Relationship between structure and stability of a Halipegus occidualis component population in green frogs: a test of selective treatment

The aggregated nature of helminth parasite populations has led to the suggestion that selectively treating heavily infected hosts can efficiently reduce parasite abundance and morbidity within a host population. Moreover, it has been postulated that a selective treatment protocol might have long-term effects on parasite transmission by disrupting the stability attributed to aggregated parasite population distributions by theoretical models. Long-term investigation has demonstrated year-to-year consistency in the population dynamics of Halipegus occidualis in green frogs from Charlie's Pond, North Carolina. In 1996, removal of all but 1 worm from each frog with > or =15 worms reduced the estimated component worm population by 45%, thereby decreasing mean intensity and aggregation (variance-to-mean ratio) of H. occidualis in the frogs by 85% and 63%, respectively. The following year, mean intensity, aggregation, and host colonization trends returned to pretreatment levels, indicating no effect of worm removal and demonstrating the stability of this host-parasite system. Although this result might be attributable to inefficient treatment or the presence of infection reservoirs, it is suggested that parasite population stability in this system might be governed by prevalence rather than intensity of adult worms. Therefore, repeated selective treatment might effectively modify intensity-dependent morbidity in similar host-parasite systems but should not affect further parasite transmission.     

Host-parasite dynamics and the evolution of host immunity and parasite fecundity strategies

We explore evolutionarily stable co-evolution of host-macroparasite interactions in a discrete-time two-species population dynamics model, in which the dynamics may be stable, cyclic or chaotic. The macroparasites are assumed to harm host individuals through decreased reproductive output. Hosts may develop costly immune responses to defend themselves against parasites. Parasites compete with conspecifics by adjusting their fecundities. Overall, the presence of both parasites and the immune response in hosts produces more stable dynamics and lower host population sizes than that observed in the absence of the parasites. In our evolutionary analyses, we show that maximum parasite fecundity is always an evolutionarily stable strategy (ESS), irrespective of the type of population interaction, and that maximum parasite fecundity generally induces a minimum parasite population size through over-exploitation of the host. Phenotypic polymorphisms with respect to immunity in the host species are common and expected in ESS host strategies: the benefits of immunication depend on the frequency of the immune hosts in the population. In particular, the steady-state proportions of immune hosts depend, in addition to all the parameters of the parasite dynamics only on the cost of immunity and on the virulence of parasites in susceptible hosts. The implicit ecological dynamics of the host-parasite interaction affect the proportion of immune host individuals in the population. Furthermore, when changes in certain population parameters cause the dynamics of the host-parasite interaction to move from stability to cyclicity and then to chaos, the proportion of immune hosts tends to decrease; however, we also detected counter-examples to this result. As a whole, incorporating immunological and genetic aspects, as well as life-history trade-offs, into host-macroparasite dynamics produces a rich extension to the patterns observed in the models of ecological interactions and epidemics, and deserves more attention than is currently the case.     

From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

Using social networks to deduce whether residents or dispersers spread parasites in a lizard population

1. Heterogeneity of host behaviour can play an important role in the spread of parasites and pathogens around wildlife populations. Social networks have previously been suggested to represent transmission pathways within a population, but where the dynamics of host-parasite interactions are difficult to observe, networks may also be used to provide insights into transmission processes. 2. Pygmy bluetongue lizards, Tiliqua adelaidensis, occupy individual territories, live exclusively in burrows constructed by spiders in Australian native grasslands and are hosts to a tick, Bothriocroton hydrosauri, and a nematode, Pharyngodon wandillahensis. 3. On five monthly occasions, the locations of all individual lizards in three study plots were used to construct weighted, undirected networks based on proximity of adjacent burrows. 4. The networks were used to explore alternative hypotheses about the spread of each parasite through the population: that stable population members that remained in the same burrow over the study period played a major role in influencing the pattern of infection or that dispersing individuals played a more significant role. 5. For ticks, host individuals that were infected were more connected in the network than uninfected hosts and this relationship remained significant for connections to residents in the population, but not for connections to dispersers. 6. For nematodes, infected and uninfected hosts did not differ in their overall strength of connection in the network, but infected hosts were more connected to dispersers than were uninfected hosts, suggesting that lizards moving across the population are the major agents for the transmission of nematodes. 7. This study shows how network analyses can provide new insights into alternative pathways of parasite spread in wildlife populations, where it is difficult to make direct observations of transmission-related behaviours.     

Conflict between parasites with different transmission strategies infecting an amphipod host

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host-parasite relationships.     

Genetics of host-parasite interactions

The evolution of host susceptibility or resistance to parasites has important consequences for the evolution of parasite virulence, host sexual selection, population dynamics of both host and parasite populations, and programs of biological control. The general observation of a fraction of Individuals within a population that is not parasitized, and/or the variability in parasite intensity among hosts, may reflect several phenomena acting at different levels of ecological organization. Yet, host-parasite coevolution requires host susceptibility and parasite virulence to be genetically variable. In spite of evolutionary and epidemiological implications of genetic heterogeneities in host-parasite systems, evidence concerning natural populations is still scarce. Here, we wish to emphasize why we need a better knowledge of the genetics of host-parasite interaction in natural populations and to review the evidence concerning the heritability of host susceptibility or resistance to parasites in natural populations of animals.     

Parasitoid-mediated transmission of an iridescent virus

We examined the interaction between an invertebrate iridescent virus (IIV) isolated from Spodoptera frugiperda (J.E. Smith) and the solitary ichneumonid endoparasitoid Eiphosoma vitticolle Cresson. In choice tests, parasitoids examined and stung significantly more virus infected than healthy larvae, apparently due to a lack of defense reaction in virus infected hosts. Parasitoid-mediated virus transmission was observed in 100% of the female parasitoids that stung a virus infected host in the laboratory. Each female parasitoid transmitted the virus to an average (+/-SE) of 3.7+/-0.3 larvae immediately after stinging an infected larva. Caged field experiments supported this result; virus transmission to healthy larvae only occurred in cages containing infected hosts (as inoculum) and parasitoids (as vectors). The virus was highly detrimental to parasitoid development because of premature host death and lethal infection of the developing endoparasitoid. Female parasitoids that emerged from virus infected hosts did not transmit the virus to healthy hosts. We suggest that the polyphagous habits of many noctuid parasitoids combined with the catholic host range of most IIVs may represent a mechanism for the transmission of IIVs between different host species in the field.     

On the stability of polymorphic host-pathogen populations

The stability of populations of hosts and micro-parasites is investigated where each consists of n varieties that are equal in every respect except that each strain of parasites can infect only one specific strain of hosts and none of the others. Collectively the host strains are limited by a carrying capacity and through this limitation the host populations interact with each other. Hosts are assumed to reproduce asexually or such that different strains do not mate or are not fertile if they do. When the excess death rate caused by the pathogenic parasites is sufficiently large, then the host population is regulated to an equilibrium below the carrying capacity of the environment. This polymorphic equilibrium is shown to be locally asymptotically stable. When one of the parasite strains is absent, then all the other strains die out asymptotically. However, if host resistance to all infectious strains of parasites is achieved at the cost of a lower birthrate of the resistant host strain, then, if a certain condition for the various parameters is satisfied, stable coexistence between infected and resistant hosts is possible. There are many examples where susceptibility and resistance of hosts depends upon the conformation of specific proteins that are involved in host-parasite interactions and hence upon alleles at genetic loci that code for these proteins. We propose that polymorphism in wildtype populations which has been the subject of much theorizing in mathematical genetics may be due to host-pathogen interactions. Our model suggests how a polymorphic population, once established, can remain polymorphic indefinitely.     

How parasites can promote the expression of social behaviour in their hosts

Recent theory on the role of parasites in the evolution of social behaviour has emphasized the costs of social behaviour to hosts. However, parasites whose primary effect on host fitness is to reduce fecundity can favour the evolutionary origin or maintenance of social behaviour, including eusociality, under certain conditions. If the parasites are not readily transmitted among members of social groups, then other group members will not be selected to reject infected individuals as social partners, nor will adaptive suicide or avoidance of grouping be selectively favoured for infected individuals. Rather, total or partial parasitic castration may promote the expression of helping behaviour by infected individuals. Some parasites may therefore act to increase variance in direct reproductive value within populations or societies, and to promote reproductive division of labour. The necessary conditions of reduced host fecundity and low within-group transmission are met in some insect-parasite systems, and could occur in other host-parasite systems as well.     

Selective predation and productivity jointly drive complex behavior in host-parasite systems

Successful invasion of a parasite into a host population and resulting host-parasite dynamics can depend crucially on other members of a host's community such as predators. We do not fully understand how predation intensity and selectivity shape host-parasite dynamics because the interplay between predator density, predator foraging behavior, and ecosystem productivity remains incompletely explored. By modifying a standard susceptible-infected model, we show how productivity can modulate complex behavior induced by saturating and selective foraging behavior of predators in an otherwise stable host-parasite system. When predators strongly prefer parasitized hosts, the host-parasite system can oscillate, but predators can also create alternative stable states, Allee effects, and catastrophic extinction of parasites. In the latter three cases, parasites have difficulty invading and/or persisting in ecosystems. When predators are intermediately selective, these more complex behaviors become less important, but the host-parasite system can switch from stable to oscillating and then back to stable states along a gradient of predator control. Surprisingly, at higher productivity, predators that neutrally select or avoid parasitized hosts can catalyze extinction of both hosts and parasites. Thus, synergy between two enemies can end disastrously for the host. Such diverse outcomes underscore the crucial importance of the community and ecosystem context in which host-parasite interactions occur.     

Influencing random transmission is a neutral character in hosts

This study introduces an individual-based model on a host-parasite assemblage to investigate whether hosts are necessarily selected for obstructing the transmission of virulent parasites to conspecifics. Contrary to the widespread notion, a host's ability to influence parasite transmission within the host population is a neutral character provided that parasite transmission routes are random, with no reference to genetic relatedness. Due to a lack of selection pressure under such circumstances, hosts may fail to evolve counteradaptations against manipulations by parasites to enhance transmission. However, vertically biased transmission (biased toward kin) selects hosts for a decrease of parasite transmission, while it is also known to select parasites to decrease virulence. Horizontally biased transmission routes (biased toward nonrelated conspecifics) select hosts to increase parasite transmission. In this case, their interests coincide with that of their virulent parasites in enhancing transmission to conspecifics. This finding yields the predictions that hosts infected by virulent pathogens, but unable to recover from disease, should be prone to emigrate from their natal territories and also to enhance transmission at a distance from their natal ranges. These results may considerably improve our understanding of the epidemiology of contagious pathogens and the evolution of social and sexual behavior in host species.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Octosporea bayeri: fumidil B inhibits vertical transmission in Daphnia magna

Microsporidia are a highly successful and ecologically diverse group of parasites, and thus represent interesting model systems for research on host-parasite interactions. However, such research often requires the ability to cure hosts of infections, a difficult task, given the short lifespan of most invertebrates and the efficient vertical transmission of some parasites. To our knowledge, few treatments are available to cure microsporidiosis in invertebrate hosts, and protocols have not yet been developed to inhibit vertical transmission and thereby cure host lines. We present a protocol for inhibiting vertical transmission of the microsporidian parasite Octosporea bayeri in the freshwater crustacean Daphnia magna. We used 100 mg/L Fumidil B dissolved in the culture medium of the host. This technique allowed Daphnia to survive and reproduce and inhibited vertical transmission of the parasite. The method presented here may be of general interest for other aquatic host-parasite systems involving microsporidia.     

Populations and infectious diseases: Dynamics and evolution

The host-parasite or host-pathogen system was analyzed from dynamical and evolutionary viewpoints using simple mathematical models incorporating vertical transmission, immunity and its loss. We first analyzed a model without density regulation of host population. In the analysis on dynamics, the condition for the pathogen to work as a density regulating factor was obtained. In the analysis on evolution, criteria for the evolution of host and pathogen were proposed. These criteria implies that the evolution of hosts should result in an increase in infected host density, whereas the evolution of pathogens a decrease in susceptible host density. The direction of evolution at some parameters of host and that of pathogen were examined when the parameters were independently and freely changeable. Among the parameters, only reduction in additional mortality due to infection was the evolutionary trend common to both host and pathogen. In all the other parameters examined, trend of evolution predicted in host is reversed in pathogen. We then analyzed whether the obtained criteria still hold in models with density regulation of hosts. Using randomly generated parameter sets, we obtained the result that the criteria should hold very likely though they do not always hold. We discussed evolution of virulence when there is a constraint between the traits.     

A model for the coevolution of immunity and immune evasion in vector-borne diseases with implications for the epidemiology of malaria

We describe a model of host-parasite coevolution, where the interaction depends on the investments by the host in its immune response and by the parasite in its ability to suppress (or evade) its host's immune response. We base our model on the interaction between malaria parasites and their mosquito hosts and thus describe the epidemiological dynamics with the Macdonald-Ross equation of malaria epidemiology. The qualitative predictions of the model are most sensitive to the cost of the immune response and to the intensity of transmission. If transmission is weak or the cost of immunity is low, the system evolves to a coevolutionarily stable equilibrium at intermediate levels of investment (and, generally, at a low frequency of resistance). At a higher cost of immunity and as transmission intensifies, the system is not evolutionarily stable but rather cycles around intermediate levels of investment. At more intense transmission, neither host nor parasite invests any resources in dominating its partner so that no resistance is observed in the population. These results may help to explain the lack of encapsulated malaria parasites generally observed in natural populations of mosquito vectors, despite strong selection pressure for resistance in areas of very intense transmission.     

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.     

The Relationship between Parasite Fitness and Host Condition in an Insect - Virus System

Research in host-parasite evolutionary ecology has demonstrated that environmental variation plays a large role in mediating the outcome of parasite infection. For example, crowding or low food availability can reduce host condition and make them more vulnerable to parasite infection. This observation that poor-condition hosts often suffer more from parasite infection compared to healthy hosts has led to the assumption that parasite productivity is higher in poor-condition hosts. However, the ubiquity of this negative relationship between host condition and parasite fitness is unknown. Moreover, examining the effect of environmental variation on parasite fitness has been largely overlooked in the host-parasite literature. Here we investigate the relationship between parasite fitness and host condition by using a laboratory experiment with the cabbage looper Trichoplusia ni and its viral pathogen, AcMNPV, and by surveying published host-parasite literature. Our experiments demonstrated that virus productivity was positively correlated with host food availability and the literature survey revealed both positive and negative relationships between host condition and parasite fitness. Together these data demonstrate that contrary to previous assumptions, parasite fitness can be positively or negatively correlated with host fitness. We discuss the significance of these findings for host-parasite population biology.     

Novel application of species richness estimators to predict the host range of parasites

Host range is a critical life history trait of parasites, influencing prevalence, virulence and ultimately determining their distributional extent. Current approaches to measure host range are sensitive to sampling effort, the number of known hosts increasing with more records. Here, we develop a novel application of results-based stopping rules to determine how many hosts should be sampled to yield stable estimates of the number of primary hosts within regions, then use species richness estimation to predict host ranges of parasites across their distributional ranges. We selected three mistletoe species (hemiparasitic plants in the Loranthaceae) to evaluate our approach: a strict host specialist (Amyema lucasii, dependent on a single host species), an intermediate species (Amyema quandang, dependent on hosts in one genus) and a generalist (Lysiana exocarpi, dependent on many genera across multiple families), comparing results from geographically-stratified surveys against known host lists derived from herbarium specimens. The results-based stopping rule (stop sampling bioregion once observed host richness exceeds 80% of the host richness predicted using the Abundance-based Coverage Estimator) worked well for most bioregions studied, being satisfied after three to six sampling plots (each representing 25 host trees) but was unreliable in those bioregions with high host richness or high proportions of rare hosts. Although generating stable predictions of host range with minimal variation among six estimators trialled, distribution-wide estimates fell well short of the number of hosts known from herbarium records. This mismatch, coupled with the discovery of nine previously unrecorded mistletoe-host combinations, further demonstrates the limited ecological relevance of simple host-parasite lists. By collecting estimates of host range of constrained completeness, our approach maximises sampling efficiency while generating comparable estimates of the number of primary hosts, with broad applicability to many host-parasite systems.     

The evolution of parasite virulence, superinfection, and host resistance

We analyze the evolutionary consequences of host resistance (the ability to decrease the probability of being infected by parasites) for the evolution of parasite virulence (the deleterious effect of a parasite on its host). When only single infections occur, host resistance does not affect the evolution of parasite virulence. However, when superinfections occur, resistance tends to decrease the evolutionarily stable (ES) level of parasite virulence. We first study a simple model in which the host does not coevolve with the parasite (i.e., the frequency of resistant hosts is independent of the parasite). We show that a higher proportion of resistant host decreases the ES level of parasite virulence. Higher levels of the efficiency of host resistance, however, do not always decrease the ES parasite virulence. The implications of these results for virulence management (evolutionary consequences of public health policies) are discussed. Second, we analyze the case where host resistance is allowed to coevolve with parasite virulence using the classical gene-for-gene (GFG) model of host-parasite interaction. It is shown that GFG coevolution leads to lower parasite virulence (in comparison with a fully susceptible host population). The model clarifies and relates the different components of the cost of parasitism: infectivity (ability to infect the host) and virulence (deleterious effect) in an evolutionary perspective.     

Microsporidian life cycles and diversity: the relationship between virulence and transmission

The microsporidia are obligate intracellular parasites which have diverse life cycles involving both horizontal and vertical transmission and parasitise a wide range of vertebrate and invertebrate hosts. In this paper we consider the life cycles and diversity of the microsporidia. We focus in particular on the relationship between parasite transmission and virulence and its implications for host-parasite coevolution. The use of horizontal and vertical routes of transmission varies between species and there is a strong link between transmission and virulence. Horizontal transmission is characterised by a high parasite burden and associated pathogenicity. In contrast, vertical transmission is characterised by low virulence, which has led to under-reporting of this important transmission route. Vertically transmitted microsporidia may also cause male killing or feminisation of their host, with implications for host population sex ratio and stability. Phylogenetic analysis shows that vertical transmission occurs in diverse branches of the Microspora. We find that there is evidence for vertical transmission in both vertebrate and invertebrate hosts and conclude that it is a common or possibly even ubiquitous transmission route within this phylum.