Sex biases in prevalence of disease are often attributed to intrinsic factors, such as physiological differences while a proximate role of extrinsic factors such as behavioural or ecological differences may be more difficult to establish. We combined large-scale screening for the presence and lineage identity of avian malaria (haemosporidian) parasites, in 1234 collared flycatchers (Ficedula albicollis) with life-history information from each bird to establish the location and timing of infection. We found an overall infection rate of 36.2% ± 0.03 (95% CI) with 25 distinct malaria lineages. Interestingly, first-year breeding males and females had similar infection prevalence while females accrued a significantly higher infection rate than males later in life. The sex difference in infection rate was driven by the most abundant Haemoproteus, lineage, hPHSIB1, while the infection rate of Plasmodium lineages was similar in males and females. Furthermore, when infections were assigned to an apparent transmission location, we found that the sex difference in infection rate trend was driven by lineages transmitted in Europe, more specifically by one lineage (the hPHSIB1), while no similar pattern was found in African lineages. We deduce that the observed infection patterns are likely to be caused by differences in breeding behaviour, with incubating females (and nestling individuals of both sexes) being easy targets for the biting insects that are the vectors of avian malaria parasites. Overall, our results are most consistent with ecological factors rather than intrinsic factors underlying the observed sex-biased infection rate of avian malaria in collared flycatchers.

An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution.

The almost universally-occurring aggregated distributions of helminth burdens in host populations have major significance for parasite population ecology and evolutionary biology, but the mechanisms generating heterogeneity remain poorly understood. For the direct life cycle monogenean Discocotyle sagittata infecting rainbow trout, Oncorhynchus mykiss, variables potentially influencing aggregation can be analysed individually. This study was based at a fish farm where every host individual becomes infected by D. sagittata during each annual transmission period. Worm burdens were examined in one trout population maintained in isolation for 9 years, exposed to self-contained transmission. After this year-on-year recruitment, prevalence was 100% with intensities 10–2628, mean 576, worms per host. Parasite distribution, amongst hosts with the same age and environmental experience, was highly aggregated with variance to mean ratio 834 and negative binomial parameter, k, 0.64. The most heavily infected 20% of fish carried around 80% of the total adult parasite population. Aggregation develops within the first weeks post-infection; hosts typically carried intensities of successive age-specific cohorts that were consistent for that individual, such that heavily-infected individuals carried high numbers of all parasite age classes. Results suggest that host factors alone, operating post-infection, are sufficient to generate strongly overdispersed parasite distributions, rather than heterogeneity in exposure and initial invasion.

Removal of parasite free-living stages by predators has previously been suggested an important factor controlling parasite transmission in aquatic habitats. Experimental studies of zooplankton predation on macroparasite larvae are, however, scarce. We tested whether trematode cercariae, which are often numerous in shallow waters, are suitable prey for syntopic zooplankters. Feeding rates and survival of freshwater cyclopoids (Megacyclops viridis, Macrocyclops distinctus), calanoids (Arctodiaptomus paulseni), cladocerans (Sida crystallina) and rotifers Asplanchna spp., fed with cercariae of Diplostomum pseudospathaceum, a common fish trematode, were studied. In additional long-term experiments, we studied reproduction of cyclopoids fed with cercariae. All tested zooplankton species consumed cercariae. The highest feeding rates were observed for cyclopoids (33 ± 12 cercariae ind−1 h−1), which actively reproduced (up to one egg clutch day−1) when fed ad libitum with cercariae. Their reproductive characteristics did not change significantly with time, indicating that cercariae supported cyclopoids’ dietary needs. Mortality of rotifers and cladocerans was high (25–28% individuals) when exposed to cercariae in contrast to cyclopoids and calanoids (<2%). Cercariae clogged the filtration apparatus of cladocerans and caused internal injuries in predatory rotifers, which ingested cercariae. Observed trophic links between common freshwater zooplankters and cercariae may significantly influence food webs and parasite transmission in lentic ecosystems.

The microsporidian parasite Hamiltosporidium tvaerminnensis can infect Daphnia magna both horizontally (through environmental spores) and vertically (through parthenogenetic and sexually produced eggs). The spores of H. tvaerminnensis come in three distinguishable morphologies, which are thought to have different roles in the transmission of the parasite. In this study, we examined the role of the two most common spore morphologies (i.e. oval-shaped spores and pear-shaped spores) in horizontal transmission of H. tvaerminnensis. To this end, we infected hosts with solutions consisting of either mostly oval- or mostly pear-shaped spores, and quantified infection rates, parasite-induced host mortality and mean number of parasite spores produced per host. We found that spore morphology by itself did not influence infection rates and parasite-induced host mortality. Instead, host clone and parasite isolate interacted with spore morphology in shaping infection outcome and mortality. Thus, there appear to be strong genotype-by-genotype (G × G) interactions in this system. While there is no dispute that H. tvaerminnensis can transmit both vertically and horizontally, our findings do not support theoretical predictions that different spore morphologies hold different roles in horizontal transmission of H. tvaerminnensis.

The transmission from one host to another constitutes a challenging obstacle for parasites and is a key determinant of their fitness. Due to their complex life histories involving several different hosts, the free-living dispersal stages (cercariae) of digenean trematodes show a huge diversity in morphology and behaviour. On a finer scale, we still have an extremely limited understanding of the inter- and intraspecific variation in transmission strategies of many trematode species. Here, we present a novel method to study the movement patterns of cercariae of four New Zealand trematode species (Coitocaecum parvum, Maritrema poulini, Apatemon sp. and Aporocotylid sp. I.) via automated video tracking. This approach allows to quantify parameters otherwise not measurable and clearly illustrates the individual strategies of parasites to search for their respective target hosts. Cercariae that seek out an evasive fish target hosts showed higher swimming speeds (acceleration and velocity) and travelled further distances, compared with species searching for high-density crustacean hosts. Automated video tracking provides a powerful tool for such detailed analyses of parasites’ host-searching strategies and can enhance our understanding of complex host–parasite interactions, ranging from parasite community structure to the transmission of potential disease agents.

Recent results suggest that bivalves can play an important role in restraining the spread of various aquatic infections. However, the ability of mussels to remove free-living stages of macroparasites and reduce their transmission is still understudied, especially for freshwater ecosystems. We investigated the influence of the common freshwater mussel (Anodonta anatina) on the transmission of a trematode (eye fluke, Diplostomum pseudospathaceum), which frequently infects fish in farms and natural habitats. In our experiments, mussels caused a significant decrease (P < 0·001) in the abundance of trematode free-living stages, from 6520 to 1770 cercariae L−1 on average (about 4-fold in 2 h). Individual clearance rates of mussels were 0·6‒3·7 L per hour (mean 1·9). These tests were followed by experimental infections of rainbow trout (Oncorhynchus mykiss) with different doses of D. pseudospathaceum cercariae in the presence or absence of mussels. Exposure of fish to cercariae in the presence of mussels significantly (P < 0·05) reduced the infection intensities in fish (by 30–40%) at all exposure doses. Our results indicate that freshwater bivalves can markedly reduce local cercariae densities and could be useful in mitigation of trematodoses harmful to fish farming.

Heterogeneities in parasite infection among conspecific hosts often manifest as sex- or size-biased infections, which are typically attributed to differential host susceptibility and exposure. Since parasite fitness is often tied to host quality, host preference by parasites is likely to be under strong selection. We test the hypothesis that host preference is sufficient to generate variability in infection rate among conspecifics. Specifically, we ask whether the mite Macrocheles muscaedomesticae is able to discriminate between Drosophila hydei hosts of different sex and size, while explicitly accounting for the potential confounding effects of these two factors. Our results indicate a preference for female hosts, but this preference appears to be driven by size and not sex per se. When differences in body size were controlled for, the sex-biased infection disappeared, while mites presented with the choice of two female flies of disparate sizes were more likely to select the larger host. Across the distribution of fly body weight in this study, mites preferentially attached to flies of intermediate size. This study provides evidence that mite choice for certain host types can play an important role in parasite transmission, even in the absence of differential susceptibility or exposure among hosts.

Although many parasites are transmitted between hosts by a suite of arthropod vectors, the impact of vector biodiversity on parasite transmission is poorly understood. Positive relationships between host infection prevalence and vector species richness (SR) may operate through multiple mechanisms, including (i) increased vector abundance, (ii) a sampling effect in which species of high vectorial capacity are more likely to occur in species-rich communities, and (iii) functional diversity whereby communities comprised species with distinct phenologies may extend the duration of seasonal transmission. Teasing such mechanisms apart is impeded by a lack of appropriate data, yet could highlight a neglected role for functional diversity in parasite transmission. We used statistical modelling of extensive host, vector and microparasite data to test the hypothesis that functional diversity leading to longer seasonal transmission explained variable levels of disease in a wildlife population. We additionally developed a simple transmission model to guide our expectation of how an increased transmission season translates to infection prevalence. Our study demonstrates that vector SR is associated with increased levels of disease reporting, but not via increases in vector abundance or via a sampling effect. Rather, the relationship operates by extending the length of seasonal transmission, in line with theoretical predictions.

Parasites that primarily infect white-tailed deer (Odocoileus virginianus), such as liver flukes (Fascioloides magna) and meningeal worm (Parelaphostrongylus tenuis), can cause morbidity and mortality when incidentally infecting moose (Alces alces). Ecological factors are expected to influence spatial variation in infection risk by affecting the survival of free-living life stages outside the host and the abundance of intermediate gastropod hosts. Here, we investigate how ecology influenced the fine-scale distribution of these parasites in deer in Voyageurs National Park, Minnesota. Deer pellet groups (N = 295) were sampled for the presence of P. tenuis larvae and F. magna eggs. We found that deer were significantly more likely to be infected with P. tenuis in habitats with less upland deciduous forest and more upland mixed conifer forest and shrub, a pattern that mirrored microhabitat differences in gastropod abundances. Deer were also more likely to be infected with F. magna in areas with more marshland, specifically rooted-floating aquatic marshes (RFAMs). The environment played a larger role than deer density in determining spatial patterns of infection for both parasites, highlighting the importance of considering ecological factors on all stages of a parasite's life cycle in order to understand its occurrence within the definitive host.

Many studies have identified various host behavioural and ecological traits that are associated with parasite infection, including host gregariousness. By use of meta-analyses, we investigated to what degree parasite prevalence, intensity and species richness are correlated with group size in gregarious species. We predicted that larger groups would have more parasites and higher parasite species richness. We analysed a total of 70 correlations on parasite prevalence, intensity and species richness across different host group sizes. Parasite intensity and prevalence both increased positively with group size, as expected. No significant relationships were found between host group size and parasite species richness, suggesting that larger groups do not harbour more rare or novel parasite species than smaller groups. We further predicted that the mobility of the host (mobile, sedentary) and the mode of parasite transmission (direct, indirect, mobile) would be important predictors of the effects of group sizes on parasite infection. It was found that group size was positively correlated with the prevalence and intensity of directly and indirectly transmitted parasites. However, a negative relationship was observed between group size and mobile parasite intensity, with larger groups having lower parasite intensities. Further, intensities of parasites did not increase with group size of mobile hosts, suggesting that host mobility may negate parasite infection risk. The implications for the evolution and maintenance of sociality in host species are discussed, and future research directions are highlighted.

In Mar Chiquita coastal lagoon (Argentina), the reefs of the invasive polychaete Ficopomatus enigmaticus (Serpulidae) serve as concentration areas for invertebrates and vertebrates and as potential foci of parasite transmission (mainly digeneans). To analyse the role of F. enigmaticus as facilitator of parasite transmission, and to evaluate the influence of the habitats selected by 2 species of cochliopid snails (Heleobia conexa and Heleobia australis), on the richness and on the prevalence of the digenean assemblages that parasitize them, 1945 snails were collected from 2 sampling sites. The comparisons between larval digenean communities parasitizing both snail hosts revealed significant differences related to the overall prevalence and the prevalence contributed by birds in the snails collected from reefs. These results support the idea that the reefs may increase the number of links between intermediate and definitive hosts of digeneans, facilitating parasite transmission only when the aggregates of F. enigmaticus become the unique habitat of the snail host. This first report of an exotic species acting as facilitator of parasite transmission in an estuarine area highlights the importance of analysing the effects of the assimilation process of exotic species by recently colonized environments (including the possible effects on parasite transmission).

The ‘pygmaeus’ microphallids (MPG) are a closely related group of 6 digenean (Platyhelminthes: Trematoda) Microphallus species that share a derived 2-host life cycle in which metacercariae develop inside daughter sporocysts in the intermediate host (intertidal and subtidal gastropods, mostly of the genus Littorina) and are infective to marine birds (ducks, gulls and waders). Here we investigate MPG transmission patterns in coastal ecosystems and their diversification with respect to historical events, host switching and host-parasite co-evolution. Species phylogenies and phylogeographical reconstructions are estimated on the basis of 28S, ITS1 and ITS2 rDNA data and we use a combination of analyses to test the robustness and stability of the results, and the likelihood of alternative biogeographical scenarios. Results demonstrate that speciation within the MPG was not associated with co-speciation with either the first intermediate or final hosts, but rather by host-switching events coincident with glacial cycles in the Northern Hemisphere during the late Pliocene/Pleistocene. These resulted in the expansion of Pacific biota into the Arctic-North Atlantic and periodic isolation of Atlantic and Pacific populations. Thus we hypothesize that contemporary species of MPG and their host associations resulted from fragmentation of populations in regional refugia during stadials, and their subsequent range expansion from refugial centres during interstadials.

Manipulation of host phenotype (e.g. behaviour, appearance) is suggested to be a common strategy to enhance transmission in trophically transmitted parasites. However, in many systems, evidence of manipulation comes exclusively from laboratory studies and its occurrence in natural host populations is poorly understood. Here, we examined the potential for host manipulation by Diplostomum eye flukes indirectly by quantifying the physiological effects of parasites on fish. Earlier laboratory studies have shown that Diplostomum infection predisposes fish to predation by birds (definitive hosts of the parasites) by reducing fish vision through cataract formation. However, occurrence of cataracts and the subsequent potential for host manipulation in natural fish populations has remained poorly explored. We studied the occurrence of eye fluke-induced cataracts from 7 common fish species (Gymnocephalus cernuus, Rutilus rutilus, Leuciscus leuciscus, Alburnus alburnus, Osmerus eperlanus, Coregonus lavaretus and Gasterosteus aculeatus) from the Bothnian Bay in the Baltic Sea. We found that the parasite-induced cataracts were common in fish and they also reached high levels which are likely to predispose fish to predation. However, we observed such cataracts only in species with the highest parasite abundances, which suggests that only certain hosts may be strongly affected by the infection.

Host-parasite interactions are shaped by the co-evolutionary arms race of parasite virulence, transmission success as well as host resistance and recovery. The virulence and fitness of parasites may depend on host condition, which is mediated, for instance, by host energy constraints. Here, we investigated to what extent stress imposed by predation threat and environmental pollutants influences host-parasite interactions. We challenged the crustacean host Daphnia magna with the sterilizing bacterial endoparasite Pasteuria ramosa and simultaneously exposed the host to fish kairomones, the pesticide carbaryl or both stressors. While parasite virulence, measured as impact on host mortality and sterilization, increased markedly after short-term pesticide exposure, it was not influenced by predation threat. Parasite fitness, measured in terms of produced transmission stages, decreased both in fish and pesticide treatments. This effect was much stronger under predation threat than carbaryl exposure, and was attributable to reduced somatic growth of the host, presumably resulting in fewer resources for parasite development. While the indirect impact of both stressors on spore loads provides evidence for host condition-dependent parasite fitness, the finding of increased virulence only under carbaryl exposure indicates a stronger physiological impact of the neurotoxic chemical compared with the effect of a non-toxic fish kairomone.

The route of transmission and host finding behaviour are fundamental components of a parasite's fitness. Riccardoella limacum, a haematophagous mite, lives in the mantle cavity of helicid land snails. To date it has been assumed that this parasitic mite is transmitted during courtship and mating of the host. Here we present experimental evidence for a new transmission route in the host snail Arianta arbustorum. Parasite-free snails were kept on soil on which previously infected host snails had been maintained for 6 weeks. R. limacum was successfully transmitted via soil without physical contact among hosts in 10 out of 22 (45·5%) cases. In a series of experiments we also examined the off-host locomotion of R. limacum on snail mucus and control substrates using an automated camera system. Parasitic mites showed a preference to move on fresh mucus. Our results support the hypothesis that R. limacum uses mucus trails to locate new hosts. These findings should be considered in commercial snail farming and when examining the epidemiology of wild populations.

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 defensive glands of beetles, Tenebrio molitor, infected with metacestodes (cysticercoids) of Hymenolepis diminuta are everted less frequently upon stimulation, and contain less toluquinone (methylbenzoquinone) and m-cresol, than glands of uninfected controls. These differences, as shown in predation trials with wild rats, increase the likelihood that both cysticercoids and beetles will be ingested by the tapeworm's definitive host. This is the first documented case of a parasite inhibiting the chemical defence of an intermediate host, and one of only a few reports of parasite-induced manipulation of host biology supported by empirical evidence implicating facilitated parasite transmission between host species.