Plerocerci of the trypanorhynch cestode Progrillotia dasyatidis Beveridge, Neifar & Euzet, 2004 (Progrillotiidae) were isolated from the gallbladder of the three-spined stickleback Gasterosteus aculeatus from a small freshwater marsh in the Lake Atanasovsko Wetlands, a coastal area adjacent to the Black Sea coast, Bulgaria. The parasite was recorded in five out of 134 fish individuals studied (prevalence 3.73%, intensity 1–7, mean intensity 2.40 ± 1.17 and mean abundance 0.09 ± 0.06). A description of the plerocerci is presented, expanding data on intraspecific variation. The present report is the first record of P. dasyatidis from G. aculeatus (new host record) and from Bulgaria (new geographical record). Recording only plerocerci with evaginated scoleces in the sticklebacks is consistent with the hypothesis that teleosts are paratenic hosts and not intermediate hosts of P. dasyatidis.

How parasites alter host feeding ecology remains elusive in natural populations. A powerful approach to investigate the link between infection and feeding ecology is quantifying unique and shared responses to parasite infection in related host species within a common environment. Here, 9 pairs of sympatric populations of the three-spined and nine-spined stickleback fishes were sampled across a range of freshwater and brackish habitats to investigate how parasites alter host feeding ecology: (i) biotic and abiotic determinants of parasite community composition, and (ii) to what extent parasite infection correlates with trophic niche specialization of the 2 species, using stable isotope analyses (δ15N and δ13C). It was determined that parasite community composition and host parasite load varied among sites and species and were correlated with dissolved oxygen. It was also observed that the digenean Cyathocotyle sp.'s abundance, a common directly infecting parasite with a complex life cycle, correlated with host δ13C in a fish species-specific manner. In 6 sites, correlations were found between parasite abundance and their hosts' feeding ecology. These effects were location-specific and occasionally host species or host size-specific. Overall, the results suggest a relationship between parasite infection and host trophic niche which may be an important and largely overlooked ecological factor. The population specificity and variation in parasite communities also suggest this effect is multifarious and context-dependent.

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.

We performed a long-term natural experiment investigating the impact of the diphyllobotriidean cestode Schistocephalus solidus on the body condition and clutch size (CS) of threespine stickleback Gasterosteus aculeatus, its second intermediate host, and the growth of larval parasites in host fish. We tested the hypothesis that single S. solidus infections were more virulent than multiple infections. We also asked whether the metrics of mean and total parasite mass (proxies for individual and total volume, respectively) were consistent with predictions of the resource constraints or the life history strategy (LHS) hypothesis for the growth of, hence exploitation by, larval helminths in intermediate hosts. The samples were drawn from Walby Lake, Alaska in eight of 11 years. Host body condition and CS (egg number per spawning bout) decreased significantly with intensity after adjustments for host size and parasite index. Thus, infections have an increasingly negative impact on measures of host fitness with greater intensity, in contrast to the hypothesis that single infections are more harmful than multiple infections. We also found that mean parasite mass decreased with intensity while total parasite mass increased with intensity as predicted by the LHS hypothesis.

Long-term population dynamics of three-spined stickleback Gasterosteus aculeatus in the White Sea during the 20th century has patterns similar to that of eelgrass Zostera marina. In this study we address possible mechanisms of such association through analysis of spatial distribution of juvenile stickleback in the wild and their substrate preferences in experimental conditions. Samples from different habitats (Z. marina, Fucus spp.) in 13 localities of Kandalaksha Bay have shown that the juvenile sticklebacks occurred mainly in the eelgrass beds. Their density was significantly lower in fucoids. In the experiments, carried out in August 2008–2009, the juveniles were offered the following types of substrates: brown macroalgae (dense and scarce), eelgrass and control (no substrate). In the experiments sticklebacks also showed a tendency to prefer eelgrass to fucoids, even if the density of the latter was higher. This may explain their higher densities associated with eelgrass in the wild.

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.

Today, three-spined stickleback Gasterosteus aculeatus are the most abundant fish in the White Sea and are close to their historical maximum. Based on observations from 2011–2013, this study reports quantitative and qualitative characteristics of juvenile stickleback diet during periods of active feeding in coastal Zostera seagrass beds. The following planktonic taxa dominated stomach contents: copepods Temora longicornis and Microsetella norvegica, ciliophora Helicostomella subulata. Benthic organisms such as Oligochaetae and Orthocladiinae also played an important role, whereas the literature suggests they were once rare in marine stickleback diets. Consumption patterns depended on fish size, with the most pronounced diet shift taking place as juveniles reached a length of 15 mm, in late August. In larger juveniles the highest correlation between the abundance of food organisms in stomachs and in the sea was observed for Orthocladiinae, suggesting that they are the preferred food. Overall, changes in diet followed changes in the abundance of available food organisms, but food selectivity analysis of planktonic organisms showed that M. norvegica were actively selected by juveniles.

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.

Trophically-transmitted parasites generally need to undergo a period of development in the intermediate host before reaching infectivity. During this vulnerable period, manipulation of the host to reduce susceptibility to predation would be advantageous for parasites, because it increases the probability of surviving until infectivity and thus the probability of transmission. We tested this ‘predation suppression’ hypothesis in 2 parasite species that use copepods as first hosts: the tapeworm Schistocephalus solidus and the nematode Camallanus lacustris. In a series of prey choice experiments, we found that copepods harbouring uninfective, still-developing worm larvae were less frequently consumed by stickleback predators than uninfected copepods. The levels of predation suppression were similar in the two parasite species, suggestive of convergent evolution. Additionally, copepods harbouring 2 worms of a given species were not more susceptible to predation than those with 1 worm, suggesting that excessive larval parasite growth does not increase host susceptibility to predation. Our results support the idea that parasites can suppress intermediate host susceptibility to predation while uninfective, but we also note that the available studies suggest that this effect is weaker than the frequently observed enhancement of host predation by infective helminth larvae.

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.

Plerocercoids of the pseudophyllidean cestode Schistocephalus solidus infect the three-spined stickleback Gasterosteus aculeatus, with important consequences for the biology of host fish. Techniques for culturing the parasite in vitro and generating infective stages that can be used to infect sticklebacks experimentally have been developed, and the system is increasingly used as a laboratory model for investigating aspects of host-parasite interactions. Recent experimental laboratory studies have focused on the immune responses of hosts to infection, the consequences of infection for the growth and reproductive development of host fish and the effects of infection on host behaviour. Here we introduce the host and the parasite, review the major findings of these recent experimental infection studies and identify further aspects of host parasite interactions that might be investigated using the system.

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.

Alternative mating tactics are found in many species, and may have important implications for population genetics and speciation. The existence of such alternative mating tactics is well-documented in the three-spined stickleback Gasterosteus aculeatus, and sneaking and egg-stealing may occur in a significant proportion of matings under natural conditions. Sneaking can impose high costs on territorial males, both in terms of reduced reproductive output and caring for unrelated offspring. We ask whether territorial males adjust their behaviour in response to the risk of sneaking. In a field study of three-spined sticklebacks on the Isle of Arran, Scotland, territorial males were presented with glass bottles containing either a male, a female or neither, to address whether territorial males were more aggressive to other males in the presence of a female, and whether territorial males courted females less in the presence of another male. Behavioural observations showed that territorial males did not behave more aggressively towards rival males in the presence of a female, but did reduce their rate of courtship towards females in the presence of rival males. We conclude that territorial males adopt behavioural strategies that may reduce their risk of reproductive parasitism.

The acanthocephalan parasite Pomphorhynchus laevis is transmitted by a suitable intermediate host such as the amphipod Gammarus pulex to its definitive fish host. Parasite-induced alterations in both appearance and behaviour concur to render infected gammarids more vulnerable to predation, thus promoting parasite transmission. Experimental infection of laboratory bred full- and half-sib groups of three-spined sticklebacks (Gasterosteus aculeatus) provided evidence that the parasite imposes a survival cost proportional to the severity of infection on its final host. Variation among sibships in the susceptibility to infection was consistent. When given a choice, fish consumed significantly more infected than uninfected prey. Overall, more resistant fish did not prey upon infected gammarids more often than did relatively susceptible fish. Only fish with a relatively high physical condition properly adjusted prey selection to the extent of their parasite susceptibility, thus exploiting the enhanced profitability of infected prey.

Viviparous gyrodactylid monogeneans which are detached from their host may form an important source of infection in fish communities. This is particularly significant for these ectoparasites which have no specific free-living stage and where transmission usually occurs through transfer of adult parasites when fish come into close contact. In this study, in vitro survival of Gyrodactylus gasterostei was correlated with changes in tissue ultrastructure of parents and their embryos during detachment and following return to a host. At 10 °C, detached worms survived for up to 89 h (50% survival = 20 h) with mortality influenced by both age-independent and age-dependent factors. The gastrodermis of attached, fed parasites is syncytial and contains a variety of vesicles and feeding vacuoles. However, following detachment and starvation, degenerative changes occur within the gastrodermis, eventually leading to marked damage to the embryo/s. When starved worms reattached to a fish, they began browsing on host epithelial cells within 1 min and ultrastructural evidence for phagocytic activity in the gastrodermis was detected after 5 min. Putative waste vacuoles increased in abundance after 5–30 min on the new host, coinciding with the reappearance of electron-dense vesicles and possibly indicating completion of the first intracellular cycle of digestion. Parental feeding directly influenced the normal cyclical maturation and regression of the uterine lining between births. In extreme cases, starvation led to detached parasites (6·1%) aborting their embryos. However, even short periods off the host influenced development and survival of embryos, suggesting that temporary interruption of nutrient flow to the embryo can significantly affect gyrodactylid reproductive rates.

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.

Following deglaciation of the Cook Inlet region of Alaska approximately 16 000 years ago, anadromous threespine stickleback (Gasterosteus aculeatus) rapidly colonized emerging lakes and rivers forming resident, freshwater populations. Although the precise body shape of the ancestral marine population is unknown, marine sticklebacks sampled from both Pacific and Atlantic sites present remarkably little body shape variation among populations, which suggests that the morphology of any of the marine populations could be used to represent the ancestral phenotype. To infer the net evolutionary trajectories of body shape change in the Cook Inlet radiation, derived body shapes of lacustrine samples were compared to the presumptive, primitive body shape, represented by the mean shape of two anadromous samples from Cook Inlet. In general, some derived body shape traits are shared by all freshwater populations but many traits evolved in opposite directions. The principal axes of shape variation among freshwater sample means were computed using Principal Components Analysis. The strong correlation between the direction of the principal component axes and lake habitat variables suggest that populations evolved toward selection peaks that are biased along the component axes due to biotic and abiotic features of the lakes.