Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

While the host immune system is often considered the most important physiological mechanism against parasites, precontact mechanisms determining exposure to parasites may also affect infection dynamics. For instance, chemical cues released by hosts can attract parasite transmission stages. We used the freshwater snail Lymnaea stagnalis and its trematode parasite Echinoparyphium aconiatum to examine the role of host chemical attractiveness, physiological condition, and immune function in determining its susceptibility to infection. We assessed host attractiveness through parasite chemo‐orientation behavior; physiological condition through host body size, food consumption, and respiration rate; and immune function through two immune parameters (phenoloxidase‐like and antibacterial activity of hemolymph) at an individual level. We found that, although snails showed high variation in chemical attractiveness to E. aconiatum cercariae, this did not determine their overall susceptibility to infection. This was because large body size increased attractiveness, but also increased metabolic activity that reduced overall susceptibility. High metabolic rate indicates fast physiological processes, including immune activity. The examined immune traits, however, showed no association with susceptibility to infection. Our results indicate that postcontact mechanisms were more likely to determine snail susceptibility to infection than variation in attractiveness to parasites. These may include localized immune responses in the target tissue of the parasite. The lack of a relationship between food consumption and attractiveness to parasites contradicts earlier findings that show food deprivation reducing snail attractiveness. This suggests that, although variation in resource level over space and time can alter infection dynamics, variation in chemical attractiveness may not contribute to parasite‐induced fitness variation within populations when individuals experience similar environmental conditions.     

Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris

Parasites infect hosts non-randomly as genotypes of hosts vary in susceptibility to the same genotypes of parasites, but this specificity may be modulated by environmental factors such as nutrition. Nutrition plays an important role for any physiological investment. As immune responses are costly, resource limitation should negatively affect immunity through trade-offs with other physiological requirements. Consequently, nutritional limitation should diminish immune capacity in general, but does it also dampen differences among hosts? We investigated the effect of short-term pollen deprivation on the immune responses of our model host Bombus terrestris when infected with the highly prevalent natural parasite Crithidia bombi. Bumblebees deprived of pollen, their protein source, show reduced immune responses to infection. They failed to upregulate a number of genes, including antimicrobial peptides, in response to infection. In particular, they also showed less specific immune expression patterns across individuals and colonies. These findings provide evidence for how immune responses on the individual-level vary with important elements of the environment and illustrate how nutrition can functionally alter not only general resistance, but also alter the pattern of specific host–parasite interactions.     

Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction

Whether or not organisms become infected by parasites is likely to be a complex interplay between host and parasite genotypes, as well as the physiological condition of both species. Details of this interplay are very important because physiology‐driven susceptibility has the potential to confound genetic coevolutionary responses. Here we concentrate on how physiological aspects of infection may interfere with genetic‐based infectivity in a snail–trematode (Potamopyrgus antipodarum/Microphallus sp.) interaction by asking: (1) how does host condition affect susceptibility to infection? and (2) how does host condition affect the survival of infected individuals? We manipulated host condition by experimentally varying resources. Contrary to our expectation, host condition did not affect susceptibility to infection, suggesting that genetics are more important than physiology in this regard. However, hosts in poor condition had higher parasite‐induced mortality than hosts in good condition. Taken together, these results suggest that coevolutionary interactions with parasites may depend on host condition, not by altering susceptibility, but rather by affecting the likelihood of parasite transmission.     

Temporal patterns of genetic variation for resistance and infectivity in a Daphnia-microparasite system

Theoretical studies have indicated that the population genetics of host-parasite interactions may be highly dynamic. with parasites perpetually adapting to common host genotypes and hosts evolving resistance to common parasite genotypes. The present study examined temporal variation in resistance of hosts and infectivity of parasites within three populations of Daphnia magna infected with the sterilizing bacterium Pasteuria ramosa. Parasite isolates and host clones were collected in each of two years (1997, 1998) from one population; in two other populations, hosts were collected from both years, but parasites from only the first year. We then performed infection experiments (separately for each population) that exposed hosts to parasites from the same year or made combinations involving hosts and parasites from different years. In two populations, patterns were consistent with the evolution of host resistance: either infectivity or the speed with which parasites sterilized hosts declined from 1997 to 1998. In another population, infectivity, virulence, and parasite spore production did not vary among host-year or parasite-year. For this population, we also detected strong within-population genetic variation for resistance. Thus, in this case, genetic variability for fitness-related traits apparently did not translate into evolutionary change. We discuss a number of reasons why genetic change may not occur as expected in parasite-host systems, including negative correlations between resistance and other traits, gene flow, or that the dynamic process itself may obscure the detection of gene frequency changes.     

Manipulation of host-resource dynamics impacts transmission of trophic parasites

Many complex life cycle parasites rely on predator–prey interactions for transmission, whereby definitive hosts become infected via the consumption of an infected intermediate host. As such, these trophic parasites are embedded in the larger community food web. We postulated that exposure to infection and, hence, parasite transmission are inherently linked to host foraging ecology, and that perturbation of the host-resource dynamic will impact parasite transmission dynamics. We employed a field manipulation experiment in which natural populations of the eastern chipmunk (Tamias striatus) were provisioned with a readily available food resource in clumped or uniform spatial distributions. Using replicated longitudinal capture-mark-recapture techniques, replicated supplemented and unsupplemented control sites were monitored before and after treatment for changes in infection levels with three gastro-intestinal helminth parasites. We predicted that definitive hosts subject to food supplementation would experience lower rates of exposure to infective intermediate hosts, presumably because they shifted their diet away from the intermediate host towards the more readily available resource (sunflower seeds). As predicted, prevalence of infection by the trophically transmitted parasite decreased in response to supplemental food treatment, but no such change in infection prevalence was detected for the two directly transmitted parasites in the system. The fact that food supplementation only had an impact on the transmission of the trophically transmitted parasite, and not the directly transmitted parasites, supports our hypothesis that host foraging ecology directly affects exposure to parasites that rely on the ingestion of intermediate hosts for transmission. We concluded that the relative availability of different food resources has important consequences for the transmission of parasites and, more specifically, parasites that are embedded in the food web. The broader implications of these findings for food web dynamics and disease ecology are discussed.     

Eating yourself sick: transmission of disease as a function of foraging ecology

Species interactions may profoundly influence disease outbreaks. However, disease ecology has only begun to integrate interactions between hosts and their food resources (foraging ecology) despite that hosts often encounter their parasites while feeding. A zooplankton–fungal system illustrated this central connection between foraging and transmission. Using experiments that varied food density for Daphnia hosts, density of fungal spores and body size of Daphnia , we produced mechanistic yet general models for disease transmission rate based on broadly applicable components of feeding biology. Best performing models could explain why prevalence of infection declined at high food density and rose sharply as host size increased (a pattern echoed in nature). In comparison, the classic mass-action model for transmission performed quite poorly. These foraging-based models should broadly apply to systems in which hosts encounter parasites while eating, and they will catalyse future integration of the roles of Daphnia as grazer and host.     

Advice of the rose: experimental coevolution of a trematode parasite and its snail host

Understanding host-parasite coevolution requires multigenerational studies in which changes in both parasite infectivity and host susceptibility are monitored. We conducted a coevolution experiment that examined six generations of interaction between a freshwater snail (Potamopyrgus antipodarum) and one of its common parasites (the sterilizing trematode, Microphallus sp.). In one treatment (recycled), the parasite was reintroduced into the same population of host snails. In the second treatment (lagged), the host snails received parasites from the recycled treatment, but the addition of these parasites did not begin until the second generation. Hence any parasite-mediated genetic changes of the host in the lagged treatment were expected to be one generation behind those in the recycled treatment. The lagged treatment thus allowed us to test for time lags in parasite adaptation, as predicted by the Red Queen model of host-parasite coevolution. Finally, in the third treatment (control), parasites were not added. The results showed that parasites from the recycled treatment were significantly more infective to snails from the lagged treatment than from the recycled treatment. In addition, the hosts from the recycled treatment diverged from the control hosts with regard to their susceptibility to parasites collected from the field. Taken together, the results are consistent with time lagged, frequency-dependent selection and rapid coevolution between hosts and parasites.     

EVOLUTIONARY PATTERNS OF ALTERED BEHAVIOR AND SUSCEPTIBILITY IN PARASITIZED HOSTS

Adaptation is the usual context for interpreting parasite-host interactions. For example, altered host behavior is often interpreted as a parasite adaptation, because in some cases it enhances parasite transmission. Resistance to parasites also has obvious adaptive value for hosts. However, it is difficult to evaluate the adaptive significance of host-parasite interactions without considering the historical context in which these traits have evolved and if they can be predicted by host (or parasite) phylogeny. We examined the influence of host phylogeny on patterns of altered behavior and resistance to parasitism in a cockroach-acanthocephalan system. A consensus cladogram for cockroach subfamilies was produced from the morphological data of McKittrick. We used this cladogram to predict patterns of altered host behavior in seven cockroach host species. Each species was experimentally infected with a single species of acanthocephalan, Moniliformis moniliformis, a parasite that is transmitted when cockroaches are eaten by rodent final hosts. Activity patterns, substrate choices, and responses to light were measured for control and infected animals. These data were recoded into a behavioral matrix of discrete characters. We determined the most parsimonious distribution of the behavioral characters on the tree obtained from McKittrick's data. We then measured the concordance between the behavioral data and the cockroach cladogram with the consistency index (CI). We compared the observed CI to the expected value based on a randomization of observed character states. For three different models of evolutionary character change, there was no evidence of strong concordance (significantly large CI) between altered host behavior and host relationships. Parsimony analysis of the interior nodes of the phylogenetic reconstruction suggested that unaltered behavior was the ancestral state for most host behaviors. We also compared host phylogeny to a data set on the susceptibility of 29 cockroach species to infection with M. moniliformis. At the species level, there was a significant concordance between susceptibility and host phylogeny. This pattern was consistent with the finding that susceptibility of species varied significantly among different subfamilies. However, at the subfamily level, susceptibility was not strongly concordant with phylogeny. We predict that, given enough time, resistance should be lost in subfamilies that are currently resistant to parasitism. In spite of the potential importance of phylogeny in the evolution of behavior and susceptibility, we found little evidence for phylogenetic effects in this system. We conclude that changes in the behavioral responses of hosts to parasites and, to a lesser extent, changes in susceptibility are more frequent than cockroach speciation events in different cockroach lineages. This finding strengthens the assertion that at least some of the altered behaviors are adaptive for host and/or parasite.     

Parasites, sex, and clonal diversity in natural snail populations

Under the Red Queen hypothesis, host-parasite coevolution selects against common host genotypes. Although this mechanism might underlie the persistence of sexual reproduction, it might also maintain high clonal diversity. Alternatively, clonal diversity might be maintained by multiple origins of parthenogens from conspecific sexuals, a feature in many animal groups. Herein, we addressed the maintenance of overall genetic diversity by coevolving parasites, as predicted by the Red Queen hypothesis. We specifically examined the contribution of parasites to host clonal diversity and the frequency of sexually reproducing individuals in natural stream populations of Potamopyrgus antipodarum snails. We also tested the alternative hypothesis that clonal diversity is maintained by the input of clones by mutation from sympatric sexuals. Clonal diversity and the frequency of sexual individuals were both positively related to infection frequency. Surprisingly, although clones are derived by mutation from sexual snails, parasites explained more of the genotypic variation among parthenogenetic subpopulations. Our findings thus highlight the importance of parasites as drivers of clonal diversity, as well as sex.     

Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites

Co-infecting parasite genotypes typically compete for host resources limiting their fitness. The intensity of such competition depends on whether parasites are reproducing in a host, or using it primarily as a transmission vehicle while not multiplying in host tissues (referred to as 'competition hypothesis'). Alternatively, simultaneous attack and co-infection by several parasite genotypes might facilitate parasite infection because such a diverse attack could present an additional challenge to host immune defence (referred to as 'facilitation hypothesis'). We tested the competition hypothesis by comparing the production of transmission stages (cercariae) from snails infected with one or two genotypes of the trematode Diplostomum pseudospathaceum. We found that cercarial production did not differ between the two groups of snails, suggesting lower per genotype production in double infections, and competition for host resources. Second, we tested the facilitation hypothesis by comparing parasite infection success on fishes (proportion of parasites establishing in the host) using cercariae originating from single-infected snails, double-infected snails and artificial mixtures of the single genotypes. In both cases, we found higher infection success when fishes were challenged with two parasite genotypes instead of one, supporting the facilitation hypothesis. Our results suggest that constraints defining the success of multiple genotype infections in parasites with multiple host life cycles include both between-genotype resource competition in the host and performance of host immune defences against a diverse parasite challenge.     

Effects of intermediate host genetic background on parasite transmission dynamics: a case study using Schistosoma mansoni

For parasites that require multiple hosts to complete their development, genetic interplay with one host may impact parasite transmission and establishment in subsequent hosts. In this study, we used microsatellite loci to address whether the genetic background of snail intermediate hosts influences life-history traits and transmission patterns of dioecious trematode parasites in their definitive hosts. We performed experimental Schistosoma mansoni infections utilizing two allopatric populations of Biomphalaria glabrata snails and assessed intensities and sex ratios of adult parasites in mouse definitive hosts. Our results suggest that the genetic background of hosts at one point in a parasite’s life cycle can influence the intensities and sex ratios of worms in subsequent hosts.     

Use of trade-off theory to advance understanding of herbivore–parasite interactions

• 1 Trade‐off theory has been extensively used to further our understanding of animal behaviour. In mammalian herbivores, it has been used to advance our understanding of their reproductive, parental care and foraging strategies. Here, we detail how trade‐off theory can be applied to herbivore–parasite interactions, especially in foraging environments.
• 2 Foraging is a common mode of uptake of parasites that represent the most pervasive challenge to mammalian fitness and survival. Hosts are hypothesized to alter their foraging behaviour in the presence of parasites in three ways: (i) hosts avoid foraging in areas that are contaminated with parasites; (ii) hosts select diets that increase their resistance and resilience to parasites; and (iii) hosts select for foods with direct anti‐parasitic properties (self‐medication). We concentrate on the mammalian herbivore literature to detail the recent advances made using trade‐off frameworks to understand the mechanisms behind host–parasite interactions in relation to these three hypotheses.
• 3 In natural systems, animals often face complex foraging decisions including nutrient intake vs. predation risk, nutrient intake vs. sheltering and nutrient intake vs. parasite risk trade‐offs. A trade‐off framework is detailed that can be used to interpret mammal behaviour in complex environments, and may be used to advance the self‐medication hypothesis.
• 4 The use of trade‐off theory has advanced our understanding of the contact process between grazing mammalian hosts and their parasites transmitted via the faecal–oral route. Experimental manipulation of the costs and benefits of a nutrient intake vs. parasite risk trade‐off has shown that environmental conditions (forage quality and quantity) and the physiological state (parasitic and immune status) of a mammalian host can both affect the behavioural decisions of foraging animals.
• 5 Naturally occurring trade‐offs and the potential to manipulate their costs and benefits enables us to identify the abilities and behavioural rules used by mammals when making decisions in complex environments and thus predict animal behaviour.

     

Impact of parasitic mite infection on a terrestrial snail

Summary

Although parasitic infections have been shown to be critical for growth, reproduction and survival of many vertebrates, little is known about the impact of parasites on invertebrate hosts and particular on molluscs. Therefore, it is of interest how parasites may affect their invertebrate hosts and how hosts can manage the detrimental effect of infections. In the present study, the naturally widespread parasitic mite Riccardoella limacum, which has been suggested to play an important role in the ecology of the land snail Arianta arbustorum, was artificially transferred to A. arbustorum. We experimentally examined the effect of the parasite on the food consumption, shell growth, and survival of its host. Surprisingly, we found minor impacts in some traits, i.e. we found that infected and uninfected snails similarly completed their shell growth, attained sexual maturity, and allocated equal energy into their albumen glands. However, infected snails consumed less and showed a significantly higher mortality after winter than uninfected snails.     

Interactions between the parasite's previous and current environment mediate the outcome of parasite infection

The study of parasite virulence has generally focused on the conditions under which virulence is expected to increase or decrease over time and how the interactions between hosts and their environments may mediate the outcome of infection. Recently, parasite traits such as transmission, offspring production, and development have also been shown to be influenced by environmental variation. What is unclear is how variation in the parasite's environment may impact virulence. Recent theory demonstrates that plasticity can promote the evolution of decreased virulence; thus, understanding whether the parasite's environment can mediate virulence can improve predictions regarding the outcome of parasite infection. Here, an obligate mosquito parasite was reared in hosts fed high or low levels of food. Parasite oocysts (offspring) produced in these two host environments were subsequently fed to uninfected hosts. Parasites originating from well-fed hosts were found to be more virulent to these subsequent hosts compared to parasites originating from poorly fed hosts. Additionally, this effect was apparent only when current hosts were food deprived. These results demonstrate that parasite virulence was mediated by a cross-generational effect of the environment and that the overall outcome of infection was modified by variation in both the parasite's and host's environments.     

Within-host competitive interactions as a mechanism for the maintenance of parasite diversity

Variation among parasite strains can affect the progression of disease or the effectiveness of treatment. What maintains parasite diversity? Here I argue that competition among parasites within the host is a major cause of variation among parasites. The competitive environment within the host can vary depending on the parasite genotypes present. For example, parasite strategies that target specific competitors, such as bacteriocins, are dependent on the presence and susceptibility of those competitors for success. Accordingly, which parasite traits are favoured by within-host selection can vary from host to host. Given the fluctuating fitness landscape across hosts, genotype by genotype (G×G) interactions among parasites should be prevalent. Moreover, selection should vary in a frequency-dependent manner, as attacking genotypes select for resistance and genotypes producing public goods select for cheaters. I review competitive coexistence theory with regard to parasites and highlight a few key examples where within-host competition promotes diversity. Finally, I discuss how within-host competition affects host health and our ability to successfully treat infectious diseases.     

Nest mate size, but not short-term need, influences begging behavior of a generalist brood parasite

Hosts of generalist brood parasites often vary with regardsto their life-history traits, and these differences have thepotential to influence the competitive environment experiencedby brood-parasitic nestlings. Although begging by brood parasitesis more exaggerated than their hosts, it is unclear if generalistbrood parasites modulate their begging behavior relative tohost size. I examined the begging behavior of brown-headed cowbird(Molothrus ater) nestlings when competing against nest matesthat differ in size and under different levels of short-termneed. Cowbird nestlings begged on nearly all feeding visits,responded to adults as fast as (or faster than) their nest mates,and typically begged more intensively than their nest mates.Latency to beg, time spent begging, and maximum begging postureof cowbirds were similar during supplementation and deprivationtreatments, indicating begging intensity was not influencedby short-term need. Time spent begging by cowbirds varied amonghosts of 3 different sizes when short-term need was standardized,suggesting that nest mate size strongly influenced begging behavior.Cowbirds obtained more food when competing against an intermediate-sizedhost due to lower provisioning rates of small hosts or becauseof increased competitive ability of large host nestlings. Overall,cowbirds obtained the greatest volume of food per unit timespent begging when competing against intermediate hosts, butthis value approached that of the small host when adjusted formodal brood size. These results demonstrate that cowbirds adjusttheir begging relative to the size of the hosts against whichthey compete but not to levels of short-term need.     

Genotypic vs. condition effects on parasite-driven rare advantage

Models and empirical studies of coevolution assume host resistance and parasite infectivity are genetically based. However, nongenetic physiological or environmental influences could alter host susceptibility even when the relationship is genetically based. In this experiment we examined the influence of host genotype, host condition at the time of infection (age and reproductive status), and their interaction on resistance of the freshwater snail Potamopyrgus antipodarum) to its dominant trematode parasite (Microphallus sp.). We used a laboratory infection experiment of a clonal snail population to determine the susceptibility of juveniles, brooding adult females, and nonbrooding adult females. We found a significant effect of both life-history state and clonal genotype on the prevalence of infection. However, the relative susceptibility of different clonal genotypes was not altered by condition; genotypes that were rare in the natural population were less infected than those that were common for each life-history state. These results suggest that although host condition affects susceptibility, it does not disrupt the specificity of the match between parasites and common clonal genotypes. Hence these findings support the Red Queen hypothesis for the maintenance of sex under genetically based host-parasite interactions.     

EFFECTS OF EPISTASIS ON INFECTIVITY RANGE DURING HOST‐PARASITE COEVOLUTION

Understanding how parasites adapt to changes in host resistance is crucial to evolutionary epidemiology. Experimental studies have demonstrated that parasites are more capable of adapting to gradual, rather than sudden changes in host phenotype, as the latter may require multiple mutations that are unlikely to arise simultaneously. A key, but as yet unexplored factor is precisely how interactions between mutations (epistasis) affect parasite evolution. Here, we investigate this phenomenon in the context of infectivity range, where parasites may experience selection to infect broader sets of genotypes. When epistasis is strongly positive, we find that parasites are unlikely to evolve broader infectivity ranges if hosts exhibit sudden, rather than gradual changes in phenotype, in close agreement with empirical observations. This is due to a low probability of fixing multiple mutations that individually confer no immediate advantage. When epistasis is weaker, parasites are more likely to evolve broader infectivity ranges if hosts make sudden changes in phenotype, which can be explained by a balance between mutation supply and selection. Thus, we demonstrate that both the rate of phenotypic change in hosts and the form of epistasis between mutations in parasites are crucial in shaping the evolution of infectivity range.     

Larval trematode infections and spatial distributions of snails

Abstract. The hypothesis that infecting trematodes influence the spatial distribution of the estuarine snail Ilyanassa obsoleta was tested. This work was conducted in the Savages Ditch habitat, Rehoboth Bay, DE, USA, which has an essentially flat, sandy-mud bottom bordered by saltmarsh shorelines and many infected snails. In 1996, two groups of snails were individually marked and released from one location after being screened for trematode infections. One group, transplanted from sites where snails tended not to be infected, consisted of snails that tested as uninfected. The other group consisted of snails native to Savages Ditch. Species of trematode carried by each snail was recorded. Marked snails were found and their positions were recorded until 2001. Snails were in five infection categories: (1) not infected, and infected with (2) Himasthla quissetensis , or (3) Lepocreadium setiferoides or (4) Zoogonus rubellus , or (5) with both H. quissetensis and Z. rubellus . The results show that the spatial distributions of snails depended on whether or not they were infected and, if infected, on which trematode species they carried. To complete life cycles, these parasites must accomplish transmission from the first (the snail) to the second intermediate hosts by short-lived, swimming cercariae. These data do not allow resolution of why snails distributed as they did, but sighting distributions of infected snails can be related to distributions of second hosts and it is proposed that parasites engender host snail distributions that improve chances of transmission.     

Parasites promote host gene flow in a metapopulation

Local adaptation is a powerful mechanism to maintain genetic diversity in subdivided populations. It counteracts the homogenizing effect of gene flow because immigrants have an inferior fitness in the new habitat. This picture may be reversed in host populations where parasites influence the success of immigrating hosts. Here we report two experiments testing whether parasite abundance and genetic background influences the success of host migration among pools in a Daphnia magna metapopulation. In 22 natural populations of D. magna, immigrant hosts were found to be on average more successful when the resident populations experienced high prevalences of a local microsporidian parasite. We then determined whether this success is due to parasitism per se, or the genetic background of the parasites. In a common garden competition experiment, we found that parasites reduced the fitness of their local hosts relatively more than the fitness of allopatric host genotypes. Our experiments are consistent with theoretical predictions based on coevolutionary host-parasite models in metapopulations. A direct consequence of the observed mechanism is an elevated effective migration rate for the host in the metapopulation.