Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Enhanced transmission of drug-resistant parasites to mosquitoes following drug treatment in rodent malaria

The evolution of drug resistant Plasmodium parasites is a major challenge to effective malaria control. In theory, competitive interactions between sensitive parasites and resistant parasites within infections are a major determinant of the rate at which parasite evolution undermines drug efficacy. Competitive suppression of resistant parasites in untreated hosts slows the spread of resistance; competitive release following treatment enhances it. Here we report that for the murine model Plasmodium chabaudi, co-infection with drug-sensitive parasites can prevent the transmission of initially rare resistant parasites to mosquitoes. Removal of drug-sensitive parasites following chemotherapy enabled resistant parasites to transmit to mosquitoes as successfully as sensitive parasites in the absence of treatment. We also show that the genetic composition of gametocyte populations in host venous blood accurately reflects the genetic composition of gametocytes taken up by mosquitoes. Our data demonstrate that, at least for this mouse model, aggressive chemotherapy leads to very effective transmission of highly resistant parasites that are present in an infection, the very parasites which undermine the long term efficacy of front-line drugs.     

Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna

Knowledge of the processes favouring the establishment of exotic parasites is poor. Herein, we test the characteristics of successful exotic parasites that have co-established in the remote island archipelago of New Zealand, due to the introduction of numerous avian host species. Our results show that avian malaria parasites (AM; parasites of the genus Plasmodium) that successfully invaded are more globally generalist (both geographically widespread and with a broad taxonomic range of hosts) than AM parasites not co-introduced to New Zealand. Furthermore, the successful AM parasites are presently more prevalent in their native range than AM parasites found in the same native range but not co-introduced to New Zealand. This has resulted in an increased number and greater taxonomic diversity of AM parasites now in New Zealand.     

PHYLOGENETIC RELATIONSHIPS AMONG PAPER WASP SOCIAL PARASITES AND THEIR HOSTS (HYMENOPTERA: VESPIDAE; POLISTINAE)

Abstract— Cladistic analyses of data from allozyme polymorphisms in paper wasp social parasites and their hosts do not support the hypothesis that social parasites are most closely related to their hosts. Electrophoretic data are adduced for nine species of Polistes , including all three known species of social parasites ( Sulcopolistes ) and their hosts. Three different coding methods are investigated; in no case do the social parasites cluster most closely with their hosts. Rather, there is limited evidence that they form a monophyletic group. However, formal taxonomic recognition of Sulcopolistes is not justified, as it renders Polistes sensu stricto paraphyletic. Although the social parasites are not most closely related to their hosts, hosts and parasites belong in the same subgenus and share many characteristics that may have facilitated the exploitation and deception practised by the parasites on the hosts.     

The Immune Response of Hemocytes of the Insect Oncopeltus fasciatus against the Flagellate Phytomonas serpens

The genus Phytomonas includes parasites that are etiological agents of important plant diseases, especially in Central and South America. These parasites are transmitted to plants via the bite of an infected phytophagous hemipteran. Despite the economic impact of these parasites, many basic questions regarding the genus Phytomonas remain unanswered, such as the mechanism by which the parasites cope with the immune response of the insect vector. In this report, using a model of systemic infection, we describe the function of Oncopeltus fasciatus hemocytes in the immune response towards the tomato parasite Phytomonas serpens. Hemocytes respond to infection by trapping parasites in nodular structures and phagocytizing the parasites. In electron microscopy of hemocytes, parasites were located inside vacuoles, which appear fused with lysosomes. The parasites reached the O. fasciatus salivary glands at least six hours post-infection. After 72 hours post-infection, many parasites were attached to the salivary gland outer surface. Thus, the cellular responses did not kill all the parasites.     

Virulence, drug sensitivity and transmission success in the rodent malaria, Plasmodium chabaudi

Here, we test the hypothesis that virulent malaria parasites are less susceptible to drug treatment than less virulent parasites. If true, drug treatment might promote the evolution of more virulent parasites (defined here as those doing more harm to hosts). Drug-resistance mechanisms that protect parasites through interactions with drug molecules at the sub-cellular level are well known. However, parasite phenotypes associated with virulence might also help parasites survive in the presence of drugs. For example, rapidly replicating parasites might be better able to recover in the host if drug treatment fails to eliminate parasites. We quantified the effects of drug treatment on the in-host survival and between-host transmission of rodent malaria (Plasmodium chabaudi) parasites which differed in virulence and had never been previously exposed to drugs. In all our treatment regimens and in single- and mixed-genotype infections, virulent parasites were less sensitive to pyrimethamine and artemisinin, the two antimalarial drugs we tested. Virulent parasites also achieved disproportionately greater transmission when exposed to pyrimethamine. Overall, our data suggest that drug treatment can select for more virulent parasites. Drugs targeting transmission stages (such as artemisinin) may minimize the evolutionary advantage of virulence in drug-treated infections.     

Trematode parasites infect or die in snail hosts

The Red Queen hypothesis is based on the assumption that parasites must genetically match their hosts to infect them successfully. If the parasites fail, they are assumed to be killed by the host's immune system. Here, we tested this using sympatric (mostly susceptible) and allopatric (mostly resistant) populations of a freshwater snail and its trematode parasite. We determined whether parasites which do not infect are either killed or passed through the host's digestive tract and remain infectious. Our results show that parasites do not get a second chance: they either infect or are killed by the host. The results suggest strong selection against parasites that are not adapted to local host genotypes.     

Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite

Biologists commonly assume that parasites are locally adapted since they have shorter generation times and higher fecundity than their hosts, and therefore evolve faster in the arms race against the host's defences. As a result, parasites should be better able to infect hosts within their local population than hosts from other allopatric populations. However, recent mathematical modelling has demonstrated that when hosts have higher migration rates than parasites, hosts may diversify their genes faster than parasites and thus parasites may become locally maladapted. This new model was tested on the Canarian endemic lizard and its blood parasite (haemogregarine genus). In this host–parasite system, hosts migrate more than parasites since lizard offspring typically disperse from their natal site soon after hatching and without any contact with their parents who are potential carriers of the intermediate vector of the blood parasite (a mite). Results of cross-infection among three lizard populations showed that parasites were better at infecting individuals from allopatric populations than individuals from their sympatric population. This suggests that, in this host–parasite system, the parasites are locally maladapted to their host.     

Coevolution of recovery ability and virulence.

Most models for coevolution of hosts and parasites are based on the assumption that resistance of hosts to parasites is an all-or-nothing effect. In many cases, for example where parasites require an appropriate receptor on host cells, this is a reasonable assumption. However, in many other cases, for example where hosts mount an immune response, this picture may be too simple. An immune system is expensive to maintain, which poses a question as to how much of its resources a host should allocate to resist parasites: if the risk of infection is low, natural selection may favour hosts with less effective immune systems. As optimal allocation to defence will depend on the force of infection, and the force of infection, in turn, depends on the level of defence in the rest of the host population, a game-theoretic approach is necessary. Here I analyse a simple model for the evolution of the ability to recover from infection. If parasites are not allowed to coevolve, the outcome is a single evolutionarily stable strategy (ESS). If the parasites coevolve, multiple evolutionary outcomes are possible, one in which the parasites are relatively avirulent and common and the hosts invest little in recovery ability, and another (the escalated arms race) where parasites are rare but virulent and the hosts invest heavily in defence.     

Exploiting structural biology in the fight against parasitic diseases

Despite spectacular advances in structural biology over the past half-century, only approximately 2% of the structures in the Protein Data Bank are from eukaryotic parasites and less than 0.5% are from multicellular parasites. Even when only major human pathogens are considered, 3D structures of parasites are vastly underrepresented. Yet approximately one-third of the global burden of human disease comes from parasites. It is time to divert greater effort and resources in structural biology to benefit the fight against parasitic diseases. Using as leverage recent technological and methodological advances, a concerted effort to determine macromolecular structures from parasite pathogens would provide invaluable mechanistic insights on vital processes of the parasites and would suggest novel strategies for inhibiting infection.     

Tolerance is the key to understanding antimalarial drug resistance

The evolution of antimalarial drug resistance is often considered to be a single-stage process in which parasites are either fully resistant or completely sensitive to a drug. However, this does not take into account the important intermediate stage of drug tolerance. Drug-tolerant parasites are killed by the high serum concentrations of drugs that occur during direct treatment of the human host. However, these parasites can spread in the human population because many drugs persist long after treatment, and the tolerant parasites can infect people in which there are residual levels of the drugs. This intermediate stage between fully sensitive and fully resistant parasites has far-reaching implications for the evolution of drug-resistant malaria.     

Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove

DNA-sequence analyses of avian haemosporidian parasites, primarily of passerine birds, have described the phylogenetic relationships of major groups of these parasites, which are in general agreement with morphological taxonomy. However, less attention has been paid to haemosporidian parasites of non-passerine birds despite morphological and DNA-sequence evidence for unique clades of parasites in these birds. Detection of haemosporidian parasites in the Galapagos archipelago has raised conservation concerns and prompted us to characterise the origins and diversity of these parasites in the Galapagos dove (Zenaida galapagoensis). We used partial mitochondrial cytochrome b (cyt b) and apicoplast caseinolytic protease C (ClpC) genes to develop a phylogenetic hypothesis of relationships of haemosporidian parasites infecting New World Columbiformes, paying special attention to those parasites infecting the endemic Galapagos dove. We identified a well-supported and diverse monophyletic clade of haemosporidian parasites unique to Columbiformes, which belong to the sub-genus Haemoproteus (Haemoproteus). This is a sister clade to all the Haemoproteus (Parahaemoproteus) and Plasmodium parasites so far identified from birds as well as the Plasmodium parasites of mammals and reptiles. Our data suggest that the diverse Haemoproteus parasites observed in Galapagos doves are not endemic to the archipelago and likely represent multiple recent introductions.     

Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?

Parasites are common in many ecosystems, yet because of their nature, they do not fossilise readily and are very rare in the geological record. This makes it challenging to study the evolutionary transition that led to the evolution of parasitism in different taxa. Most studies on the evolution of parasites are based on phylogenies of extant species that were constructed based on morphological and molecular data, but they give us an incomplete picture and offer little information on many important details of parasite–host interactions. The lack of fossil parasites also means we know very little about the roles that parasites played in ecosystems of the past even though it is known that parasites have significant influences on many ecosystems. The goal of this review is to bring attention to known fossils of parasites and parasitism, and provide a conceptual framework for how research on fossil parasites can develop in the future. Despite their rarity, there are some fossil parasites which have been described from different geological eras. These fossils include the free‐living stage of parasites, parasites which became fossilised with their hosts, parasite eggs and propagules in coprolites, and traces of pathology inflicted by parasites on the host's body. Judging from the fossil record, while there were some parasite–host relationships which no longer exist in the present day, many parasite taxa which are known from the fossil record seem to have remained relatively unchanged in their general morphology and their patterns of host association over tens or even hundreds of millions of years. It also appears that major evolutionary and ecological transitions throughout the history of life on Earth coincided with the appearance of certain parasite taxa, as the appearance of new host groups also provided new niches for potential parasites. As such, fossil parasites can provide additional data regarding the ecology of their extinct hosts, since many parasites have specific life cycles and transmission modes which reflect certain aspects of the host's ecology. The study of fossil parasites can be conducted using existing techniques in palaeontology and palaeoecology, and microscopic examination of potential material such as coprolites may uncover more fossil evidence of parasitism. However, I also urge caution when interpreting fossils as examples of parasites or parasitism‐induced traces. I point out a number of cases where parasitism has been spuriously attributed to some fossil specimens which, upon re‐examination, display traits which are just as (if not more) likely to be found in free‐living taxa. The study of parasite fossils can provide a more complete picture of the ecosystems and evolution of life throughout Earth's history.     

The occurrence of strongylid nematodes in the epididymides of wood mice

The recent discovery of a larval nematode in the epididymides of free-living wood mice (Apodemus sylvaticus) suggests a sexual transmission of these parasites. They have been placed within the bursate nematodes (order Strongylida) through 18S rDNA analysis, suggesting that they are undetermined metastrongyloid nematodes. The possibility that these parasites are transmitted sexually opens an intriguing field of research because sexually transmitted metazoan parasites are known to occur mainly in invertebrates, whereas in vertebrates sexually transmitted parasites are usually microparasites such as viruses, bacteria and protozoa.     

P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions

The ookinete surface proteins (P25 and P28) are proven antimalarial transmission-blocking vaccine targets, yet their biological functions are unknown. By using single (Sko) and double gene knock-out (Dko) Plasmodium berghei parasites, we show that P25 and P28 share multiple functions during ookinete/oocyst development. In the midgut of mosquitoes, the formation of ookinetes lacking both proteins (Dko parasites) is significantly inhibited due to decreased protection against lethal factors, including protease attack. In addition, Dko ookinetes have a much reduced capacity to traverse the midgut epithelium and to transform into the oocyst stage. P25 and P28 are partially redundant in these functions, since the efficiency of ookinete/oocyst development is only mildly compromised in parasites lacking either P25 or P28 (Sko parasites) compared with that of Dko parasites. The fact that Sko parasites are efficiently transmitted by the mosquito is a compelling reason for including both target antigens in transmission-blocking vaccines.     

Comparison of in vitro-cultured and wild-type Perkinsus marinus. I. Pathogen virulence

Perkinsus marinus is a highly contagious pathogen of the eastern oyster Crassostrea virginica. Until recently, transmission studies have employed wild-type parasites isolated directly from infected oysters. Newly developed methods to propagate P. marinus in vitro have led to using cultured parasites for infection studies, but results suggest that cultured parasites are less virulent than wild-type parasites In this paper, we report results of experiments designed to quantify differences between wild-type and cultured P. marinus virulence and to test the following hypotheses: (1) in vitro-cultured parasites are less virulent than wild-type parasites; (2) virulence decreases gradually during in vitro culture; (3) virulence of in vitro cultures can be restored by in vivo passage; (4) virulence changes with culture phase. Our results demonstrate that parasites freshly isolated from infected hosts are much more virulent than those propagated in culture, indicating a potential deficiency in the culture medium used. Virulence was lost immediately in culture and, for that reason, the practice of repassing cultured cells through the host to restore virulence does not work for P. marinus. Virulence was also associated with culture phase: log-phase parasites were significantly more virulent than those obtained from lag- or stationary-phase cultures.     

Host age and structure of the component communities of parasites in river minnow Phoxinus phoxinus (L.)

Species composition and structure of the communities of fish parasites in river minnow Phoxinus phoxinus (L.) from the Pechora river were investigated in two of the Pechora-Ilychsky Biosphere Nature Reserve, Komi Republic. The component communities of the parasites in river minnow are shown to have a one-year cycle including the states of development, completion, and destruction. Communities in the state of development are characterized by a low variety of species, low values of Shannon index, often high values of domination index, presence of only two groups of parasites in the structure described by variational curved of the conditional biomasses of species, deviation of the conditional biomasses of species from the linear regression, and sum of errors of the regression equations lower a threshold value. The communities consist of young individual parasites and their larval stages. Completed community is characterized by the following properties. There are three groups of parasites, differing in allometric index, in the structure, discerned by the ratio of conditional biomasses of the species included. Conditional biomasses of species in ecologically safe reservoirs lie on the segments of straight lines. Species variety reaches its maximum. Species are presented mainly by mature specimens and larval stages of the parasites using fish as intermediate host. Community in the state of destruction shows low values of domination index and relatively small variety pf species. Such community is consist of one or two groups of species, which are represented by mature, oviparous, and dying individuals. There are larval stages of parasites using fish as intermediate hosts. Dominant species or species groups, as well as values of indexes describing the component communities of parasites, can be different in mature river minnow from different geographical regions. However, the number of groups of parasites, formed by the ratio of conditional biomasses, remains constant, and sum of errors of the regression equations characterizing the communities is always below 0.25. Component communities of parasites in young river minnows differ from the communities in mature fishes by lower variety of species. Lower biomass, and lower number of individual parasites. The communities of parasites in 0+ old fishes are often characterized by lesser number of groups of parasites, classified by the ratio of their biomasses, and presence of two dominate species. It is often impossible to count the sum of errors of the regression equations describing spread in values of biomasses of the species forming the community.     

Enhanced detection of Plasmodium vivax liver stages by cytocentrifugation

Malaria parasites circulating in the blood or developing in the mosquito host can easily be seen and studied. We know much less about malaria parasites in the liver not only because of their location, but also because there are so few of them. Hepatic parasites are most often grown within hepatoma cells in culture, stained and visualized on slides under direct microscopy. In this report, Chitraporn Karnasuta and George Watt investigate the potential of cytocentrifugation as a tool for improving the detection of liver-stage malaria parasites.     

Mobile genetic elements colonizing the genomes of metazoan parasites

A substantial fraction of the genome of most eukaryotes, including those of metazoan parasites, is predicted to comprise repetitive sequences. Mobile genetic elements (MGEs) will make up much of these repetitive sequences, particularly the interspersed sequences. This article reviews information on MGEs that have colonized the genomes of metazoan parasites (i.e. parasites of parasites). Helminth and mosquito genomes, in particular, are compared with those of better-understood model organisms. MGEs from the genomes of metazoan parasites can be expected to have practical uses in transgenesis and epidemiological studies.     

Environmental parasitology: What can parasites tell us about human impacts on the environment?

There are a variety of ways that environmental changes affect parasites, suggesting that information on parasites can indicate anthropogenic impacts. Parasitism may increase if the impact reduces host resistance or increases the density of intermediate or definitive hosts. Parasitism may decrease if definitive or intermediate host density declines or parasites suffer higher mortality directly (eg. from toxic effects on parasites) or indirectly (infected hosts suffer differentially high mortality). Although these scenarios are opposing, they can provide a rich set of predictions once we understand the true associations between each parasite and impact. In this review, Kevin Lafferty discusses how parasite ecologists have used and can use parasites to assess environmental quality.