Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites

Maturation time is a pivotal life-history trait of parasitic nematodes, determining adult body size, as well as daily and total fecundity. Recent theoretical work has emphasized the influence of prematurational mortality on the optimal values of age and size at maturity in nematodes. Eosinophils are a family of white blood cells often associated with infections by parasitic nematodes. Although the role of eosinophils in nematode resistance is controversial, recent work has suggested that the action of these immune effectors might be limited to the larval stages of the parasite. If eosinophils act on larval survival, one might predict, in line with theoretical models, that nematode species living in hosts with large eosinophil numbers should show reduced age and size at maturity. We tested this prediction using the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Pinworms are highly host specific and are expected to be involved in a coevolutionary process with their hosts. We found that the body size of female parasites was negatively correlated with eosinophil concentration, whereas the concentration of two other leucocyte families-neutrophils and lymphocytes-was unrelated to female body size. Egg size of parasites also decreased with host eosinophil concentration, independently of female size. Male body size was unrelated to host immune parameters. Primates with the highest immune defence, therefore, harbour small female pinworms laying small eggs. These results are in agreement with theoretical expectations and suggest that life histories of oxyurid parasites covary with the immune defence of their hosts. Our findings illustrate the potential for host immune defence as a factor driving parasite life-history evolution.     

Short-term rates of parasite evolution predict the evolution of host diversity

Coevolution with parasites has been implicated as an important factor driving the evolution of host diversity. Studies to date have focussed on gross effects of parasites: how host diversity differs in the presence vs. absence of parasites. But parasite-imposed selection is likely to show rapid variation through time. It is unclear whether short-term fluctuations in the strength of parasite-imposed selection tend to affect host diversity, because increases in host diversity are likely to be constrained by both the supply of genetic variation and ecological processes. We followed replicate populations of coevolving, initially isogenic, bacteria and phages through time, measuring host diversity (with respect to bacterial colony morphologies), host density and rates of parasite evolution. Both host density and time-lagged rates of parasite evolution were good independent predictors of the magnitude of bacterial within- and between-population diversities. Rapid parasite evolution and low host density decreased host within-population diversity, but increased between-population diversity. This study demonstrates that short-term changes in the rate of parasite evolution can predictably drive patterns of host diversity.     

The evolution of parasite manipulation of host dispersal

We investigate the evolution of manipulation of host dispersal behaviour by parasites using spatially explicit individual-based simulations. We find that when dispersal is local, parasites always gain from increasing their hosts' dispersal rate, although the evolutionary outcome is determined by the costs-to-benefits ratio. However, when dispersal can be non-local, we show that parasites investing in an intermediate dispersal distance of their hosts are favoured even when the manipulation is not costly, due to the intrinsic spatial dynamics of the host-parasite interaction. Our analysis highlights the crucial importance of ecological spatial dynamics in evolutionary processes and reveals the theoretical possibility that parasites could manipulate their hosts' dispersal.     

The dynamics of parasite incidence across host species

Whilst it is well known that many parasites occasionally switch from one host species to another and thus spread within a host clade, the patterns of spread and the observed heterogeneity in parasite incidence between host taxa are not well understood. Here, we develop a simple stochastic model as a first attempt to understand these ‘incidence dynamics’. Based on the empirically supported assumption that the probability of successful transmission from an infected to a new host species declines with increasing genetic distance between them, we study the impact of different phylogenetic histories of the host clade on the pattern of spread and the average incidence of the parasites. Our results suggest that host phylogeny alone can lead to heterogeneous parasite incidence.     

The immunology of myiasis: parasite survival and host defense strategies

Infestations by dipterous larvae that feed on dead or living vertebrate tissues for a variable period are known as myiases; these infestations reduce host physiological functions, destroy host tissues and cause significant economic losses to livestock worldwide. Recent advances in understanding the specific and nonspecific immune responses of hosts to infestation by myiasis-causing larvae and the immunological strategies evolved by larvae against the host are reviewed here. The practical implications of immunological knowledge for diagnostic and vaccination strategies are also discussed, with a view to developing environmentally sustainable control methods to be used as an alternative to chemical treatments.     

The evolution of parasite virulence, superinfection, and host resistance

We analyze the evolutionary consequences of host resistance (the ability to decrease the probability of being infected by parasites) for the evolution of parasite virulence (the deleterious effect of a parasite on its host). When only single infections occur, host resistance does not affect the evolution of parasite virulence. However, when superinfections occur, resistance tends to decrease the evolutionarily stable (ES) level of parasite virulence. We first study a simple model in which the host does not coevolve with the parasite (i.e., the frequency of resistant hosts is independent of the parasite). We show that a higher proportion of resistant host decreases the ES level of parasite virulence. Higher levels of the efficiency of host resistance, however, do not always decrease the ES parasite virulence. The implications of these results for virulence management (evolutionary consequences of public health policies) are discussed. Second, we analyze the case where host resistance is allowed to coevolve with parasite virulence using the classical gene-for-gene (GFG) model of host-parasite interaction. It is shown that GFG coevolution leads to lower parasite virulence (in comparison with a fully susceptible host population). The model clarifies and relates the different components of the cost of parasitism: infectivity (ability to infect the host) and virulence (deleterious effect) in an evolutionary perspective.     

Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission

A host’s first line of defense in response to the threat of parasitic infection is behavior, yet the efficacy of anti-parasite behaviors in reducing infection are rarely quantified relative to immunological defense mechanisms. Larval amphibians developing in aquatic habitats are at risk of infection from a diverse assemblage of pathogens, some of which cause substantial morbidity and mortality, suggesting that behavioral avoidance and resistance could be significant defensive strategies. To quantify the importance of anti-parasite behaviors in reducing infection, we exposed larval Pacific chorus frogs (Pseudacris regilla) to pathogenic trematodes (Ribeiroia and Echinostoma) in one of two experimental conditions: behaviorally active (unmanipulated) or behaviorally impaired (anesthetized). By quantifying both the number of successful and unsuccessful parasites, we show that host behavior reduces infection prevalence and intensity for both parasites. Anesthetized hosts were 20–39% more likely to become infected and, when infected, supported 2.8-fold more parasitic cysts. Echinostoma had a 60% lower infection success relative to the more deadly Ribeiroia and was also more vulnerable to behaviorally mediated reductions in transmission. For Ribeiroia, increases in host mass enhanced infection success, consistent with epidemiological theory, but this relationship was eroded among active hosts. Our results underscore the importance of host behavior in mitigating disease risk and suggest that, in some systems, anti-parasite behaviors can be as or more effective than immune-mediated defenses in reducing infection. Considering the severe pathologies induced by these and other pathogens of amphibians, we emphasize the value of a broader understanding of anti-parasite behaviors and how co-occurring stressors affect them.     

Acquired immunity and stochasticity in epidemic intervals impede the evolution of host disease resistance

Disease can generate intense selection pressure on host populations, but here we show that acquired immunity in a population subject to repeated disease outbreaks can impede the evolution of genetic disease resistance by maintaining susceptible genotypes in the population. Interference between the life-history schedule of a species and periodicity of the disease has unintuitive effects on selection intensity, and stochasticity in outbreak period further reduces the rate of spread of disease-resistance alleles. A general age-structured population genetic model was developed and parameterized using empirical data for phocine distemper virus (PDV) epizootics in harbor seals. Scenarios with acquired immunity had lower levels of epizootic mortality compared with scenarios without acquired immunity for the first PDV outbreaks, but this pattern was reversed after about five disease cycles. Without acquired immunity, evolution of disease resistance was more rapid, and long-term population size variation is efficiently dampened. Acquired immunity has the potential to significantly influence rapid evolutionary dynamics of a host population in response to age-structured disease selection and to alter predicted selection intensities compared with epidemiological models that do not consider such feedback. This may have important implications for evolutionary population dynamics in a range of human, agricultural, and wildlife disease settings.     

寄生虫与宿主的关系

对寄生虫与宿主的关系进行论述,探求寄生关系的实质,明确这二者之间的关系是认识寄生虫病发生发展规律,更好地防治寄生虫病的基础.     

Host-parasite relatedness in wood ducks: patterns of kinship and parasite success

We investigated the role of kinship in intraspecific nest parasitismof wood ducks (Aix sponsa). Among waterfowl, female philopatrycreates the potential for female relatives to nest in proximity.Costs of intraspecific nest parasitism to host females may bereduced if parasites lay eggs with kin. However, previous observationsof marked wood ducks indicated that females avoided parasitizingclutch mates or the female that incubated them. To further examinethe role of kinship, we determined the genotypes of 27 host-parasitepairs at five microsatellite loci. Average relatedness betweenhosts and all females laying parasitic eggs was only 0.04 ±0.03. Parasites appeared to choose hosts randomly with respectto kinship from among females with nests in the neighborhoodand those within the entire study area. However, host relatednessto the parasite with the greatest number of young leaving thenest was 0.11 ± 0.03, which was greater than expectedif eggs were accepted randomly from neighboring females or fromfemales present on the entire study area (p = .03 and p = .02,respectively). These patterns may reflect parasitism of randomlyselected nests followed by differential acceptance by hosts,differential hatching success of related parasites (e.g., dueto greater laying synchrony), or a mixture of parasitic strategies,one with a focus on related hosts and the other on unrelatedhosts. Genetic data revealed that social relationships did notalways reflect true relatedness and that success of primaryparasites was associated with kinship to hosts.     

The evolution of host resistance: tolerance and control as distinct strategies

In response to parasitic infection, hosts may evolve defences that reduce the deleterious effects on survivorship. This may be interpreted as a form of resistance, as long as infected hosts are able to either recover or reproduce. Here we distinguish two important routes to this form of resistance. An infected host may either: (1) tolerate pathogen damage, or (2) control the pathogen by inhibiting its growth. A model is constructed to examine the evolutionary dynamics of tolerance and control to a free-living microparasite, where both forms of resistance are costly in terms of other life-history traits. We do not observe polymorphism of tolerant genotypes. In contrast, the evolution of control may lead to disruptive selection, and ultimately dimorphism of extreme strains. The optimal host genotype also varies with the type of resistance-individuals invest more in tolerance and pay a greater cost. The free-living framework used makes the distinction between tolerance and control explicit but the distinction applies equally to directly transmitted parasites. Due to the evolutionary differences exhibited, it is important to design experiments that distinguish between the two forms of resistance.     

Imaging host cell-Leishmania interaction dynamics implicates parasite motility, lysosome recruitment, and host cell wounding in the infection process

Leishmania donovani causes human visceral leishmaniasis. The parasite infectious cycle comprises extracellular flagellated promastigotes that proliferate inside the insect vector, and intracellular nonmotile amastigotes that multiply within infected host cells. Using primary macrophages infected with virulent metacyclic promastigotes and high spatiotemporal resolution microscopy, we dissect the dynamics of the early infection process. We find that motile promastigotes enter macrophages in a polarized manner through their flagellar tip and are engulfed into host lysosomal compartments. Persistent intracellular flagellar activity leads to reorientation of the parasite flagellum toward the host cell periphery and results in oscillatory parasite movement. The latter is associated with local lysosomal exocytosis and host cell plasma membrane wounding. These findings implicate lysosome recruitment followed by lysosome exocytosis, consistent with parasite-driven host cell injury, as key cellular events in Leishmania host cell infection. This work highlights the role of promastigote polarity and motility during parasite entry.     

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.