SELECTION AND STRAIN SPECIFICITY OF COMPATIBILITY BETWEEN SNAIL INTERMEDIATE HOSTS AND THEIR PARASITIC SCHISTOSOMES

Many theoretical models of host-parasite coevolution assume that variation in host resistance to parasite infection is, at least partially, genetically determined and specific to the strain of infecting parasite. However, very few experimental studies have been conducted to test this assumption in animal-parasite systems. Biomphalaria glabrata snails serve as the intermediate hosts of Schistosoma mansoni. Although some snails are resistant to infection, there is no evidence of fixation of resistance in field populations. Two possible explanations for this are high fitness costs associated with resistance and a dynamic coevolution between parasite and host, perhaps involving matching alleles or gene-for-gene interactions. Two strains of B. glabrata were artificially selected for either resistance or susceptibility to each of two strains of S. mansoni parasite for three generations. Third-generation snails were then were exposed to either the parasite strain to which they had been selected or to a different parasite strain. In both host strains, resistance and susceptibility (compatibility) were found to be heritable. Moreover, compatibility to one parasite strain was not associated with compatibility to another strain, implying no genetic trade-off. Our results are discussed in terms of potential mechanisms of resistance in this host-parasite system and their implications to general coevolutionary theory.     

Towards an understanding of the epigenetics of schistosomes: a comparative epigenomic study

As in perhaps all eukaryotes, schistosomes use a supplementary information transmitting system, the epigenetic inheritance system, to shape genetic information and to produce different phenotypes. In contrast to other important parasites, the study of epigenetic phenomena in schistosomes is still in its infancy. Nevertheless, we are beginning to grasp what goes on behind the epigenetic scene in this parasite. We have developed techniques of native chromatin immunoprecipitation (N-ChIP) and associated the necessary bioinformatics tools that allow us to run genome-wide comparative chromatin studies on Schistosoma mansoni at different stages of its life cycle, on different strains and on different sexes. We present here an application of such an approach to study the genetic and epigenetic basis for a phenotypic trait, the compatibility of S. mansoni with its invertebrate host Biomphalaria glabrata. We have applied the ChIP procedure to two strains that are either compatible or incompatible with their intermediate host. The precipitated DNA was sequenced and aligned to a reference genome and this information was used to determine regions in which both strands differ in their genomic sequence and/or chromatin structure. This procedure allowed us to identify candidate genes that display either genetic or epigenetic difference between the two strains.     

Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata

Host-parasite coevolution is often described as a process of reciprocal adaptation and counter adaptation, driven by frequency-dependent selection. This requires that different parasite genotypes perform differently on different host genotypes. Such genotype-by-genotype interactions arise if adaptation to one host (or parasite) genotype reduces performance on others. These direct costs of adaptation can maintain genetic polymorphism and generate geographic patterns of local host or parasite adaptation. Fixation of all-resistant (or all-infective) genotypes is further prevented if adaptation trades off with other host (or parasite) life-history traits. For the host, such indirect costs of resistance refer to reduced fitness of resistant genotypes in the absence of parasites. We studied (co)evolution in experimental microcosms of several clones of the freshwater protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. After two and a half years of culture, inoculation of evolved and naive (never exposed to the parasite) hosts with evolved and founder parasites revealed an increase in host resistance, but not in parasite infectivity. A cross-infection experiment showed significant host clone-by-parasite isolate interactions, and evolved hosts tended to be more resistant to their own (local) parasites than to parasites from other hosts. Compared to naive clones, evolved host clones had lower division rates in the absence of the parasite. Thus, our study indicates de novo evolution of host resistance, associated with both direct and indirect costs. This illustrates how interactions with parasites can lead to the genetic divergence of initially identical populations.     

Inbreeding within human Schistosoma mansoni: do host-specific factors shape the genetic composition of parasite populations?

The size, structure and distribution of host populations are key determinants of the genetic composition of parasite populations. Despite the evolutionary and epidemiological merits, there has been little consideration of how host heterogeneities affect the evolutionary trajectories of parasite populations. We assessed the genetic composition of natural populations of the parasite Schistosoma mansoni in northern Senegal. A total of 1346 parasites were collected from 14 snail and 57 human hosts within three villages and individually genotyped using nine microsatellite markers. Human host demographic parameters (age, gender and village of residence) and co-infection with Schistosoma haematobium were documented, and S. mansoni infection intensities were quantified. F-statistics and clustering analyses revealed a random distribution (panmixia) of parasite genetic variation among villages and hosts, confirming the concept of human hosts as ‘genetic mixing bowls'' for schistosomes. Host gender and village of residence did not show any association with parasite genetics. Host age, however, was significantly correlated with parasite inbreeding and heterozygosity, with children being more infected by related parasites than adults. The patterns may be explained by (1) genotype-dependent ‘concomitant immunity'' that leads to selective recruitment of genetically unrelated worms with host age, and/or (2) the ‘genetic mixing bowl'' hypothesis, where older hosts have been exposed to a wider variety of parasite strains than children. The present study suggests that host-specific factors may shape the genetic composition of schistosome populations, revealing important insights into host–parasite interactions within a natural system.     

Discussion of the relationships between Schistosoma and their intermediate hosts, assessment of the degree of host-parasite compatibility and evaluation of schistosome taxonomy.

Studies of the spectrum of the intermediate hosts of schistosomes and the relationships between parasites and intermediate host snails have been carried out with each researcher using different methods. A comparison between compatibility studies has therefore been impossible. The following three basic problems in these kind of studies are discussed in this paper: (1) the standardization of experimental materials such as schistosomes, intermediate and final hosts, (2) the methods involved in the experiments, and (3) the sort of data which must be collected. Standardized methods and materials are described in this paper. The relationships between the genus Schistosoma and the intermediate host snails belonging to the two genera Biomphalaria and Bulinus, and the mechanisms behind the process resulting in various degrees of compatibility between the two involved organisms are reviewed and discussed. Why certain combinations of schistosomes and snails result in the production of cercariae and others do not is still unknown, but there is now some indication of a camouflage behaviour during the intramolluscan stages, e.g., the larvae in the snails cover themselves with snail material and are not recognized as foreign objects. The same mechanism has already been found in the schistosomules in the final host. Much of the confusion in the discussion of the relationships between schistosomes and intermediate hosts is the result of a lack of an objective way to describe and assess the compatibility between the two. Based on a series of experiments with S. haematobium, S. intercalatum, S. bovis, S. mansoni, and several species of possible intermediate hosts, the following index for estimating the degree of compatibility is proposed: the total cercarial production from 100 exposed snails (TCP/100 exposed snails). Seven classes have been suggested: the first one (Class 0) with a TCP/100 exposed snails of zero, is called 'refractory'; the next one (Class I) called 'not very compatible' has a TCP /100 exposed snails between 1 and 10,000; the last group (Class IV) called 'extremely compatible' produced more than 500,001 per 100 exposed snails during the entire lifespan. The ability to use a spectrum of intermediate hosts and the compatibility in the taxonomy of schistosomes is discussed. The results for the different species of schistosomes indicated that each species consists of strains with 'hybrid populations' in between.     

Dispersal in a parasitic worm and its two hosts: consequence for local adaptation

Characterizing host and parasite population genetic structure and estimating gene flow among populations is essential for understanding coevolutionary interactions between hosts and parasites. We examined the population genetic structure of the trematode Schistosoma mansoni and its two host species (the definitive host Rattus rattus and the intermediate host Biomphalaria glabrata) using microsatellite markers. Parasites were sampled from rats. The study was conducted in five sites of the Guadeloupe Island, Lesser Antilles. Mollusks display a pattern of isolation by distance whereas such a pattern is not found neither in schistosomes nor in rats. The comparison of the distribution of genetic variability in S. mansoni and its two host species strongly suggests that migration of parasites is principally determined by that of the vertebrate host in the marshy focus of Guadeloupe. However, the comparison between genetic differentiation values in schistosomes and rats suggests that the efficacy of the schistosome rat-mediated dispersal between transmission sites is lower than expected given the prevalence, parasitic load and migration rate of rats among sites. This could notably suggest that rat migration rate could be negatively correlated to the age or the infection status of individuals. Models made about the evolution of local adaptation in function of the dispersal rates of hosts and parasites suggest that rats and mollusks should be locally adapted to their parasites.     

Why do all host species not show defense against avian brood parasitism: evolutionary lag or equilibrium?

Avian brood parasitism reduces the reproductive success of hosts and is therefore expected to select for host defenses against parasitism, such as an ability to reject parasitic eggs. Field studies have shown that some hosts recognize and reject parasitism, whereas others do not, and the degree of the defense varies from population to population. One long-standing debate concentrates on the differences in the distribution of host defenses observed in hosts parasitized by the brown-headed cowbird and the common cuckoo. The cowbird's hosts show either few or nearly perfect defenses, whereas the cuckoo's hosts have defenses varying from none to complete, with most falling in between the two extremes. To explore the mechanisms underlying this pattern, I constructed a mathematical model in which host defense is assumed to be genetically determined and analyzed how the host defense is established under parasitic pressure. The model shows that differences in the defense-level distribution can be attributed to the difference in the parasite's breeding strategy, generalized or specialized: hosts parasitized by generalists show perfect, none, or intermediate levels of the defense depending on the host abundances, whereas hosts parasitized by specialists always exhibit either none or intermediate levels of the defense if the parasite lacks counter defenses such as egg mimicry. This result provides a testable explanation for the existence of accepter species of the brown-headed cowbird, which might reconcile the previously conflicting hypotheses.     

Parasite-mediated selection in experimental metapopulations of Daphnia magna

In metapopulations, only a fraction of all local host populations may be infected with a given parasite species, and limited dispersal of parasites suggests that colonization of host populations by parasites may involve only a small number of parasite strains. Using hosts and parasites obtained from a natural metapopulation, we studied the evolutionary consequences of invasion by single strains of parasites in experimental populations of the cyclical parthenogen Daphnia magna. In two experiments, each spanning approximately one season, we monitored clone frequency changes in outdoor container populations consisting of 13 and 19 D. magna clones, respectively. The populations were either infected with single strains of the microsporidian parasites Octosporea bayeri or Ordospora colligata or left unparasitized. In both experiments, infection changed the representation of clones over time significantly, indicating parasite-mediated evolution in the experimental populations. Furthermore, the two parasite species changed clone frequencies differently, suggesting that the interaction between infection and competitive ability of the hosts was specific to the parasite species. Taken together, our results suggest that parasite strains that invade local host populations can lead to evolutionary changes in the genetic composition of the host population and that this change is parasite-species specific.     

SUBOPTIMAL VIRULENCE OF AN INSECT-PARASITIC NEMATODE

Recent considerations of parasite virulence have focused on the adverse effects that parasites can have on the survival of their hosts. Many parasites, however, reduce host fitness by an equally deleterious but different means, by causing partial or complete sterility of their hosts. A model of optimal parasite virulence is developed in which a quantity of host resources can be allocated to either host or parasite reproduction. Increases in parasite reproduction thus cause reductions in host fertility. The model shows that under a wide variety of ecological conditions, such parasites should completely sterilize their hosts. Only when opportunities for horizontal transmission are very limited should the parasites appropriate less than all of a host's reproductive resources. Field and laboratory evidence shows that the nematode parasite Howardula aoronymphium is relatively avirulent to one of its principal host species, Drosophila falleni, whereas it is much more virulent to D. putrida and D. neotestacea, suggesting that there may be substantial vertical transmission in D. falleni. However, epidemiological studies in the field and laboratory assays of host specificity strongly suggest that the three host species share a single parasite pool in natural populations, indicating that parasites in all three host species experience high levels of horizontal transmission. Thus, the low virulence of H. aoronymphium to D. falleni is not consistent with the model of optimal parasite virulence. It is proposed that this suboptimal virulence in D. falleni is a consequence of populations of H. aoronymphium being selected to exploit simultaneously several different host species. As a result, virulence may not be optimal in any one host. One must, therefore, consider the full range of host species in assessing a parasite's virulence.     

The scaling of dose with host body mass and the determinants of success in experimental cercarial infections

Experimental studies of parasite transmission can help to elucidate life cycles, measure the success of infective stages under different conditions, or test the efficacy of vaccination or other forms of protection against parasitic infection. By combining the results of experiments on a particular parasite taxon, one may also answer questions such as how experimental infection doses are chosen, or what determines infection success. Here, focusing on trematodes, analyses are conducted on data compiled from a total of 145 cercarial infection experiments (62 on non-schistosomes, 83 on schistosomes) obtained from 115 studies. All of these involved experimental exposure of individual hosts to a single known dose of cercariae under controlled laboratory conditions. Across these studies, the cercarial dose used showed a strong positive relationship with the body mass of the target host, independently of the taxonomic identity of that host or of the method of infection used. Although justification for the chosen dose was rarely given, the larger the target host, the more cercariae it was exposed to. Across all experiments, there was also evidence for a weak but significant dose-dependent effect on infection success: the higher the dose used in an experiment, the smaller the proportion of cercariae recovered from the host. This effect was mitigated by either host body mass (for schistosomes) or host taxonomic identity (for non-schistosomes), with infection being lower in fish than in other host types. Experimental procedures also impacted significantly on infection success, namely the infection method used (for schistosomes) and the time between infection and recovery of parasites (for non-schistosomes). Overall, this analysis of published experimental results provides evidence of both biological processes and confounding methodological effects, and it provides strong arguments for greater rationale in the design of experimental infection studies.     

Host-parasite interactions for virulence and resistance in a malaria model system

A rich body of theory on the evolution of virulence (disease severity) attempts to predict the conditions that cause parasites to harm their hosts, and a central assumption to many of these models is that the relative virulence of pathogen strains is stable across a range of host types. In contrast, a largely nonoverlapping body of theory on coevolution assumes that the fitness effects of parasites on hosts is not stable across host genotype, but instead depends on host genotype by parasite genotype interactions. If such genetic interactions largely determine virulence, it becomes difficult to predict the strength and direction of selection on virulence. In this study, we tested for host-by-parasite interactions in a medically relevant vertebrate disease model: the rodent malaria parasite Plasmodium chabaudi in laboratory mice. We found that parasite and particularly host main effects explained most of the variance in virulence (anaemia and weight loss), resistance (parasite burden) and transmission potential. Host-by-parasite interactions were of limited influence, but nevertheless had significant effects. This raises the possibility that host heterogeneity may affect the rate of any parasite response to selection on virulence. This study of rodent malaria is one of the first tests for host-by-parasite interactions in any vertebrate disease; host-by-parasite interactions typical of those assumed in coevolutionary models were present, but were by no means pervasive.     

Experimental evolution with a multicellular host causes diversification within and between microbial parasite populations—Differences in emerging phenotypes of two different parasite strains

Host‐parasite coevolution is predicted to have complex evolutionary consequences, potentially leading to the emergence of genetic and phenotypic diversity for both antagonists. However, little is known about variation in phenotypic responses to coevolution between different parasite strains exposed to the same experimental conditions. We infected Caenorhabditis elegans with one of two strains of Bacillus thuringiensis and either allowed the host and the parasite to experimentally coevolve (coevolution treatment) or allowed only the parasite to adapt to the host (one‐sided parasite adaptation). By isolating single parasite clones from evolved populations, we found phenotypic diversification of the ancestral strain into distinct clones, which varied in virulence toward ancestral hosts and competitive ability against other parasite genotypes. Parasite phenotypes differed remarkably not only between the two strains, but also between and within different replicate populations, indicating diversification of the clonal population caused by selection. This study highlights that the evolutionary selection pressure mediated by a multicellular host causes phenotypic diversification, but not necessarily with the same phenotypic outcome for different parasite strains.     

Multiple infections,kin selection and the evolutionary epidemiology of parasite traits

The coinfection of a host by several parasite strains is known to affect selective pressures on parasite strategies of host exploitation. I present a general model of coinfections that ties together kin selection models of virulence evolution and epidemiological models of multiple infections. I derive an analytical expression for the invasion fitness of a rare mutant in a population with an arbitrary distribution of the multiplicity of infection (MOI) across hosts. When a single mutation affects parasite strategies in all MOI classes, I show that the evolutionarily stable level of virulence depends on a demographic average of within‐host relatedness across all host classes. This generalization of previous kin selection results requires that within‐host parasite densities do not vary between hosts. When host exploitation strategies are allowed to vary across classes, I show that the strategy of host exploitation in a focal MOI class depends on the relative magnitudes of parasite reproductive values in the focal class and in the next. Thus, in contrast to previous findings, lower within‐host relatedness in competitive parasite interactions can potentially correspond to either higher or lower levels of virulence.     

Genotype specificity among hosts,pathogens, and beneficial microbes influences the strength of symbiont‐mediated protection

The microbial symbionts of eukaryotes influence disease resistance in many host‐parasite systems. Symbionts show substantial variation in both genotype and phenotype, but it is unclear how natural selection maintains this variation. It is also unknown whether variable symbiont genotypes show specificity with the genotypes of hosts or parasites in natural populations. Genotype by genotype interactions are a necessary condition for coevolution between interacting species. Uncovering the patterns of genetic specificity among hosts, symbionts, and parasites is therefore critical for determining the role that symbionts play in host‐parasite coevolution. Here, we show that the strength of protection conferred against a fungal pathogen by a vertically transmitted symbiont of an aphid is influenced by both host‐symbiont and symbiont‐pathogen genotype by genotype interactions. Further, we show that certain symbiont phylogenetic clades have evolved to provide stronger protection against particular pathogen genotypes. However, we found no evidence of reciprocal adaptation of co‐occurring host and symbiont lineages. Our results suggest that genetic variation among symbiont strains may be maintained by antagonistic coevolution with their host and/or their host's parasites.     

Differential propagation of the metazoan parasite Myxobolus cerebralis by Limnodrilus hoffmeisteri, Ilyodrilus templetoni, and genetically distinct strains of Tubifex tubifex

Whirling disease, caused by the parasite Myxobolus cerebralis, has infected rainbow trout (Oncorhynchus mykiss) and other salmonid fish in the western United States, often with devastating results to native populations but without a discernible spatial pattern. The parasite develops in a complex 2-host system in which the aquatic oligochaete Tubifex tubifex is an obligate host. Because substantial differences in whirling disease severity in different areas of North America did not seem explainable by environmental factors or features of the parasite or its fish host, we sought to determine whether ecological or genetic variation within oligochaete host populations may be responsible. We found large differences in compatibility between the parasite and various laboratory strains of T. tubifex that were established from geographic regions with different whirling disease histories. Moreover, 2 closely related species of tubificids, Limnodrilus hoffmeisteri and Ilyodrilus templetoni, which occur naturally in mixed species assemblages with T. tubifex, were incompatible with M. cerebralis. Virulence of the parasite was directly correlated with the numbers of triactinomyxon spores that developed within each strain of T. tubifex. Thus, the level of virulence was directly related to the compatibility between the host strain and the parasite. Genetic analyses revealed relationships that were in agreement with the level of parasite production. Differences in compatibilities between oligochaetes and M. cerebralis may contribute to the spatial variance in the severity of the disease among salmonid populations.     

The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): susceptibility of Oncovhynchus mykiss (Walbaum) under experimental conditions

An experimental epidemiological approach was chosen to study the survival and infection dynamics of Gyrodactylus salaris on juvenile rainbow trout, Oncorhynchus mykiss , in the laboratory. A marked heterogeneity in the host stock was apparent. The rainbow trout could be divided into three groups on the basis of parasite survival and infection pattern on individually isolated fish: (1) hosts receptive to initial parasite attachment, but unreceptive to parasite establishment and reproduction; (2) hosts moderately susceptible to parasite establishment and reproduction, but which, after a period of restricted parasite population growth, responded, recovered and eliminated the parasites; and (3) hosts very susceptible to parasite infection and reproduction, but which, after a period of significant parasite population growth, responded, recovered and eliminated the parasites. These different patterns are considered to reflect genetic differences between host individuals. Parasite aggregation was also shown to be an important factor in the outcome of the host-parasite association. The parasites were finally eliminated on the individually isolated hosts, but not on hosts maintained in batches and so host population size and immigration of fresh. previously unexposed, hosts appeared to be important for growth and maintenance of the parasite population. The parasite was not found to cause host mortality. Rainbow trout was a suitable host for G. salaris , capable of transmitting the parasite to new localities as a consequence of stocking programmes or migratory behaviour.     

Influence of host profitability and microenvironmental conditions on parasite specialization on a main and an alternative hosts

Parasite success depends on both host profitability and the microenvironment provided by the host, which together define host-parasite compatibility and can differ between hosts. We experimentally disentangled the effects of host profitability and microenvironmental conditions provided by nest material on the reproduction of a nest-based ectoparasite when exploiting its main and an alternative avian host species. Parasite reproductive performance was similar on both hosts when breeding in nests of their own species, suggesting no difference in host-parasite compatibility between hosts. The apparent parasite specialization could therefore result from differences in host-parasite encounter processes. However, when hosts were successful, the main host produced more young in infested nests, whereas the alternative host produced less; furthermore, host reproductive performance was higher in nests of the main host species, suggesting that this nest material alleviates parasitism cost. Therefore, our results suggest different evolutionary responses to parasites of the main and alternative hosts, with either higher tolerance or higher resistance, modulated by nest material.     

Similarity in ectoparasite faunas of Palaearctic rodents as a function of host phylogenetic, geographic or environmental distances: Which matters the most?

Different host species harbour parasite faunas that are anywhere from very similar to very different in species composition. A priori, the similarity in the parasite faunas of any two host species should decrease with increases in either the phylogenetic distance, the distinctness of the environments occupied or the geographical distance between these hosts. We tested these predictions using extensive data on the faunas of fleas (Insecta: Siphonaptera) and gamasid mites (Acari: Parasitiformes) parasitic on rodents across the Palaearctic. For each pair of host species, we computed the similarity in parasite faunas based on both species composition as well as the phylogenetic and/or taxonomic distinctness of parasite species. Phylogenetic distances between hosts were based on patristic distances through a rodent phylogeny, geographic distances were computed from geographic range data, and environmental dissimilarity was measured from the average climatic and vegetation scores of each host range. Using multiple regressions on distance matrices to assess the separate explanatory power of each of the three dependent variables, environmental dissimilarity between the ranges of host species emerged as the best predictor of dissimilarity between parasite faunas, especially for fleas; in the case of mites, phylogenetic distance between host species was also important. A closer look at the data indicates that the flea and mite faunas of two hosts inhabiting different environments are always different, whilst hosts living in similar environments can have either very similar or dissimilar parasite faunas. Additional tests showed that dissimilarity in flea or mite faunas between host geographic ranges was best explained by dissimilarity in vegetation, followed by dissimilarity in climatic conditions. Thus, external environmental factors may play greater roles than commonly thought in the evolution of host-parasite associations.     

VIRULENCE AND COMPETITIVENESS: TESTING THE RELATIONSHIP DURING INTER‐ AND INTRASPECIFIC MIXED INFECTIONS

Understanding the reasons why different parasites cause different degrees of harm to their hosts is an important objective in evolutionary biology. One group of models predicts that if hosts are infected with more than one strain or species of parasite, then competition between the parasites will select for higher virulence. While this idea makes intuitive sense, empirical data to support it are rare and equivocal. We investigated the relationship between fitness and virulence during both inter‐ and intraspecific competition for a fungal parasite of insects, Metarhizium anisopliae. Contrary to theoretical expectations, competition favored parasite strains with either a lower or a higher virulence depending on the competitor: when in interspecific competition with an entomopathogenic nematode, Steinernema feltiae, less virulent strains of the fungus were more successful, but when competing against conspecific fungi, more virulent strains were better competitors. We suggest that the nature of competition (direct via toxin production when competing against the nematode, indirect via exploitation of the host when competing against conspecific fungal strains) determines the relationship between virulence and competitive ability.