Evidence for host variation in parasite tolerance in a wild fish population

Hosts can protect themselves against parasites by actively reducing parasites burden (i.e. resistance) or by limiting the damages caused by parasites (i.e. tolerance). Disentangling between tolerance and resistance is important for predicting the evolutionary outcomes of host-parasite interaction. Dace (Leuciscus leuciscus) are often parasitized by the ectoparasite Tracheliastes polycolpus which feeds on (and destroys) fins, reducing thus the host’s condition. We tested the hypothesis that genetically-based variation in ectoparasite tolerance exists in a wild dace population. We found that moderately heterozygous dace, which are less resistant than highly heterozygous or homozygous dace, tolerated better the effect imposed by T. polycolpus for a given parasite burden. However, tolerance also varied upon environmental conditions, suggesting that genetic and environmentally-based variation exists for both resistance and tolerance in this natural host-parasite system. Moreover, a negative genetic correlation may exist between tolerance and resistance, and hence several evolutionary outcomes are possible in this interacting system.     

Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail–trematode interaction

Reciprocal adaptation between interacting species may occur in some regions (coevolutionary ‘hotspots’) and not others (‘coldspots’). In a previous study, we found hotspots and coldspots along a continuous depth gradient in two different New Zealand lakes. Specifically, we found that Microphallus sp. trematodes were locally adapted to Potamopyrgus antipodarum snails collected from shallow‐water margins of the lakes, but not to snails collected from deep‐water habitats. As sexual snails were more common in the shallow water, and asexual snails more common in the deep water, the results were also consistent with the Red Queen hypothesis, which predicts that sex should be favored in environments with coevolving parasites. Here, we repeated our earlier experiment to determine whether the results are robust over time (two years) and space (three lakes). We also tested whether our measure of parasite local adaptation was sensitive to parasite dose. Our results suggest that shallow‐water habitats are temporally stable coevolutionary hotspots, and that the pattern is spatially robust over three lake populations. We also found that, while parasite dose affects the magnitude of local adaptation, it does not obscure the signature of local adaptation in this snail–trematode system.     

Persistence of host and parasite populations subject to experimental size-selective removal

Predators have the potential to limit the spread of pathogens not only by selecting infected prey but also by shaping prey demographics. We tested this idea with an epidemiological experiment in which we simulated variable levels of size-selective predation on zooplankton hosts and monitored the persistence of host and parasite populations. In the absence of simulated predation, the virulent protozoan Caullerya mesnili frequently drove its host Daphnia galeata to extinction. Uninfected control populations showed lower extinction rates and higher average densities than infected populations in the absence of simulated predation (all of the latter went extinct or remained infected). With a weak removal rate of the largest hosts, the proportion of populations in which the parasite drove the host to extinction decreased, while the number of populations in which the host persisted and the parasite went extinct increased. Host-parasite coexistence was also observed in some cases. With intermediate levels of removal, most of the parasite populations went extinct, while the host populations persisted. With an even higher removal rate, Daphnia were driven to extinction as well. Thus, variation in one factor, size-selective mortality, resulted in four different patterns of population dynamics. Our results highlight the potential role of predation in shaping the epidemiology and community structure of host-parasite systems.     

Evidence for host allozymes present on electrophoretic gels of trematode parasites (Digenea: Plagiorchiiformes)

An allozyme analysis of trematode species Glypthelmins californiensis, Glypthelmins quieta, Glypthelmins pennsylvaniensis, Glypthelmins hyloreus, and Haplometrana intestinalis from hosts Rana aurora, Rana clamitans, Hyla crucifer, Pseudacris triseriata, and Rana pretiosa, using starch gel electrophoresis, revealed allozymes for glucose-phosphate isomerase, lactate dehydrogenase, malate dehydrogenase, and isocitrate dehydrogenase that were similar in electrophoretic mobility to host tissue controls. Host allozymes were present on gels for only a fraction of the individual parasite samples examined and could be differentiated from parasite allozymes using host tissue controls. Based on these findings, it is suggested that host samples be included on each electrophoretic gel in genetic studies of parasites to reduce the likelihood of errors due to host enzyme contamination of parasite samples.     

Eimeria maxima: the influence of host genotype on parasite reproduction as revealed by quantitative real-time PCR

The influence of host genotype on susceptibility to infection with Eimeria species has long been recognised, but beyond monitoring pathological severity or magnitude of oocyst excretion attempts to quantify fluctuations in parasite reproduction within the host have previously relied upon labour-intensive microscopic analysis. The development and application of a quantitative real-time PCR assay has opened this biological 'black box', permitting the sensitive and reproducible enumeration of parasite genomes throughout the course of infection. Generic and species-specific quantitative PCR methods are described, based upon the conserved 5S ribosomal RNA coding sequence of nine avian and murine Eimeria species and the Eimeria maxima MIC1 gene, respectively. These complementary assays have been applied to study the influence of host genotype on resistance to infection with E. maxima, revealing significant differences in parasite load between 'resistant' Line C and 'susceptible' Line 15I inbred chickens 5 days after infection. Parasite DNA remained detectable up to 20 days post-infection; 11 days after the last oocysts had been detected leaving the host.     

The effect of host heterogeneity and parasite intragenomic interactions on parasite population structure

Understanding the processes that shape the genetic structure of parasite populations and the functional consequences of different parasite genotypes is critical for our ability to predict how an infection can spread through a host population and for the design of effective vaccines to combat infection and disease. Here, we examine how the genetic structure of parasite populations responds to host genetic heterogeneity. We consider the well-characterized molecular specificity of major histocompatibility complex binding of antigenic peptides to derive deterministic and stochastic models. We use these models to ask, firstly, what conditions favour the evolution of generalist parasite genotypes versus specialist parasite genotypes? Secondly, can parasite genotypes coexist in a population? We find that intragenomic interactions between parasite loci encoding antigenic peptides are pivotal in determining the outcome of evolution. Where parasite loci interact synergistically (i.e. the recognition of additional antigenic peptides has a disproportionately large effect on parasite fitness), generalist parasite genotypes are favoured. Where parasite loci act multiplicatively (have independent effects on fitness) or antagonistically (have diminishing effects on parasite fitness), specialist parasite genotypes are favoured. A key finding is that polymorphism is not stable and that, with respect to functionally important antigenic peptides, parasite populations are dominated by a single genotype.     

Abundance/host size relationship in a fish trematode community.

The abundance of six species of trematodes: Aphanurus stossichi, Bacciger israelensis, Diphterostomum israelense, Plagioporus idoneus, Leprocreadium album and L. pegorchis, parasitic in the digestive tract of marine teleostei (Sparidae) collected near Jounieh (east Mediterranean), was analysed as a function of the host-size. In two parasite/host systems, infections were observed from the lowest size classes of the sample, with a clear tendency to an increase of abundance in older fish. In four others, parasites appear only above a rather high threshold class, young individuals never being infected. In the last three parasite/host systems, host invasion may occur early or late, but infection decreases above a well defined size class, old fishes rarely or never being infected. A given trematode species, when parasitizing several host species, shows similar abundance/host size relationships, e.g., P. idoneus in Diplodus vulgaris and Oblada melanura. When more than one species of trematode infects a single host species, curves can be markedly distinct; for instance, L. pegorchis was collected from Pagellus erythrinus below 15 cm. whereas D. israelense parasitized the same fish approximately above the same size. There is no evidence that such a replacement of one trematode by another in the course of host growth is a result of inter-specific competition.     

Effects of host age, host density and parent age on reproduction of the filth fly parasite Urolepis rufipes (Hymenoptera: Pteromalidae)

Urolepis rufipes Ashmead, a pteromalid wasp, was recently discovered parasitizing house fly and stable fly pupae in eastern Nebraska dairies. Studies have been conducted on the biology of this parasite to evaluate its potential as a biological control agent of stable flies (Stomoxys calcitrans (L.] and house flies (Musca domestica L.). House fly pupae were suitable as hosts for U.rufipes at all ages; however, significantly higher parasitism occurred on host pupae aged 96-120 h. Parasite-induced mortality (host mortality without progeny production) was higher than for other pteromalid parasites of filth flies under similar conditions. Parasitism increased with parasite--host ratio at 20 degrees C; however, the opposite was noted at 30 degrees C for parasite--host ratios ranging from 5:50 to 50:50. Fly eclosion decreased as parasite--host ratio increased at 20 degrees C, and no host eclosion occurred at the highest parasite--host ratios (20:50 and 50:50) at 30 degrees C. Females produced an average of 18.6 female and 7.6 male progeny. 88% of the progeny were produced during the first 6 days post parental eclosion. The short life span, low progeny emergence rate and high per cent host eclosion, in comparison with other parasite species, suggests that the Nebraska strain of U.rufipes may not an effective biological control agent of house flies.     

Intraspecific competition for host resources in a parasite

1. Download : Download high-res image (260KB)
2. Download : Download full-size image

     

Assortative pairing in Gammarus insensibilis (Amphipoda) infected by a trematode parasite

We have investigated the influence of Microphallus papillorobustus (Trematoda) on the reproductive biology and mating patterns of its intermediate host Gammarus insensibilis (Amphipoda). Infected Gammarus species show altered behaviour which renders them more susceptible to predation by Charadriiform birds, the parasite's definitive hosts. In a natural population of G. insensibilis, mean parasite intensity was higher for unpaired individuals than for paired individuals. Fecundity was reduced in infected amphipods. Size-assortative pairing was significant, although infected males were found with smaller females compared to uninfected males of the same size. There was also a positive assortative pairing by parasitic prevalence. Vertical segregation between infected and uninfected individuals, male-male competition for access to uninfected females, and female choice may explain assortative mating for prevalence. This study provides the first empirical evidence that parasites can have a direct effect on patterns of mating in gammarids.     

Host condition as a constraint for parasite reproduction

Environmental stress has been suggested to increase host susceptibility to infections and reduce host ability to resist parasite growth and reproduction, thus benefiting parasites. This prediction stems from expected costs of immune defence; hosts in poor condition should have less resources to be allocated to immune function. However, the alternative hypothesis for response to environmental stress is that hosts in poor condition provide less resources for parasites and/or suffer higher mortality, leading to reduced parasite growth, reproduction and survival. We contrasted these alternative hypotheses in a trematode–snail ( Diplostomum spathaceum – Lymnaea stagnalis ) system by asking: (1) how host condition affects parasite reproduction (amount and quality of produced transmission stages) and (2) how host condition affects the survival of infected host individuals. We experimentally manipulated host condition by starving the snails, and found that parasites produced fewer and poorer quality transmission stages in stressed hosts. Furthermore, starvation increased snail mortality. These findings indicate that in well-established trematode infections, reduced ability of immune allocation has no effect on host exploitation by parasites. Instead, deteriorating resources for the snail host can directly limit the amount of resources available for the parasite. This, together with increased host mortality, may have negative effects on parasite populations in the wild.     

Dissecting the effect of a heterogeneous environment on the interaction between host and parasite fitness traits

Environmental variation can alter the probability of parasitic infection or the fitness consequence of infection, and thus has the potential to dramatically alter the dynamics of host parasite coevolution. Here we investigated the effect of a changing temperature on host-parasite interactions using the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa. By reciprocally varying (1) the temperature at which exposure to parasites occurred and (2) the temperature at which within-host parasite growth occurred, and measuring several fitness-related traits, we show that while there are temperature combinations that favour either host or parasite, there are also conditions that favour neither, that is, negative fitness consequences for the host without fitness benefits for the parasite. This result highlights the importance of considering a heterogeneous rather than static environment in coevolutionary studies, while also showing support for an optimal virulence strategy in castrating parasites.     

Microsatellite loci from the trematode Lecithochirium fusiforme,a parasite of the European conger eel

Seven polymorphic loci containing dinucleotide repeats and one trinucleotide microsatellite were developed for the hemiurid fluke Lecithochirium fusiforme, a parasite of the European conger eel Conger conger. All parasites that were collected from a single individual host (a total of 54 specimens) were genotyped. The number of alleles ranged from two to eight. The observed and expected heterozygosities ranged from 0.057 to 0.736 and from 0.091 to 0.794, respectively. Hardy–Weinberg deviations were statistically significant for two loci. These markers will be useful for study of parasite transmission patterns and population genetic structure.     

Differential susceptibility to a trematode parasite among genotypes of the Mytilus edulis/galloprovincialis complex

We show that parasitism by the trematode Prosorhynchus squamatus in parental and introgressed Mytilus edulis/galloprovincialis (Bivalvia) mussels occurs in individuals with a predominantly M. edulis genome. This result suggests that the restricted specificity of P. squamatus is dependent on genetic factor(s) present in M. edulis. Because of its strong pathogenic effects (i.e. total castration and possible death), this parasite may be a source of intense selection against M. edulis genomes when they are present in a site. As a consequence, it may favour the geographic extension of the M. galloprovincialis genome. Previous studies have indicated that, in hybrid zones, recombinant genotypes are more susceptible to parasitic infections than either parental genotype. We demonstrate that this is not the case for the M. edulis/M. galloprovincialis system, and that the parental genotype alone determines susceptibility.     

Trypanosoma cruzi: effect of phenothiazines on the parasite and its interaction with host cells.

Phenothiazines were observed to have a direct effect on Trypanosoma cruzi and on its in vitro interaction with host cells. They caused lysis of trypomastigotes (50 uM/24 h) and, in axenic medium, dose-dependent inhibition of amastigote and, to a lesser extent, epimastigote proliferation. Treatment of infected peritoneal macrophages with 12.5 uM chlorpromazine or triflupromazine inhibited the infection; this effect was found to be partially reversible if the drugs were removed after 24 h of treatment. At 60 uM, the drugs caused damage to amastigotes interiorized in heart muscle cells. However, the narrow margin of toxicity between antitrypanosomal activity and damage to host cells mitigates against in vivo investigation at the present time. Possible hypotheses for the mechanism of action of phenothiazines are discussed.     

Anthelmintic treatment alters the parasite community in a wild mouse host

Individuals are often co-infected with several parasite species, yet the consequences of drug treatment on the dynamics of parasite communities in wild populations have rarely been measured. Here, we experimentally reduced nematode infection in a wild mouse population and measured the effects on other non-target parasites. A single oral dose of the anthelmintic, ivermectin, significantly reduced nematode infection, but resulted in a reciprocal increase in other gastrointestinal parasites, specifically coccidial protozoans and cestodes. These results highlight the possibility that drug therapy may have unintended consequences for non-target parasites and that host–parasite dynamics cannot always be fully understood in the framework of single host–parasite interactions.     

The parasite capacity of the host population

The estimation of parasitic pressure on the host populations is frequently required in parasitological investigations. The empirical values of prevalence of infection are used for this, however the latter one as an estimation of parasitic pressure on the host population is insufficient. For example, the same prevalence of infection can be insignificant for the population with high reproductive potential and excessive for the population with the low reproductive potential. Therefore the development of methods of an estimation of the parasitic pressure on the population, which take into account the features the host population, is necessary. Appropriate parameters are to be independent on view of the researcher, have a clear biological sense and be based on easily available characteristics. The methods of estimation of parasitic pressure on the host at the organism level are based on various individual viability parameters: longevity, resistance to difficult environment etc. The natural development of this approach for population level is the analysis of viability parameters of groups, namely, the changing of extinction probability of host population under the influence of parasites. Obviously, some critical values of prevalence of infection should exist; above theme the host population dies out. Therefore the heaviest prevalence of infection, at which the probability of host population size decreases during the some period is less than probability of that increases or preserves, can serve as an indicator of permissible parasitic pressure on the host population. For its designation the term "parasite capacity of the host population" is proposed. The real parasitic pressure on the host population should be estimated on the comparison with its parasite capacity. Parasite capacity of the host population is the heaviest possible prevalence of infection, at which, with the generation number T approaching infinity, there exists at least one initial population size ni(0) for which the probability of size decrease through T generations is less than the probability of its increase. [formula: see text] The estimation of the probabilities of host population size changes is necessary for the parasite capacity determination. The classical methods for the estimation of extinction probability of population are unsuitable in this case, as these methods require the knowledge of population growth rates and their variances for all possible population sizes. Thus, the development methods of estimate of extinction probability of population, based on the using of available parameters (sex ratio, fecundity, mortality, prevalence of infection PI) is necessary. The population size change can be considered as the Markov process. The probabilities of all changes of population size for a generation in this case are described by a matrix of transition probabilities of Markov process (pi) with dimensions Nmax x Nmax (maximum population size). The probabilities of all possible size changes for T generations can be calculated as pi T. Analyzing the behaviour matrix of transition at various prevalence of infection, it is possible to determine the parasite capacity of the host population. In constructing of the matrix of transition probabilities, should to be taken into account the features the host population and the influence of parasites on its reproductive potential. The set of the possible population size at a generation corresponds to each initial population size. The transition probabilities for the possible population sizes at a generation can be approximated to the binomial distribution. The possible population sizes at a generation nj(t + 1) can be calculated as sums of the number of survived parents N1 and posterities N2; their probabilities--as P(N1) x P(N2). The probabilities of equal sums N1 + N2 and nj(t + 1) > or = Nmax are added. The number of survived parents N1 may range from 0 to (1-PI) x ni(t). The survival probabilities can be estimated for each N1 as [formula: see text] The number of survived posterities N2 may range from 0 to N2max (the maximum number of posterities). N2max is [formula: see text] and the survival probabilities for each N2, is defined as [formula: see text] where [formula: see text], ni(t) is the initial population size (including of males and infected specimens of host), PI is the prevalence of infection, Q1 is the survival probabilities of parents, Pfemales is the frequency of females in the host population, K is the number of posterities per a female, and Q2 is the survival probabilities of posterities. When constructing matrix of transition probabilities of Markov process (pi), the procedure outlined above should be repeated for all possible initial population size. Matrix of transition probabilities for T generations is defined as pi T. This matrix (pi T) embodies all possible transition probabilities from the initial population sizes to the final population sizes and contains a wealth of information by itself. From the practical point of view, however, the plots of the probability of population size decrease are more suitable for analysis. They can be received by summing the probabilities within of lines of matrix from 0 to ni--1 (ni--the population size, which corresponds to the line of the matrix). Offered parameter has the number of advantages. Firstly, it is independent on a view of researcher. Secondly, it has a clear biological sense--this is a limit of prevalence, which is safe for host population. Thirdly, only available parameters are used in the calculation of parasite capacity: population size, sex ratio, fecundity, mortality. Lastly, with the availability of modern computers calculations do not make large labour. Drawbacks of this parameter: 1. The assumption that prevalence of infection, mortality, fecundity and sex ratio are constant in time (the situations are possible when the variability of this parameters can not be neglected); 2. The term "maximum population size" has no clear biological sense; 3. Objective restrictions exist for applications of this mathematical approach for populations with size, which exceeds 1000 specimens (huge quantity of computing operations--order Nmax 3*(T-1), work with very low probabilities). The further evolution of the proposed approach will allow to transfer from the probabilities of size changes of individual populations to be probabilities of size changes of population systems under the influence of parasites. This approach can be used at the epidemiology and in the conservation biology.     

Cryptic diversity and patterns of host specificity in trematode flatworms

The widespread utilization of molecular markers has revealed that a broad spectrum of taxa contain sets of morphologically cryptic, but genetically distinct lineages ( Bickford et al. 2007 ). The identification of cryptic taxa is important as an accurate appreciation of diversity is crucial for a proper understanding of evolutionary and ecological processes. An example is the study of host specificity in parasitic taxa, where an apparent generalist may be found to contain a complex of several more specific species ( Smith et al. 2006 ). Host specificity is a key life history trait that varies greatly among parasites ( Poulin & Keeney 2007 ). While some can exploit a wide range of hosts, others are confined to just a single species. Access to additional hosts increases the resources available to a parasite. However, physiological or ecological constraints can restrict the extension of host range. Furthermore, there may be a trade‐off between relaxed specificity and performance: generalism can decrease a parasites ability to adapt to each individual host species, and increase exposure to competition from other parasites ( Poulin 1998 ). Despite the central role that host specificity plays in parasite life history, relatively little is known about how host range is determined in natural systems, and data from field studies are required to evaluate among competing ideas. In this issue, an exciting paper by Locke et al. (2010) makes a valuable contribution toward the understanding of host specificity in an important group of trematode flatworms. Using molecular methods, Locke et al. reveal an almost four‐fold increase in the appreciated diversity of their focal group. In combination with a large and elegant sampling design this allows them to accurately assess host specificity for each taxon, and thus draw key insights into the factors that control host range in a dominant parasite group.