Inter- and intraspecific conflicts between parasites over host manipulation

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.     

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.     

Intraspecific conflict over host manipulation between different larval stages of an acanthocephalan parasite

Competitive interactions between coinfecting parasites are expected to be strong when they affect transmission success. When transmission is enhanced by altering host behaviour, intraspecific conflict can lead to 'coinfection exclusion' by the first-in parasite or to a 'sabotage' of behavioural manipulation by the youngest noninfective parasite. We tested these hypotheses in the acanthocephalan parasite Pomphorhynchus laevis, reversing phototaxis in its intermediate host Gammarus pulex. No evidence was found for coinfection exclusion in gammarids sequentially exposed to infection. Behavioural manipulation was slightly weakened but not cancelled in gammarids infected with mixed larval stages. Therefore, coinfecting infective and noninfective larvae both suffered competition, potentially resulting in delayed transmission and increased risk of mortality, respectively. Consequently, noninfective larva is not just a 'passive passenger' in the manipulated host, which raises interesting questions about the selective pressures at play and the mechanisms underlying manipulation.     

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.     

Host manipulation by parasites: a multidimensional phenomenon

The diversity of ways in which parasites manipulate the phenotype of their hosts to increase their transmission has been well‐documented during the past decades. Parasites clearly have the potential to alter a broad range of phenotypic traits in their hosts, extending from behaviour and colour to morphology and physiology. While the vast majority of studies have concentrated on few, often only one, host characters, there is increasing evidence that manipulative parasites alter multiple characteristics of their host's phenotype. These alterations can occur simultaneously and/or successively through time, making parasitically modified organisms undoubtedly more complex than traditionally viewed. Here, we briefly review the multidimensionality of host manipulation by parasites, discuss its possible significance and evolution, and propose directions for further research. This view should prove to be an extremely useful approach, generating a series of testable hypotheses regarding the ecology of parasitized hosts, and leading to a better comprehension of complex host–parasite relationships.     

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.     

Effects of genetic similarity on the life‐history strategy of co‐infecting trematodes: are parasites capable of intrahost kin recognition?

For conspecific parasites sharing the same host, kin recognition can be advantageous when the fitness of one individual depends on what another does; yet, evidence of kin recognition among parasites remains limited. Some trematodes, like Coitocaecum parvum, have plastic life cycles including two alternative life‐history strategies. The parasite can wait for its intermediate host to be eaten by a fish definitive host, thus completing the classical three‐host life cycle, or mature precociously and produce eggs while still inside its intermediate host as a facultative shortcut. Two different amphipod species are used as intermediate hosts by C. parvum, one small and highly mobile and the other larger, sedentary, and burrow dwelling. Amphipods often harbour two or more C. parvum individuals, all capable of using one or the other developmental strategy, thus creating potential conflicts or cooperation opportunities over transmission routes. This model was used to test the kin recognition hypothesis according to which cooperation between two conspecific individuals relies on the individuals' ability to evaluate their degree of genetic similarity. First, data showed that levels of intrahost genetic similarity between co‐infecting C. parvum individuals differed between host species. Second, genetic similarity between parasites sharing the same host was strongly linked to their likelihood of adopting identical developmental strategies. Two nonexclusive hypotheses that could explain this pattern are discussed: kin recognition and cooperation between genetically similar parasites and/or matching genotypes involving parasite genotype–host compatibility filters.     

Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage

Many trophically transmitted parasites with complex life cycles manipulate their intermediate host behavior in ways facilitating their transmission to final host by predation. This facilitation generally results from lowering host's antipredatory defenses when the parasite is infective to the final host. However, a recent theoretical model predicts that an optimal parasitic strategy would be to protect the intermediate host from predation when noninfective, before switching to facilitation when the infective stage is reached. We tested this hypothesis in the fish acanthocephalan parasite Pomphorhynchus laevis using the amphipod Gammarus pulex as intermediate host. Gammarids parasitized by noninfective stage of P. laevis (acanthella) hid significantly more under refuges than uninfected ones. In addition, acanthella-infected gammarids were less predated upon by trout than uninfected ones. As predicted, a switch toward decreased antipredatory behavior of G. pulex and enhanced vulnerability to predation was found when P. laevis reached the stage infective to its final host. The parasites appear to be able to exploit plasticity in host antipredatory responses, and shift the host optimal response toward their own optimal balance.     

The ecological success of a social parasite increases with manipulation of collective host behaviour

Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite‐induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find that colonies that were manipulated into attacking their Dufour‐treated nestmates were less aggressive towards the slavemaker than those that did not show slavemaker‐induced nestmate attack. Slavemakers benefited from altering their hosts’ aggression, as both the likelihood that slavemakers survived host encounters and slavemaker prevalence in ant communities increased with slavemaker‐induced nestmate attack. Finally, we show that Temnothorax longispinosus colonies were more susceptible to manipulation than Temnothorax curvispinosus colonies. This explains why T. curvispinosus colonies responded with more aggression towards invading slavemakers, why they were less likely to let slavemakers escape and why they were less frequently parasitized by the slavemaker than T. longispinosus. Our findings highlight that large‐scale geographic variation in resistance to manipulation can have important implications for the prevalence and host preference of parasites.     

VARIATION BETWEEN POPULATIONS AND LOCAL ADAPTATION IN ACANTHOCEPHALAN‐INDUCED PARASITE MANIPULATION

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative effect of all parasite infections on host survival. Both parasite and host origins influenced infection success. We found a tendency for higher infectivity in sympatric versus allopatric combinations, but detailed analyses revealed significant differences for two populations only. Conversely, no pattern of local adaptation was found for behavioral manipulation, but manipulation ability varied among parasite origins. This suggests that parasites may adapt their investment in behavioral manipulation according to some of their host's characteristics. In addition, all naturally infected host populations were less sensitive to parasite manipulation compared to a naive host population, suggesting that hosts may evolve a general resistance to manipulation.     

Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission?

Trophically transmitted parasites often alter their intermediate host's phenotype, thereby predisposing the hosts to increased predation. This is generally considered a parasite strategy evolved to enhance transmission to the next hosts. However, the adaptive value of host manipulation is not clear as it may be associated with costs, such as increased susceptibility to predators that are unsuitable next hosts for the parasites. We examined the ratio between the benefits and costs of host manipulation for transmission success of Acanthocephalus lucii (Acanthocephala), a parasite that alters the hiding behaviour and pigmentation of its isopod hosts. We experimentally compared the susceptibility of infected and uninfected isopods to predation by perch (Perca fluvialis; definitive host of the parasite) and dragonfly larvae (dead end). We found that the parasite predisposed the isopods to predation by both predators. However, the increased predation vulnerability of the infected isopods was higher towards perch. This suggests that, despite the costs due to non-host predation, host manipulation may still be advantageous for the parasite.     

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.     

Dynamic flux of microvesicles modulate parasite–host cell interaction of Trypanosoma cruzi in eukaryotic cells

Extracellular vesicles released from pathogens may alter host cell functions. We previously demonstrated the involvement of host cell‐derived microvesicles (MVs) during early interaction between Trypanosoma cruzi metacyclic trypomastigote (META) stage and THP‐1 cells. Here, we aim to understand the contribution of different parasite stages and their extracellular vesicles in the interaction with host cells. First, we observed that infective host cell‐derived trypomastigote (tissue culture‐derived trypomastigote [TCT]), META, and noninfective epimastigote (EPI) stages were able to induce different levels of MV release from THP‐1 cells; however, only META and TCT could increase host cell invasion. Fluorescence resonance energy transfer microscopy revealed that THP‐1‐derived MVs can fuse with parasite‐derived MVs. Furthermore, MVs derived from the TCT–THP‐1 interaction showed a higher fusogenic capacity than those from META– or EPI–THP‐1 interaction. However, a higher presence of proteins from META (25%) than TCT (12%) or EPI (5%) was observed in MVs from parasite–THP‐1 interaction, as determined by proteomics. Finally, sera from patients with chronic Chagas disease at the indeterminate or cardiac phase differentially recognized antigens in THP‐1‐derived MVs resulting only from interaction with infective stages. The understanding of intracellular trafficking and the effect of MVs modulating the immune system may provide important clues about Chagas disease pathophysiology.     

When trophically‐transmitted parasites combine predation enhancement with predation suppression to optimize their transmission

Trophically‐transmitted parasites are known for their ability to enhance predation of their intermediate host but they are less known for their ability to suppress predation. We review recent literature on host manipulation explaining why and when in its life cycle a parasite benefits from preventing the predation of its host. Predation suppression occurs in intermediate hosts as long as the parasite larva has not reached the developmental conditions allowing it to successfully establish in the next host (competency). We also examine the possibility that predation suppression may occur in hosts harbouring competent larvae (post competency) since some parasites have been shown to manipulate host behaviour in a way that decreases the risk of parasite death through non‐host predation (i.e. the consumption of its intermediate host by a predator that does not risk infection). Predation suppression when the parasite is competent has to be considered with respect to non‐host predation risk and is not mutually exclusive with predation enhancement. We use the recent theoretical advances in host manipulation to investigate the conditions under which predation suppression could evolve post competency.     

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.     

How parasite interaction strategies alter virulence evolution in multi‐parasite communities

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within‐host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite‐induced host mortality). Yet we still know little about how within‐host interactions affect the evolution of parasite virulence in multi‐parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within‐host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.     

Survival of the feces: Does a nematode lungworm adaptively manipulate the behavior of its cane toad host?

Parasites can enhance their fitness by modifying the behavior of their hosts in ways that increase rates of production and transmission of parasite larvae. We used an antihelminthic drug to experimentally alter infections of lungworms (Rhabdias pseudosphaerocephala) in cane toads (Rhinella marina). We then compared subsequent behaviors of dewormed toads versus toads that retained infections. Both in the laboratory and in the field, the presence of parasites induced hosts to select higher body temperatures (thereby increasing rates of lungworm egg production), to defecate in moister sites, and to produce feces with higher moisture content (thereby enhancing survival of larvae shed in feces). Because those behavioral modifications enhance rather than decrease parasite fitness, they are likely to have arisen as adaptive manipulations of host behavior rather than as host adaptations to combat infection or as nonadaptive consequences of infection on host physiology. However, the mechanisms by which lungworms alter cane toad thermal preference and defecation are not known. Although many examples of host manipulation by parasites involve intermediate hosts facilitating their own demise, our findings indicate that manipulation of definitive hosts can be as subtle as when and where to defecate.     

Cuckoos versus hosts in insects and birds: adaptations,counter‐adaptations and outcomes

Avian parents and social insect colonies are victimized by interspecific brood parasites—cheats that procure costly care for their dependent offspring by leaving them in another species' nursery. Birds and insects defend themselves from attack by brood parasites; their defences in turn select counter‐strategies in the parasite, thus setting in motion antagonistic co‐evolution between the two parties. Despite their considerable taxonomic disparity, here we show striking parallels in the way that co‐evolution between brood parasites and their hosts proceeds in insects and birds. First, we identify five types of co‐evolutionary arms race from the empirical literature, which are common to both systems. These are: (a) directional co‐evolution of weaponry and armoury; (b) furtiveness in the parasite countered by strategies in the host to expose the parasite; (c) specialist parasites mimicking hosts who escape by diversifying their genetic signatures; (d) generalist parasites mimicking hosts who escape by favouring signatures that force specialization in the parasite; and (e) parasites using crypsis to evade recognition by hosts who then simplify their signatures to make the parasite more detectable. Arms races a and c are well characterized in the theoretical literature on co‐evolution, but the other types have received little or no formal theoretical attention. Empirical work suggests that hosts are doomed to lose arms races b and e to the parasite, in the sense that parasites typically evade host defences and successfully parasitize the nest. Nevertheless hosts may win when the co‐evolutionary trajectory follows arms race a, c or d. Next, we show that there are four common outcomes of the co‐evolutionary arms race for hosts. These are: (1) successful resistance; (2) the evolution of defence portfolios (or multiple lines of resistance); (3) acceptance of the parasite; and (4) tolerance of the parasite. The particular outcome is not determined by the type of preceding arms race but depends more on whether hosts or parasites control the co‐evolutionary trajectory: tolerance is an outcome that parasites inflict on hosts, whereas the other three outcomes are more dependent on properties intrinsic to the host species. Finally, our review highlights considerable interspecific variation in the complexity and depth of host defence portfolios. Whether this variation is adaptive or merely reflects evolutionary lag is unclear. We propose an adaptive explanation, which centres on the relative strength of two opposing processes: strategy‐facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy‐blocking, in which one line of defence may relax selection on another so completely that it causes it to decay. We suggest that when strategy‐facilitation outweighs strategy‐blocking, hosts will possess complex defence portfolios and we identify selective conditions in which this is likely to be the case.     

Superinfection and the coevolution of parasite virulence and host recovery

Parasite strategies of host exploitation may be affected by host defence strategies and multiple infections. In particular, within‐host competition between multiple parasite strains has been shown to select for higher virulence. However, little is known on how multiple infections could affect the coevolution between host recovery and parasite virulence. Here, we extend a coevolutionary model introduced by van Baalen (Proc. R. Soc. B, 265, 1998, 317) to account for superinfection. When the susceptibility to superinfection is low, we recover van Baalen's results and show that there are two potential evolutionary endpoints: one with avirulent parasites and poorly defended hosts, and another one with high virulence and high recovery. However, when the susceptibility to superinfection is above a threshold, the only possible evolutionary outcome is one with high virulence and high investment into defence. We also show that within‐host competition may select for lower host recovery, as a consequence of selection for more virulent strains. We discuss how different parasite and host strategies (superinfection facilitation, competitive exclusion) as well as demographic and environmental parameters, such as host fecundity or various costs of defence, may affect the interplay between multiple infections and host–parasite coevolution. Our model shows the interplay between coevolutionary dynamics and multiple infections may be affected by crucial mechanistic or ecological details.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.