Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences

Carbohydrates on parasite surfaces have been shown to play an important role in host–parasite coevolution, mediating host non-self recognition and parasite camouflage. Parasites that switch hosts can change their surface molecules to remain undetected by the diverse immune systems of their different hosts. However, the question of individual variation in surface sugar composition and its relation to infectivity, virulence, immune evasion and growth of a parasite in its different hosts is as yet largely unexplored. We studied such fitness consequences of variation in surface sugars in a sympatric host–parasite system consisting of the cestode Schistocephalus solidus and its intermediate hosts, a copepod and the three-spined stickleback. Using lectins to analyse the sugar composition, we show that the tapeworm changes its surface according to the invertebrate or vertebrate host. Importantly, sugar composition seems to be genetically variable, as shown by differences among tapeworm sibships. These differences are related to variation in parasite fitness in its second intermediate host, i.e. infectivity and growth. Surface sugar composition may thus be a proximate correlate of the evolutionarily relevant variability in infectivity and virulence of parasites in different hosts.     

Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle

Many diseases are caused by parasites with complex life cycles that involve several hosts. If parasites cope better with only one of the different types of immune systems of their host species, we might expect a trade-off in parasite performance in the different hosts, that likely influences the evolution of virulence. We tested this hypothesis in a naturally co-evolving host-parasite system consisting of the tapeworm Schistocephalus solidus and its intermediate hosts, a copepod, Macrocyclops albidus, and the three-spined stickleback Gasterosteus aculeatus. We did not find a trade-off between infection success in the two hosts. Rather, tapeworms seem to trade-off adaptation towards different parts of their hosts' immune systems. Worm sibships that performed better in the invertebrate host also seem to be able to evade detection by the fish innate defence systems, i.e. induce lower levels of activation of innate immune components. These worm variants were less harmful for the fish host likely due to reduced costs of an activated innate immune system. These findings substantiate the impact of both hosts' immune systems on parasite performance and virulence.     

Competitive Growth Strategies in Intermediate Hosts: Experimental Tests of a Parasite life-History Model Using the Cestode, Schistocephalus solidus

In parasites with a complex life cycle, the fitness of an individual depends on its probability of reaching the final host and on its fecundity. Because larval growth in intermediate hosts may affect both transmission and adult size, selection should optimize growth patterns that are conditional on the presence and number of conspecific competitors. A recent model predicts that the total parasite volume per host should increase with intensity if larvae are able to vary growth depending on the number of conspecifics in the host (Life History Strategy hypothesis, i.e. LHS). Further, we would here expect growth rates to increase with intensity. By contrast, under the simplest alternative hypothesis of Resource Constraints (i.e. RC), the total parasite volume should remain constant. We experimentally infected copepods Macrocyclops albidus with the cestode Schistocephalus solidus to achieve 1, 2 or 3 parasites per host taking care that hosts had similar quality status at each infection level, and compared larval growth trajectories at the three intensity levels. The asymptotic total parasite volume was larger in double and triple infections than in single infections. Furthermore, the asymptotic total parasite volume was significantly larger in triple than in double infections but only in larger copepods that were less constrained by a host-size ceiling effect. These results, together with the fact that growth rates increased with intensity, support the LHS hypothesis: procercoids of a tapeworm may “count” their conspecific competitors in their first intermediate host to harvest its resources strategically until the next step in their complex life cycle. Co-ordinating editor: A. Biere     

A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations

Epidemiological models generally assume that the number of susceptible individuals that become infected within a unit of time depends on the density of the hosts and the concentration of parasites (i.e. mass-action principle). However, empirical studies have found significant deviations from this assumption due to biotic and abiotic factors, such as seasonality, the spatial structure of the host population and host heterogeneity with respect to immunity and susceptibility. In this paper, we examine the effect of the dose level of the bacterial endoparasite Pasteuria ramosa on the infection rate of its host, the water flea Daphnia magna. Using seven host clones and two parasite isolates, we measure the fraction of infected hosts after exposure to eight different parasite doses to determine whether there is variation in the infection process across different host clone-parasite isolate combinations. In five combinations, a pronounced dose-dependent infection pattern was found. Using a likelihood approach, we compare the infection data of these five combinations to the fit of three mathematical models: a mass-action model, a parasite antagonism model (i.e. an increase in the parasite dose leads to an under-proportionate increase in the infection rate per host) and a heterogeneous host model. We found that the host heterogeneity model, in which we assumed the existence of non-inherited phenotypic differences in host susceptibilities to the parasite, provides the best fit. Our analysis suggests that among 5 out of the 14 host clone-parasite isolate combinations that resulted in appreciable infections, non-genetic host heterogeneity plays an important role.     

When parasites disagree: Evidence for parasite‐induced sabotage of host manipulation

Host manipulation is a common parasite strategy to alter host behavior in a manner to enhance parasite fitness usually by increasing the parasite's transmission to the next host. In nature, hosts often harbor multiple parasites with agreeing or conflicting interests over host manipulation. Natural selection might drive such parasites to cooperation, compromise, or sabotage. Sabotage would occur if one parasite suppresses the manipulation of another. Experimental studies on the effect of multi‐parasite interactions on host manipulation are scarce, clear experimental evidence for sabotage is elusive. We tested the effect of multiple infections on host manipulation using laboratory‐bred copepods experimentally infected with the trophically transmitted tapeworm Schistocephalus solidus. This parasite is known to manipulate its host depending on its own developmental stage. Coinfecting parasites with the same aim enhance each other's manipulation but only after reaching infectivity. If the coinfecting parasites disagree over host manipulation, the infective parasite wins this conflict: the noninfective one has no effect. The winning (i.e., infective) parasite suppresses the manipulation of its noninfective competitor. This presents conclusive experimental evidence for both cooperation in and sabotage of host manipulation and hence a proof of principal that one parasite can alter and even neutralize manipulation by another.     

Identification of the copepod intermediate host of the introduced broad fish tapeworm, Diphyllobothrium latum, in Southern Chile

The broad fish tapeworm, Diphyllobothrium latum, is an exotic species in both Chile and Argentina, and until now, its copepod host has remained unknown in South American waters. The objective of this study was to identify calanoid copepod species that may be intermediate hosts for D. latum in Lake Panguipulli, Chile. In this lake, the highest levels of infection by this tapeworm occur in the introduced rainbow trout, Oncorhynchus mykiss. Of the 2 calanoid copepods found in Lake Panguipulli, Diaptomus diabolicus and Boeckella gracilipes, only D. diabolicus became infected on experimental exposure to coracidia. Prevalence (mean intensity) of experimental infection in adult copepods was 73.2% (2.8 procercoids per host). Diaptomus diabolicus has been demonstrated to be a new intermediate host; this is the first record of a copepod host for D. latum in South America.     

Nonhost species reduce parasite infection in a focal host species within experimental fish communities

The dilution effect describes the negative association between host biodiversity and the risk of infectious disease. Tests designed to understand the relative roles of host species richness, host species identity, and rates of exposure within experimental host communities would help resolve ongoing contention regarding the importance and generality of dilution effects. We exposed fathead minnows to infective larvae of the trematode, Ornithodiplostomum ptychocheilus in minnow‐only containers and in mixed containers that held 1–3 other species of fish. Parasite infection was estimated as the number of encysted worms (i.e., brainworms) present in minnows following exposure. The results of exposure trials showed that nonminnow fish species were incompatible with O. ptychocheilus larvae. There was no reduction in mean brainworm counts in minnows in mixed containers with brook sticklebacks or longnose dace. In contrast, brainworm counts in minnows declined by 51% and 27% in mesocosms and aquaria, respectively, when they co‐occurred with emerald shiners. Dilution within minnow + shiner containers may arise from shiner‐induced alterations in minnow or parasite behaviors that reduced encounter rates between minnows and parasite larvae. Alternatively, shiners may act as parasite sinks for parasite larvae. These results highlight the role of host species identity in the dilution effect. Our results also emphasize the complex and idiosyncratic effects of host community composition on rates of parasite infection within contemporary host communities that contain combinations of introduced and native species.     

Molecular targets for detection and immunotherapy in Cryptosporidium parvum

Cryptosporidium parvum is an obligate protozoan parasite responsible for the diarrheal illness cryptosporidiosis in humans and animals. Although C. parvum is particularly pathogenic in immunocompromised hosts, the molecular mechanisms by which C. parvum invades the host epithelial cells are not well understood. Characterization of molecular-based antigenic targets of C. parvum is required to improve the specificity of detection, viability assessments, and immunotherapy (treatment). A number of zoite surface (glyco)proteins are known to be expressed during, and believed to be involved in, invasion and infection of host epithelial cells. In the absence of protective treatments for this illness, antibodies targeted against these zoite surface (glyco)proteins offers a rational approach to therapy. Monoclonal, polyclonal and recombinant antibodies represent useful immunotherapeutic means of combating infection, especially when highly immunogenic C. parvum antigens are utilized as targets. Interruption of life cycle stages of this parasite via antibodies that target critical surface-exposed proteins can potentially decrease the severity of disease symptoms and subsequent re-infection of host tissues. In addition, development of vaccines to this parasite based on the same antigens may be a valuable means of preventing infection. This paper describes many of the zoite surface glycoproteins potentially involved in infection, as well as summarizes many of the immunotherapeutic studies completed to date. The identification and characterization of antibodies that bind to C. parvum-specific cell surface antigens of the oocyst and sporozoite will allow researchers to fully realize the potential of molecular-based immunotherapy to this parasite.     

Genetically resistant sheep avoid parasites to a greater extent than do susceptible sheep

Livestock breeding programmes have created resistant (R) and susceptible (S) sheep that differ in their ability to control parasites through their immune function but potentially also their grazing behaviour (i.e. parasite avoidance). Using the Perendale genetic lines, we tested the hypothesis that R-sheep avoid parasites more effectively, reducing their parasite exposure/challenge, compared with S-sheep. However, in grazing systems, parasite-rich areas are also forage rich, suggesting that parasite avoidance behaviours are associated with nutritional penalties. We first created a naturally heterogeneous sward structure of gaps and tussocks and then used focal behavioural observations to quantify the sward selection of R- and S-sheep. Tussock swards were more nitrogen rich (41%), offered increased forage intake rates (32%) and contained 17 times more parasite larvae than gap swards. All the animals avoided grazing the tussock swards. However, the R-sheep grazed the tussock swards to a lesser degree than the S-sheep. We conclude that selection for genetic resistance has resulted in animals that, despite being well armed to fight parasitism through improved immune function, adopt parasite avoidance strategies with associated nutritional disadvantages. This experiment highlights the role of host behaviour in the control of parasitism and suggests that animals can be bred to avoid disease.     

Infectivity of two nematode parasites, Camallanus lacustris and Anguillicola crassus, in a paratenic host, the three-spined stickleback Gasterosteus aculeatus

Three-spined sticklebacks Gasterosteus aculeatus are frequent paratenic hosts of the nematode parasites Anguillicola crassus and Camallanus lacustris. As paratenic hosts, sticklebacks could spread infection by carrying high numbers of infective stages. In contrast, low infective ability of either parasite for the paratenic host could hinder the spread of infection. In the present study, G. aculeatus was, for the first time, infected under controlled laboratory conditions with defined doses of the parasites. Sticklebacks were exposed to 6, 12, 18 and 24 parasite larvae to determine the infective ability of the 2 nematode species. There were significantly higher infection rates for C. lacustris (18 to 49%) than for A. crassus (4 to 14%) at each exposure dose. In C. lacustris-infected sticklebacks, infection rates tended to be highest after exposure to 12 C. lacustris larvae and lowest after exposure to 24 parasites. In A. crassus-infected sticklebacks, no effect of parasite exposure dose on infection rates was observed. Immunity parameters such as respiratory burst activity and lymphocyte proliferation of head kidney leukocytes recorded 18 wk post exposure were not significantly affected by either parasite or exposure dose. Granulocyte:lymphocyte ratios were elevated only within the stickleback group showing the highest infection intensity of C. lacustris, i.e. to those exposed 18 parasites.     

Lack of preference for infective faeces in Hymenolepis diminuta-infected beetles (Tenebrio molitor)

The beetle-tapeworm life cycle provides a convenient system to study how host behaviour influences the probability of re-infection because initial and secondary infections can be tracked. The beetle, Tenebrio molitor, is infected with the tapeworm Hymenolepis diminuta when it ingests rat faeces containing tapeworm eggs, which upon hatching undergo five morphologically distinct stages while developing inside the beetle. In a series of preference trials, both individual and groups of previously infected beetles were exposed to baits of infective (faeces with eggs) and uninfective faeces. Beetles did not differ in the amount of time spent or in the number of occurrences at each bait type, suggesting that infected beetles show no preference for infective faeces. This may be a host adaptation to avoid further infection, parasite manipulation to avoid competition for host resources, or both. Further, once infected, beetles are no more or no less likely to become re-infected than uninfected beetles. An analysis of the mean and variance of infection suggests that some individuals are highly susceptible to and some are highly resistant to infection, with males being more variable than females. This could explain the higher load of cysticercoids observed in males.     

Variation and covariation in infectivity,virulence and immunodepression in the host–parasite association Gammarus pulex–Pomphorhynchus laevis

Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis, in infecting and in immunodepressing its amphipod host, Gammarus pulex. We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infectivity, the intensity of immunodepression and virulence were variable among parasite sibships. Infectivity and the level of immunodepression were not correlated across parasite sibships. Whereas infectivity was unrelated to host mortality, we found that gammarids that were exposed to the parasite sibships that immunodepressed their hosts the most survived better. This positive covariation between host survival and immunodepression suggests that gammarids exposed to the less immunodepressive parasites could suffer from damage imposed by a higher activity of the phenoloxidase.     

Mechanisms of protective immunity in Hymenolepis nana/mouse model.

Some immunological and parasitological aspects related to the infection of Hymenolepsis nana in mice are summarized in this review, focusing on the immune effector mechanisms involved in this host/parasite relationship. H. nana is a small cestode tapeworm of man and mice. A primary egg-infection determines within few days a strong immunity. Immunity elicited by low-level primary infection is effective as a high-level infection. The protective role of both humoral and cell-mediated immunity is summarized. The histological findings demonstrate that eosinophils and mast-cells are implicated as effector cells. This review is an attempt to re-examine, at low-level infection, the immune mechanisms in H. nana/mouse model.     

Diapause of copepods as an element for stabilizing the parasite system of some fish helminths

The analysis of infection dynamics of copepods, which are the intermediate hosts of three helminth species of freshwater fishes (Triaenophorus crassus, Proteocephalus exiguus and P. percae), has shown that diapause in the life cycle of the copepods is favourable for preserving the infection in the waterbody until physiological prerequisites for successful infection of the final host are acquired. The peculiarity of a copepod's life cycle may determine the strategy of a parasite in its preimaginal phase as a waiting stage, and the duration of the residence of helminth larvae in copepods that have an obligatory diapause, is one of the elements the provide stability in parasite systems.     

Relative helminth size in crustacean hosts: in vivo determination, and effects of host gender and within-host competition in a copepod infected by a cestode

Crustaceans are important hosts for a number of helminth parasites, and they are increasingly used as models for studying the physiology, ecology and evolution of parasite-host interactions. In ecological studies, this interaction is commonly described only in terms of prevalence and number of larvae per infected host. However, the volume of helminth parasites can vary greatly, and this variation can potentially give important insights into the nature of a parasite-host relationship. It may influence and be influenced, for example, by within-host competition, host size, growth, and life history. Here we present a simple method that allows rapid approximation of the absolute and relative volumes of cestode larvae within copepod hosts of various developmental stages (nauplii, copepodites and adults). The measurements are taken in vivo without much disturbance of the animals, i.e. the technique allows study of growth and development of the parasites in relation to that of their hosts. The principles of this technique can be adopted to other helminth parasites and other crustacean hosts. Using this method in the copepod Macrocyclops albidus infected with the cestode Schistocephalus solidus, we found that the relative parasite size (= `parasite index') ranged from 0.5% to 6.5% of host size 14 days after infection. It was greater in male than in female hosts. With increasing number of parasites per host, the total parasite volume increased while the mean volume of the individual parasites decreased. The magnitude of the observed parasite indices, the large variation that was found within a sample of 46 infected adult copepods, and the observed correlates suggest that this new index can indeed be an important measure of parasite success and its pathogenecity.     

Whether larval amphibians school does not affect the parasite aggregation rule: testing the effects of host spatial heterogeneity in field and experimental studies

Almost all macroparasites show over‐dispersed infections within natural host populations such that most parasites are distributed among a few heavily‐infected individuals. Despite the importance of parasite aggregation for understanding system stability, the potential for population regulation, and super‐spreading events, many questions persist about its underlying drivers. Theoretically, aggregation results from heterogeneity in host exposure, resistance, and tolerance. However, few studies have examined how host spatial arrangement – which likely affects both parasite encounter and density‐dependent interactions – influences infection and dispersion, representing a critical gap in our current knowledge regarding the possible drivers of parasite aggregation. Using field data from over 165 ponds and 8000 hosts, we evaluated how the spatial clustering of amphibian larvae within ponds 1) varied among different amphibian species, and 2), affected the distribution of parasites within the host population using Taylor's power law. A complementary mesocosm experiment used field‐guided manipulations of the spatial arrangement of larval amphibians to create a gradient in host clustering while controlling host density, thereby testing for spatial effects on both infection success and aggregation by three different trematode species. Our field data indicated that larval amphibians exhibited significant spatial clustering that was well captured by Taylor's power law (R² 0.92 to 0.97 for different host species), but the residual variation only weakly correlated with observed patterns of trematode parasite over‐dispersion. Correspondingly, experimental manipulation of host clustering had no effects on parasite infection success or the degree of parasite aggregation among cages or mesocosms. Given the importance of parasite over‐dispersion for host populations and disease dynamics, we advocate for further investigations of host and parasite spatial aggregation, particularly studies that incorporate and/or control for heterogeneity in exposure and susceptibility.     

Protective immune mechanisms against the metacestode of Echinococcus multilocularis

Infection with the larval stage of the fox tapeworm Echinococcus multilocularis results in a life-threatening hepatic disease concerning humans and intermediate rodent hosts. Immunoepidemiological surveys provided information that a large proportion of infected individuals may demonstrate either constitutional resistance to early post-oncospheral development of the parasite or late resistance to disease by exhibiting an intrahepatic died-out parasite lesion. Similar events have been found in secondary infections of laboratory rodents. Dissection of humoral and cell-mediated immune responses in susceptible versus resistant individuals provides insight into immunological pathways associated with the different outcome of infection. Survival strategy of the metacestode obviously focuses on the crucial role played by the parasite laminated layer. This layer protects the metacestode from host effector mechanisms which can potentially kill the proliferating germinative compartments in case of resistant hosts. Bruno Gottstein and Richard Felleisen here discuss the need to search for more parameters discriminating between the different immune pathways in order to find out (immunogenetic?) predispositions responsible for the respective phenomena.     

Cuticular reactivity of early larval stages of Ascaris suum: binding of fractions of immune serum to the surface of infective and parasitic stage larvae as detected by the mixed antiglobulin test.

Infective stage and early parasitic larvae of Ascaris suum were evaluated for surface reactivity with serum from uninfected and hyperimmune guinea-pigs. Cuticular binding of serum components was assessed by the mixed antiglobulin test.Ensheathed infective larvae bound both normal serum proteins and 7S protein from immune serum over the entire sheath surface. Parasitic larvae recovered at 16 and 25 h post infection (h.p.i.) were poorly reactive, and binding occurred only to sites on the head and tail regions. Larvae recovered at 48 and 72 h.p.i. were highly reactive over the entire cuticle.Host serum protein was not detectable on the surface of parasitic larvae when harvested from guineapigs after a primary infection until the larvae had been in the host for 72 h. However larvae recovered from hyperimmune animals had host serum protein detectable on the cuticle as early as 16 h.p.i.     

Alterations in carbohydrate and fatty acid levels of Lymantria dispar larvae caused by a microsporidian infection and potential adverse effects on a co-occurring endoparasitoid,Glyptapanteles liparidis

Infection of Lymantria dispar host larvae by the entomopathogenic microsporidium Vairimorpha sp. has a negative impact on the performance of the endoparasitic braconid Glyptapanteles liparidis. To investigate possible causes for this effect, we studied to what extent nutritional host suitability is altered by the microsporidium. Therefore, we analyzed carbohydrates and fatty acids in host larvae after Vairimorpha infection and/or parasitism by G. liparidis. Trehalose levels were significantly reduced in the hemolymph of infected hosts. After day five post infection, it was detected only in traces. Four to six days later, the glycogen resources were depleted in infected larvae. Parasitism by G. liparidis, on the other hand, led to increased hemolymph trehalose levels during the early endoparasitic phase but to a significant decrease at the end of its larval development. No effect of parasitism on the glycogen content was ascertained. Hemolymph levels of the fatty acids analyzed, such as palmitic, stearic, oleic, linoleic, and linolenic acid, were significantly reduced in microsporidia-infected L. dispar. Vairimorpha sp. develops as an intracellular parasite in the fat body of the host larva and synthesis of trehalose and fatty acids may be disturbed. Moreover, microsporidia may also harness metabolites or energy produced by host cells. We conclude that the microsporidia-induced decrease in hemolymph carbohydrates and fatty acids adversely affects growth and development of parasitoid larvae.     

The relationship between larval size and fitness in the tapeworm Schistocephalus solidus: bigger is better?

In organisms with complex life cycles, fitness often increases with body size at the transition from larva to adult. The translation of larval size into fitness, however, can depend on the source of size variation, with size, per se, not always increasing adult success. In parasitic worms, many factors influence larval growth, but little is known about the consequences of this growth variation. We examined how the size of the tapeworm Schistocephalus solidus in its copepod first intermediate host affects infection success and growth in the stickleback second host. Moreover, we assessed whether the conspicuous growth variation caused by copepod size is fitness‐relevant. Using larvae of the same age, we found that larger worms had a substantially higher infection probability and they tended to still be slightly larger after several months of growth in fish. However, big larvae from bigger copepods did not have higher fitness, suggesting that being large relative to the host, but not necessarily large in general, is important. These findings clarify some aspects of the life history strategy of S. solidus (e.g. why there is a flat ontogenetic reaction norm across copepod stages), but also raise questions (e.g. why growth costs have been hard to document). More generally, our results indicate that larval size can correlate with fitness in helminths, but that not all size variation is predictive of success in the next host.