Stylops ater is an endoparasite of the mining bee Andrena vaga with extreme sexual dimorphism and hypermetamorphosis. Its population structure, parasitization mode, genetic diversity and impact on host morphology were examined in nesting sites in Germany to better understand this highly specialized host–parasite interaction. The shift in host emergence due to stylopization was proven to be especially strong in A. vaga. Around 10% of bees hosted more than 1 Stylops, with at maximum 4. A trend in Stylops' preference for hosts of their own sex and a sex-specific position of extrusion from the host abdomen was found. Invasion of Andrena eggs by Stylops primary larvae was depicted for the first time. Cephalothoraces of female Stylops were smaller in male and pluristylopized hosts, likely due to lower nutrient supply. The genes H3, 18S and cytochrome c oxidase subunit 1 were highly conserved, revealing near-absence of local variation within Stylops. Ovaries of hosts with male Stylops contained poorly developed eggs while those of hosts with female Stylops were devoid of visible eggs, which might be due to a higher protein demand of female Stylops. Male Stylops, which might have a more energy-consuming development, led to a reduction in head width of their hosts. Host masculinization was present in the leaner shape of the metabasitarsus of stylopized females and is interpreted as a by-product of manipulation of the host's endocrine system to shift its emergence. Stylopization intensified tergal hairiness, most strongly in hosts with female Stylops, near the point of parasite extrusion, hinting towards substance-induced host manipulation.

Many parasites manipulate host behaviour to enhance their transmission. Baculoviruses induce enhanced locomotory activity (ELA) combined with subsequent climbing behaviour in lepidopteran larvae, which facilitates viral dispersal. However, the mechanisms underlying host manipulation system are largely unknown. Previously, larval locomotion during ELA was summarized as the distance travelled for a few minutes at several time points, which are unlikely to characterize ELA precisely, as ELA typically persists for several hours. In this study, we modified a recently developed method using time-lapse recording to characterize locomotion of Bombyx mori larvae infected with B. mori nucleopolyhedrovirus (BmNPV) for 24 h at 3 s resolution. Our data showed that the locomotion of the mock-infected larvae was restricted to a small area, whereas the BmNPV-infected larvae exhibited a large locomotory area. These results indicate that BmNPV dysregulates the locomotory pattern of host larvae. Furthermore, both the mock- and BmNPV-infected larvae showed periodic cycles of movement and stationary behaviour with a similar frequency, suggesting the physiological mechanisms that induce locomotion are unaffected by BmNPV infection. In contrast, the BmNPV-infected larvae exhibited fast and long-lasting locomotion compared with mock-infected larvae, which indicates that locomotory speed and duration are manipulated by BmNPV.

Certain species of parasites have the apparent ability to alter the behaviour of their host in order to facilitate the completion of their own life cycle. While documented in hairworms (phylum Nematomorpha), the ability for mermithid parasites (from the sister phylum Nematoda) to force hosts to enter water remains more enigmatic. Here, we present the first experimental evidence in a laboratory setting that an insect which normally never enters open water (the European earwig Forficula auricularia) will readily enter the water when infected with a mermithid nematode (Mermis nigrescens). Only adult mermithids appear capable of inducing this polarising shift in behaviour, with mermithid length being a very strong predictor of whether their host enters water. However, mermithid length was only weakly associated with how long it took an earwig to enter water following the beginning of a trial. Considering the evidence presented here and its alignment with a proteomic investigation on the same host–parasite system, this study provides strong evidence for adaptive behavioural manipulation and a foundational system for further behavioural and mechanistic exploration.

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted 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.

Factors that drive parasite specificity and differences in infection dynamics among alternative host species are important for ecology and evolution of host–parasite interactions, but still often poorly known in natural systems. Here, we investigated spatiotemporal dynamics of infection, host susceptibility and parasite-induced changes in host phenotype in a rarely explored host–parasite system, the Australapatemon sp. trematode infecting two sympatric species of freshwater leeches, Erpobdella octoculata and Helobdella stagnalis. We show significant variation in infection abundance between the host species in both space and time. Using experimental infections, we also show that most of this variation likely comes from interspecific differences in exposure rather than susceptibility. Moreover, we demonstrate that the hiding behaviour of E. octoculata, but not that of H. stagnalis, was impaired by the infection irrespective of the parasite abundance. This may increase susceptibility of E. octoculata to predation by the final avian host. We conclude that differences in patterns of infection and in behavioural alterations among alternative sympatric host species may arise in narrow spatial scales, which emphasises the importance of local infection and transmission dynamics for parasite life cycles.

Parasitic infection often results in alterations to the host's phenotype, and may modify selection pressures for host populations. Elucidating the mechanisms underlying these changes is essential to understand the evolution of host–parasite interactions. A variety of mechanisms may result in changes in the host's behavioural phenotype, ranging from simple by-products of infection to chemicals directly released by the parasite to alter behaviour. Another possibility may involve parasites freely moving to certain sites within tissues, at specific times of the day to induce behavioural changes in the host. We tested the hypothesis that parasites shift to certain sites within the host by quantifying the location and activity of the trematode Tylodelphys sp., whose mobile metacercarial stages remain unencysted in the eyes of the second intermediate fish host, the common bully (Gobiomorphus cotidianus). This parasite's definitive host is a piscivorous bird feeding exclusively during daytime. Ocular obstruction and metacercarial activity were assessed within the sedated host's eye at three time points 24 h−1 period, using video captured via an ophthalmoscope. Although observed metacercarial activity did not change between time periods, ocular obstruction was significantly reduced at night. Increased visual obstruction specifically during the foraging time of the parasite's definitive host strongly suggests that the parasite's activity pattern is adaptive.

Host manipulation is a common strategy of parasites employed to increase their fitness by changing the phenotype of their hosts. Whether host manipulation might be affected by environmental factors such as resource availability, has received little attention. We experimentally infected laboratory-bred copepods with the cestode Schistocephalus solidus, submitted infected and uninfected copepods to either a high or a low food treatment, and measured their behaviour. Infection reduced host activity and speed in both feeding treatments. However, the difference between the infected and uninfected copepods was smaller under low food conditions, because uninfected, but not infected, copepods moved slower under these conditions. We suggest that these differences are mediated by the physical condition of copepods rather than changes in how strongly the parasite manipulated host behaviour. Additionally, we measured three fitness-relevant traits (growth, development and infection rate in the next host) of the parasite to identify potential trade-offs with host manipulation. The largest parasites in copepods appeared the least manipulative, i.e. their hosts showed the smallest behavioural alterations, but this may again reflect variation in copepod condition, rather than life history trade-offs between parasite growth and host manipulation. Our results point to the possibility that parasite transmission depends on environmental conditions.

Changes in host phenotype are often attributed to manipulation that enables parasites to complete trophic transmission cycles. We characterized changes in host phenotype in a colonial host–endoparasite system that lacks trophic transmission (the freshwater bryozoan Fredericella sultana and myxozoan parasite Tetracapsuloides bryosalmonae). We show that parasitism exerts opposing phenotypic effects at the colony and module levels. Thus, overt infection (the development of infectious spores in the host body cavity) was linked to a reduction in colony size and growth rate, while colony modules exhibited a form of gigantism. Larger modules may support larger parasite sacs and increase metabolite availability to the parasite. Host metabolic rates were lower in overtly infected relative to uninfected hosts that were not investing in propagule production. This suggests a role for direct resource competition and active parasite manipulation (castration) in driving the expression of the infected phenotype. The malformed offspring (statoblasts) of infected colonies had greatly reduced hatching success. Coupled with the severe reduction in statoblast production this suggests that vertical transmission is rare in overtly infected modules. We show that although the parasite can occasionally infect statoblasts during overt infections, no infections were detected in the surviving mature offspring, suggesting that during overt infections, horizontal transmission incurs a trade-off with vertical transmission.

Freshwater gammarids infected with the acanthocephalan parasite Polymorphus minutus show behavioural alterations but also differ from uninfected individuals in their appearance because of the carotenoid-based colouration of the parasite visible through the cuticle. However, it's not clear whether this phenotypic alteration is an adaptation favouring parasite transmission to the definitive host. To test this hypothesis, we investigated the selective preference of mallard towards two prey types: uninfected gammarids on which we applied a dot of inconspicuous brown paint, and uninfected gammarids on which we applied a dot of bright orange paint to mimic the change in appearance due to P. minutus without changes in host behaviour. Mallards showed a significant preference for orange-painted gammarids regardless of how gammarids were distributed (isolated or aggregated). This suggests that parasite's colouration may play a role in enhanced transmission to definitive avian hosts. The role of P. minutus’ colouration in the conspicuousness of gammarids has however to be balanced by the extent to which mallards use visual cues to forage in the field. From the perspective of a multidimensional manipulation, this study suggests that the change in appearance may act synergistically with the changes in behaviour to promote transmission to waterbirds.

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.

Many complex life cycle parasites exhibit seasonal transmission between hosts. Expression of parasite traits related to transmission, such as the manipulation of host phenotype, may peak in seasons when transmission is optimal. The acanthocephalan Acanthocephalus lucii is primarily transmitted to its fish definitive host in spring. We assessed whether the parasitic alteration of 2 traits (hiding behaviour and coloration) in the isopod intermediate host was more pronounced at this time of year. Refuge use by infected isopods was lower, relative to uninfected isopods, in spring than in summer or fall. Infected isopods had darker abdomens than uninfected isopods, but this difference did not vary between seasons. The level of host alteration was unaffected by exposing isopods to different light and temperature regimes. In a group of infected isopods kept at 4°C, refuge use decreased from November to May, indicating that reduced hiding in spring develops during winter. Keeping isopods at 16°C instead of 4°C resulted in higher mortality but not accelerated changes in host behaviour. Our results suggest that changes in host and/or parasite age, not environmental conditions, underlie the seasonal alteration of host behaviour, but further work is necessary to determine if this is an adaptive parasite strategy to be transmitted in a particular season.

Phenotypic alterations induced by parasites in their intermediate hosts often result in enhanced trophic transmission to appropriate final hosts. However, such alterations may also increase the vulnerability of intermediate hosts to predation by non-host species. We studied the influence of both infection with 3 different acanthocephalan parasites (Pomphorhynchus laevis, P. tereticollis, and Polymorphus minutus) and the availability of refuges on the susceptibility of the amphipod Gammarus pulex to predation by 2 non-host predators in microcosms. Only infection with P. laevis increased the vulnerability of amphipods to predation by crayfish, Orconectes limosus. In contrast, in the absence of refuges, the selectivity of water scorpions, Nepa cinerea, for infected prey was significant and did not differ according to parasite species. When a refuge was available for infected prey, however, water scorpion selectivity for infected prey differed between parasite species. Both P. tereticollis- and P. laevis-infected gammarids were more vulnerable than uninfected ones, whereas the reverse was true of P. minutus-infected gammarids. These results suggest that the true consequences of phenotypic changes associated with parasitic infection in terms of increased trophic transmission of parasites deserve further assessment.

Host manipulation by trophically transmitted parasites may predispose infected hosts to predation and in this way enhance parasite transmission. In most study systems, however, the evidence comes from laboratory studies, and therefore knowledge of the effect of manipulation on parasite transmission efficiency in the wild is still limited. Here we examined the effect of Diplostomum spathaceum (Trematoda) eye flukes on the susceptibility of fish intermediate hosts to predation by bird definitive hosts. Our earlier studies have shown that the parasite alters fish phenotype and increases their susceptibility to artificial predation under laboratory conditions. In the present field study, we allowed wild birds to feed on fish from cages placed into a lake, and found that predation vulnerability of infected fish did not differ from that of controls. However, we suggest that the experimental set-up likely affected the result because the cages allowed gulls, which caught most of the fish in the study, to feed on fish in an easy, unnatural manner by standing on the edges of the cages. Nevertheless, considerable predation was observed, which provides important initial evidence of how this question should be addressed in the wild.

The complexity of the life-cycle of many parasitic helminths has driven the evolution of several well-documented adaptations serving to facilitate the completion of each difficult step in the cycle. In some trematode taxa, selection has even favoured the truncation of the life-cycle: progenetic larval stages (metacercariae) are capable of producing eggs inside their usual intermediate hosts, eliminating the need to be transmitted by predation to a definitive host. In some species, progenesis is shown by all individuals, whereas in other species both the normal and truncated life-cycles coexist in the same populations. Here, the strategies chosen by normal and progenetic metacercariae of the trematode Coitocaecum parvum are investigated and compared. Normal metacercariae, i.e. metacercariae that only develop into adults following ingestion by a suitable fish definitive host, were not capable of manipulating the behaviour of their amphipod intermediate host in ways that could facilitate their capture by fish. These metacercariae were associated with increased mortality in amphipods. Progenetic metacercariae, on the other hand, showed lower virulence levels than normal metacercariae. At the time of their death, amphipods harbouring progenetic metacercariae contained close to the maximum number of eggs that can be produced by progenetic metacercariae, suggesting that the parasite lowers its virulence to keep its host alive long enough to maximize egg output. The maintenance of the 2 strategies in the C. parvum population suggests that they may have equal fitness payoffs: progenesis and low virulence guarantee the production of at least some eggs, whereas the normal life-cycle and its associated higher virulence in the intermediate host provides a low probability of much higher fecundity.

Numerous studies have demonstrated that parasites with complex life-cycles can cause phenotypic modifications in their hosts that lead to an increased rate of transmission, and suggest that these modifications are the result of parasitic adaptations to manipulate the host. Little attention is paid, however, to separating the possibility of adaptive host manipulation from incidental (if fortuitous) side-effects of infection. In this study we combine statistical and analytical tools to interpret the impact of the macroparasite Ligula intestinalis L. (Cestoda, Pseudophyllidea) on the behaviour of its intermediate fish host (the roach, Rutilus rutilus L.), using field data on a natural system. Two distinct sets of generalized linear models agree that both the presence and the intensity of infection contribute to a modified behavioural response in the host. This was illustrated by a preference for the lake-edge in infected fish during autumn. Furthermore, the effect of parasites upon their host is heterogeneous with respect to parasite size, with larger parasite individuals having a disproportionate impact. A series of game-theoretic models of adaptive host manipulation illustrate a potential rationale for a size-dependent manipulation strategy in parasites. These findings illustrate the potential complexity and functionality of the impact of L. intestinalis upon its fish host, which together reduce the parsimony of the alternative ‘incidental effect’ hypothesis.

Parasites are able to influence intermediate hosts in a way that optimizes their growth and transmission to the next host. Macrocyclops albidus (Copepoda) suffer from a reduced escaping ability and an increased level of general activity, when infected with Schistocephalus solidus (Cestoda). This facilitates predation by the subsequent host, the three-spined stickleback. However, instead of adaptive host manipulation by the tapeworm, the altered copepod behaviour might be explained more simply as a constraint of the infection. Energy depletion could lead to decreased muscle performance and increased food searching activity. Furthermore, resource allocation among host tissues might change after infection. We therefore analysed the amount of storage lipids and muscle tissue before and after experimental infection. To determine the amount of muscles, we developed a new polarization-microscopic technique. Irrespective of infection, lipids and muscles were predictors of copepod survival. However, we found no effect of the parasite infection on muscles or lipids, and no indication of a change in resource allocation between these tissues. Our study suggests that behavioural changes in infected copepods are mediated by a mechanism different from energy depletion or a re-allocation of resources between muscles and lipids. We rather propose that the tapeworms directly manipulate copepod behaviour.

Different parasite species sharing the same intermediate host species may have similar or conflicting interests, depending on whether they are at the same stage in their life-cycle or whether they share the same definitive host. In the New Zealand cockle, Austrovenus stutchburyi, metacercariae of the digenean Meiogymnophallus sp. are positively associated with metacercariae of Curtuteria australis. This relationship is found in different cockle samples, and is independent of cockle shell size, which suggests that it is not merely the product of metacercariae accumulation over time. Both digenean species have the same definitive host, oystercatchers. Metacercariae of C. australis manipulate the phenotype of cockles, impairing the cockle's ability to burrow in the sediments. This makes the host more susceptible to oystercatcher predation. Thus Meiogymnophallus sp. can benefit by associating with C. australis and may hitch a ride with the manipulator parasite. This is supported by the finding that cockles impaired by C. australis and lying at the sediment surface harbour greater numbers of Meiogymnophallus than buried cockles. A third digenean species, whose sporocysts are found in cockles and which is not transmitted by predation, occurred only in surface cockles. Finally, a parasitic copepod with a direct life-cycle was found evenly distributed among buried and surface cockles, independently of their metacercarial loads. These results show that different parasite species do not use cockles in a random fashion, and that not all patterns of host use are consistent with shared or conflicting interests among parasites.