Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala)

The relationship between the exposure of organisms to chemicals and subsequent alterations in various biochemical processes (commonly referred to as biomarkers) is of growing importance in environmental and ecotoxicological research. However, parasites which also affect the physiological homeostasis of their hosts, and thus may alter biomarker reactions, are usually ignored in environmental research. To address this deficit, we have used the host-parasite system Gammarus roeseli naturally infected with cystacanths of the acanthocephalan Polymorphus minutus to investigate whether infection of gammarids with parasites alters their heat shock protein response following exposure to palladium (Pd). After 24 days of metal exposure relative levels of heat shock protein hsp70 were analysed in the tissues of parasites and intermediate hosts. Simultaneously, the metal accumulation in gammarids and parasites was determined. As none of the infected gammarids showed hsp70 levels at the end of the Pd exposure (either exposed or not), infected and unparasitized G. roeseli were exposed to heat. Again, only uninfected gammarids showed a temperature-dependent increase in hsp70 levels. Interestingly, although the intermediate hosts showed no hsp70 response, exposure to Pd and heat results in increasing hsp70 in the parasites within in the haemocoel of G. roeseli. Heat experiments with isolated cystacanths also showed increasing hsp70 levels in P. minutus with temperature. Concerning uninfected G. roeseli, exposure to Pd and heat causes a hsp70 response. Pd concentrations were found to be higher in the larval parasites than in the gammarids. This result clearly contradicts previous results, as high metal accumulation was so far only described from adult acanthocephalans. Our findings provide experimental evidence that parasites alter the biomarker responses of their host and that the infection status of test animals is extremely important for ecotoxicological studies.     

Role of complex II in anaerobic respiration of the parasite mitochondria from Ascaris suum and Plasmodium falciparum.

Parasites have developed a variety of physiological functions necessary for existence within the specialized environment of the host. Regarding energy metabolism, which is an essential factor for survival, parasites adapt to low oxygen tension in host mammals using metabolic systems that are very different from that of the host. The majority of parasites do not use the oxygen available within the host, but employ systems other than oxidative phosphorylation for ATP synthesis. In addition, all parasites have a life cycle. In many cases, the parasite employs aerobic metabolism during their free-living stage outside the host. In such systems, parasite mitochondria play diverse roles. In particular, marked changes in the morphology and components of the mitochondria during the life cycle are very interesting elements of biological processes such as developmental control and environmental adaptation. Recent research has shown that the mitochondrial complex II plays an important role in the anaerobic energy metabolism of parasites inhabiting hosts, by acting as quinol-fumarate reductase.     

How parasitism and pollution affect the physiological homeostasis of aquatic hosts

Parasitism poses a serious threat to hosts under certain circumstances, while the well-being of organisms is also negatively affected by environmental pollution. Little information is available on the simultaneous effects of parasites and pollutants on the physiological homeostasis of organisms. The present paper demonstrates that parasites: (i) may influence the metabolism of pollutants in infected hosts, (ii) interact with pollution in synergistic or antagonistic ways, and (iii) may induce physiological reactions in hosts which were thought to be pollutant-induced. Experimental studies on the uptake and accumulation of metals by fish reveal that fish infected with acanthocephalans have lower metal levels than uninfected hosts; e.g. Pomphorhynchus laevis reduces lead levels in fish bile, thereby diminishing or impeding the hepatic intestinal cycling of lead, which may reduce the quantity of metals available for fish. Alterations in pollutant uptake and accumulation in different intermediate and final hosts due to parasites are thus very important in the field of ecotoxicology. In addition to such alterations, there is a close interaction between the effects of pollutants and parasites which seems to be mediated at least partly by the endocrine system, which itself is closely related to the immune system in fish. Laboratory studies on eels experimentally infected with the swimbladder nematode Anguillicola crassus reveal that toxic chemicals such as polychlorinated biphenyls produce immunosuppressive effects which facilitate parasite infection. Similarly, an increase in serum cortisol concentration in eels due to chemical exposure and infection is correlated with decreasing levels of anti-A. crassus antibodies. Furthermore, parasites are able to elicit physiological changes which are attributed to chemicals with endocrine disrupting activity, e.g. the cestode Ligula intestinalis is known to suppress gonad development in roach. The most thoroughly documented examples of endocrine disruption in wild fish are in roach, and it is conceivable that this disruption is not only due to chemical activity but also to parasites such as L. intestinalis or species of the phylum Microspora.     

Host manipulation by parasites: a multidimensional phenomenon

The diversity of ways in which parasites manipulate the phenotype of their hosts to increase their transmission has been well‐documented during the past decades. Parasites clearly have the potential to alter a broad range of phenotypic traits in their hosts, extending from behaviour and colour to morphology and physiology. While the vast majority of studies have concentrated on few, often only one, host characters, there is increasing evidence that manipulative parasites alter multiple characteristics of their host's phenotype. These alterations can occur simultaneously and/or successively through time, making parasitically modified organisms undoubtedly more complex than traditionally viewed. Here, we briefly review the multidimensionality of host manipulation by parasites, discuss its possible significance and evolution, and propose directions for further research. This view should prove to be an extremely useful approach, generating a series of testable hypotheses regarding the ecology of parasitized hosts, and leading to a better comprehension of complex host–parasite relationships.     

Pesticide exposure strongly enhances parasite virulence in an invertebrate host model

Parasites are a common and constant threat to organisms at all levels of phyla. The virulence of a parasite, defined as the impact on survival and reproduction of its host, depends on the specific host–parasite combination and can also be influenced by environmental conditions. Environmental pollution might be an additional factor influencing host–parasite interactions. We here aimed to test whether the combined stress of pollutant exposure and parasite challenge results in stronger impacts on host organisms than expected from the single stressors applied alone. We used the water flea Daphnia magna and two of its endoparasites, the bacterium Pasteuria ramosa and the microsporidium Flabelliforma magnivora, as invertebrate host–parasite models. For each parasite, we tested in a full‐factorial design for interactions between parasitism and pollution using the neurotoxic pesticide carbaryl as a model substance. Sublethal concentrations of the pesticide synergistically enhanced the virulence of both parasites by increasing host mortality. Furthermore, host castration induced by P. ramosa was accelerated by carbaryl exposure. These effects likely reflect decreased host resistance due to direct or indirect immunosuppressive activity of carbaryl. The present study provides experimental evidence that the in vivo development of infectious diseases can be influenced by a pesticide at environmentally realistic concentrations. This implies that host–parasite interactions and subsequently co‐evolution might be influenced by environmental pollution at toxicant concentrations being sublethal to parasite‐free hosts. Standard toxicity testing as employed in the current way of conducting ecological risk assessments for anthropogenic substances does not consider natural antagonists such as infectious diseases, and thereby likely underestimates the impact these substances may pose to natural populations in the environment.     

The cost of phage resistance in a plant pathogenic bacterium is context‐dependent

Parasites are ubiquitous features of living systems and many parasites severely reduce the fecundity or longevity of their hosts. This parasite‐imposed selection on host populations should strongly favor the evolution of host resistance, but hosts typically face a trade‐off between investment in reproductive fitness and investment in defense against parasites. The magnitude of such a trade‐off is likely to be context‐dependent, and accordingly costs that are key in shaping evolution in nature may not be easily observable in an artificial environment. We set out to assess the costs of phage resistance for a plant pathogenic bacterium in its natural plant host versus in a nutrient‐rich, artificial medium. We demonstrate that mutants of Pseudomonas syringae that have evolved resistance via a single mutational step pay a substantial cost for this resistance when grown on their tomato plant hosts, but do not realize any measurable growth rate costs in nutrient‐rich media. This work demonstrates that resistance to phage can significantly alter bacterial growth within plant hosts, and therefore that phage‐mediated selection in nature is likely to be an important component of bacterial pathogenicity.     

The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review

Parasites are attracting increasing interest from parasite ecologists as potential indicators of environmental quality due to the variety of ways in which they respond to anthropogenic pollution. In environmental impact studies certain organisms provide valuable information about the chemical state of their environment not through their presence or absence but instead through their ability to concentrate environmental toxins within their tissues. Free living invertebrates, notably bivalve molluscs, are commonly employed in this role as `sentinel organisms' to monitor the concentrations of bioavailable metals in aquatic ecosystems. Also certain parasites, particularly intestinal acanthocephalans of fish, can accumulate heavy metals to concentrations orders of magnitude higher than those in the host tissues or the environment. The comparison of metal accumulation capacities between acanthocephalans and established free living sentinel organisms revealed significantly higher concentrations of several elements in Acanthocephalus lucii (Müller) than in the Zebra mussel Dreissena polymorpha (Pallas) which is a commonly used bioindicating organism in Europe. In contrast to the high heavy metal concentrations recorded in adult acanthocephalans, the larval stages in their respective crustacean intermediate hosts show little tendency to accumulate metals. A number of experimental studies demonstrate a clear time dependent accumulation of lead for acanthocephalans in their final hosts. These investigations provide evidence that the extremely high metal concentrations in intestinal acanthocephalans of fish are not the result of a slow process of accumulation but instead a relatively rapid uptake to a steady-state level. Thus, metal concentrations in adult acanthocephalans respond rapidly to changes in environmental exposure of their hosts. The value of parasites for environmental monitoring will be discussed in detail in the present article.     

Punch in the gut: parasite tolerance of phytochemicals reflects host diet

Gut parasites of plant-eating insects are exposed to antimicrobial phytochemicals that can reduce infection. Trypanosomatid gut parasites infect insects of diverse nutritional ecologies as well as mammals and plants, raising the question of how host diet-associated phytochemicals shape parasite evolution and host specificity. To test the hypothesis that phytochemical tolerance of trypanosomatids reflects the chemical ecology of their hosts, we compared related parasites from honey bees and mosquitoes – hosts that differ in phytochemical consumption – and contrasted our results with previous studies on phylogenetically related, human-parasitic Leishmania. We identified one bacterial and 10 plant-derived substances with known antileishmanial activity that also inhibited honey bee parasites associated with colony collapse. Bee parasites exhibited greater tolerance of chrysin – a flavonoid found in nectar, pollen and plant resin-derived propolis. In contrast, mosquito parasites were more tolerant of cinnamic acid – a product of lignin decomposition present in woody debris-rich larval habitats. Parasites from both hosts tolerated many compounds that inhibit Leishmania, hinting at possible trade-offs between phytochemical tolerance and mammalian infection. Our results implicate the phytochemistry of host diets as a potential driver of insect–trypanosomatid associations and identify compounds that could be incorporated into colony diets or floral landscapes to ameliorate infection in bees.     

Environmental parasitology: stressor effects on aquatic parasites

Anthropogenic stressors are causing fundamental changes in aquatic habitats and to the organisms inhabiting these ecosystems. Yet, we are still far from understanding the diverse responses of parasites and their hosts to these environmental stressors and predicting how these stressors will affect host–parasite communities. Here, we provide an overview of the impacts of major stressors affecting aquatic ecosystems in the Anthropocene (habitat alteration, global warming, and pollution) and highlight their consequences for aquatic parasites at multiple levels of organisation, from the individual to the community level. We provide directions and ideas for future research to better understand responses to stressors in aquatic host–parasite systems.     

The dynamics of preferential host switching: Host phylogeny as a key predictor of parasite distribution*

Parasites often jump to and become established in a new host species. There is much evidence that the probability of such host shifts decreases with increasing phylogenetic distance between donor and recipient hosts, but the consequences of such preferential host switching remain little explored. We develop a computational model to investigate the dynamics of parasite host shifts in the presence of this phylogenetic distance effect. In this model, a clade of parasites evolves on an evolving clade of host species where parasites can cospeciate with their hosts, switch to new hosts, speciate within hosts or become extinct. Our model predicts that host phylogenies are major determinants of parasite distributions across trees. In particular, we predict that trees consisting of few large clades of host species and those with fast species turnover should harbor more parasites than trees with many small clades and those that diversify more slowly. Within trees, large clades are predicted to exhibit a higher fraction of infected species than small clades. We discuss our results in the light of recent cophylogenetic studies in a wide range of host–parasite systems.     

Pollution and parasitism in the aquatic environment

The studies of aquatic parasitology and of aquatic pollution effects both have experienced increasing interest during the recent fifteen years. Although considerable effort has been spent on studying the role of pollution as a cause or a trigger of anomalies, tumors and infectious diseases in aquatic organisms, the interactions between pollution and parasitism have been largely neglected by scientists.Pollution and other man-made alterations of the aquatic environment may affect a parasite community directly by acting on free-living parasite stages or on ectoparasites, or indirectly by acting on the intermediate or the definitive host population. Certain pollution conditions favour the propagation of parasites by excluding their natural predators, by reducing the resistance of their hosts or by providing improved living conditions for their intermediate hosts. In a number of experimental studies parasitized organisms have been shown to suffer from greater mortalities when exposed to high temperature, to low oxygen stress or to high levels of dissolved heavy metal salts, when compared to nonparasitized control animals. Unfortunately, field studies on synergistic effects of pollution and parasites on host populations are still scarce and seldom offer more than qualitative observations and theoretical evaluations.The complexity of the pollution-parasite-host system complicates the use of parasites as indicators of pollution effects. However, experience from aquaculture practice teaches that a number of (mostly ecto-) parasites are more susceptible to certain chemicals (used as parasiticides) and to artificial alterations of salinity, temperature or oxygen content of the water than their hosts. Accordingly, it is postulated that during future studies the composition of ectoparasitic faunas of aquatic organisms might turn out to become a useful and quickly reacting indicator for effects of certain pollution conditions, such as anthropogene oxygen deficiency, salt introduction from salines into freshwater ecosystems, and introduction of certain heavy metal salts.     

Evolutionary ecology of the interactions between aphids and their parasitoids

Many organisms, including entomopathogenous fungi, predators or parasites, use aphids as ressources. Parasites of aphids are mostly endoparasitoid insects, i.e. insects which lay eggs inside the body of an other insect which will die as a result of their development. In this article, we review the consequences of the numerous pecularities of aphid biology and ecology for their endoparasitoids, notably the Aphidiinae (Hymenoptera: Braconidae). We first examine the various mechanisms used by aphids for defence against these enemies. We then explore the strategies used by aphidiine parasitoids to exploit their aphid hosts. Finally, we consider the responses of both aphids and parasitoids to ecological constraints induced by seasonal cycles and to environmental variations linked to host plants and climate. The fundamental and applied interest of studying these organisms is discussed.     

Parasites: Small Players with Crucial Roles in the Ecological Theater

Effective management of our natural resources requires an understanding of ecosystem structure and function; effectively, an ecosystem-based approach to management. Parasites occur, albeit cryptically, in almost all ecosystems, yet they are usually neglected in studies on populations and communties of organisms. Parasites can have pronounced or subtle effects on hosts affecting host behavior, growth, fecundity, and mortality. Furthermore, parasites may regulate host population dynamics and influence community structure. Many parasites have complex life cycles and depend for transmission on the presence of a variety of invertebrate and vertebrate intermediate hosts. Often transmission involves predator–prey interactions. Thus, parasites reflect the hosts position in the food web and are indicative of changes in ecosystem structure and function. Parasites can provide information on population structure, evolutionary hypotheses, environmental stressors, trophic interactions, biodiversity, and climatic conditions. I use examples from diverse freshwater and marine systems to demonstrate that parasites should be incorporated into research and monitoring programs to maximize information gathered in ecosystem-based studies and resource management.Supplementary Tables 3, 4, 5, 6 and additional references for this article are available for viewing by subscribers only at     

Parasites and the regional distribution of bumblebee species

Parasites and regional processes may be important to structure local species assemblages In particular, it has been hypothesized that widely distributed and abundant species should harbour more parasite species which could give them a competitive advantage in local species assemblages Empirical evidence bearing on these points are scarce and mainly restricted to vertebrate hosts or plants The aim of this study was to provide data in insect hosts and to test whether the patterns in field populations conform with those correlates expected from the parasite-host distribution hypothesis We investigated species assemblages of bumblebees at 12 different sites in a mesoscale region with their parasites over two consecutive years Parasites included dipteran and hymenopteran parasitoids. nematodes, mites, and protozoa The mean number of parasite species per host species ranged from 1 to 8 To account for sampling effort, all data were corrected for sample size effects The number of parasite species per average host individual (parasite load) ranged from 0 09 to 0 75 In cross-species comparisons, the number of parasite species per host species was positively correlated with regional distribution, i e the number of sites a host species occupied m the region, and with the average local host abundance The same relationships were found for parasite load In addition, parasite load correlated positively with average colony size of the host species, but not with body size of the individuals Bumblebee species were bimodally distributed When separated into widely-distributed and locally-occurring species, common hosts harboured more parasite species than rare ones Moreover, workers of common species individually had higher parasite loads From these results, we conclude that some of the necessary preconditions for parasites being able to affect the distribution and occurrence of their hosts are met in bumblebees The findings support a general pattern that parasite loads correlate positively with local abundance and geographical distribution of their hosts, also on mesoscales usually considered in ecological studies     

Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes

The uptake and expression of extracellular DNA has been established as a mechanism for horizontal transfer of genes between bacterial species. Such transfer can support acquisition of advantageous elements, including determinants that affect the interactions between infectious organisms and their hosts. Here we show that erythrocyte-stage Plasmodium falciparum malaria parasites spontaneously take up DNA from the host cell cytoplasm into their nuclei. We have exploited this finding to produce levels of reporter expression in P.falciparum that are substantially improved over those obtained by electroporation protocols currently used to transfect malaria parasites. Parasites were transformed to a drug-resistant state when placed into cell culture with erythrocytes containing a plasmid encoding the human dihydrofolate reductase sequence. The findings reported here suggest that the malaria genome may be continually exposed to exogenous DNA from residual nuclear material in host erythrocytes.     

A meta‐analysis of ant social parasitism: host characteristics of different parasitism types and a test of Emery’s rule

Abstract 1. In ant social parasitism, the process by which parasite–host systems evolved and the types of invasion mechanisms parasites use are being debated. Emery’s rule, for example, states that social parasites are the closest relatives to their hosts. The present study uses previously published data to test whether Emery’s rule applies equally to all parasitism types (i.e. xenobiosis, temporary, dulosis, and inquilinism). In addition, this study also investigates other links between parasite–host relatedness and host biology, which has implications for understanding the invasion mechanisms used by certain parasites. 2. We find that xenobiotic parasites typically use distantly‐related host species that are of at least medium colony size. Temporary parasites often have multiple host species that are very closely related to the parasite and hosts with medium‐size colonies. Dulotic parasites frequently have multiple host species that are slightly less related and of any size. Lastly, inquiline parasites tend to have a single, very closely related, host species with medium‐size colonies. 3. Parasites tend to be more closely related to host species if they have a single host species or when the host has a large colony size. In contrast, parasites with multiple host species or hosts of small colony size tend to be less related to their hosts. 4. This study is the first to examine trends in ant social parasitism across all known parasite species. Our meta‐analysis shows that Emery’s rule applies to inquilinism and temporary parasitism, but not to dulosis and xenobiosis. Our results also suggest that both parasitism type and parasite–host relatedness predict the number of hosts and host colony size. It may be that a chemical mimicry mechanism allows invasion of large host colonies, but requires close relatedness of parasite and host, and concentration on a single host species.     

Pleiotropic action of parasites: How to be good for the host

Parasites reduce the reproductive output of their hosts, limit their growth, and sometimes even castrate or hill them. Under certain conditions however, a parasitized host may be better off than an uninfected one. Such 'nice' parasites have a 'pleiotropic' action on their hosts. Parasites can be pleiotropic either in space (in which case they have a beneficial effect on the host in one environment while being detrimental in another) or in time (the parasite is beneficial at one stage of the host's development and 'costly' at another stage). Such pleiotropic parasites may constitute the intermediate stage between parasitism and mutualism.     

Host range and local parasite adaptation

Parasites may be expected to become locally adapted to their hosts. However, while many empirical studies have demonstrated local parasite adaptation, others have failed to demonstrate it, or have shown local parasite maladaptation. Researchers have suggested that gene flow can swamp local parasite-host dynamics and produce local adaptation only at certain geographical scales; others have argued that evolutionary lags can account for both null and maladaptive results. In this paper, we use item response theory (IRT) to test whether host range influences the likelihood of parasites locally adapting to their hosts. We collated 32 independent experiments testing for local adaptation, where parasites could be assigned as having either broad or narrow host ranges (BHR and NHR, respectively). Twenty-five tests based on BHR parasites had a significantly lower average effect size than seven NHR tests, indicating that studies based on BHR parasites are less likely to demonstrate local parasite adaptation. We argue that this may relate to evolutionary lags during diffuse coevolution of BHR parasites with their hosts, rather than differences in experimental approaches or other confounds between BHR and NHR studies.     

The flexibility of Apicomplexa parasites in lipid metabolism

Apicomplexa are obligate intracellular parasites responsible for major human infectious diseases such as toxoplasmosis and malaria, which pose social and economic burdens around the world. To survive and propagate, these parasites need to acquire a significant number of essential biomolecules from their hosts. Among these biomolecules, lipids are a key metabolite required for parasite membrane biogenesis, signaling events, and energy storage. Parasites can either scavenge lipids from their host or synthesize them de novo in a relict plastid, the apicoplast. During their complex life cycle (sexual/asexual/dormant), Apicomplexa infect a large variety of cells and their metabolic flexibility allows them to adapt to different host environments such as low/high fat content or low/high sugar levels. In this review, we discuss the role of lipids in Apicomplexa parasites and summarize recent findings on the metabolic mechanisms in host nutrient adaptation.     

IMMUNE EVASION AND THE EVOLUTION OF MOLECULAR MIMICRY IN PARASITES

Parasites that are molecular mimics express proteins which resemble host proteins. This resemblance facilitates immune evasion because the immune molecules with the specificity to react with the parasite also cross‐react with the host's own proteins, and these lymphocytes are rare. Given this advantage, why are not most parasites molecular mimics? Here we explore potential factors that can select against molecular mimicry in parasites and thereby limit its occurrence. We consider two hypotheses: (1) molecular mimics are more likely to induce autoimmunity in their hosts, and hosts with autoimmunity generate fewer new infections (the “costly autoimmunity hypothesis”); and (2) molecular mimicry compromises protein functioning, lowering the within‐host replication rate and leading to fewer new infections (the “mimicry trade‐off hypothesis”). Our analysis shows that although both hypotheses may select against molecular mimicry in parasites, unique hallmarks of protein expression identify whether selection is due to the costly autoimmunity hypothesis or the mimicry trade‐off hypothesis. We show that understanding the relevant selective forces is necessary to predict how different medical interventions will affect the proportion of hosts that experience the different infection types, and that if parasite evolution is ignored, interventions aimed at reducing infection‐induced autoimmunity may ultimately fail.