Ecological conditions that favor the evolution of intermediate-virulence in an environmentally transmitted parasite

In this paper we develop and analyze several populaion-dynamic models of an environmentally transmitted symbiotic parasite infecting an isolated population of susceptible hosts. In our most basic model infection acts only to decrease the average lifetime of the infected host, parasites are only transmitted to uninfected hosts, there is no recovery from infection, and the rate of parasite transmission is an increasing function of the level of parasite virulence. It is shown that invasion of the parasite-free equilibrium cannot occur for virulence levels that are either too high or too low. We then incorporate a number of modifications to the model, among them the possibility that host fertility is reduced by infection, and that transmission rate depends additionally on susceptible host density. It is shown that the essential nature of the conditions for invasion are preserved. Thus, natural selection for intermediate virulence is a generic property of a broad class of population models.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni

The amphipod crustacean Gammarus duebeni hosts two species of vertically transmitted microsporidian parasites, Nosema granulosis and Microsporidium sp. A. Here it is demonstrated that these co-occurring parasite species both cause infected females to produce female-biased broods. A survey of European G. duebeni populations demonstrates that these two parasites co-occur in six of 10 populations. These findings contrast with the theoretical prediction that two vertically transmitted feminizing parasites should not coexist in a panmictic population of susceptible hosts at equilibrium. Possible explanations for the co-occurrence of the two feminizing microsporidia in G. duebeni include the recent invasion of a new parasite, horizontal transmission of one or both parasites and the spread of alleles for resistance to the dominant parasite in host populations.     

Host patch selection induced by parasitism: basic reproduction ratio r(0) and optimal virulence

The effects of parasites on the behavior of their hosts are well documented. For example, parasites may affect the habitat selection of the host individual. We used variables aggregation methods to investigate the way in which parasites affect the spatial pattern of susceptible hosts. We developed a simple epidemiological model, taking into account both the reproduction processes of hosts (density-dependent birth and death) and infection, considered separately on two different patches, and the migration of susceptible hosts between these two patches. We used the complete model of three equations to generate an aggregated model describing the dynamics of the combined susceptible and infected host populations. We obtained the basic reproduction ratio (R(0)) from the aggregated model, and then studied the effect of the migratory behavior of susceptible hosts on the ability of the parasite to invade the system. We also used the basic reproduction ratio to investigate the evolution of parasite virulence in relation to the migration decisions of susceptible hosts. We found that host investment in avoidance of the infected patch leads to an increase in optimal virulence if host investment is costly.     

The evolution of covert,silent infection as a parasite strategy

Many parasites and pathogens cause silent/covert infections in addition to the more obvious infectious disease-causing pathology. Here, we consider how assumptions concerning superinfection, protection and seasonal host birth and transmission rates affect the evolution of such covert infections as a parasite strategy. Regardless of whether there is vertical infection or effects on sterility, overt infection is always disadvantageous in relatively constant host populations unless it provides protection from superinfection. If covert infections are protective, all individuals will enter the covert stage if there is enough vertical transmission, and revert to overt infections after a ‘latent’ period (susceptible, exposed, infected epidemiology). Seasonal variation in transmission rates selects for non-protective covert infections in relatively long-lived hosts with low birth rates typical of many mammals. Variable host population density caused by seasonal birth rates may also select for covert transmission, but in this case it is most likely in short-lived fecund hosts. The covert infections of some insects may therefore be explained by their outbreak population dynamics. However, our models consistently predict proportions of covert infection, which are lower than some of those observed in nature. Higher proportions of covert infection may occur if there is a direct link between covert infection and overt transmission success, the covert infection is protective or the covert state is the result of suppression by the host. Relatively low proportions of covert transmission may, however, be explained as a parasite strategy when transmission opportunities vary.     

A model of predator-prey dynamics as modified by the action of a parasite

A predator-prey population is described in which the prey population may be either a secondary host or a primary host to a parasite, but the predator is always a primary host. Those prey that have been invaded by the parasite have their behavior modified so as to make them more susceptible to predation. The model is described by a system of three autonomous ordinary differential equations. Conditions for persistence of all populations are given in the case that both populations are primary hosts. A brief discussion of the stability of the interior equilibrium is given.     

Population dynamics of botanical epidemics involving primary and secondary infection

In this paper we study the dynamical properties of models for botanical epidemics, especially for soil-borne fungal infection. The models develop several new concepts, involving dual sources of infection, host and inoculum dynamics. Epidemics are modelled with respect to the infection status of whole plants and plant organs (the G model) or to lesion density and size (the SW model). The infection can originate in two sources, either from the initial inoculum (primary infection) or by a direct transmission between plant tissue (secondary infection). The first term corresponds to the transmission through the free-living stages of macroparasites or an external source of infection in certain medical models, whereas the second term is equivalent to direct transmission between the hosts in microparasitic infections. The models allow for dynamics of host growth and inoculum decay. We show that the two models for root and lesion dynamics can be derived as special cases of a single generic model. Analytical and numerical methods are used to analyse the behaviour of the models for static, unlimited (exponential) and asymptotically limited host growth with and without secondary infection, and with and without decay of initial inoculum. The models are shown to exhibit a range of epidemic behaviour within single seasons that extends from simple monotonic increase with saturation of the host population, through temporary plateaux as the system switches from primary to secondary infection, to effective elimination of the pathogen by the host outgrowing the fungal infection. For certain conditions, the equilibrium values are shown to depend on initial conditions. These results have important consequences for the control of plant disease. They can be applied beyond soil-borne plant pathogens to mycorrhizal fungi and aerial pathogens while the principles of primary and secondary infection with host and inoculum dynamics may be used to link classical models for both microparasitic and macroparasitic infections.     

The evolution of parasite virulence and transmission rate in a spatially structured population

If the transmission occurs through local contact of the individuals in a spatially structured population, the evolutionarily stable (ESS) traits of parasite might be quite different from what the classical theory with complete mixing predicts. In this paper, we theoretically study the ESS virulence and transmission rate of a parasite in a lattice-structured host population, in which the host can send progeny only to its neighboring vacant site, and the transmission occurs only in between the infected and the susceptible in the nearest-neighbor sites. Infected host is assumed to be infertile. The analysis based on the pair approximation and the Monte Carlo simulation reveal that the ESS transmission rate and virulence in a lattice-structured population are greatly reduced from those in completely mixing population. Unlike completely mixing populations, the spread of parasite can drive the host to extinction, because the local density of the susceptible next to the infected can remain high even when the global density of host becomes very low. This demographic viscosity and group selection between self-organized spatial clusters of host individuals then leads to an intermediate ESS transmission rate even if there is no tradeoff between transmission rate and virulence. The ESS transmission rate is below the region of parasite-driven extinction by a finite amount for moderately large reproductive rate of host; whereas, the evolution of transmission rate leads to the fade out of parasite for small reproductive rate, and the extinction of host for very large reproductive rate.     

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.     

Scaling and spatial dynamics in plant-pathogen systems: from individuals to populations

Components of transmission for primary infection from soil-borne inoculum and secondary (plant to plant) infection are estimated from experiments involving single plants. The results from these individual-based experiments are used in a probabilistic spatial contact process (cellular automaton) to predict the progress of an epidemic. The model accounts for spatial correlations between infected and susceptible plants due to inhomogeneous mixing caused by restricted movement of the pathogen in soil. It also integrates nonlinearities in infection, including small stochastic differences in primary infection that become amplified by secondary infection. The model predicts both the mean and the variance of the infection dynamics of R. solani when compared with replicated epidemics in populations of plants grown in microcosms. The broader consequences of the combination of experimental and modelling approaches for scaling-up from individual to population behaviour are discussed. <br>     

Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni

Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46% of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45% of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39% of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24%) and survival (44%) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution.     

HIV-1/parasite co-infection and the emergence of new parasite strains

HIV-1 and parasitic infections co-circulate in many populations, and in a few well-studied examples HIV-1 co-infection is known to amplify parasite transmission. There are indications that HIV-1 interacts significantly with many other parasitic infections within individual hosts, but the population-level impacts of co-infection are not well-characterized. Here we consider how alteration of host immune status due to HIV-1 infection may influence the emergence of novel parasite strains. We review clinical and epidemiological evidence from five parasitic diseases (malaria, leishmaniasis, schistosomiasis, trypanosomiasis and strongyloidiasis) with emphasis on how HIV-1 co-infection alters individual susceptibility and infectiousness for the parasites. We then introduce a simple modelling framework that allows us to project how these individual-level properties might influence population-level dynamics. We find that HIV-1 can facilitate invasion by parasite strains in many circumstances and we identify threshold values of HIV-1 prevalence that allow otherwise unsustainable parasite strains to invade successfully. Definitive evidence to test these predicted effects is largely lacking, and we conclude by discussing challenges in interpreting available data and priorities for future studies.     

Host age modulates within-host parasite competition

In many host populations, one of the most striking differences among hosts is their age. While parasite prevalence differences in relation to host age are well known, little is known on how host age impacts ecological and evolutionary dynamics of diseases. Using two clones of the water flea Daphnia magna and two clones of its bacterial parasite Pasteuria ramosa, we examined how host age at exposure influences within-host parasite competition and virulence. We found that multiply-exposed hosts were more susceptible to infection and suffered higher mortality than singly-exposed hosts. Hosts oldest at exposure were least often infected and vice versa. Furthermore, we found that in young multiply-exposed hosts competition was weak, allowing coexistence and transmission of both parasite clones, whereas in older multiply-exposed hosts competitive exclusion was observed. Thus, age-dependent parasite exposure and host demography (age structure) could together play an important role in mediating parasite evolution. At the individual level, our results demonstrate a previously unnoticed interaction of the host''s immune system with host age, suggesting that the specificity of immune function changes as hosts mature. Therefore, evolutionary models of parasite virulence might benefit from incorporating age-dependent epidemiological parameters.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Dose-dependent infection rates of parasites produce the Allee effect in epidemiology

In many epidemiological models of microparasitic infections it is assumed that the infection process is governed by the mass-action principle, i.e. that the infection rate per host and per parasite is a constant. Furthermore, the parasite-induced host mortality (parasite virulence) and the reproduction rate of the parasite are often assumed to be independent of the infecting parasite dose. However, there is empirical evidence against those three assumptions: the infection rate per host is often found to be a sigmoidal rather than a linear function of the parasite dose to which it is exposed; and the lifespan of infected hosts as well as the reproduction rate of the parasite are often negatively correlated with the parasite dose. Here, we incorporate dose dependences into the standard modelling framework for microparasitic infections, and draw conclusions on the resulting dynamics. Our model displays an Allee effect that is characterized by an invasion threshold for the parasite. Furthermore, in contrast to standard epidemiological models a parasite strain needs to have a basic reproductive rate that is substantially greater than 1 to establish an infection. Thus, the conditions for successful invasion of the parasite are more restrictive than in mass-action infection models. The analysis further suggests that negative correlations of the parasite dose with host lifespan and the parasite reproduction rate helps the parasite to overcome the invasion constraints of the Allee-type dynamics.     

Local adaptation of a holoparasitic plant,Cuscuta europaea: variation among populations

Locally adapted parasites have higher infectivity and/or fitness on sympatric than on allopatric hosts. We tested local adaptation of a holoparasitic plant, Cuscuta europaea, to its host plant, Urtica dioica. We infected hosts from five sites with holoparasites from the same five sites and measured local adaptation in terms of infectivity and parasite performance (biomass) in a reciprocal cross‐infection experiment. The virulence of the parasite did not differ between sympatric and allopatric hosts. Overall, parasites had higher infectivity on sympatric hosts but infectivity and parasite performance varied among populations. Parasites from one of the populations showed local adaptation in terms of performance, whereas parasites from one of the populations had higher infectivity on allopatric hosts compared with sympatric hosts. This among‐population variation may be explained by random variation in parasite adaptation to host populations or by time‐lagged co‐evolutionary oscillations that lead to fluctuations in the level of local adaptation.     

Invasion and persistence of plant parasites in a spatially structured host population

Spatial structure is of central importance in the dynamics of plant-parasite interactions and is imposed by the growth habit and distribution of host plants and by parasite dispersal which is frequently restricted. To investigate the effects of spatial heterogeneity on the dynamics of plant parasites we introduce a simple model for epidemic development within a spatially structured host population. Here the host population is subdivided into a number of patches which are linked to allow for transmission from one patch to another with the connections defining the spatial structure of the host population. Three key parameters are identified that play a critical role in the ability of the parasite to invade and persist within the host population: the within-patch parasite basic reproductive number which characterises the infection dynamics at the local spatial scale; and the neighbourhood of interaction which describes which patches interact with which and the strength of coupling between patches within the neighbourhood which together characterise the spread of the parasite over larger spatial scales. Using both deterministic and stochastic formulations of the model, we investigate how the thresholds and probabilities of invasion and persistence are affected by these parameters, by demographic stochasticity and by differences in the initial level of infection.     

Testing a key assumption of host‐pathogen theory: density and disease transmission

Conventional disease theory suggests that extinction with density‐dependent transmission is unlikely as the threshold host density (KT) is greater than zero. Extinction may result if transmission is frequency dependent or the pathogen has an environmental reservoir. Given the importance of understanding how pathogens affect species richness and diversity there are few empirical tests of these conclusions. We used an Ambystoma tigrinum–Ambystoma tigrinum virus (ATV) model system in the laboratory to examine disease transmission dynamics. Susceptible A. tigrinum larvae were exposed to three different densities and proportions of infected larvae for 24 h. We then housed susceptible hosts individually for 28 days and monitored them for infection. The density of infected hosts to which susceptible hosts were exposed was the best predictor of infection (p=0.037). There was no effect of host clutch on the probability of becoming infected (p=0.67). Larvae in the highest density treatments died sooner than larvae in lower density treatments (p<0.001). Asymptomatic but infected hosts shed sufficient virus into the water in a 24‐h period to infect susceptible hosts without any direct contact between individuals. ATV transmission was best described by a power function, leading to the prediction that extinction of A. tigrinum as a result of this pathogen is unlikely. Indeed, field observations show that larval salamander populations that experience ATV‐driven epidemics may decrease, but not to extinction, and then recover. Disease is proposed as a possible explanation for the global decline of amphibians. Ranaviruses infect many amphibian populations, but based on our results may not be a general cause of declines to extinction. In contrast, frequency dependent transmission, environmental reservoirs and alternative hosts may be the most likely explanation for the enigmatic decline, at times to extinction, of some amphibian populations as a result of emerging infectious diseases, like the chytrid fungus Batrachochytrium dendrobatidis.     

Genetic variation changes the interactions between the parasitic plant-ecosystem engineer Rhinanthus and its hosts

Within-species genetic variation is a potent factor influencing between-species interactions and community-level structure. Species of the hemi-parasitic plant genus Rhinanthus act as ecosystem engineers, significantly altering above- and below-ground community structure in grasslands. Here, we show the importance of genotypic variation within a single host species (barley-Hordeum vulgare), and population-level variation among two species of parasite (Rhinanthus minor and Rhinanthus angustifolius) on the outcome of parasite infection for both partners. We measured host fitness (number of seeds) and calculated parasite virulence as the difference in seed set between infected and uninfected hosts (the inverse of host tolerance). Virulence was determined by genetic variation within the host species and among the parasite species, but R. angustifolius was consistently more virulent than R. minor. The most tolerant host had the lowest inherent fitness and did not gain a fitness advantage over other infected hosts. We measured parasite size as a proxy for transmission ability (ability to infect further hosts) and host resistance. Parasite size depended on the specific combination of host genotype, parasite species and parasite population, and no species was consistently larger. We demonstrate that the outcome of infection by Rhinanthus depends not only on the host species, but also on the underlying genetics of both host and parasite. Thus, genetic variations within host and parasite are probably essential components of the ecosystem-altering effects of Rhinanthus.