The cestode Schistocephalus solidus is a common parasite in freshwater threespine stickleback populations, imposing strong fitness costs on their hosts. Given this, it is surprising how little is known about the timing and development of infections in natural stickleback populations. Previous work showed that young-of-year stickleback can get infected shortly after hatching. We extended this observation by comparing infection prevalence of young-of-year stickleback from 3 Alaskan populations (Walby, Cornelius and Wolf lakes) over 2 successive cohorts (2018/19 and 2019/20). We observed strong variation between sampling years (2018 vs 2019 vs 2020), stickleback age groups (young-of-year vs 1-year-old) and sampling populations.

Remarkably few attempts have been made to estimate contemporary effective population size (Ne) for parasitic species, despite the valuable perspectives it can offer on the tempo and pace of parasite evolution as well as coevolutionary dynamics of host–parasite interactions. In this study, we utilized multi-locus microsatellite data to derive single-sample and temporal estimates of contemporary Ne for a cestode parasite (Schistocephalus solidus) as well as three-spined stickleback hosts (Gasterosteus aculeatus) in lakes across Alaska. Consistent with prior studies, both approaches recovered small and highly variable estimates of parasite and host Ne. We also found that estimates of host Ne and parasite Ne were sensitive to assumptions about population genetic structure and connectivity. And, while prior work on the stickleback–cestode system indicates that physiographic factors external to stickleback hosts largely govern genetic variation in S. solidus, our findings indicate that stickleback host attributes and factors internal to the host – namely body length, genetic diversity and infection – shape contemporary Ne of cestode parasites.

Host manipulation whereby a parasite increases its transmission to a subsequent host by altering the behaviour of its current host is very far spread. It also occurs in host–parasite systems that are widely distributed. This offers the potential for local adaptation. The tapeworm Schistocephalus solidus modifies its first intermediate copepod host's predation susceptibility to suit its own needs by reducing its activity before it becomes infective and increasing it thereafter. To investigate potential differences in host manipulation between different populations and test for potential local adaptation with regard to host manipulation, I experimentally infected hosts from two distinct populations with parasites from either population in a fully crossed design. Host manipulation differed between populations mostly once the parasite had reached infectivity. These differences in infective parasites were mostly due to differences between different parasite populations. In not yet infective parasites, however, host population also had a significant effect on host manipulation. There was no evidence of local adaptation; parasites were able to manipulate foreign and local hosts equally well. Likewise, hosts were equally poor at resisting host manipulation by local and foreign parasites.

Trophically transmitted parasites must trade-off own growth on one hand and energy drain from the intermediate host on the other hand, since killing the host before transmission to the next host is a dead end for both parasites and hosts. This challenge becomes especially intriguing when multiple parasites find themselves within the same individual host. The tapeworm Schistocephalus solidus may gain more than 98% of its final body mass within few months infecting its three-spined stickleback (Gasterosteus aculeatus) intermediate host. During these months the tapeworms may achieve a mass even larger than its host. We studied virulence of single and multiple infections of S. solidus, by comparing body condition of wild stickleback hosts in two perennial stickleback populations located at high latitudes, and each population was studied in two different years. Our results demonstrated multiple compared with single infections to be a highly significant predictor of the condition of stickleback hosts, with multiple-infected hosts having relatively higher body condition. However, this applied only after adjusting for parasite mass, which was another significant predictor for host condition. Thus, our results suggested that, at a given parasite mass, S. solidus was more harmful towards their host's body condition in single compared with multiple infections.

Anthropogenic activities are having profound impacts on species interactions, with further consequences for populations and communities. We investigated the influence that anthropogenic eutrophication has on the prevalence of the parasitic tapeworm Schistocephalus solidus in threespine stickleback Gasterosteus aculeatus populations. We caught stickleback from four areas along the coast of Finland, and within each area from one undisturbed and one eutrophied habitat. We found the prevalence of the parasite to be lower in the eutrophied habitats at the start of the breeding season, probably because of fewer piscivorous birds that transmit the parasite. However, while the prevalence of the parasite declined across the season in the undisturbed habitat, it did less so in eutrophied habitats. We discuss different processes that could be behind the differences, such as lower predation rate on infected fish, higher food availability and less dispersal in eutrophied habitats. We found no effect of eutrophication on the proportion of infected stickleback that entered reproductive condition. Together with earlier findings, this suggests that eutrophication increases the proportion of infected stickleback that reproduce. This could promote the evolution of less parasite resistant populations, with potential consequences for the viability of the interacting parties of the host–parasite system.

We surveyed nine populations of the three-spined stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus from south-central Alaska for two apparent forms of tolerance to infection in females capable of producing egg clutches notwithstanding large parasite burdens. Seven populations exhibited fecundity reduction, whereas two populations showed fecundity compensation. Our data suggest that fecundity reduction, a side effect resulting from nutrient theft, occurs in two phases of host response influenced by the parasite : host body mass (BM) ratio. The first is significantly reduced ovum mass without significant reduction in clutch size, and the second one involves significant reductions in both ovum mass and clutch size. Thus, ovum mass of host females who are functionally being starved through nutrient theft seems to be more readily influenced by parasitism and, therefore, decreased before clutch size is reduced. This inference is consistent with expectations based on the biology of and effect of feeding ration on reproduction in stickleback females. Fecundity compensation appears to be uncommon among populations of three-spined stickleback in Alaska and rare among populations throughout the northern hemisphere. Fecundity reduction seems to be common, at least among stickleback populations in Alaska.

Simultaneous hermaphrodites maximize their fitness by optimizing their investment into male or female functions. Allocation of resources to male function (tissues, traits, and/or behaviours increasing paternity) is predicted to increase as density, and the associated level of sperm competition, increases. We tested whether the simultaneous hermaphroditic cestode Schistocephalus solidus uses cues of potential partner densities in its fish intermediate host to improve its male reproductive success in the final host. We had two worms, one originating from a multiple infection in the fish intermediate host and one from a single infection, sequentially compete to fertilize the eggs of a third worm. The fertilization rates of the two competitors nearly always differed from the 50–50 null expectation, sometimes considerably, implying there was a ‘winner’ in each experimental competition. However, we did not find a significant effect of density in the fish host (single vs multiple) or mating order on paternity. Additional work will be needed to identify the traits and environmental conditions that explain the high variance in male reproductive success observed in this experiment.

The activity of hepatic glutathione-S-transferase (GST) was analysed in 3 different fish species with respect to fish sex and infection with parasites. In both sexes of laboratory bred three-spined sticklebacks (Gasterosteus aculeatus) experimentally infected with Schistocephalus solidus (Cestoda), a significantly lower GST-activity was found for infected fish compared to control. After field sampling of roach (Rutilus rutilus) from Lake Müggelsee (MS) and the Reservoir Listertalsperre (LTS), the GST-activity showed significantly lower values for males infected with Ligula intestinalis from MS (25%) and for infected females from LTS (55%). L. intestinalis-infected female chub (Leuciscus cephalus) from LTS also appeared to have a lower GST-activity. Thus, it could be shown that the presence of parasites significantly affects GST-activity in different fish species resulting in a decreased GST-activity due to infection. Our results therefore emphasize the need for more integrative approaches in environmental pollution research to clearly identify the possible effects of parasites in an effort to develop biomarkers for evaluating environmental health.

An analysis of the metrics of Schistocephalus solidus infection of the threespine stickleback, Gasterosteus aculeatus, in Walby Lake, Alaska, showed that an epizootic ended between 1996 and 1998 and another occurred between 1998 and 2003. The end of the first epizootic was associated with a crash in population size of the stickleback, which serves as the second intermediate host. The likely cause of the end of that epizootic is mass mortality of host fish over winter in 1996–1997. The deleterious impact of the parasite on host reproduction and increased host predation associated with parasitic manipulation of host behaviour and morphology to facilitate transmission might also have played a role, along with unknown environmental factors acting on heavily infected fish or fish in poor condition. The second epizootic was linked to relatively high levels of prevalence and mean intensity of infection, but parasite:host mass ratios were quite low at the peak and there were no apparent mass deaths of the host. A number of abiotic and biotic factors are likely to interact to contribute to the occurrence of epizootics in S. solidus, which appear to be unstable and variable. Epizootics appear to depend on particular and, at times, rare sets of circumstances.

The objective of this study was to investigate the means by which Schistocephalus solidus might reduce annual fecundity in female threespine stickleback fish (Gasterosteus aculeatus) through processes of oocyte development. Histological examinations of specimens from one lake in Alaska in 2000 and 2001 were used to analyse the effects of S. solidus on recruitment of primary growth oocytes into vitellogenesis, atresia of vitellogenic oocytes, and the interspawning interval. The ratio of primary growth to late secondary growth (late vitellogenic) oocytes was significantly greater (P<0·01) among infected fish than uninfected ones in early-season samples from 2000 and 2001, revealing a decrease in recruitment of oocytes from primary growth into vitellogenic oocytes among infected females. The difference was marginally non-significant (P=0·087) in a mid-season sample from 2001 due to reductions in the entire pool of vitellogenic (early and late secondary growth) oocytes recruited prior to the spawning season in this determinate-fecundity species. Atresia among all vitellogenic oocytes was low and did not differ between infected and uninfected females. Histological estimations of the interspawning interval using post-ovulatory follicles showed no significant differences between infected and uninfected fish, suggesting that the number of spawnings in stickleback females each spawning season is unaffected by S. solidus infection. Thus, annual fecundity appears to be reduced only through recruitment of oocytes into vitellogenesis.

Many parasites that use intermediate hosts are transmitted to the next host through predation. If the next host's fitness is strongly reduced by the parasite, it is under selection either to recognize and avoid infected intermediate hosts or to exclude that prey species from its diet when alternative prey are available. We investigated the predator-prey interaction between laboratory bred three-spined sticklebacks (Gasterosteus aculeatus), the second intermediate host of the cestode Schistocephalus solidus, from 2 parasitized and 1 unparasitized population, and different prey types: infected and uninfected copepods and size-matched Daphnia as alternative prey. Copepods with infective procercoids were more active, had a lower swimming ability and were easier to catch than uninfected controls. The sticklebacks preferred moving copepods. Therefore parasitized copepods were preferentially attacked and consumed. There was no effect of the sticklebacks' parent population being parasitized or not. The sticklebacks switched from Daphnia to (uninfected) copepods in the course of a hunting sequence; this switch occurred earlier in smaller fish. With this strategy the fish maximized their feeding rate: Daphnia were easier to catch than copepods but increasingly difficult to swallow when the stomach was filling up especially for smaller fish. However, there was no indication that sticklebacks from infected populations either consumed Daphnia rather than copepods or switched later in the hunting sequence to consuming copepods than fish from an uninfected population. Thus, sticklebacks did not avoid parasitized prey although S. solidus usually has a high prevalence and causes a strong fitness reduction in its stickleback host.

This study shows that ingestion of Schistocephalus solidus coracidia was related to general activity of Macrocyclops albidus copepods at the time of exposure. The lower the activity of the host, the fewer parasites it ingested. In an earlier study it was shown that large M. albidus copepods were less likely to become infected with S. solidus than small copepods, which could potentially be caused by differential ingestion of parasites. However, the current study did not show any evidence for such an effect arising through differential ingestion. Body size was not related to ingestion of parasites, but was positively correlated to activity. So, even though size did not significantly relate to ingestion of parasites, if anything, through their higher activity large copepods rather than small copepods may have ingested more parasites. This study indicates that differences in resistance to this parasite do not come about through differential ingestion of parasites. Also, an earlier study failed to show differential elimination of the parasite from the haemocoel. This leaves avoidance of penetration through the gut wall as the most plausible candidate causing large copepods to be more resistant to this parasite than small copepods.

The outcome of a parasite infection is the result of the interaction between the host and the parasite. In the system we studied, there are 3 critical stages for the outcome of infection of the (intermediate) host, the copepod Macrocyclops albidus, with the cestode Schistocephalus solidus. During the establishment phase of the parasite, the host may firstly avoid ingesting the parasite and, secondly, may prevent the parasite from entering the body cavity and, thirdly, during the growth phase of the parasite, the host's immune system may eliminate the parasite from the body cavity. We were able to study the growth phase separately from the establishment phase. The establishment phase was influenced by characteristics of the host as well as characteristics of the parasites. Small copepods and males performed poorly; they were more often infected and had a lower survival. Parasites from different sib-groups differed in infectivity. During the growth phase some disappearance of parasites was observed. However, this could not be related to any of the studied characteristics of the host, and the sib-groups of parasites did not seem to differ in their likelihood to disappear. Instead, we suggest that disappearance of parasites, once they have entered the body cavity, may be due to intrinsic mortality of the parasites, independent of the host or the sib-group that the parasites belong to. This indicates that the crucial interactions between host and parasite determining the outcome of infection takes place in the short time-period between ingestion and penetration of the gut-wall.

Experiments are often carried out in the laboratory under artificial conditions. Although this can control for confounding factors, it may eliminate important factors that under natural conditions mediate the interaction under investigation. Here, we show that different results can be gained in the field and in the laboratory regarding host–parasite interaction. In the field, courting three-spined stickleback males, Gasterosteus aculeatus, were less often infected with plerocercoids of a cestode tapeworm, Schistocephalus solidus, than shoaling males. However, when a random sample of males was allowed to nest and court females in individual aquaria in the laboratory, both uninfected and infected males built nests and courted females. Moreover, while the few infected males that courted females in the field expressed less red nuptial coloration than uninfected courting males, there was no difference in redness between infected and uninfected males in the laboratory. We argue that the different results gained in the field and in the laboratory are due to differences in the cost of reproduction, due to differences in the resource pool of the males. The favourable conditions in the laboratory exclude factors such as predation risk, social interactions, and fluctuating environmental conditions that may use up resources in the field and mediate the effect of the parasite.

The cestode Schistocephalus solidus is a simultaneous hermaphrodite that grows in 2 intermediate hosts and reproduces rapidly within a few days in the gut of a bird. Reproduction takes place by self- or cross-fertilization. Here, it was tested whether egg production differs between S. solidus that reproduce alone and those that are allowed to reproduce in pairs. Egg production in an in vitro system was found to depend on the cestodes' social situation. When kept alone, larger cestodes produced larger eggs. This was not so when kept in pairs – the difference between these 2 reproductive modes being highly significant in this respect. Further experiments revealed that, within the first 3 days, these hermaphrodites produced a larger total egg mass when kept alone than when kept in pairs. This was also reflected by the energy contents of the cestodes after this time-span: selfers had used up more energy than paired worms. Furthermore, S. solidus appeared to adjust its investment per egg depending on whether the offspring will be the result of self- or cross-fertilization. Selfers produced larger numbers of eggs, but these eggs were smaller and contained even smaller embryos per given egg size than eggs of potentially outbreeding cestodes. Selfed eggs reached lower hatching rates. Although this is to be expected from inbreeding depression it may also be an effect of the reduced maternal investment per egg. The observed phenotypic plasticity in the reproduction of S. solidus is discussed within 4 evolutionary frameworks: local mate competition adjusted for hermaphrodites, the hermaphrodite's dilemma, bet-hedging, and sib-competition.

In an experiment to study the infectivity, growth and virulence of Schistocephalus solidus in their first intermediate host, copepods of the species Macrocyclops albidus were kept singly and exposed to up to 9 coracidia. Eleven or 14 days post-infection (p.i.) the presence and growth of the cestode larvae relative to survival, growth and reproduction of their host was determined. As expected, the probability of a copepod becoming infected increased with increasing numbers of parasites administered. However, the chances of a single coracidium establishing in a copepod also increased with increasing numbers of coracidia administered, which indicates that the parasites profit from a dilution effect of the host's defence. Copepod size or developmental stage had no significant effect on the infection, but 14 days p.i., constraining effects of copepod size on the growth of the parasites were apparent. Moreover, procercoids in multiple infections grew smaller and developed their cercomer at a smaller size than those in single infections. No significant effect of the parasite on host mortality was found within the observation period. However, growth between the 5th copepodid stage and adult stage was negatively affected by infection. An infection with S. solidus was also strongly linked with host reproduction: infected females were more likely to bear an egg sac at the end of the experiment than non-infected ones. These egg sacs, however, contained fewer eggs.