The characteristics of the ixodid tick-vertebrate animal parasitic system]

The parasitic system ixodid tick (parasite)--vertebrate animal (host) is relatively stable in space and time. Equilibrium state in the system is maintained at the low levels of the hosts' infection and moderate intensity of their immunity. Parasite sensitizes the host's organism at the stage of feeding on antigens of its saliva and the host develops different degrees of resistance preventing the subsequent individuals of ticks from normal feeding. Antitick immunity is species specific. Its intensity is defined by the species belonging of the parasite and host, intensity and intervals between infections, availability of "anti-immune mechanisms" in tick and by many other factors, which are realized at the feeding stage. Regulation of the number of ticks, depending on their abundance in the host's population, is attained due to the oversparse, close to negative binomial distribution on hosts. This mechanism functions on the principle of feedback, so that at the excessive number of the parasite some individuals in the host's population, which are especially subjected to infection, do not cope with parasitic burden and die. However, ticks, which failed to finish their feeding and represent a disproportionately great part of the whole parasite's population, die together with them and the parasitic system quickly restores its stability. In anthropocoenoses and ecosystems at different stages of anthropogenic transformation mutual regulation mechanisms of the parasite and host number break down. As a consequence, extremely high rises in the number of ticks and epizootics of agricultural animals associated with them can occur.     

Regulation of vole populations by the nematode <Emphasis Type="Italic">Trichuris arvicolae</Emphasis>: insights from modelling

The goal of this study is to determine whether a parasitic nematode may regulate, or destabilise by inducing demographic cycles, its host populations. We explore three host–parasite systems through population dynamic models. The hosts considered are the fossorial water vole, Arvicola terrestris, the common vole Microtus arvalis and the bank vole Myodes (Clethrionomys) glareolus and the parasitic nematode is Trichuris arvicolae. Three differential equation-based mathematical models are developed including host immunity and the existence of trade-off between immunity and host survival. Using parameters estimated from field data and laboratory observations, all these models show that T. arvicolae can induce host population regulation but not demographic cycles. The regulation effect of the nematode is un-ambiguous for the water vole (reduction of 50.2% of the host population size), but less obvious for the common vole (5.9%) and even less for the bank vole (1.4%). Important biological parameters to be taken into account in such models are discussed. Experimental confirmation of the regulatory potential of the nematode and of the costs of mounting an immune response against this nematode are now required. Communicated by W. Lutz     

Linking community assembly and structure across scales in a wild mouse parasite community

Understanding what processes drive community structure is fundamental to ecology. Many wild animals are simultaneously infected by multiple parasite species, so host–parasite communities can be valuable tools for investigating connections between community structures at multiple scales, as each host can be considered a replicate parasite community. Like free‐living communities, within‐host–parasite communities are hierarchical; ecological interactions between hosts and parasites can occur at multiple scales (e.g., host community, host population, parasite community within the host), therefore, both extrinsic and intrinsic processes can determine parasite community structure. We combine analyses of community structure and assembly at both the host population and individual scales using extensive datasets on wild wood mice (Apodemus sylvaticus) and their parasite community. An analysis of parasite community nestedness at the host population scale provided predictions about the order of infection at the individual scale, which were then tested using parasite community assembly data from individual hosts from the same populations. Nestedness analyses revealed parasite communities were significantly more structured than random. However, observed nestedness did not differ from null models in which parasite species abundance was kept constant. We did not find consistency between observed community structure at the host population scale and within‐host order of infection. Multi‐state Markov models of parasite community assembly showed that a host's likelihood of infection with one parasite did not consistently follow previous infection by a different parasite species, suggesting there is not a deterministic order of infection among the species we investigated in wild wood mice. Our results demonstrate that patterns at one scale (i.e., host population) do not reliably predict processes at another scale (i.e., individual host), and that neutral or stochastic processes may be driving the patterns of nestedness observed in these communities. We suggest that experimental approaches that manipulate parasite communities are needed to better link processes at multiple ecological scales.     

Host densities as determinants of abundance in parasite communities

Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The effects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the effects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the first macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.     

Epizootiology of Syphacia obvelata from a domestic mouse population on the subantarctic Kerguelen Archipelago

The effects of abundance, age, and sex of feral domestic mice Mus musculus domesticus on infections with the nematode parasite Syphacia obvelata were analyzed during a long-term study of the mouse population on Guillou Island (1.45 km2), a part of the subantarctic Kerguelen Archipelago. The population dynamics of the nematode did not follow the variation in host abundance. However, depending on the year, differences in pinworm abundance were found between the age classes and sex. Such patterns suggest that parasitic infections may have been modulated by host-intrinsic factors, e.g., either by the way of innate or adaptive immunity, rather than extrinsic factors, e.g., host abundance.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Short-term seasonal changes in parasite community structure in northern leopard froglets (Rana pipiens) inhabiting agricultural wetlands

Parasite community structure can change seasonally with shifts in host habitat and in diet. However, anthropogenic activity may influence the natural changes in transmission dynamics of different parasite species. Effects of seasonal and agricultural activity on the parasite communities of newly metamorphosed northern leopard frogs (Rana pipiens) were investigated in July and September 2001 in 5 wetlands, 3 of which were exposed to pesticide runoff from surrounding agriculture. Nineteen parasite taxa were found. Component community richness was consistently high at the pristine reference wetland, whereas the communities at a managed reference wetland remained depauperate. Infracommunity richness increased throughout the season, but more so in frogs resident in agricultural wetlands. Digeneans using frogs as intermediate hosts dominated the communities, although many species were much lower in abundance in September, suggesting mortality of heavily infected frogs. Mean abundance of Haematoloechus spp. was positively related to that of odonate naiads in the frog diet, which appeared to reflect differential second intermediate host availability between reference and agricultural wetlands. Although virtually absent from wetlands in July just after frog metamorphosis, monoxenous nematodes were more prevalent and abundant at agricultural wetlands as the season progressed. Our results suggest that agricultural activity may further facilitate the transmission of monoxenous nematodes as frogs become more terrestrial.     

Coevolutionary genetics of hosts and parasites with quantitative inheritance

Summary A model of host—parasite coevolution is analysed. A host resistance trait and a parasite virulence trait interact to determine the outcome of a parasitic attack, where each trait is determined by quantitative genetic variation. The resistance and virulence traits are assumed to have a fitness cost. Each host and parasite genotype is treated as a separate species in a multidimensional Lotka—Volterra system in which the numerical abundance of each genotype is free to change. Thus, the epidemiological effects of fluctuating population sizes are analysed jointly with changes in genotype frequencies. Population sizes fluctuate increasingly as the parasites' reproductive capacity increases and as resistance and virulence benefits per unit cost decline. The patterns of genetic variability depend mainly on the stability of population sizes and on the shape of the relationship between the costs and benefits of a trait.     

Host–parasite determinants of parasite population structure: lessons from bats and mites on the importance of time

By definition, parasitic organisms are strongly dependant on their hosts, and for a great majority, this dependence includes host-to-host transmission. Constraints imposed by the host's spatial distribution and demography, in combination with those of the parasite, can lead to a metapopulation structure, where parasite populations are highly stochastic (i.e. prone to frequent extinctions and re-colonizations) and where drift becomes a major force shaping standing genetic variation. This, in turn, will directly affect the observed population structure, along with the ability of the parasite to adapt (or co-adapt) to its host. However, only a specific consideration of temporal dynamics can reveal the extent to which drift shapes parasite population structure; this is rarely taken into account in population genetic studies of parasitic organisms. The study by Bruyndonckx et al. in this issue of Molecular Ecology does just this and, in doing so, illustrates how a comparison of host–parasite co-structures in light of temporal dynamics can be particularly informative for understanding the ecological and evolutionary constraints imposed by the host. More specifically, the authors examine spatial and temporal population genetic data of a parasitic mite Spinturnix bechsteini that exclusively exploits the Bechstein's bat Myotis bechsteinii and consider these data in relation to host–parasite life histories and the population structure of the host.     

Elucidating relationships between P.falciparum prevalence and measures of genetic diversity with a combined genetic-epidemiological model of malaria

There is an abundance of malaria genetic data being collected from the field, yet using these data to understand the drivers of regional epidemiology remains a challenge. A key issue is the lack of models that relate parasite genetic diversity to epidemiological parameters. Classical models in population genetics characterize changes in genetic diversity in relation to demographic parameters, but fail to account for the unique features of the malaria life cycle. In contrast, epidemiological models, such as the Ross-Macdonald model, capture malaria transmission dynamics but do not consider genetics. Here, we have developed an integrated model encompassing both parasite evolution and regional epidemiology. We achieve this by combining the Ross-Macdonald model with an intra-host continuous-time Moran model, thus explicitly representing the evolution of individual parasite genomes in a traditional epidemiological framework. Implemented as a stochastic simulation, we use the model to explore relationships between measures of parasite genetic diversity and parasite prevalence, a widely-used metric of transmission intensity. First, we explore how varying parasite prevalence influences genetic diversity at equilibrium. We find that multiple genetic diversity statistics are correlated with prevalence, but the strength of the relationships depends on whether variation in prevalence is driven by host- or vector-related factors. Next, we assess the responsiveness of a variety of statistics to malaria control interventions, finding that those related to mixed infections respond quickly (∼months) whereas other statistics, such as nucleotide diversity, may take decades to respond. These findings provide insights into the opportunities and challenges associated with using genetic data to monitor malaria epidemiology.     

Highly contrasted population genetic structures in a host–parasite pair in the Caribbean Sea

Evolution and population genetic structure of marine species across the Caribbean Sea are shaped by two complex factors: the geological history and the present pattern of marine currents. Characterizing and comparing the genetic structures of codistributed species, such as host–parasite associations, allow discriminating the relative importance of environmental factors and life history traits that influenced gene flow and demographic events. Using microsatellite and Cytochrome Oxidase I markers, we investigated if a host–parasite pair (the heart urchin Meoma ventricosa and its parasitic pea crab Dissodactylus primitivus) exhibits comparable population genetic structures in the Caribbean Sea and how the observed patterns match connectivity regions from predictive models and other taxa. Highly contrasting patterns were found: the host showed genetic homogeneity across the whole studied area, whereas the parasite displayed significant differentiation at regional and local scales. The genetic diversity of the parasitic crabs (both in microsatellites and COI) was distributed in two main groups, Panama–Jamaica–St Croix on the one hand, and the South‐Eastern Caribbean on the other. At a smaller geographical scale, Panamanian and Jamaican parasite populations were genetically more similar, while more genetic differentiation was found within the Lesser Antilles. Both species showed a signature of population expansion during the Quaternary. Some results match predictive models or data from previous studies (e.g., the Western‐Eastern dichotomy in the parasite) while others do not (e.g., genetic differentiation within the Lesser Antilles). The sharp dissimilarity of genetic structure of these codistributed species outlines the importance of population expansion events and/or contrasted patterns of gene flow. This might be linked to differences in several life history traits such as fecundity (higher for the host), swimming capacity of larval stages (higher for the parasite), and habitat availability (higher for the host).     

Adaptive population structure shifts in invasive parasitic mites,Varroa destructor

Comparative studies of genetic diversity and population structure can shed light on the ecological and evolutionary factors governing host–parasite interactions. Even though invasive parasites are considered of major biological importance, little is known about their adaptative potential when infesting the new hosts. Here, the genetic diversification of Varroa destructor, a novel parasite of Apis mellifera originating from Asia, was investigated using population genetics to determine how the genetic structure of the parasite changed in distinct European populations of its new host. To do so, mites infesting two categories of hosts in four European regions were compared: (a) adapted hosts surviving through means of natural selection, thereby expected to impose strong selective pressure on the mites, and (b) treated host populations, surviving mite infestations because acaricides are applied, therefore characterized by a relaxed selection imposed by the host on the mites. Significant genetic divergence was found across regions, partially reflecting the invasion pattern of V. destructor throughout Europe and indicating local adaptation of the mite to the host populations. Additionally, varying degrees of genotypic changes were found between mites from adapted and treated colonies. Altogether, these results indicate that V. destructor managed to overcome the genetic bottlenecks following its introduction in Europe and that host‐mediated selection fostered changes in the genetic structure of this mite at diverse geographic scales. These findings highlight the potential of parasites to adapt to their local host populations and confirm that adaptations developed within coevolutionary dynamics are a major determinant of population genetic changes.     

Depression of host population abundance by direct life cycle macroparasites

Simple population models are used to identify the factors which determine the degree to which direct life cycle macroparasites depress their host populations from disease free equilibrium levels. The impact of parasitic infection is shown to be related to a range of biological characteristics of the host and parasite. The most important theoretical predictions are as follows: (1) certain threshold conditions must be satisfied (concerning host density and the rates of host and parasite reproduction) to enable the pathogen to persist with the host population; (2) parasites of low to intermediate pathogenicity are the most effective suppressors of host population growth while highly pathogenic species are likely to cause their own extinction but not that of their host; (3) the statistical distribution of parasite numbers per host has a major influence on the degree of host population depression; (4) host population with high reproductive potential are better able to withstand the impact of pathogens; (5) density dependent constraints on parasite population growth within, or on the host, whether induced by competition for finite resources or immunological attack, restrict the regulatory influence of the parasites; (6) parasites with the ability to multiply directly within the host are the most effective suppressors of host population growth and may cause the extinction of the host and hence themselves.Theoretical predictions are discussed in light of (a) the use of pathogens as biological control agents of pest species and (b) the effects of disease control on host population growth.     

Patterns of diversity and abundance of fleas and mites in the Neotropics: host‐related,parasite‐related and environment‐related factors

The effects of host‐related, parasite‐related and environmental factors on the diversity and abundance of two ectoparasite taxa, fleas (Insecta: Siphonaptera) and mites (Acari: Mesostigmata), parasitic on small mammals (rodents and marsupials), were studied in different localities across Brazil. A stronger effect of host‐related factors on flea than on mite assemblages, and a stronger effect of environmental factors on mite than on flea assemblages were predicted. In addition, the effects of parasite‐related factors on flea and mite diversity and abundance were predicted to manifest mainly at the scale of infracommunities, whereas the effects of host‐related and environmental factors were predicted to manifest mainly at the scale of component and compound communities. This study found that, in general, diversity and abundance of flea and mite assemblages at two lower hierarchical levels (infracommunities and component communities) were affected by host‐related, parasite‐related and environmental factors, and compound communities were affected mainly by host‐related and environmental factors. The effects of factors differed between fleas and mites: in fleas, community structure and abundance depended on host diversity to a greater extent than in mites. In addition, the effects of factors differed among parasite assemblages harboured by different host species.     

The role of parasites in regulating host abundance

It has been 11 years since Anderson and May demonstrated the theoretical ability of helminth parasites to regulate host population abundance. In this review we consider how their work has advanced our understanding of the role of parasites in host populations. In particular Marilyn Scott and Andy Dobson consider three questions. What is meant by regulation? Is there empirical evidence that parasites can regulate host population abundance? Is it possible to predict the sort of host parasite association where one is most likely to be able to detect parasites as a major regulatory force?     

The soybean cyst nematode, Heterodera glycines: a genetic model system for the study of plant-parasitic nematodes

Despite advances in understanding plant responses to nematode infection, little information exists regarding parasitic mechanisms. Recently, it has become possible to perform genetic analysis of soybean cyst nematode. Integration of classic and reverse genetics and genomic approaches for the parasite, with host genetics and genomics will expand our knowledge of nematode parasitism.     

Genetics of host-parasite interactions

The evolution of host susceptibility or resistance to parasites has important consequences for the evolution of parasite virulence, host sexual selection, population dynamics of both host and parasite populations, and programs of biological control. The general observation of a fraction of Individuals within a population that is not parasitized, and/or the variability in parasite intensity among hosts, may reflect several phenomena acting at different levels of ecological organization. Yet, host-parasite coevolution requires host susceptibility and parasite virulence to be genetically variable. In spite of evolutionary and epidemiological implications of genetic heterogeneities in host-parasite systems, evidence concerning natural populations is still scarce. Here, we wish to emphasize why we need a better knowledge of the genetics of host-parasite interaction in natural populations and to review the evidence concerning the heritability of host susceptibility or resistance to parasites in natural populations of animals.     

From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

Impacts of parasitic plants on natural communities

Parasitic plants have profound effects on the ecosystems in which they occur. They are represented by some 4000 species and can be found in most major biomes. They acquire some or all of their water, carbon and nutrients via the vascular tissue of the host's roots or shoots. Parasitism has major impacts on host growth, allometry and reproduction, which lead to changes in competitive balances between host and nonhost species and therefore affect community structure, vegetation zonation and population dynamics. Impacts on hosts may further affect herbivores, pollinators and seed vectors, and the behaviour and diversity of these is often closely linked to the presence and abundance of parasitic plants. Parasitic plants can therefore be considered as keystone species. Community impacts are mediated by the host range of the parasite (the diversity of species that can potentially act as hosts) and by their preference and selection of particular host species. Parasitic plants can also alter the physical environment around them--including soil water and nutrients, atmospheric CO2 and temperature--and so may also be considered as ecosystem engineers. Such impacts can have further consequences in altering the resource supply to and behaviour of other organisms within parasitic plant communities.     

The invasion, persistence and spread of infectious diseases within animal and plant communities

Recent theoretical and empirical studies of the population biology of infectious diseases have helped to improve our understanding of the major factors that influence the three phases of a successful invasion, namely initial establishment, persistence in the longer term and spread to other host communities. Of central importance in all three phases is the magnitude of the basic reproductive rate or transmission potential of the parasite. The value of this parameter is determined by a variety of biological properties of the association between an individual parasite and its host and the interaction between their populations. The recent epidemic of acquired immunodeficiency syndrome (AIDS) in North America and Europe is employed to illustrate the factors that promote disease establishment and spread. The frequency distribution of the number of different sexual partners per unit of time within homosexual communities is shown to be of central importance with respect to future trends in the incidence of AIDS. Broader aspects of pathogen invasion are examined by reference to simple mathematical models of three species associations, which mirror parasite introduction into resident predator-prey, host-parasite and competitive interactions. Many outcomes are possible, depending on the values of the numerous parameters that influence multi-species population interactions. Pathogen invasion is shown to have far-reaching implications for the structure and stability of ecological communities.