to be the sum of the individual components for primary and secondary infection. This indicates that if parasite invasion is not possible through primary or secondary infection alone, when the two modes of transmission are combined, the parasite may be able to invade. The invasion criteria demonstrate that there is a threshold population of susceptible hosts below which the parasite is unable to invade. If there are nonlinearities in the population dynamics (arising through either the transmission process or the host response), there are also threshold densities for the infected hosts and parasite populations below which invasion does not occur. The implications of the results for the control of plant disease are discussed.     

Cross‐continental comparison of parasite communities in a wide‐ranging carnivore suggests associations with prey diversity and host density

1. Parasites are integral to ecosystem functioning yet often overlooked. Improved understanding of host–parasite associations is important, particularly for wide‐ranging species for which host range shifts and climate change could alter host–parasite interactions and their effects on ecosystem function.
2. Among the most widely distributed mammals with diverse diets, gray wolves (Canis lupus) host parasites that are transmitted among canids and via prey species. Wolf–parasite associations may therefore influence the population dynamics and ecological functions of both wolves and their prey. Our goal was to identify large‐scale processes that shape host–parasite interactions across populations, with the wolf as a model organism.
3. By compiling data from various studies, we examined the fecal prevalence of gastrointestinal parasites in six wolf populations from two continents in relation to wolf density, diet diversity, and other ecological conditions.
4. As expected, we found that the fecal prevalence of parasites transmitted directly to wolves via contact with other canids or their excreta was positively associated with wolf density. Contrary to our expectations, the fecal prevalence of parasites transmitted via prey was negatively associated with prey diversity. We also found that parasite communities reflected landscape characteristics and specific prey items available to wolves.
5. Several parasite taxa identified in this study, including hookworms and coccidian protozoans, can cause morbidity and mortality in canids, especially in pups, or in combination with other stressors. The density–prevalence relationship for parasites with simple life cycles may reflect a regulatory role of gastrointestinal parasites on wolf populations. Our result that fecal prevalence of parasites was lower in wolves with more diverse diets could provide insight into the mechanisms by which biodiversity may regulate disease. A diverse suite of predator–prey interactions could regulate the effects of parasitism on prey populations and mitigate the transmission of infectious agents, including zoonoses, spread via trophic interactions.

     

Bottom–up regulation of parasite population densities in freshwater ecosystems

Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m²) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi‐host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact‐transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.     

The effect of host heterogeneity and parasite intragenomic interactions on parasite population structure

Understanding the processes that shape the genetic structure of parasite populations and the functional consequences of different parasite genotypes is critical for our ability to predict how an infection can spread through a host population and for the design of effective vaccines to combat infection and disease. Here, we examine how the genetic structure of parasite populations responds to host genetic heterogeneity. We consider the well-characterized molecular specificity of major histocompatibility complex binding of antigenic peptides to derive deterministic and stochastic models. We use these models to ask, firstly, what conditions favour the evolution of generalist parasite genotypes versus specialist parasite genotypes? Secondly, can parasite genotypes coexist in a population? We find that intragenomic interactions between parasite loci encoding antigenic peptides are pivotal in determining the outcome of evolution. Where parasite loci interact synergistically (i.e. the recognition of additional antigenic peptides has a disproportionately large effect on parasite fitness), generalist parasite genotypes are favoured. Where parasite loci act multiplicatively (have independent effects on fitness) or antagonistically (have diminishing effects on parasite fitness), specialist parasite genotypes are favoured. A key finding is that polymorphism is not stable and that, with respect to functionally important antigenic peptides, parasite populations are dominated by a single genotype.     

Population structure of a parasitic plant and its perennial host

Characterization of host and parasite population genetic structure and estimation of gene flow among populations are essential for the understanding of parasite local adaptation and coevolutionary interactions between hosts and parasites. We examined two aspects of population structure in a parasitic plant, the greater dodder (Cuscuta europaea) and its host plant, the stinging nettle (Urtica dioica), using allozyme data from 12 host and eight parasite populations. First, we examined whether hosts exposed to parasitism in the past contain higher levels of genetic variation. Second, we examined whether host and parasite populations differ in terms of population structure and if their population structures are correlated. There was no evidence that host populations differed in terms of gene diversity or heterozygosity according to their history of parasitism. Host populations were genetically more differentiated (F(ST) = 0.032) than parasite populations (F(ST) = 0.009). Based on these F(ST) values, gene flow was high for both host and parasite. Such high levels of gene flow could counteract selection for local adaptation of the parasite. We found no significant correlation between geographic and genetic distance (estimated as pairwise F(ST)), either for the host or for the parasite. Furthermore, host and parasite genetic distance matrices were uncorrelated, suggesting that sites with genetically similar host populations are unlikely to have genetically similar parasite populations.     

A host–microparasite model with a resistant host

The theory of heterozygote advantage is often used to explain the genetic variation found in natural populations. If a large population randomly mates and the various genotypes have the same growth and death rates, the evolution of the genotypes follows Hardy–Weinberg proportions and polymorphism results. When other environmental stresses, like predators, prey and diseases, are present, polymorphism may or may not occur depending on how the various genotypes are affected by the stress. In this paper, we use a basic host–microparasite model to demonstrate that polymorphism can occur even if one genotype suffers a higher death rate than the others in the absence of the parasite if the heterozygote has resistance or immunity to the parasite.     

Combined impacts of Allee effects and parasitism

Despite their individual importance for population dynamics and conservation biology, the combined impacts of Allee effects and parasitism have received little attention. We built a mathematical model to compare the dynamics of populations with or without Allee effects when infected by microparasites. We show that the influence of an Allee effect takes the form of a tradeoff. The presence of an Allee effect in host populations may protect them, by reducing the range of population sizes that allow parasite spread. Yet if infection spreads, the Allee effect weakens host populations by reducing their size and by widening the range of parasite species that lead them to extinction. These results have important implications for predicting the survival of threatened populations or the success of reintroductions, and may help define size ranges within which given populations should be maintained to prevent both epidemics and Allee effects driven extinctions.     

Host patch traits have scale-dependent effects on diversity in a stickleback parasite metacommunity

Many metacommunities are distributed across habitat patches that are themselves aggregated into groups. Perhaps the clearest example of this nested metacommunity structure comes from multi-species parasite assemblages, which occupy individual hosts that are aggregated into host populations. At both spatial scales, we expect parasite community diversity in a given patch (either individual host or population) to depend on patch characteristics that affect colonization rates and species sorting. But, are these patch effects consistent across spatial scales? Or, do different processes govern the distribution of parasite community diversity among individual hosts, versus among host patches? To answer these questions, we document the distribution of parasite richness among host individuals and among populations in a metapopulation of threespine stickleback Gasterosteus aculeatus. We find some host traits (host size, gape width) are associated with increased parasite richness at both spatial scales. Other patch characteristics affect parasite richness only among individuals (sex), or among populations (lake size, lake area, elevation and population mean heterozygosity). These results demonstrate that some rules governing parasite richness in this metacommunity are shared across scales, while others are scale-specific.     

Host defence mediates interspecific competition in ectoparasites

1. Interspecific competition influences which, how many and where species coexist in biological communities. Interactions between species in different trophic levels can mediate interspecific competition; e.g. predators are known to reduce competition between prey species by suppressing their population sizes. A parallel phenomenon may take place in host-parasite systems, with host defence mediating competition between parasite species. 2. We experimentally investigated the impact of host defence (preening) on competitive interactions between two species of feather-feeding lice: 'wing' lice Columbicola columbae and 'body' lice Campanulotes compar. Both species are host-specific parasites that co-occur on rock pigeons Columba livia. 3. We show that wing lice and body lice compete and that host defence mediates the magnitude of this competitive interaction. 4. Competition is asymmetrical; wing louse populations are negatively impacted by body lice, but not vice versa. This competitive asymmetry is consistent with the fact that body lice predominate in microhabitats on the host's body that offer the most food and the most space. 5. Our results indicate that host-defence-mediated competition can influence the structure of parasite communities and may play a part in the evolution of parasite diversity.     

Low humidity reduces ectoparasite pressure: implications for host life history evolution

A parasite's potential effect, or "pressure", can influence the life history strategy of its host. In environments with high parasite pressure, hosts invest more in anti-parasite defense, which may limit their investment in other life history components, such as survival. This tradeoff is difficult to study in natural populations because pressure is hard to quantify. Pressure is not necessarily correlated with the abundance of the parasite. A host population can be under high pressure, yet have few parasites, because members of the population have invested heavily in defense. Therefore, the extent to which parasite pressure varies among host populations, and the cause of such variation, remain largely undocumented. In this paper we show that birds in arid regions have fewer ectoparasitic lice than birds in humid regions. We show experimentally that low humidity reduces the number of lice on birds, even when host defense is held constant. Comparisons of ambient humidity to humidity beneath the plumage demonstrate that plumage does not provide a buffer for lice against low humidity. Our results confirm that an abiotic factor can cause substantial variation in parasite pressure among host populations. We suggest that humidity may influence host life history evolution through its impact on ectoparasites.     

The genetic population structure of the ant Plagiolepis xene-implications for genetic vulnerability of obligate social parasites

Obligatory social parasites, such as ant species that need colonies of other ant species for reproduction, are rare and many of them are classified as vulnerable. This is especially the case with highly adapted permanent inquilines that are specialised on one or a few host species. Their rarity may be due to reduced dispersal abilities, as a result of reduced body size, altered wing morphology, and curtailed nuptial flight, eventually leading to inbreeding. Furthermore, the host populations may differ in their ability to resist the parasite, yet the conditions of successful parasite invasion are largely unknown. Here we investigated the population structure of the inquiline ant Plagiolepis xene and its host P. pygmaea, using microsatellite data. Genetic differentiation, inbreeding, the effective population size and nest kin structure were analysed. We found that populations of P. xene are established by a single or at most a few individuals, and that the populations were genetically highly differentiated. However, within individual host populations the parasite is able to maintain panmixia, although data on the host suggests that the local distribution of the parasite also follows patterns of substructuring in the host population. Altogether our results suggest that inquiline parasite populations are genetically highly vulnerable.     

Diet quality determines interspecific parasite interactions in host populations

The widespread occurrence of multiple infections and the often vast range of nutritional resources for their hosts allow that interspecific parasite interactions in natural host populations might be determined by host diet quality. Nevertheless, the role of diet quality with respect to multispecies parasite interactions on host population level is not clear. We here tested the effect of host population diet quality on the parasite community in an experimental study using Daphnia populations. We studied the effect of diet quality on Daphnia population demography and the interactions in multispecies parasite infections of this freshwater crustacean host. The results of our experiment show that the fitness of a low‐virulent microsporidian parasite decreased in low, but not in high‐host‐diet quality conditions. Interestingly, infections with the microsporidium protected Daphnia populations against a more virulent bacterial parasite. The observed interspecific parasite interactions are discussed with respect to the role of diet quality‐dependent changes in host fecundity. This study reflects that exploitation competition in multispecies parasite infections is environmentally dependent, more in particular it shows that diet quality affects interspecific parasite competition within a single host and that this can be mediated by host population‐level effects.     

A mathematical model for indirectly transmitted diseases

We consider a mathematical model for the indirect transmission via a contaminated environment of a microparasite between two spatially distributed host populations having non-coincident spatial domains. The parasite is benign in a first population and lethal in the second one. Global existence results are given for the resulting reaction-diffusion system coupled with an ordinary differential equation. Then, invasion and persistence of the parasite are studied. A simplified model for the transmission of a hantavirus from bank vole to human populations is then analysed.     

Similar yet different: co-analysis of the genetic diversity and structure of an invasive nematode parasite and its invasive mammalian host

Animal parasitic nematodes can cause serious diseases and their emergence in new areas can be an issue of major concern for biodiversity conservation and human health. Their ability to adapt to new environments and hosts is likely to be affected by their degree of genetic diversity, with gene flow between distinct populations counteracting genetic drift and increasing effective population size. The raccoon roundworm (Baylisascaris procyonis), a gastrointestinal parasite of the raccoon (Procyon lotor), has increased its global geographic range after being translocated with its host. The raccoon has been introduced multiple times to Germany, but not all its populations are infected with the parasite. While fewer introduced individuals may have led to reduced diversity in the parasite, admixture between different founder populations may have counteracted genetic drift and bottlenecks. Here, we analyse the population genetic structure of the roundworm and its raccoon host at the intersection of distinct raccoon populations infected with B. procyonis. We found evidence for two parasite clusters resulting from independent introductions. Both clusters exhibited an extremely low genetic diversity, suggesting small founding populations subjected to inbreeding and genetic drift with no, or very limited, genetic influx from population admixture. Comparison of the population genetic structures of both host and parasite suggested that the parasite spread to an uninfected raccoon founder population. On the other hand, an almost perfect match between cluster boundaries also suggested that the population genetic structure of B. procyonis has remained stable since its introduction, mirroring that of its raccoon host.     

Keeping the herds healthy and alert: implications of predator control for infectious disease

Predator control programmes are generally implemented in an attempt to increase prey population sizes. However, predator removal could prove harmful to prey populations that are regulated primarily by parasitic infections rather than by predation. We develop models for microparasitic and macroparasitic infection that specify the conditions where predator removal will (a) increase the incidence of parasitic infection, (b) reduce the number of healthy individuals in the prey population and (c) decrease the overall size of the prey population. In general, predator removal is more likely to be harmful when the parasite is highly virulent, macroparasites are highly aggregated in their prey, hosts are long‐lived and the predators select infected prey.     

The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.     

On the capacity of macroparasites to control insect populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.     

Parasite-mediated selection in experimental metapopulations of Daphnia magna

In metapopulations, only a fraction of all local host populations may be infected with a given parasite species, and limited dispersal of parasites suggests that colonization of host populations by parasites may involve only a small number of parasite strains. Using hosts and parasites obtained from a natural metapopulation, we studied the evolutionary consequences of invasion by single strains of parasites in experimental populations of the cyclical parthenogen Daphnia magna. In two experiments, each spanning approximately one season, we monitored clone frequency changes in outdoor container populations consisting of 13 and 19 D. magna clones, respectively. The populations were either infected with single strains of the microsporidian parasites Octosporea bayeri or Ordospora colligata or left unparasitized. In both experiments, infection changed the representation of clones over time significantly, indicating parasite-mediated evolution in the experimental populations. Furthermore, the two parasite species changed clone frequencies differently, suggesting that the interaction between infection and competitive ability of the hosts was specific to the parasite species. Taken together, our results suggest that parasite strains that invade local host populations can lead to evolutionary changes in the genetic composition of the host population and that this change is parasite-species specific.