Parasite‐induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not?

Parasite manipulation of host behaviour is a compelling example of the extended phenotype. However, in many cases, such manipulation may be incorrectly assumed. Previous work has demonstrated that Austrovenus stuchburyi cockles stranded on mud-flat surfaces due to an inability to re-burrow both contain significantly more metacercariae of the trematode Curtuteria australis and are predated by the definitive host of this parasite at a faster rate than burrowed cockles. These results have been interpreted as strong evidence for a manipulation of cockle behaviour by the trematode to facilitate transmission to the definitive host. The model presented here, however, indicates that the selective advantage to the parasite of the altered host behaviour is currently of a negligible level at our study site that is highly unlikely to have been realized as an adaptation over evolutionary time. Hence, there are no grounds on which the more parsimonious explanation, that the altered host behaviour observed is simply an incidental side-effect of infection, can be rejected. We thus maintain that for any change in the behaviour of infected hosts to be confirmed as potentially a parasite trait that has evolved in response to selection, the adaptive benefit taking into account the entire parasite life cycle may need to be considered.     

Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context

Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan parasite Pomphorhynchus laevis and its effect on the immunity and behaviour of its gammarid intermediate host Gammarus roeseli. This was done in France (an area for which G. roeseli is a recent invader) and Hungary (an area from which G. roeseli was believed to be native). As expected, we found no alteration in G. roeseli's immune defence and behaviour associated with infection by P. laevis in localities, where the gammarid is invasive. Unexpectedly, we found similar results in Hungarian populations, where the parasite was even more exposed to the host immune response. Whilst these results suggest maladaptation of the parasite to the gammarid in both countries, they also suggest that the gammarid host might be locally adapted to the parasite. Genetic analyses were performed on both the parasite and the host and the results suggest that the two subsets of populations we studied harbour rather isolated host-parasite systems, both probably deriving from a common ancestral population. We propose that G. roeseli is also of recent acquisition in Hungary, and that a recent co-evolutionary history between P. laevis and G. roeseli in association with a long generation time in the parasite has constrained parasite adaptations in Europe or even favoured host adaptation to the parasite.     

The role of parasites and pathogens in influencing generalised anxiety and predation-related fear in the mammalian central nervous system

This article is part of a Special Issue "Neuroendocrine-Immune Axis in Health and Disease." Behavioural and neurophysiological traits and responses associated with anxiety and predation-related fear have been well documented in rodent models. Certain parasites and pathogens which rely on predation for transmission appear able to manipulate these, often innate, traits to increase the likelihood of their life-cycle being completed. This can occur through a range of mechanisms, such as alteration of hormonal and neurotransmitter communication and/or direct interference with the neurons and brain regions that mediate behavioural expression. Whilst some post-infection behavioural changes may reflect 'general sickness' or a pathological by-product of infection, others may have a specific adaptive advantage to the parasite and be indicative of active manipulation of host behaviour. Here we review the key mechanisms by which anxiety and predation-related fears are controlled in mammals, before exploring evidence for how some infectious agents may manipulate these mechanisms. The protozoan Toxoplasma gondii, the causative agent of toxoplasmosis, is focused on as a prime example. Selective pressures appear to have allowed this parasite to evolve strategies to alter the behaviour in its natural intermediate rodent host. Latent infection has also been associated with a range of altered behavioural profiles, from subtle to severe, in other secondary host species including humans. In addition to enhancing our knowledge of the evolution of parasite manipulation in general, to further our understanding of how and when these potential changes to human host behaviour occur, and how we may prevent or manage them, it is imperative to elucidate the associated mechanisms involved.     

Local adaptation of a parasite to solar radiation impacts disease transmission potential,spore yield,and host fecundity*

Environmentally transmitted parasites spend time in the abiotic environment, where they are subjected to a variety of stressors. Learning how they face this challenge is essential if we are to understand how host–parasite interactions may vary across environmental gradients. We used a zooplankton–bacteria host–parasite system where availability of sunlight (solar radiation) influences disease dynamics to look for evidence of parasite local adaptation to sunlight exposure. We also examined how variation in sunlight tolerance among parasite strains impacted host reproduction. Parasite strains collected from clearer lakes (with greater sunlight penetration) were most tolerant of the negative impacts of sunlight exposure, suggesting local adaptation to sunlight conditions. This adaptation came with both a cost and a benefit for parasites: parasite strains from clearer lakes produced relatively fewer transmission stages (spores) but these strains were more infective. After experimental sunlight exposure, the most sunlight-tolerant parasite strains reduced host fecundity just as much as spores that were never exposed to sunlight. Sunlight availability varies greatly among lakes around the world. Our results suggest that the selective pressure sunlight exposure exerts on parasites may impact both parasite and host fitness, potentially driving variation in disease epidemics and host population dynamics across sunlight availability gradients.     

Novel epidemiological model of gastrointestinal nematode infection to assess grazing cattle resilience by integrating host growth,parasite, grass and environmental dynamics

Gastrointestinal nematode (GIN) infections are ubiquitous and often cause morbidity and reduced performance in livestock. Emerging anthelmintic resistance and increasing change in climate patterns require evaluation of alternatives to traditional treatment and management practices. Mathematical models of parasite transmission between hosts and the environment have contributed towards the design of appropriate control strategies in ruminants, but have yet to account for relationships between climate, infection pressure, immunity, resources, and growth. Here, we develop a new epidemiological model of GIN transmission in a herd of grazing cattle, including host tolerance (body weight and feed intake), parasite burden and acquisition of immunity, together with weather-dependent development of parasite free-living stages, and the influence of grass availability on parasite transmission. Dynamic host, parasite and environmental factors drive a variable rate of transmission. Using literature sources, the model was parametrised for Ostertagia ostertagi, the prevailing pathogenic GIN in grazing cattle populations in temperate climates. Model outputs were validated on published empirical studies from first season grazing cattle in northern Europe. These results show satisfactory qualitative and quantitative performance of the model; they also indicate the model may approximate the dynamics of grazing systems under co-infection by O. ostertagi and Cooperia oncophora, a second GIN species common in cattle. In addition, model behaviour was explored under illustrative anthelmintic treatment strategies, considering impacts on parasitological and performance variables. The model has potential for extension to explore altered infection dynamics as a result of management and climate change, and to optimise treatment strategies accordingly. As the first known mechanistic model to combine parasitic and free-living stages of GIN with host feed-intake and growth, it is well suited to predict complex system responses under non-stationary conditions. We discuss the implications, limitations and extensions of the model, and its potential to assist in the development of sustainable parasite control strategies.     

Effects of the trematode Maritrema novaezealandensis on the behaviour of its amphipod host: adaptive or not?

There are many recorded cases of parasites that are capable of altering the behaviour of their host to enhance their transmission efficiency. However, not all of these cases are necessarily the results of the parasites actively manipulating host behaviour; they may rather be the 'by-products' of pathology caused by the parasite's presence. This study investigates the effect of the microphallid trematode Maritrema novaezealandensis on the behaviour of one of its crustacean intermediate hosts, the amphipod Paracalliope novizealandiae. Uninfected amphipods were experimentally infected by exposure to M. novaezealandensis cercariae. The activity level and vertical position of experimentally infected amphipods were compared with uninfected amphipods at 2 weeks and 6 weeks post-infection, i.e. both before and after the parasite achieved infectivity to its definitive host. Infected amphipods were found to exhibit significantly lower levels of activity and to occur significantly lower in the water column than uninfected controls during both periods. Based on the timing of the change in behaviour exhibited by infected amphipods, the results suggest that the altered behaviour exhibited by P. novizealandiae infected with M. novaezealandensis is most likely due to pathology caused by the parasite rather than a case of active, and adaptive, behavioural manipulation.     

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.     

Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus)

The behaviour of dace infected with Diplostomum spathaceum was investigated in the laboratory. As the number of parasites present in the eye increased, the efficiency with which the fish fed on Gammarus pulex declined. The loss of efficiency was compensated for by an increase in the time devoted to feeding. Heavily infected fish spent more time in the surface layers of the water. This may increase the likelihood that a gull might eat the fish and thereby continue the life-cycle of the parasite. The parasite modifies the behaviour of its host in a way that increases the parasite's chances of survival at the expense of the host.     

An acanthocephalan parasite boosts the escape performance of its intermediate host facing non-host predators

Among the potential effects of parasitism on host condition, the 'increased host abilities' hypothesis is a counterintuitive pattern which might be predicted in complex-life-cycle parasites. In the case of trophic transmission, a parasite increasing its intermediate host's performance facing non-host predators improves its probability of transmission to an adequate, definitive host. In the present study, we investigated the cost of infection with the acanthocephalan Polymorphus minutus on the locomotor/escape performance of its intermediate host, the crustacean Gammarus roeseli. This parasite alters the behaviour of its intermediate host making it more vulnerable to predation by avian definitive hosts. We assessed the swimming speeds of gammarids using a stressful treatment and their escape abilities under predation pressure. Despite the encystment of P. minutus in the abdomen of its intermediate host, infected amphipods had significantly higher swimming speeds than uninfected ones (increases of up to 35%). Furthermore, when interacting with the non-host crustacean predator Dikerogammarus villosus, the highest escape speeds and greatest distances covered by invertebrates were observed for parasitized animals. The altered behaviour observed among the manipulated invertebrates supported the 'increased host abilities' hypothesis, which has until now remained untested experimentally. The tactic of increasing the ability of infected intermediate hosts to evade potential predation attempts by non-host species is discussed.     

Anthelmintic resistance revisited: under-dosing, chemoprophylactic strategies, and mating probabilities

Deterministic and stochastic models are used to examine the evolution of anthelmintic resistance among trichostrongylid parasites of domestic ruminants. We find that the relative selection pressures exerted by chemoprophylactic (preventive) control strategies, chemotherapeutic (salvage) control strategies, and regimens involving "under-dosing" are critically dependent on a variety of host and parasite parameters (particularly host immunity and grazing behaviour, parasite fecundity, and the survival of the free-living stages on the pasture). Chemoprophylactic strategies are not necessarily more likely to exert a stronger selection pressure than chemotherapeutic strategies. Similarly, as one reduces dosage levels, there is a range of dose levels where under-dosing promotes resistance and a range of dose levels where under-dosing impedes resistance. The most dangerous dose is either that necessary to kill all the susceptible homozygotes, or that necessary to kill all the susceptible homozygotes and all the heterozygotes. Which one prevails depends upon model parameters. The stochastic formulation indicates that spatial heterogeneity in transmission may be a significant force in promoting the spread of resistant genotypes--at least when infection is at low levels.     

When should a trophically transmitted parasite exploit host compensatory responses?

Parasites are known to manipulate the behavior of their hosts in ways that increase their probability of transmission. Theoretically, different evolutionary routes can lead to host manipulation, but much research has concentrated on the ‘manipulation hypothesis’ sensu stricto. Among the arsenal of host compensatory responses, however, some seem to be compatible with the parasite objectives. Another way for parasites to achieve transmission, therefore, would be to trigger specific host compensatory responses. In order to explore the conditions favoring this manipulative strategy, we developed a simulation model in which parasites may affect their hosts' behavior by using two nonmutually exclusive strategies: a manipulation sensu stricto strategy and a strategy based on the exploitation of host compensatory responses. Our model predicts that the exploitation of host compensatory responses can be evolutionary stable when the alteration improves the susceptibility to predation by final hosts without compromising host survival during parasite development. Inversely, when the behavioral modification resulting from a compensatory response conflicts with the host's interest we expect parasites to use both strategies. From this result, we conclude that the strategy based on the exploitation of host compensatory responses should be more common among nontrophically transmitted parasites. Furthermore, our findings indicate that the transmission rate of parasites in a definitive host is highest when each of the two strategies affects different traits, which supports the hypothesis that host manipulation is a multidimensional phenomenon in which each altered trait contributes independently to increase parasite transmission efficiency.     

Host behaviour–parasite feedback: an essential link between animal behaviour and disease ecology

Animal behaviour and the ecology and evolution of parasites are inextricably linked. For this reason, animal behaviourists and disease ecologists have been interested in the intersection of their respective fields for decades. Despite this interest, most research at the behaviour–disease interface focuses either on how host behaviour affects parasites or how parasites affect behaviour, with little overlap between the two. Yet, the majority of interactions between hosts and parasites are probably reciprocal, such that host behaviour feeds back on parasites and vice versa. Explicitly considering these feedbacks is essential for understanding the complex connections between animal behaviour and parasite ecology and evolution. To illustrate this point, we discuss how host behaviour–parasite feedbacks might operate and explore the consequences of feedback for studies of animal behaviour and parasites. For example, ignoring the feedback of host social structure on parasite dynamics can limit the accuracy of predictions about parasite spread. Likewise, considering feedback in studies of parasites and animal personalities may provide unique insight about the maintenance of variation in personality types. Finally, applying the feedback concept to links between host behaviour and beneficial, rather than pathogenic, microbes may shed new light on transitions between mutualism and parasitism. More generally, accounting for host behaviour–parasite feedbacks can help identify critical gaps in our understanding of how key host behaviours and parasite traits evolve and are maintained.     

THE CELLULAR IMMUNE RESPONSE OF DAPHNIA MAGNA UNDER HOST–PARASITE GENETIC VARIATION AND VARIATION IN INITIAL DOSE

In invertebrate–parasite systems, the likelihood of infection following parasite exposure is often dependent on the specific combination of host and parasite genotypes (termed genetic specificity). Genetic specificity can maintain diversity in host and parasite populations and is a major component of the Red Queen hypothesis. However, invertebrate immune systems are thought to only distinguish between broad classes of parasite. Using a natural host–parasite system with a well‐established pattern of genetic specificity, the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa, we found that only hosts from susceptible host–parasite genetic combinations mounted a cellular response following exposure to the parasite. These data are compatible with the hypothesis that genetic specificity is attributable to barrier defenses at the site of infection (the gut), and that the systemic immune response is general, reporting the number of parasite spores entering the hemocoel. Further supporting this, we found that larger cellular responses occurred at higher initial parasite doses. By studying the natural infection route, where parasites must pass barrier defenses before interacting with systemic immune responses, these data shed light on which components of invertebrate defense underlie genetic specificity.     

Oh sister,where art thou? Spatial population structure and the evolution of an altruistic defence trait

The evolution of parasite virulence and host defences is affected by population structure. This effect has been confirmed in studies focusing on large spatial scales, whereas the importance of local structure is not well understood. Slavemaking ants are social parasites that exploit workers of another species to rear their offspring. Enslaved workers of the host species Temnothorax longispinosus have been found to exhibit an effective post‐enslavement defence behaviour: enslaved workers were observed killing a large proportion of the parasites’ offspring. As enslaved workers do not reproduce, they gain no direct fitness benefit from this ‘rebellion’ behaviour. However, there may be an indirect benefit: neighbouring host nests that are related to ‘rebel’ nests can benefit from a reduced raiding pressure, as a result of the reduction in parasite nest size due to the enslaved workers’ killing behaviour. We use a simple mathematical model to examine whether the small‐scale population structure of the host species could explain the evolution of this potentially altruistic defence trait against slavemaking ants. We find that this is the case if enslaved host workers are related to nearby host nests. In a population genetic study, we confirm that enslaved workers are, indeed, more closely related to host nests within the raiding range of their resident slavemaker nest, than to host nests outside the raiding range. This small‐scale population structure seems to be a result of polydomy (e.g. the occupation of several nests in close proximity by a single colony) and could have enabled the evolution of ‘rebellion’ by kin selection.     

The evolution of host manipulation by parasites: a game theory analysis

Many parasites are known to manipulate the behaviour of intermediate hosts in order to increase their probability of transmission to definitive hosts. This manipulation must have costs. Here we explore the combined effects of three such costs on the amount of effort a parasite should expend on host manipulation. Manipulation can have direct costs to future reproductive success due to energy expended to manipulate the host. There may also be indirect costs if other parasites infect the host and profit from the manipulation without paying the cost of manipulation. These “free riders” may impose a third cost by competing with manipulators for resources within the host. Using game theory analysis and several different competition models we show that intrahost competition will decrease the investment that a parasite should make in manipulation but that manipulation can, under some circumstances, be a profitable strategy even in the presence of non-manipulating competitors. The key determinants of the manipulator’s success and its investment in manipulation are the relatedness among parasites within the host, the ratio of the passive transmission rate to the efficiency of increasing transmission rate and the strength of competitive effects. Manipulation, when exploited by others, becomes an altruistic behaviour. Thus we suggest that our model may be generally applicable to cases where organisms can exploit the investment of others (possibly kin) while also competing with the organism whose investment they exploit.     

Empirical support for optimal virulence in a castrating parasite

The trade-off hypothesis for the evolution of virulence predicts that parasite transmission stage production and host exploitation are balanced such that lifetime transmission success (LTS) is maximised. However, the experimental evidence for this prediction is weak, mainly because LTS, which indicates parasite fitness, has been difficult to measure. For castrating parasites, this simple model has been modified to take into account that parasites convert host reproductive resources into transmission stages. Parasites that kill the host too early will hardly benefit from these resources, while postponing the killing of the host results in diminished returns. As predicted from optimality models, a parasite inducing castration should therefore castrate early, but show intermediate levels of virulence, where virulence is measured as time to host killing. We studied virulence in an experimental system where a bacterial parasite castrates its host and produces spores that are not released until after host death. This permits estimating the LTS of the parasite, which can then be related to its virulence. We exposed replicate individual Daphnia magna (Crustacea) of one host clone to the same amount of bacterial spores and followed individuals until their death. We found that the parasite shows strong variation in the time to kill its host and that transmission stage production peaks at an intermediate level of virulence. A further experiment tested for the genetic basis of variation in virulence by comparing survival curves of daphniids infected with parasite spores obtained from early killing versus late killing infections. Hosts infected with early killer spores had a significantly higher death rate as compared to those infected with late killers, indicating that variation in time to death was at least in part caused by genetic differences among parasites. We speculate that the clear peak in lifetime reproductive success at intermediate killing times may be caused by the exceptionally strong physiological trade-off between host and parasite reproduction. This is the first experimental study to demonstrate that the production of propagules is highest at intermediate levels of virulence and that parasite genetic variability is available to drive the evolution of virulence in this system.     

Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare

Parasites with complex life cycles, relying on trophic transmission to a definitive host, very often induce changes in the behaviour or appearance of their intermediate hosts. Because this usually makes the intermediate host vulnerable to predation by the definitive host, it is generally assumed that the parasite's transmission rate is increased, and that the modification of the host is, therefore, of great adaptive significance to the parasite. However, in the ecological "real world" other predators unsuitable as hosts may just as well take advantage of the facilitation process and significantly erode the benefit of host manipulation. Here we show that the intertidal New Zealand cockle (Austrovenus stutchburyi), manipulated by its echinostome trematode (Curtuteria australis) to rest on the sediment surface fully exposed to predation from the avian definitive host, is also subject to sublethal predation from a benthic feeding fish (Notolabrus celidotus, Labridae). The fish is targeting only the cockle-foot, in which the parasite preferentially encysts, reducing the infection intensity of manipulated cockles to levels comparable with those in non-manipulated, buried cockles. Based on the frequency and intensity of the foot cropping and predation rates on surfaced cockles by avian hosts, it is estimated that 2.5% of the parasite population in manipulated cockles is transmitted successfully whereas 17.1% is lost to fish. We argue that the adaptive significance of manipulation in the present system depends critically on the feeding behaviour of the definitive host. If cockles constitute the majority of prey items, there will be selection against manipulation. If manipulated cockles are taken as an easily accessible supplement to a diet composed mostly of other prey organisms, behavioural manipulation of the cockle host appears a high risk, high profit transmission strategy. Both these feeding behaviours of birds are known to occur in the field.     

Conflicts over host manipulation between different parasites and pathogens: Investigating the ecological and medical consequences

When parasites have different interests in regard to how their host should behave this can result in a conflict over host manipulation, i.e. parasite induced changes in host behaviour that enhance parasite fitness. Such a conflict can result in the alteration, or even complete suppression, of one parasite's host manipulation. Many parasites, and probably also symbionts and commensals, have the ability to manipulate the behaviour of their host. Non‐manipulating parasites should also have an interest in host behaviour. Given the frequency of multiple parasite infections in nature, potential conflicts of interest over host behaviour and manipulation may be common. This review summarizes the evidence on how parasites can alter other parasite's host manipulation. Host manipulation can have important ecological and medical consequences. I speculate on how a conflict over host manipulation could alter these consequences and potentially offer a new avenue of research to ameliorate harmful consequences of host manipulation.     

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.