Parasite regulation by host hormones: an old mechanism of host exploitation?

Recent experimental evidence suggests that parasites can not only evade immune responses actively but also exploit the hormonal microenvironment within the host to favor their establishment, growth and reproduction. The benefit for parasites of hormonal exploitation is so great that they have evolved structures similar to the steroid and protein hormone receptors expressed in upper vertebrates that can bind to the hormonal metabolites synthesized by the host. This strategy is exemplified by two parasites that respond to adrenal steroids and sexual steroids, respectively: Schistosoma mansoni and Taenia crassiceps. Understanding how the host endocrine system can, under certain circumstances, favor the establishment of a parasite, and characterizing the parasite hormone receptors that are involved might aid the design of hormonal analogs and drugs that affect the parasite exclusively.     

The effect of host mycorrhizal status on host plant–parasitic plant interactions

Two pot experiments were conducted to examine three-level interactions between host plants, mycorrhizal fungi and parasitic plants. In a greenhouse experiment, Poa annua plants were grown in the presence or absence of an AM fungus (either Glomus lamellosum V43a or G. mosseae BEG29) and in the presence or absence of a root hemiparasitic plant (Odontites vulgaris). In a laboratory experiment, mycorrhizal infection (Glomus claroideum BEG31) of Trifolium pratense host plants (mycorrhizal versus non-mycorrhizal) was combined with hemiparasite infection (Rhinanthus serotinus) of the host (parasitized versus non-parasitized). Infection with the two species of Glomus had no significant effect on the growth of P. annua, while hemiparasite infection caused a significant reduction in host biomass. Mycorrhizal status of P. annua hosts (i.e. presence/absence of AM fungus) affected neither the biomass nor the number of flowers produced by the attached O. vulgaris plants. Infection with G. claroideum BEG31 greatly increased the biomass of T. pratense, but hemiparasite infection had no effect. The hemiparasitic R. serotinus plants attached to mycorrhizal hosts had higher biomass and produced more flowers than plants growing with non-mycorrhizal hosts. Roots of T. pratense were colonized by the AM fungus to an extent independent of the presence or absence of the hemiparasite. Our results confirm earlier findings that the mycorrhizal status of a host plant can affect the performance of an attached root hemiparasite. However, improvement of the performance of the parasitic plant following attachment to a mycorrhizal host depends on the extent to which the AM fungi is able to enhance the growth of the host. Accepted: 23 February 2001     

Does the host matter? Variable influence of host traits on parasitism rates

Parasitism of mammals is ubiquitous, but the processes driving parasite aggregation on hosts are poorly understood, as each system seems to show unique correlations between parasitism and host traits such as sex, age, size and body mass. Genetic diversity is also posited to influence susceptibility to parasitism, and provides a quantifiable measure of an intrinsic unchanging host property, but this link has not been well established. A lack of consistency in host traits predicting parasite heterogeneity may derive from the contribution of environmental factors to parasite aggregation. To evaluate this question, a large dataset was leveraged to explore the relationship between unchanging, intrinsic host traits (heterozygosity and sex), variable host traits (age, length and body mass), and extrinsic factors (sampling date/year and population) and flea presence/absence, abundance and intensity on two species of social burrowing mammal, the black-tailed prairie dog (Cynomys ludovicianus) and the Gunnison’s prairie dog (Cynomys gunnisoni). Prairie dogs experience frequent parasitism by fleas, but the distribution of fleas among individuals is highly skewed. In these systems, intrinsic host traits were nuanced in how they predicted flea aggregation on individual prairie dogs, with sex unimportant to parasitism rates and heterozygosity increasing the probability of infection and influencing the number of fleas in divergent ways. Variable host traits interacted with each other and with environmental or geographic stochasticity to influence flea aggregation. Length and age tended to increase parasitism, whereas the effects of body mass and condition were mediated by date and other host traits to produce both positive and negative effects on parasitism. This finding suggests that the factors affecting ectoparasite infection on individuals are complex, even within species. Importantly, there was no correlation between the number of fleas on an individual in one year and the number of fleas on the same individual the next year, supporting the idea that flea aggregation is not driven by unchanging, intrinsic characteristics of the host. Rather, these findings indicate that host traits influence parasitism in nuanced ways, including interactions with environmental characteristics and stochastic factors.     

The Iron age of host–microbe interactions

Microbes exert a major impact on human health and disease by either promoting or disrupting homeostasis, in the latter instance leading to the development of infectious diseases. Such disparate outcomes are driven by the ever-evolving genetic diversity of microbes and the countervailing host responses that minimize their pathogenic impact. Host defense strategies that limit microbial pathogenicity include resistance mechanisms that exert a negative impact on microbes, and disease tolerance mechanisms that sustain host homeostasis without interfering directly with microbes. While genetically distinct, these host defense strategies are functionally integrated, via mechanisms that remain incompletely defined. Here, we explore the general principles via which host adaptive responses regulating iron (Fe) metabolism impact on resistance and disease tolerance to infection.     

Do distances among host patches and host density affect the distribution of a specialist parasitoid?

The effect of spatial habitat structure and patchiness may differ among species within a multi-trophic system. Theoretical models predict that species at higher trophic levels are more negatively affected by fragmentation than are their hosts or preys. The absence or presence of the higher trophic level, in turn, can affect the population dynamics of lower levels and even the stability of the trophic system as a whole. The present study examines different effects of spatial habitat structure with two field experiments, using as model system the parasitoid Cotesia popularis which is a specialist larval parasitoid of the herbivore Tyria jacobaeae. One experiment examines the colonisation rate of the parasitoid and the percentage parasitism at distances occurring on a natural scale; the other experiment examines the dispersal rate and the percentage parasitism in relation to the density of the herbivore and its host plant. C. popularis was able to reach artificial host populations at distances up to the largest distance created (at least 80 m from the nearest source population). Also, the percentage parasitism did not differ among the distances. The density experiment showed that the total number of herbivores parasitised was higher in patches with a high density of hosts, regardless of the density of the host plant. The percentage parasitism, however, was not related to the density of the host. The density of the host plant did have a (marginally) significant effect on the percentage parasitism, probably indicating that the parasitoid uses the host plant of the herbivore as a cue to find the herbivore itself. In conclusion, the parasitoid was not affected by the spatial habitat structure on spatial scales that are typical of local patches.     

Evolution of carbohydrate antigens--microbial forces shaping host glycomes?

Many glycans show remarkably discontinuous distribution across evolutionary lineages. These differences play major roles when organisms belonging to different lineages interact as host-pathogen or host-symbiont. Certain lineage-specific glycans have become important signals for multicellular host organisms, which use them as molecular signatures of their pathogens and symbionts through recognition by a toolkit of innate defense molecules. In turn, pathogens have evolved to exploit host lineage-specific glycans and are constantly shaping the glycomes of their hosts. These interactions take place in the face of numerous critical endogenous functions played by glycans within host organisms. Whether due to simple evolutionary divergence or adaptive changes under natural selection resulting from endogenous functional requirements, once different lineages elaborate on differential glycomes these mutual differences provide opportunities for host exploitation and/or pathogen defense between lineages. Such phylogenetic molecular recognition mechanisms will augment and likely contribute to the maintenance of lineage-specific differences in glycan repertoires.     

Coevolution of dispersal in a parasitoid–host system

Interspecific interactions and the evolution of dispersal are both of interest when considering the potential impact of habitat fragmentation on community ecology, but the interaction between these processes is not well studied. We address this by considering the coevolution of dispersal strategies in a host–parasitoid system. An individual-based host–parasitoid metapopulation model was constructed for a patchy environment, allowing for evolution in dispersal rates of both species. Highly rarefied environments with few suitable patches selected against dispersal in both species, as did relatively static environments. Provided that parasitoids persist, all the variables studied led to stable equilibria in dispersal rates for both species. There was a tendency toward higher dispersal rates in parasitoids because of the asymmetric relationships of the two species to the patches: vacant patches are most valuable for hosts, but unsuitable for parasitoids, which require an established host population to reproduce. High host dispersal rate was favoured by high host population growth rate, and in the parasitoid by high growth rates in both species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Community-wide patterns of parasitism of a host “generalist” brood-parasitic cowbird

The brown-headed cowbird (Molothrusater) is a generalist obligate brood parasite. Despite intensive study and growing concern over the negative impact of cowbird parasitism on populations of many hosts, very little is known about the factors influencing community-wide patterns of cowbird parasitism. Using systematic nest searches, nest parasitism was studied over two breeding seasons at a study site in northeastern Illinois encompassing grassland, forest-edge, and forest habitat, supporting a diverse avian community. Parasitism was observed for 18 out of 34 altricial bird species found nesting at the study site. A total of 299 cowbird eggs and nestlings were found in 191 of a total of 593 nests. Analyses revealed several ecological and behavioral factors associated with frequency of parasitism and the resulting distribution of cowbird eggs. Much higher frequencies of parasitism were found in edge and forest habitats than in grassland. Within the edge habitat, open nests were parasitized significantly more often than cavity nests. Among open nests in the edge habitat, the two largest species were never parasitized. Host behavior, particularly egg-ejection behavior, was associated with a reduced observed frequency of parasitism, but at least three species known to eject cowbird eggs were sometimes parasitized. For six common hosts capable of rearing cowbirds, we found no correlation between level of parasitism and host nest-survivorship, suggesting that fine-grained assessments of host quality by female cowbirds do not influence patterns of parasitism among acceptable host species, or that differences in host quality are not great and/or predictable enough for such fine-grained assessments. Our results suggest that when a variety of possible nests are available, the level of parasitism on a particular species is a balance between a␣cowbird's preference for a particular species and the effectiveness of host species' defenses. A conceptual model was developed that incorporates the observed correlation of cowbird eggs or nestlings with habitat, nest-type, host species' body mass, and host behavioral defenses. Additional community-wide studies of cowbird parasitism will test if this model is applicable to other avian communities. Received: 20 December 1996 / Accepted: 17 May 1997     

Success of ectoparasites: how important is timing of host contact?

Hosts often differ in their degree of parasitism and their expression of resistance. Yet very little is known about how the availability (and allocation) of resources to parasites at pre-infective stages influences their success in initiating parasitism, or in inducing and succumbing to resistance from hosts. We studied a damselfly-mite association to address how experimental variation in the age of first contact with hosts (timing) influenced subsequent parasite fitness. We demonstrate that timing influenced the ability of larval mites to make the transition to parasitism, but was not associated with measures of physiological resistance by hosts. Timing presumably relates to the availability of resources remaining for individuals to exploit their hosts. More research is needed on the importance of such factors, from variation in host resistance and parasite success and, ultimately, to the numbers and distributions of parasites on hosts.     

Dermatophyte–host relationship of a murine model of experimental invasive dermatophytosis

Recognizing the invasive potential of the dermatophytes and understanding the mechanisms involved in this process will help with disease diagnosis and with developing an appropriate treatment plan. In this report, we present the histopathological, microbiological and immunological features of a model of invasive dermatophytosis that is induced by subcutaneous infection of Trichophyton mentagrophytes in healthy adult Swiss mice. Using this model, we observed that the fungus rapidly spreads to the popliteal lymph nodes, spleen, liver and kidneys. Similar to the human disease, the lymph nodes were the most severely affected sites. The fungal infection evoked acute inflammation followed by a granulomatous reaction in the mice, which is similar to what is observed in patients. The mice were able to mount a Th1-polarized immune response and displayed IL-10-mediated immune regulation. We believe that the model described here will provide valuable information regarding the dermatophyte–host relationship and will yield new perspective for a better understanding of the immunological and pathological aspects of invasive dermatophytosis.     

Comparative proteome profiling of host–pathogen interactions: insights into the adaptation mechanisms of Francisella tularensis in the host cell environment

The intracellular pathogens have the unique capacity to sense the host cell environment and to respond to it by alteration in gene expression and protein synthesis. Proteomic analysis of bacteria exposed directly to the host cell milieu might thus greatly contribute to the elucidation of processes leading to bacterial adaptation and proliferation inside the host cell. Here we have performed a global proteome analysis of a virulent Francisella tularensis subsp. holarctica strain during its intracellular cycle within the macrophage-like murine cell line J774.2 using the metabolic pulse-labeling of bacterial proteins with ³⁵S-methionine and ³⁵S-cysteine in various periods of infection. The two-dimensional gel analysis revealed macrophage-induced bacterial proteome changes in which 64 identified proteins were differentially expressed in comparison to controls grown in tissue culture medium. Nevertheless, activation of macrophages with interferon gamma before in vitro infection decreased the number of detected alterations in protein levels. Thus, these proteomic data indicate the F. tularensis ability to adapt to the intracellular hostile environment that is, however, diminished by prior interferon gamma treatment of host cells.     

Diversification of host use in two polyphagous butterflies: differences in oviposition specificity or host rank hierarchy?

Novel host usage may represent an initial step towards diversification or radiation onto novel hosts within an evolutionary lineage, particularly if a shift in host plant preference ranking takes place. Polyphagous stages of evolutionary lineages may represent transitional states in which novel host associations are more likely to develop, but may be more difficult to detect experimentally. The polyphagous sister species Papilio glaucus L. and Papilio canadensis (Lepidoptera: Papilionidae; these Papilio = Pterourus) are known to exhibit differences in host‐plant use, despite significant overlap in host‐use abilities, providing an opportunity to examine how host shifts in polyphagous species may occur and what the implications for future divergence may be. In particular, we were interested in (i) determining whether differences in oviposition behavior of these species were due to changes in specificity or shifts in host‐plant hierarchy, (ii) whether the varying preference for primary hosts also affected the preference for secondary hosts, and (iii) what the oviposition preferences of a new hybrid swarm population are. We examined more than 40 000 oviposition bouts from more than 400 P. glaucus, P. canadensis, and hybrid females placed in seven‐, three‐, or two‐choice assays. In each of the choice assays, leaves from plants in different plant families of varying suitability for P. glaucus and P. canadensis larvae were used. We found the primary difference between P. glaucus and P. canadensis to be limited to a Z‐linked shift in host rank hierarchy due to an acceptance of Populus tremuloides Michx. (Salicaceae) and reduced specificity for Liriodendron tulipifera L. (Magnoliaceae) in P. canadensis. In addition, we found the absence of the Z‐linked oviposition acceptance of P. tremuloides in a recently formed allochronically separated hybrid swarm population found in P. canadensis territory at the northern border of the P. glaucus and P. canadensis hybrid zone.     

A host–microparasite model with a resistant host

The theory of heterozygote advantage is often used to explain the genetic variation found in natural populations. If a large population randomly mates and the various genotypes have the same growth and death rates, the evolution of the genotypes follows Hardy–Weinberg proportions and polymorphism results. When other environmental stresses, like predators, prey and diseases, are present, polymorphism may or may not occur depending on how the various genotypes are affected by the stress. In this paper, we use a basic host–microparasite model to demonstrate that polymorphism can occur even if one genotype suffers a higher death rate than the others in the absence of the parasite if the heterozygote has resistance or immunity to the parasite.     

Comparative mapping of host–pathogen protein–protein interactions

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Endosymbiosis of Chlorella species to the ciliate Paramecium bursaria alters the distribution of the host’s trichocysts beneath the host cell cortex

Each symbiotic Chlorella of the ciliate Paramecium bursaria is enclosed in a perialgal vacuole membrane derived from the host digestive vacuole membrane. Alga-free paramecia and symbiotic algae can grow independently. Mixing them experimentally can cause reinfection. Earlier, we reported that the symbiotic algae appear to push the host trichocysts aside to become fixed beneath the host cell cortex during the algal reinfection process. Indirect immunofluorescence microscopy with a monoclonal antibody against the trichocysts demonstrates that the trichocysts change their locality to form algal attachment sites and decrease their density beneath the host cell cortex through algal reinfection. Transmission electron microscopy to detect acid phosphatase activity showed that some trichocysts near the host cell cortex are digested by the host lysosomal fusion during algal reinfection. Removal of algae from the host cell using cycloheximide recovers the trichocyst's arrangement and number near the host cell cortex. These results indicate that symbiotic algae compete for their attachment sites with preexisting trichocysts and that the algae have the ability to ensure algal attachment sites beneath the host cell cortex.