Optimality analysis of Th1/Th2 immune responses during microparasite-macroparasite co-infection, with epidemiological feedbacks

Individuals are typically co-infected by a diverse community of microparasites (e.g. viruses or protozoa) and macroparasites (e.g. helminths). Vertebrates respond to these parasites differently, typically mounting T helper type 1 (Th1) responses against microparasites and Th2 responses against macroparasites. These two responses may be antagonistic such that hosts face a 'decision' of how to allocate potentially limiting resources. Such decisions at the individual host level will influence parasite abundance at the population level which, in turn, will feed back upon the individual level. We take a first step towards a complete theoretical framework by placing an analysis of optimal immune responses under microparasite-macroparasite co-infection within an epidemiological framework. We show that the optimal immune allocation is quantitatively sensitive to the shape of the trade-off curve and qualitatively sensitive to life-history traits of the host, microparasite and macroparasite. This model represents an important first step in placing optimality models of the immune response to co-infection into an epidemiological framework. Ultimately, however, a more complete framework is needed to bring together the optimal strategy at the individual level and the population-level consequences of those responses, before we can truly understand the evolution of host immune responses under parasite co-infection.     

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).     

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.     

Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis

There is a gap in our understanding of the relative and interactive effects of different parasite species on the same host population. Here we examine the effects of the acanthocephalan Acanthocephalus galaxii, an unidentified cyclophyllidean cestode, and the trematodes Coitocaecum parvum and Microphallus sp. on several fitness components of the amphipod Paracalliope fluviatilis, using a combination of infection surveys and both survival and behavioural trials. In addition to significant relationships between specific parasites and measures of amphipod survival, maturity, mating success and behaviour, interactions between parasite species with respect to amphipod photophilia were also significant. While infection by either A. galaxii or C. parvum was associated with increased photophilia, such increases were negated by co-infection with Microphallus sp. We hypothesize that this is due to the more subtle manipulative effect of A. galaxii and C. parvum being impaired by Microphallus sp. We conclude that the low frequency at which such double infections occur in our sampled population means that such interactions are unlikely to be important beyond the scale of the host individual. Whether or not this is generally true, implying that parasitological models and theory based on single parasite species studies do generally hold, requires cross-species meta-analytical studies.     

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.     

Heterogeneous interspecific interactions in a host-parasite system

Macroparasites of vertebrates usually occur in multi-species communities, producing infections whose outcome in individual hosts or host populations may depend on the dynamics of interactions amongst the different component species. Within a single co-infection, competition can occur between conspecific and heterospecific parasite individuals, either directly or via the host's physiological and immune responses. We studied a natural single-host, multi-parasite model infection system (polystomes in the anuran Xenopus laevis victorianus) in which the parasite species show total interspecific competitive exclusion as adults in host individuals. Multi-species infection experiments indicated that competitive outcomes were dependent on infection species composition and strongly influenced by the intraspecific genetic identity of the interacting organisms. Our results also demonstrate the special importance of temporal heterogeneity (the sequence of infection by different species) in competition and co-existence between parasite species and predict that developmental plasticity in inferior competitors, and the induction of species-specific host resistance, will partition the within-host-individual habitat over time. We emphasise that such local (within-host) context-dependent processes are likely to be a fundamental determinant of population dynamics in multi-species parasite assemblages.     

A comparative approach to understanding causes and consequences of mollusc-digenean size relationships: a case study with Allocreadiid trematodes and Cyclocalyx clams

Allocreadiid flukes often parasitize and castrate sphaeriid freshwater clams. The effects of parasitic castrators on host population life history can lead to earlier reproductive onset, changes in body size, or changes in the number of reproductive events per year. However, little is known about whether species- or clade-level traits are associated with parasite prevalence. In this study, we examine if phenotypic effects, e.g., size change, seen at the population level, sort to the species or clade level. To answer this question, we determined if different-sized host species in the ecologically important, widespread, and common sphaeriid subgenus Cyclocalyx have different prevalences of allocreadiid infection. After showing that large species are more than 12 times more likely to have patent infections than small species, we examined the evolution of size within Cyclocalyx lineages. Transitions from large size to small size or vice versa have occurred at least twice and probably many times during lineage diversification, perhaps relating to trade-offs between clutch size and parasite risk. Finally, based on existing data, we show that it is unlikely that age and body size are correlated; therefore, a simple age-exposure model is not a sufficient explanation for parasite prevalence in this clade.     

The role of mathematical models in helminth population biology

This brief review aims to illustrate how theory can aid in our understanding of the factors that determine the regulation and stability of parasite abundance, and influence the impact of control measures. The current generation of models are obviously crude, and ignore much biological detail, but they are often able to capture qualitative trends observed in real communities. As such, their analysis and investigation can provide important conceptional insights or, in some circumstances, they can be of value in a predictive role (e.g. the impact of chemotherapy in human communities).This field of research, however, is still in its infancy and much remains to be done to improve biological realism in model formulation and to extent the methods of analysis and interpretation. In the latter context, for example, the current analytical methods for the study of the dynamical properties of non-linear systems of differential and partial differential equations are inadequate for many areas of biological application. Future advances in applied mathematics will, therefore, be of great importance. As far as biological realism is concerned, three areas require urgent attention. The first concerns the treatment of heterogeneity in worm loads within host communities. The generative factors of parasite aggregation are many and varied and little is understood at present of how these processes influence a parasite's population response to perturbation induced, for example, by control measures. Stochastic models are required to examine this problem but current work in this area is very limited.The second area concerns immunity to parasitic infection. Few models take account of the substantive body of experimental work which attests to the significance of host responses (both specific and non-specific) to parasite invasion as determinants of parasite abundance within both an individual host and in the community at large. A start has been made in the investigation of models which mimic acquired immunity and immunological “memory” but much refinement and elaboration is needed (Anderson &; May, 1985a). In particular, the next generation of models should address the details of antibody-antigen and cell-antigen interactions in individual hosts as well as the broader questions concerning herd immunity. Heterogeneity in immunological responsiveness as a consequence of host nutritional status or genetic background must also be condsidered.The final topic is that of population genetics. Geneticists invariably consider changes in gene frequencies without reference to changes in parasite or host abundance, ecologists and epidemiologists have tended to study changes in abundance without reference to changes in genetic structure while immunologists have focused on the mechanisms of resistance to parasitic infection without reference to population or genetic changes. It is becoming increasingly apparent that host genetic background and genetic heterogeneity within parasite populations (e.g. the malarial parasites of man) are important determinants of observed population events (Medley &; Anderson, 1985). Future research must attempt to meld the areas of genetics, population dynamics and immunology. Such an integration presents a fascinating challenge.     

The relationship between species richness and productivity in metazoan parasite communities

Biodiversity is not distributed homogeneously in space, and it often covaries with productivity. The shape of the relationship between diversity and productivity, however, varies from a monotonic linear increase to a hump-shaped curve with maximum diversity values corresponding to intermediate productivity. The system studied and the spatial scale of study may affect this relationship. Parasite communities are useful models to test the productivity-diversity relationship because they consist of species belonging to a restricted set of higher taxa common to all host species. Using total parasite biovolume per host individual as a surrogate for community productivity, we tested the relationship between productivity and species richness among assemblages of metazoan parasites in 131 vertebrate host species. Across all host species, we found a linear relationship between total parasite biovolume and parasite species richness, with no trace of a hump-shaped curve. This result remained after corrections for the potential confounding effect of the number of host individuals examined per host species, host body mass, and phylogenetic relationships among host species. Although weaker, the linear relationship remained when the analyses were performed within the five vertebrate groups (fish, amphibians, reptiles, mammals and birds) instead of across all host species. These findings agree with the classic isolationist-interactive continuum of parasite communities that has become widely accepted in parasite ecology. They also suggest that parasite communities are not saturated with species, and that the addition of new species will result in increased total parasite biovolume per host. If the number of parasite species exploiting a host population is not regulated by processes arising from within the parasite community, external factors such as host characteristics may be the main determinants of parasite diversity.     

Interactions among bacterial strains and fluke genotypes shape virulence of co-infection

Most studies of virulence of infection focus on pairwise host–parasite interactions. However, hosts are almost universally co-infected by several parasite strains and/or genotypes of the same or different species. While theory predicts that co-infection favours more virulent parasite genotypes through intensified competition for host resources, knowledge of the effects of genotype by genotype (G × G) interactions between unrelated parasite species on virulence of co-infection is limited. Here, we tested such a relationship by challenging rainbow trout with replicated bacterial strains and fluke genotypes both singly and in all possible pairwise combinations. We found that virulence (host mortality) was higher in co-infections compared with single infections. Importantly, we also found that the overall virulence was dependent on the genetic identity of the co-infecting partners so that the outcome of co-infection could not be predicted from the respective virulence of single infections. Our results imply that G × G interactions among co-infecting parasites may significantly affect host health, add to variance in parasite fitness and thus influence evolutionary dynamics and ecology of disease in unexpected ways.     

Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology

Interspecific variation in parasite species richness among host species has generated much empirical research. As in comparisons among geographical areas, controlling for variation in host body size is crucial because host size determines resource availability. Recent developments in the use of species–area relationships (SARs) to detect hotspots of biodiversity provide a powerful way to control for host body size, and to identify ‘hot’ and ‘cold hosts’ of parasite diversity, i.e. hosts with more or fewer parasites than expected from their size. Applying SAR modelling to six large datasets on parasite species richness in vertebrates, we search for hot and cold hosts and assess the effect of other ecological variables on the probability that a host species is hot/cold taking body size (and sampling effort) into account. Five non‐sigmoid SAR models were fitted to the data by optimisation; their relative likelihood was evaluated using the Bayesian information criterion, before deriving an averaged SAR function. Overall, the fit between the five SAR models and the actual data was poor; there was substantial uncertainty surrounding the fitted models, and the best model differed among the six datasets. These results show that host body size is not a strong or consistent determinant of parasite species richness across taxa. Hotspots were defined as host species lying above the upper limit of the 80% confidence interval of the averaged SAR, and coldspots as species lying below its lower limit. Our analyses revealed (1) no apparent effect of specific ecological factors (i.e. water temperature, mean depth range, latitude or population density) on the likelihood of a host species being a hot or coldspot; (2) evidence of phylogenetic clustering, i.e. hosts from certain families are more likely to be hotspots (or coldspots) than other species, independently of body size. These findings suggest that host phylogeny may sometimes outweigh specific host ecological traits as a predictor of whether or not a host species harbours more (or fewer) parasite species than expected for its size.     

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.     

The effect of helminth co-infection on malaria in mice: a meta-analysis

The question of how helminths may alter the course of concurrent malaria infection has attracted much interest in recent years. In particular, it has been suggested that by creating an anti-inflammatory immune environment, helminth co-infection may dampen both protective and immunopathological responses to malaria parasites, thus altering malaria infection dynamics and disease severity. Both synergistic and antagonistic interactions are reported in the literature, and the causes of variation among studies are not well understood. Here, meta-analysis of 42 mouse co-infection experiments was used to address how helminths influence malaria parasite replication and host mortality, and explore the factors explaining variation in findings. Most notably, this analysis revealed contrasting effects of helminth co-infection in lethal and resolving malaria models. Whilst co-infection exacerbated mortality and increased peak parasitaemia in ordinarily resolving malaria infections (Plasmodium chabaudi and Plasmodium yoelii), effects among lethal malaria infections (Plasmodium berghei) tended to be in the opposite direction with no change in parasitaemia. In the subset of experiments on cerebral malaria models (P. berghei ANKA strain in a susceptible host), helminth co-infection significantly delayed death. These findings are consistent with the hypothesis that depending on the existing balance of pro- and anti-inflammatory responses mounted against malaria parasites in a given host, immune responses elicited by helminth co-infection may either promote or inhibit malarial disease. However, despite such broad patterns, a prominent feature of this dataset was great heterogeneity in effects across studies. A key future challenge therefore lies in explaining the biological causes of this variation, including a more thorough exploration of non-immunological mechanisms of helminth-malaria interaction.     

Echinococcus multilocularis--a zoonosis of anthropogenic environments?

Transmission of the fox tapeworm Echinococcus multilocularis, the causative agent of human alveolar echinococcosis, is known to depend on various environmental factors which are subject to human influence. Epidemiological data suggest that in most endemic regions anthropogenic landscape changes (e.g. deforestation and agricultural practices) have led to more favourable conditions for the parasite's animal hosts, especially arvicolid rodents, thereby increasing the risk for parasite transmission and human disease. Examples are the conversion of forests or crop fields into meadows and pastures in Europe, China and North America, and overgrazing of natural grassland in central Asia. Other anthropogenic factors include interference with host population densities by wildlife disease control, changing hunting pressure and provision of new habitats, e.g. in urban areas. Domestic dogs may, under certain conditions, get involved in the otherwise largely wildlife-based transmission, and thereby greatly increase the infection pressure to humans. The introduction of neozootic host species may increase transmission, or even initiate the parasite's life-cycle in previously non-endemic regions. Lastly, the parasite itself may be accidentally introduced into non-endemic areas, if suitable host populations are present (e.g. in northern Japan).     

The scaling of parasite biomass with host biomass in lake ecosystems: are parasites limited by host resources?

The standing crop biomass of different populations or trophic levels reflects patterns of energy flow through an ecosystem. The contribution of parasites to total biomass is often considered negligible; recent evidence suggests otherwise, although it comes from a narrow range of natural systems. Quantifying how local parasite biomass, whether that of a single species or an assemblage of species sharing the same host, varies across localities with host population biomass, is critical to determine what constrains parasite populations. We use an extensive dataset on all free‐living and parasitic metazoan species from multiple sites in New Zealand lakes to measure parasite biomass and test how it covaries with host biomass. In all lakes, trematodes had the highest combined biomass among parasite taxa, ranging from about 0.01 to 0.25 g m^?2, surpassing the biomass of minor free‐living taxa. Unlike findings from other studies, the life stage contributing the most to total trematode biomass was the metacercarial stage in the second intermediate host, and not sporocysts or rediae within snail first intermediate hosts, possibly due to low prevalence and small snail sizes. For populations of single parasite species, we found no relationship between host and parasite biomass for either juvenile or adult nematodes. In contrast, all life stages of trematodes had local biomasses that correlated positively with those of their hosts. For assemblages of parasite species sharing the same host, we found strong relationships between local host population biomass and the total biomass of parasites supported. In these host–parasite biomass relationships, the scaling factor (slope in log‐log space) suggests that parasites may not be making full use of available host resources. Host populations appear capable of supporting a little more parasite biomass, and may be open to expansion of existing parasites or invasion by new ones.     

Heterogeneous selection promotes maintenance of polymorphism in host–parasite interactions

Polymorphism in loci affecting host resistance and parasite virulence is characteristic for nearly all species and this genetic variation is considered to have profound consequences for the patterns of disease incidence, prevalence and evolution. The gene-for-gene (GFG) system is a well-characterized genetic interaction of host recognition and parasite antigenic loci for a wide range of plant-parasite interactions. Long-term maintenance of polymorphism in GFG systems has remained puzzling for both theoreticians and empiricists. Traditionally this diversity has been explained by tradeoffs with other life-history traits closely linked with fitness, yet empirical evidence for such costs has remained mixed. Here we argue that incorporating simple ecological reality – spatial structuring and gradient of environmental conditions – into host–parasite research will help us understand how polymorphism is maintained. While environmental conditions (biotic and abiotic factors) have been studied in depth in plant pathology for their influence on disease severity and plant yield, they have been rarely set into an evolutionary framework. We briefly review recent data on natural plant–parasite metapopulations and theoretical models moving from single population models towards metapopulation theory to reveal in just how many ways spatial structuring may affect the coevolutionary process. We clarify also how spatially heterogeneous selection, through G×E (or G×G×E) interactions, may be particularly important for natural host–parasite interactions and suggest that this provides the unifying ground upon which future theoretical and empirical work should be build on.     

Microparasite species richness in rodents is higher at lower latitudes and is associated with reduced litter size

Parasite species loads are expected to be higher in the tropics and higher parasite species richness to have cumulative effects on host physiology or demography. Despite being regularly assumed or predicted, empirical evidence on species–latitude patterns is scarce or contradictory and studies on the impacts of concomitant infections have mainly been done at host intra‐specific level. Broad generalizations are then very hard, if not spurious. By focusing on rodent species and their non‐eukaryotic microparasites (i.e. viruses and bacteria), we investigated, using a comparative approach, microparasite species richness across rodent species according to the latitude where they occur. We also explored the links between rodents’ reproductive traits, latitude and microparasite species richness. We find for the first time in rodents that virus species richness increases towards tropical latitudes, and that rodent litter size seems to decrease when microparasite species richness increases independently from the latitude. These results support the hypotheses that rodent species in the tropics effectively harbour higher parasite species loads, at least in terms of species richness for viruses, and that parasite species richness influences rodent life‐history traits. Although some other factors, such as seasonality, were not taken into account due the lack of data, our study stresses the idea that chronic microparasite infections may have detrimental effects on their rodent host reservoirs, notably by affecting litter size.     

Lousy grouse: Comparing evolutionary patterns in Alaska galliform lice to understand host evolution and host–parasite interactions

Understanding both sides of host–parasite relationships can provide more complete insights into host and parasite biology in natural systems. For example, phylogenetic and population genetic comparisons between a group of hosts and their closely associated parasites can reveal patterns of host dispersal, interspecies interactions, and population structure that might not be evident from host data alone. These comparisons are also useful for understanding factors that drive host–parasite coevolutionary patterns (e.g., codivergence or host switching) over different periods of time. However, few studies have compared the evolutionary histories between multiple groups of parasites from the same group of hosts at a regional geographic scale. Here, we used genomic data to compare phylogenomic and population genomic patterns of Alaska ptarmigan and grouse species (Aves: Tetraoninae) and two genera of their associated feather lice: Lagopoecus and Goniodes. We used whole‐genome sequencing to obtain hundreds of genes and thousands of single‐nucleotide polymorphisms (SNPs) for the lice and double‐digest restriction‐associated DNA sequences to obtain SNPs from Alaska populations of two species of ptarmigan. We found that both genera of lice have some codivergence with their galliform hosts, but these relationships are primarily characterized by host switching and phylogenetic incongruence. Population structure was also uncorrelated between the hosts and lice. These patterns suggest that grouse, and ptarmigan in particular, share habitats and have likely had historical and ongoing dispersal within Alaska. However, the two genera of lice also have sufficient dissimilarities in the relationships with their hosts to suggest there are other factors, such as differences in louse dispersal ability, that shape the evolutionary patterns with their hosts.     

The effects of parasites on fish populations--theoretical aspects

This brief review has indicated how essential aspects of relevant epidemiological considerations may be included into models of fisheries. The main conclusions to emerge from the crude models outlined above are that the ability of a pathogen to establish itself is dependent upon the relative magnitudes of the threshold host density for parasite establishment, Ht, and the level of the host population density at its current level of exploitation H(E). If Ht is less than H(E), the parasite will always be able to establish itself. Disease prevalence would also seem to be roughly independent of the level of exploitation of the fishery, providing exploited population density is significantly higher than the threshold density for disease establishment.The complications introduced by the presence of disease will in general further increase the levels of uncertainty that fisheries managers have to contend with (Beddington, 1984). In cases where pathogens are having a serious impact on the fishery it would seem sensible to develop methods to quantify the impact of the parasite on the host (Lester, 1984). The simple models discussed here can, moreover, readily be extended to include other factors which can be important in determining management strategies for fisheries where parasites and disease are an important consideration. Three particularly important such considerations are: inclusion of age-structure and more realistic density-dependent recruitment functions in the host population (May, 1980); consideration of the immune response of the host to the parasite (Anderson &; May, 1979); and inclusion of environmental stockasticity (May, Beddington, Horwood &; Shepherd 1978; Ludwig &; Walters, 1981).     

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)