Cestode Schistocephalus Solidus Research Articles

Tapeworm infection affects sleep-like behavior in three-spined sticklebacks

Sleep is a complex and conserved biological process that affects several body functions and behaviors. Evidence suggests that there is a reciprocal interaction between sleep and immunity. For instance, fragmented sleep can increase the probability of parasitic infections and reduce the ability to fight infections. Moreover, viral and bacterial infections alter the sleep patterns of infected individuals. However, the effects of macro-parasitic infections on sleep remain largely unknown, and measuring sleep in non-model organisms remains challenging. In this study, we investigated whether macro-parasite infections could alter sleep-like behavior of their hosts. We experimentally infected three-spined sticklebacks (Gasterosteus aculeatus), a freshwater fish, with the tapeworm Schistocephalus solidus and used a hidden Markov model to characterize sleep-like behavior in sticklebacks. One to four days after parasite exposure, infected fish showed no difference in sleep-like behavior compared with non-exposed fish, and fish that were exposed-but-not-infected only showed a slight reduction in sleep-like behavior during daytime. Twenty-nine to 32 days after exposure, infected fish showed more sleep-like behavior than control fish, while exposed-but-not-infected fish showed overall less sleep-like behavior. Using brain transcriptomics, we identified immune- and sleep-associated genes that potentially underlie the observed behavioral changes. These results provide insights into the complex association between macro-parasite infection, immunity, and sleep in fish and may thus contribute to a better understanding of reciprocal interactions between sleep and immunity.

Population-level immunologic variation in wild threespine stickleback (Gasterosteusaculeatus)

Wild organisms are regularly exposed to a wide range of parasites, requiring the management of an effective immune response while avoiding immunopathology. Currently, our knowledge of immunoparasitology primarily derives from controlled laboratory studies, neglecting the genetic and environmental diversity that contribute to immune phenotypes observed in wild populations. To gain insight into the immunologic variability in natural settings, we examined differences in immune gene expression of two Alaskan stickleback (Gasterosteus aculeatus) populations with varying susceptibility to infection by the cestode Schistocephalus solidus. Between these two populations, we found distinct immune gene expression patterns at the population level in response to infection with fish from the high-infection population displaying signs of parasite-driven immune manipulation. Further, we found significant differences in baseline immune gene profiles between the populations, with uninfected low-infection population fish showing signatures of inflammation compared to uninfected high-infection population fish. These results shed light on divergent responses of wild populations to the same parasite, providing valuable insights into host-parasite interactions in natural ecosystems.

Opening a can of worms: a test of the co-infection facilitation hypothesis

Parasitic infections are a global occurrence and impact the health of many species. Coinfections, where two or more species of parasite are present in a host, are a common phenomenon across species. Coinfecting parasites can interact directly or indirectly via their manipulation of (and susceptibility to) the immune system of their shared host. Helminths, such as the cestode Schistocephalus solidus, are well known to suppress immunity of their host (threespine stickleback, Gasterosteus aculeatus), potentially facilitating other parasite species. Yet, hosts can evolve a more robust immune response (as seen in some stickleback populations), potentially turning facilitation into inhibition. Using wild-caught stickleback from 20 populations with non-zero S. solidus prevalence, we tested an a priori hypothesis that S. solidus infection facilitates infection by other parasites. Consistent with this hypothesis, individuals with S. solidus infections have 18.6% higher richness of other parasites compared to S. solidus-uninfected individuals from the same lakes. This facilitation-like trend is stronger in lakes where S. solidus is particularly successful but is reversed in lakes with sparse and smaller cestodes (indicative of stronger host immunity). These results suggest that a geographic mosaic of host–parasite co-evolution might lead to a mosaic of between-parasite facilitation/inhibition effects.

Local adaptation and host specificity to copepod intermediate hosts by the tapeworm Schistocephalus solidus.

Host-parasite coevolution may lead to patterns of local adaptation in either the host or parasite. For parasites with complex multi-host life cycles, this coevolution may be more challenging as they must adapt to multiple geographically varying hosts. The tapeworm Schistocephalus solidus exhibits some local adaptation to its second intermediate host, threespine stickleback, to which the parasite is strictly specialized. However, the tapeworm's adaptation to its first intermediate host (any of a number of copepod species) is not documented. We investigated if there was local adaptation and host specify in the tapeworm Schistocephalus solidus to its copepod first intermediate hosts. We exposed copepods from five lakes in Vancouver Island (BC, Canada) to local (i.e. same lake) and foreign tapeworms in a reciprocal exposure experiment. Results indicate that the tapeworm is not locally adapted to the copepods. Instead, we observed moderate-effect host specificity, infection rates being higher in certain copepod species than in others. Infection rates also varied among cestode populations. These results show that although S. solidus infects multiple copepod genera, they are not equally competent hosts. Differences in S. solidus epidemiology among lakes is likely to be driven more by this partial specialization, than by local adaptation to first intermediate hosts.

A new technique to study nutrient flow in host-parasite systems by carbon stable isotope analysis of amino acids and glucose

Stable isotope analysis of individual compounds is emerging as a powerful tool to study nutrient origin and conversion in host-parasite systems. We measured the carbon isotope composition of amino acids and glucose in the cestode Schistocephalus solidus and in liver and muscle tissues of its second intermediate host, the three-spined stickleback (Gasterosteus aculeatus), over the course of 90 days in a controlled infection experiment. Similar linear regressions of δ13C values over time and low trophic fractionation of essential amino acids indicate that the parasite assimilates nutrients from sources closely connected to the liver metabolism of its host. Biosynthesis of glucose in the parasite might occur from the glucogenic precursors alanine, asparagine and glutamine and with an isotope fractionation of − 2 to – 3 ‰ from enzymatic reactions, while trophic fractionation of glycine, serine and threonine could be interpreted as extensive nutrient conversion to fuel parasitic growth through one-carbon metabolism. Trophic fractionation of amino acids between sticklebacks and their diets was slightly increased in infected compared to uninfected individuals, which could be caused by increased (immune-) metabolic activities due to parasitic infection. Our results show that compound-specific stable isotope analysis has unique opportunities to study host and parasite physiology.

Secretion of extracellular vesicles during ontogeny of the tapeworm Schistocephalus solidus

We provide the first ultrastructural evidence of the secretion of extracellular vesicles (EVs) across all parasitic stages of the tapeworm Schistocephalus solidus (Müller, 1776) (Cestoda: Diphyllobothriidea) using a laboratory life cycle model. We confirmed the presence of EV-like bodies in all stages examined, including the hexacanth, procercoids in the copepod, Macrocyclops albidus (Jurine, 1820), plerocercoids from the body cavity of the three-spined stickleback, Gasterosteus aculeatus Linnaeus, and adults cultivated in artificial medium. In addition, we provide description of novel tegumental structures potentially involved in EV biogenesis and the presence of unique elongated EVs similar to those previously described only in Fasciola hepatica Linnaeus, 1758 (Trematoda), Hymenolepis diminuta (Rudolphi, 1819) (Cestoda), and Trypanosoma brucei Plimmer et Bradford, 1899 (Kinetoplastida).

Implication of the myo‐inositol pathway in behavioural alterations of infected threespine sticklebacks

Abstract Threespine sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus display impairments in their anti‐predator responses. They also have increased expression of the gene encoding the IMPase 1 enzyme in their brains, which is part of a key step in myo‐inositol synthesis. IMPase 1 and myo‐inositol levels are the targets of lithium treatment in patients with bipolar disorder. Although promising candidates, we do not know if IMPase 1 and myo‐inositol are directly implicated in the changes in risky behaviours measured in Schistocephalus‐infected fish. Understanding the molecular mechanisms directly or indirectly involved in these behavioural alterations is crucial to understand the evolution of host–parasite interactions. Here, we increased myo‐inositol levels of uninfected fish and inhibited IMPase 1 activity in infected fish to test the prediction that it would decrease and increase their anti‐predator behaviour respectively. We found that uninfected fish with increased myo‐inositol levels (by injecting exogenous myo‐inositol or by inducing endogenous production using an osmotic challenge) did not decrease their anti‐predator responses. However, infected fish treated with lithium chloride had some of their anti‐predator behaviours restored, but not all. They spent less time swimming close to the surface, showed lowered activity, had a higher latency to feed in a novel environment and spent more time frozen after a predator attack. Our results suggest that the target of lithium treatment is implicated in the risky behaviours of infected fish and supports the idea that the parasite‐associated alteration in behaviour has a multifactorial nature. Read the free Plain Language Summary for this article on the Journal blog.

Evolutionary gain and loss of a pathological immune response to parasitism.

Parasites impose fitness costs on their hosts. Biologists often assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests that selection may sometimes favor loss of resistance, which may result in alternative stable states where some populations are resistant and others are tolerant. Intraspecific variation in immune costs is rarely surveyed in a manner that tests evolutionary patterns, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes, they gained resistance to the freshwater-associated cestode Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation are a commonly observed phenotype that contributes to suppression of cestode growth and viability but also imposes a substantial cost on fecundity. Combining genetic mapping and population genomics, we find that opposing selection generates immune system differences between tolerant and resistant populations, consistent with divergent optimization.

Population-level variation in parasite resistance due to differences in immune initiation and rate of response.

Closely related populations often differ in resistance to a given parasite, as measured by infection success or failure. Yet, the immunological mechanisms of these evolved differences are rarely specified. Does resistance evolve via changes to the host's ability to recognize that an infection exists, actuate an effective immune response, or attenuate that response? We tested whether each of these phases of the host response contributed to threespine sticklebacks’ recently evolved resistance to their tapeworm Schistocephalus solidus. Although marine stickleback and some susceptible lake fish permit fast‐growing tapeworms, other lake populations are resistant and suppress tapeworm growth via a fibrosis response. We subjected lab‐raised fish from three populations (susceptible marine “ancestors,” a susceptible lake population, and a resistant lake population) to a novel immune challenge using an injection of (1) a saline control, (2) alum, a generalized pro‐inflammatory adjuvant that causes fibrosis, (3) a tapeworm protein extract, or (4) a combination of alum and tapeworm protein. With enough time, all three populations generated a robust fibrosis response to the alum treatments. Yet, only the resistant population exhibited a fibrosis response to the tapeworm protein alone. Thus, these populations differed in their ability to respond to the tapeworm protein but shared an intact fibrosis pathway. The resistant population also initiated fibrosis faster in response to alum, and was able to attenuate fibrosis, unlike the susceptible populations’ slow but longer lasting response to alum. As fibrosis has pathological side effects that reduce fecundity, the faster recovery by the resistant population may reflect an adaptation to mitigate the costs of immunity. Broadly, our results confirm that parasite detection and immune initiation, activation speed, and immune attenuation simultaneously contribute to the evolution of parasite resistance and adaptations to infection in natural populations.

How cunning is the puppet-master? Cestode-infected fish appear generally fearless

Trophically transmitted parasites have life cycles that require the infected host to be eaten by the correct type of predator. Such parasites should benefit from an ability to suppress the host’s fear of predators, but if the manipulation is imprecise the consequence may be increased predation by non-hosts, to the detriment of the parasite. Three-spined sticklebacks (Gasterosteus aculeatus) infected by the cestode Schistocephalus solidus express reduced antipredator behaviours, but it is unknown whether this is an example of a highly precise manipulation, a more general manipulation, or if it can even be attributed to mere side effects of disease. In a series of experiments, we investigated several behaviours of infected and uninfected sticklebacks. As expected, they had weak responses to simulated predatory attacks compared to uninfected fish. However, our results suggest that the parasite induced a general fearlessness, rather than a precise manipulation aimed at the correct predators (birds). Infected fish had reduced responses also when attacked from the side and when exposed to odour from a fish predator, which is a “dead-end” for this parasite. We also tested whether the reduced anti-predator behaviours were mere symptoms of a decreased overall vigour, or due to parasite-induced hunger, but we found no support for these ideas. We propose that even imprecise manipulations of anti-predator behaviours may benefit parasites, for example, if other behaviours are altered in a way that increases the exposure to the correct predator.

Got the travel bug?

Like many of us in 2021, I miss the glee of traveling to new and exciting locations on vacation (and can't wait to get back these adventures post-pandemic). Yet, what I don't miss are the inevitable bugs I pick up along the way. Whether it be a cold or a stomach flu, many of us come down with some sort of infection when we are away from home. Many things could contribute to these illnesses, including travel-induced sleep deprivation, novel foods or the concentration of viruses on mass transit. But, could it be that our bodies are just not primed to defend us against the diseases in foreign locales? Agnes Piecyk from the Max Planck Institute for Evolutionary Biology, Germany, and colleagues from the USA and Germany wanted to investigate this theory to figure out whether hosts and parasites develop specialized relationships depending on their geographic origin.So, they took advantage of a host–parasite system that is found throughout the northern hemisphere: the three-spined stickleback Gasterosteus aculeatus and its tapeworm Schistocephalus solidus. The stickleback picks up this nasty worm in a way commonly found on our own human travels – in its food. One of its favourite foods, the copepod, is commonly infected by this parasite. Once consumed, the parasite burrows through the fish's gut, invading its body and quickly growing to fill every nook and cranny of the fish's insides. The parasite steals much of its host's food, forcing the stickleback to feed constantly to keep up with its own energy needs and the demand of its unwanted guest. This voracious feeding makes it less likely to take shelter to avoid predators because of an overwhelming need for food, attracting the attention of its primary predators – and the next host in the parasite's life cycle – fish-eating birds. The parasite then gladly makes its way to the bird's gut, where it sexually reproduces, starting the process again when the bird deposits the parasite's eggs back into waterways containing the copepod (its first host) through its feces. This incredible chain of events has evolved through an evolutionary arms race among the parasite and its three host species.Using sticklebacks and tapeworms from Europe and Alaska, the researchers set about testing the feasibility of inter-continental infections, exposing Alaskan sticklebacks to European tapeworms and vice versa. Surprisingly, while the Alaskan parasite readily infected the European fish host, the Alaskan stickleback put up a stronger fight against the European tapeworm, with hosts from certain Alaskan regions effectively preventing infection altogether. For those unlucky fish that succumbed to infection, their worms varied greatly in size depending on the host's origin. In addition, even when the Alaskan sticklebacks did pick up an infection, their immune systems succeeded in keeping the worm in check, with much smaller worms relative to their body size than European sticklebacks. While we would typically cheer the hosts that entirely prevented a parasite invasion, those uninfected sticklebacks were skinnier than otherwise healthy sticklebacks, indicating the hidden energetic cost of their unseen battle.While the researchers’ work sheds light on the complex interactions between hosts and parasites on a local scale, we still have much to learn about how these geographic differences develop and whether there are epidemiological implications due to geographic differences in disease susceptibility. And hopefully this knowledge might one day help us to avoid the dreaded vacation bug (once we are finally back out there, galivanting in exciting new places).

Temperature-induced reorganisation of Schistocephalus solidus (Cestoda) proteome during the transition to the warm-blooded host.

ABSTRACTThe protein composition of the cestode Schistocephalus solidus was measured in an experiment simulating the trophic transmission of the parasite from a cold-blooded to a warm-blooded host. The first hour of host colonisation was studied in a model experiment, in which sticklebacks Gasterosteus aculeatus infected with S. solidus were heated at 40°C for 1 h. As a result, a decrease in the content of one tegument protein was detected in the plerocercoids of S. solidus. Sexual maturation of the parasites was initiated in an experiment where S. solidus larvae were taken from fish and cultured in vitro at 40°C for 48 h. Temperature-independent changes in the parasite proteome were investigated by incubating plerocercoids at 22°C for 48 h in culture medium. Analysis of the proteome allowed us to distinguish the temperature-induced genes of S. solidus, as well as to specify the molecular markers of the plerocercoid and adult worms. The main conclusion of the study is that the key enzymes of long-term metabolic changes (glycogen consumption, protein production, etc.) in parasites during colonisation of a warm-blooded host are induced by temperature.

Parasite infection impairs the shoaling behaviour of uninfected shoal members under predator attack

A key benefit of sociality is a reduction in predation risk. Cohesive group behaviour and rapid collective decision making are essential for reducing predation risk in groups. Parasite infection might reduce an individuals’ grouping behaviours and thereby change the behaviour of the group as a whole. To investigate the relationship between parasite infection and grouping behaviours, we studied groups of three-spined sticklebacks, Gasterosteus aculeatus, varying the number of individuals experimentally infected with the cestode Schistocephalus solidus. We studied groups of six sticklebacks containing 0, 2, 3, 4 or 6 infected individuals before and after a simulated bird attack. We predicted that infected individuals would have reduced shoaling and swimming speed and that the presence of infected individuals within a group would reduce group cohesion and speed. Uninfected fish increased shoaling and reduced swimming speed more than infected fish after the bird attack. In groups containing both infected and uninfected fish, the group behaviours were dominated by the more frequent character (uninfected versus infected). Interestingly, groups with equal numbers of uninfected and infected fish showed the least shoaling and had the lowest swimming speeds, suggesting that these groups failed to generate a majority and therefore displayed signs of indecisiveness by reducing their swimming speed the most. Our results provide evidence for a negative effect of infection on a group’s shoaling behaviour, thereby potentially deteriorating collective decision making. The presence of infected individuals might thus have far-reaching consequences in natural populations under predation risk.Significance statementParasite-infected individuals often show deviating group behaviours. This might reduce the anti-predator benefits of group living. However, it is unknown whether such deviations in group behaviour might influence the shoaling behaviour of uninfected group members and thereby the behaviour of the group as a whole. By experimentally infecting sticklebacks and investigating groups varying in infection rates, we show that infected sticklebacks differ in their shoaling behaviours from uninfected sticklebacks. Additionally, the presence of infected sticklebacks within the group affected the behaviour of uninfected shoal members. We show that shoals of infected fish are less cohesive and move slower compared to shoals of uninfected fish. Furthermore, we show that the infection rate of the shoal is crucial for how the group behaves.

Zone of Interaction Between the Parasite and the Host: Protein Profile of the Body Cavity Fluid of Gasterosteus aculeatus L. Infected with the Cestode Schistocephalus solidus (Muller, 1776).

During infection, the host and the parasite "communicate" with each other through various molecules, including proteins. The aim of this study was to describe the excretory-secretory proteins from the helminth Schistocephalus solidus and its intermediate host, the three-spined stickleback Gasterosteus aculeatus L., which are likely to be involved in interactions between them. Combined samples of washes from the G. aculeatus sticklebacks cavity infected with the S. solidus, and washes from the parasite surface were used as experimental samples, while washes from the uninfected fish body cavity were used as control. The obtained samples were analyzed using mass-spectrometry nLC-MS/MS. As a result of mass-spectrometry analysis 215 proteins were identified. Comparative quantitative analysis revealed significant differences in LFQ intensity between experimental and control samples for 20 stickleback proteins. In the experimental samples, we found an increase in the content of serpins, plasminogen, angiotensin 1-10, complement component C9, and a decrease in the content of triosephosphate isomerase, creatine kinase, fructose-biphosphate aldolase, superoxide dismutase, peroxidoxin-1, homocysteine-binding and fatty acid-binding proteins, compared to uninfected fish samples. In the experimental group washes, 30 S. solidus proteins were found, including malate dehydrogenase, annexin family proteins, serpins, peptidyl-prolyl cis-trans isomerase and fatty acid-binding protein. Thus, the protein composition of washes from the helminth S. solidus surface and the body cavity of infected and uninfected stickleback G. aculeatus were studied. As a result, it was shown that various components of the immune defense system predominated in the washes of infected fish and helminths.

Climate change facilitates a parasite's host exploitation via temperature-mediated immunometabolic processes.

Global climate change can influence organismic interactions like those between hosts and parasites. Rising temperatures may exacerbate the exploitation of hosts by parasites, especially in ectothermic systems. The metabolic activity of ectotherms is strongly linked to temperature and generally increases when temperatures rise. We hypothesized that temperature change in combination with parasite infection interferes with the host's immunometabolism. We used a parasite, the avian cestode Schistocephalus solidus, which taps most of its resources from the metabolism of an ectothermic intermediate host, the three-spined stickleback. We experimentally exposed sticklebacks to this parasite, and studied liver transcriptomes 50days after infection at 13°C and 24°C, to assess their immunometabolic responses. Furthermore, we monitored fitness parameters of the parasite and examined immunity and body condition of the sticklebacks at 13°C, 18°C and 24°C after 36, 50 and 64days of infection. At low temperatures (13°C), S. solidus growth was constrained, presumably also by the more active stickleback's immune system, thus delaying its infectivity for the final host to 64days. Warmer temperature (18°C and 24°C) enhanced S.solidus growth, and it became infective to the final host already after 36days. Overall, S. solidus produced many more viable offspring after development at elevated temperatures. In contrast, stickleback hosts had lower body conditions, and their immune system was less active at warm temperature. The stickleback's liver transcriptome revealed that mainly metabolic processes were differentially regulated between temperatures, whereas immune genes were not strongly affected. Temperature effects on gene expression were strongly enhanced in infected sticklebacks, and even in exposed-but-not-infected hosts. These data suggest that the parasite exposure in concert with rising temperature, as to be expected with global climate change, shifted the host's immunometabolism, thus providing nutrients for the enormous growth of the parasite and, at the same time suppressing immune defence.

Parasite infection disrupts escape behaviours in fish shoals.

Many prey species have evolved collective responses to avoid predation. They rapidly transfer information about potential predators to trigger and coordinate escape waves. Predation avoidance behaviour is often manipulated by trophically transmitted parasites, to facilitate their transmission to the next host. We hypothesized that the presence of infected, behaviourally altered individuals might disturb the spread of escape waves. We used the tapeworm Schistocephalus solidus, which increases risk-taking behaviour and decreases social responsiveness of its host, the three-spined stickleback, to test this hypothesis. Three subgroups of sticklebacks were placed next to one another in separate compartments with shelter. The middle subgroup contained either uninfected or infected sticklebacks. We confronted an outer subgroup with an artificial bird strike and studied how the escape response spread through the subgroups. With uninfected sticklebacks in the middle, escape waves spread rapidly through the entire shoal and fish remained in shelter thereafter. With infected sticklebacks in the middle, the escape wave was disrupted and uninfected fish rarely used the shelter. Infected individuals can disrupt the transmission of flight responses, thereby not only increasing their own predation risk but also that of their uninfected shoal members. Our study uncovers a potentially far-reaching fitness consequence of grouping with infected individuals.

The secretome of a parasite alters its host's behaviour but does not recapitulate the behavioural response to infection.

Parasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host-parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host-parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of S. solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial and that local adaptation between host-parasite pairs may extend to the response to the parasite's secretome content.

Behavior out of control: Experimental evolution of resistance to host manipulation.

Many parasites alter their host's phenotype in a manner that enhances their own fitness beyond the benefits they would gain from normal exploitation. Such host manipulation is rarely consistent with the host's best interests resulting in suboptimal and often fatal behavior from the host's perspective. In this case, hosts should evolve resistance to host manipulation. The cestode Schistocephalus solidus manipulates the behavior of its first intermediate copepod host to reduce its predation susceptibility and avoid fatal premature predation before the parasite is ready for transmission to its subsequent host. Thereafter, S. solidus increases host activity to facilitate transmission. If successful, this host manipulation is necessarily fatal for the host. I selected the copepod Macrocyclops albidus, a first intermediate host of S. solidus, for resistance or susceptibility to host manipulation to investigate their evolvability. Selection on the host indeed increased host manipulation in susceptible and reduced host manipulation in resistant selection lines. Interestingly, this seemed to be at least partly due to changes in the baseline levels of the modified trait (activity) rather than actual changes in resistance or susceptibility to host manipulation. Hence, hosts seem restricted in how rapidly and efficiently they can evolve resistance to host manipulation.

Early stages of infection of three-spined stickleback (Gasterosteus aculeatus) with the cestode Schistocephalus solidus.

Parasitic helminths have evolved strategies to evade their host's immune systems. Particularly, the early time of interactions between helminths and their hosts might be decisive for their infection success. We used the cestode Schistocephalus solidus, and its highly specific second intermediate host, the three-spined stickleback (Gasterosteus aculeatus) to investigate parasite infection and host cellular immune responses starting 1day postexposure (dpe). We recovered live parasites from stickleback body cavities already 24hr after exposure. Infection rates increased up to 50% and did not change from 4 dpe onwards. Thus, not all parasites had reached the body cavity at the early time points and clearance of the parasite at later time points did not occur. Stickleback head kidney leucocytes (HKLs) did not show distinct signs of activation and lymphocyte proliferation, granulocyte-to-lymphocyte ratios and respiratory burst activity of infected sticklebacks did not deviate from controls significantly. The immune system was activated only late, as indicated by an increase in the total count of HKL relative to stickleback weight (HKL per mg fish), which was significantly elevated in infected fish 32 dpe. S.solidus seems to evade leucocyte activity early during infection facilitating its establishment in the hosts' body cavity.

Parasite-infected sticklebacks increase the risk-taking behaviour of uninfected group members

Trophically transmitted parasites frequently increase their hosts' risk-taking behaviour, to facilitate transmission to the next host. Whether such elevated risk-taking can spill over to uninfected group members is, however, unknown. To investigate this, we confronted groups of 6 three-spined sticklebacks, Gasterosteus aculeatus, containing 0, 2, 4 or 6 experimentally infected individuals with a simulated bird attack and studied their risk-taking behaviour. As a parasite, we used the tapeworm Schistocephalus solidus, which increases the risk-taking of infected sticklebacks, to facilitate transmission to its final host, most often piscivorous birds. Before the attack, infected and uninfected individuals did not differ in their risk-taking. However, after the attack, individuals in groups with only infected members showed lower escape responses and higher risk-taking than individuals from groups with only uninfected members. Importantly, uninfected individuals adjusted their risk-taking behaviour to the number of infected group members, taking more risk with an increasing number of infected group members. Infected individuals, however, did not adjust their risk-taking to the number of uninfected group members. Our results show that behavioural manipulation by parasites does not only affect the infected host, but also uninfected group members, shedding new light on the social dynamics involved in host–parasite interactions.