The study of parasite population dynamics has been one of the major developments in ecology over the last 15 years (Kennedy, 1975). The seminal articles of Crofton (1971) and Anderson & May (1978, 1979; May & Anderson, 1978, 1979) began this process by illustrating the potential role of parasites in regulating or destabilizing the dynamics of wildlife host populations. Since then, a variety of empirical and theoretical studies (reviewed by Grenfell & Dobson, 1995) have explored the role of parasites in natural populations. In parallel with these population dynamical developments, a growing interest in the evolutionary ecology of parasites has also led to a large literature, examining the evolutionary impact of parasites and the importance of host-parasite coevolution (Hamilton, 1982; May & Anderson, 1990; Lively & Apanius, 1995; Read et al. 1995; Herre, this volume).

Infectious agents have considerable potential to regulate or constrain the population growth of vertebrate hosts in natural habitats. A broad theoretical framework provides many insights into how the biology of the parasite and the demography of the host interact to determine this impact. It may manifest itself as a steady influence over time via stable endemic infection or in a recurrent epidemic fashion, sometimes with unpredictable intervals between epidemics depending on the generation time of the pathogen (time from infection to recovery or host death), its ability to induce lasting immunity and the population growth rate of the host species. Building on these notions, the paper focuses on recent work on the population dynamics of genetically variable pathogen populations and examines the factors that determine the evolution of virulence and the maintenance of genetic diversity in both host and pathogen. Recent research extends conventional theoretical templates to include population genetic elements and the within-host dynamics of the parasite and its interaction with the vertebrate immune system.

Whether and how microparasites such as rabies persist in their host populations are among the fundamental questions of infectious disease epidemiology. Rabies is a fatal disease of all mammalian species, but not all mammalian species can maintain the infection as reservoirs. The approach to control depends on which of the affected species do act as reservoirs. Bringing together old and new data, we examine here the role of wild and domestic animals in maintaining rabies in the Serengeti region of Tanzania, presenting our findings in two parts. In Part I, we argue that domestic dogs are the likely reservoirs because: (1) rabies has been continuously present in the dog population since its (re)introduction in 1977, whilst (2) wildlife cases have been very rare over this period, despite intensive study of Serengeti carnivores; (3) outbreaks of rabies in wild canids (jackals) elsewhere in Africa (Zimbabwe) have followed, rather than preceded, outbreaks in the dog population; (4) all viruses isolated from wild carnivores in the Serengeti ecosystem (including the Kenyan Masai Mara) are antigenically and genetically indistinguishable from the typical domestic dog Strain; (5) dog rabies control in the Serengeti between 1958–77 apparently eliminated the disease from both dogs and wildlife. Having identified dogs as reservoirs, Part II explores some possible mechanisms of maintenance in dog populations. In theory, infection is more likely to be maintained at higher dog densities, and we provide evidence that rabies is maintained in one district with a dog density > 5/km2, but not in two other districts with densities < 1/km2. Because 5 dogs/km2 is much lower than the expected density required for persistence, we go on to investigate the role of atypical infections, showing: (1) from serology, that a substantial proportion of healthy dogs in the Serengeti have detectable serum levels of rabies-specific antibody; (2) from mathematical models that, whilst we cannot be sure what seropositivity means, persistence in low-density dog populations is more likely if seropositives are infectious carriers, rather than slow-incubators or immunes.

The population dynamics of tick-borne disease agents and in particular the mechanisms which influence their persistence are examined with reference to the flavivirus that causes louping-ill in red grouse and sheep. Pockets of infection cause heavy mortality and the infection probably persists as a consequence of immigration of susceptible hosts. Seroprevalence is positively associated with temporal variations in vectors per host, although variation between areas is associated with the abundance of mountain hares. The presence of alternative tick hosts, particularly large mammals, provides additional hosts for increasing tick abundance. Grouse alone can not support the vectors and the pathogen but both can persist when a non-viraemic mammalian host supports the tick population and a sufficiently high number of nymphs bite grouse. These alternative hosts may also amplify virus through non-viraemic transmission by the process of co-feeding, although the relative significance of this has yet to be determined. Another possible route of infection is through the ingestion of vectors when feeding or preening. Trans-ovarial transmission is a potentially important mechanism for virus persistence but has not been recorded with louping-ill and Ixodes ricinus. The influence of non-viraemic hosts, both in the multiplication of vectors and the amplification of virus through non-viraemic transmission are considered significant for virus persistence.

Native Hawaiian forest birds are facing a major extinction crisis with more than 75% of species recorded in historical times either extinct or endangered. Reasons for this catastrophe include habitat destruction, competition with non-native species, and introduction of predators and avian diseases. We tested susceptibility of Iiwi (Vestiaria coccinea), a declining native species, and Nutmeg Mannikins (Lonchura punctulata), a common non-native species, to an isolate of Plasmodium relictum from the island of Hawaii. Food consumption, weight, and parasitaemia were monitored in juvenile Iiwi that were infected by either single (low-dose) or multiple (high-dose) mosquito bites. Mortality in both groups was significantly higher than in uninfected controls, reaching 100% of high-dose birds and 90% of low-dose birds. Significant declines in food consumption and a corresponding loss of body weight occurred in malaria-infected birds. Both sex and body weight had significant effects on survival time, with males more susceptible than females and birds with low initial weights more susceptible than those with higher initial weights. Gross and microscopic lesions in malaria fatalities included massive enlargement of the spleen and liver, hyperplasia of the reticuloendothelial system with extensive deposition of malarial pigment, and overwhelming anaemia in which over 30% of the circulating erythrocytes were parasitized. Nutmeg Mannikins, by contrast, were completely refractory to infection. Our findings support previous studies documenting high susceptibility of native Hawaiian forest birds to avian malaria. This disease continues to threaten remaining high elevation populations of endangered native birds.

Nosema pyrausta is an important microsporidian pathogen of the European corn-borer, Ostrinia nubilalis (Pyralidae), a major pest of corn (maize). The population dynamics of the interaction between the moth and its pathogen have been studied previously using simple models phrased as coupled differential equations, and using large simulation models containing over 150000 coupled equations. A middle approach is adopted here and the interaction studied using an age-structured model written as a system of delay-differential equations. Although the model contains twenty four parameters, estimates for twenty of these were available in the literature. Our model provides a good qualitative match to observed within and between season dynamics and suggests which aspects of the interaction are most important in determining the nature of the system's population dynamics. More generally, we argue that in the absence of better data on insect-disease interactions in natural habitats, valuable insights can be gained by studying equivalent systems in agro-ecosystems. We also argue that models of intermediate complexity that incorporate considerable detail about the natural history of individual interactions, but which are derived from the classical models of animal ecology and epidemiology, offer the most profitable way of modelling insect-pathogen interactions in the wild.

Vertically transmitted parasites are transmitted from generation to generation of hosts usually via the host's gametes. Owing to gamete size dimorphism, the major transmission route is transovarial and selection (on the parasite) favours strategies which increase the relative frequency of the transmitting (female) host sex. These strategies impose unusual selection pressures on the host, and coevolution between hosts and vertically transmitted parasites has been implicated in speciation, in the evolution of symbiosis, and in the evolution of novel systems of host reproduction and sex determination. We review the evolutionary implications of vertically transmitted parasites in arthropods before focusing on strategies of transmission of a parasitic sex ratio distorter in Gammarus duebeni. The efficiency of parasite transmission to new hosts is a key factor underlying the relationship between vertically transmitted parasites and their hosts. Vertically transmitted parasites must overcome 2 bottlenecks in order to ensure successful infection of future host generations: first, transmission from adult to gamete; and secondly, transmission to the germ-line of the infected host. We investigate these 2 processes with regard to transovarial transmission by a microsporidian parasite in Gammarus duebeni. Parasite transmission from adult to eggs is highly efficient, with 96% of eggs of infected mothers inheriting the infection, whereas transmission to germ-line within infected embryos is relatively inefficient (72%). We measure parasite distribution between cells of developing embryos, and use these distributions to infer possible mechanisms of parasite transmission to germ-line. Parasite distribution within the embryo is dependent on host cell lineage, and is not consistent with unbiased segregation between daughter cells. These results indicate that parasites segregate together at host cell division, and may reflect a strategy of differential segregation to the host germ-line. We consider alternative parasite strategies at the cell-level in terms of their evolutionary implications.

In this paper we review the published literature on patterns of abundance and aggregation of macroparasites in wildlife host populations. We base this survey on quantitative analyses of mean burden and a number of measures of the degree of aggregation of parasite burdens between hosts. All major parasite and vertebrate host taxa were represented in the database. Mean parasite burden was found to be log-normally distributed, indicating that all parasite burdens are regulated to some degree. In addition, all but one of the parasitic infections were aggregated with respect to their hosts, and the relationship between log mean parasite burden and log variance was found to be very strong (R2 = 0·87). That is, for a given mean parasite burden there are constraints on the degree of variation in individual host burdens. The aggregated nature of the parasitic infections is also apparent from other measures of the degree of aggregation: prevalence – mean relationships, and the negative binomial parameter, k. Using a relatively new technique for parasitological infection data – tree-based models, as well as traditional linear models – a number of the parasitic infections was found to be associated with systematically lower or higher parasite burdens. Possible biological explanations for these and other patterns are proposed.

The characteristically aggregated frequency distribution of macroparasites in their hosts is a key feature of host–parasite population biology. We begin with a brief review of the theoretical literature concerning parasite aggregation. Though this work has illustrated much about both the sources and impact of parasite aggregation, there is still no definitive analysis of both these aspects. We then go on to illustrate the use of one approach to this problem – the construction of Moment Closure Equations (MCEs), which can be used to represent both the mean and second moments (variances and covariances) of the distribution of different parasite stages and phenomenological measures of host immunity. We apply these models to one of the best documented interactions involving free-living animal hosts – the interaction between trichostrongylid nematodes and ruminants. The analysis compares patterns of variability in experimental infections of Teladorsagia circumcincta in sheep with the equivalent wildlife situation – the epidemiology of T. circumcincta in a feral population of Soay sheep on St Kilda, Outer Hebrides. We focus on the relationship between mean parasite load and aggregation (inversely measured by the negative binomial parameter, k) for cohorts of hosts. The analysis and empirical data indicate that k tracks the increase and subsequent decline in the mean burden with host age. We discuss this result in terms of the degree of heterogeneity in the impact of host immunity or parasite-induced mortality required to shorten the tail of the parasite distribution (and therefore increase k) in older animals. The model is also used to analyse the relationship between estimated worm and egg counts (since only the latter are often available for wildlife hosts). Finally, we use these results to review directions for future work on the nature and impact of parasite aggregation.

This review considers three case studies based on macroparasites of anurans: (a) natural infections in the permanently-aquatic Xenopus laevis which represent the worm burdens acquired, and the implications for pathology, when hosts are exposed to continuous, year-round, transmission; (b) the desert toad, Scaphiopus couchii, which experiences invasion very briefly each year and provides a simplified system involving only a single significant infection (Pseudodiplorchis americanus); (c) the mesic Bufo bufo which has been the subject of experimental laboratory studies designed to measure the effects of Rhabdias bufonis infection on host growth, physical performance and survival. Experimental manipulation of both Scaphiopus and Bufo provide quantitative data on disease effects of macroparasites, including precise measurements of parasite-induced host mortality. Field data for Xenopus and Scaphiopus show that, despite high initial worm burdens from efficient transmission, infection levels at parasite maturity are modulated below those leading to significant disease. Experimental data for Scaphiopus and Bufo have documented the time-course and magnitude of this decline in intensities, and there is circumstantial evidence for Scaphiopus that this regulation is host-mediated. Immunological studies on Xenopus show that disease effects of the pathogenic Pseudocapillaroides xenopodis are exacerbated in thymectomised hosts and reversed by implantation of thymuses from MHC-compatible donors. Thus, whilst factorial experiments can demonstrate the potential of helminths to cause significant disease and mortality in anuran host-macroparasite interactions, powerful post-invasion regulation of worm burdens appears to exert a strong control of parasite-induced disease in natural host populations.

The natural history of fig-pollinating wasps and their associated species-specific nematodes allows the measurement of many parameters which are relevant to testing hypotheses concerning host-parasite ecology and evolution. Within fig wasps species, it is possible to estimate lifetime reproductive success of foundress wasps as a function of presence or absence of nematode parasitism (virulence). Across species, there is a wide range of host population structures which, in turn, results in a range of opportunities for either horizontal or vertical nematode transmission. Therefore, estimates of virulence can be related to opportunities for transmission across a group of closely related hosts and their parasites. Further, the dynamics of the nematode infections over ecological and short-term evolutionary timescales can be monitored, giving added insight into the interpretation of the virulence estimates. Moreover, several scales of longer term evolutionary relationships are either known directly from fossil evidence or can be inferred from molecular data, providing deeper temporal context for the observed patterns. This combination of attributes permits detailed testing of hypotheses concerning the factors that potentially influence the evolution of virulence in host-parasite systems, and further, population and simulation models of the system that incorporate the parameter estimates can clarify the interpretation of how those factors act. There is little evidence suggesting that intermediate and long-term evolutionary relationships explain current levels of virulence. That is, it appears that virulence can change rapidly relative to speciation events, and that the nematodes do not tend to become ‘benign over time’. Instead, it appears that host population structure can influence the evolution of parasite virulence by affecting the relative opportunities for horizontal to vertical transmission, which, in turn, influences the relative costs and benefits of virulence to the nematodes. At one level, increased opportunities for horizontal transmission decouple the reproductive interests of the individual nematodes from those of the individual hosts that they are directly parasitizing, thereby reducing the cost of virulence to individual nematodes. At another level, increased opportunities of horizontal transmission also increases the relative frequency of hosts infected by multiple strains of nematodes. This promotes the evolution of more virulent forms by increasing the relative importance of within-host competition among nematode strains, thereby favouring strains that ‘eat more host sooner’. An interesting property of the fig-nematode systems is that the proportion of infected hosts does not change dramatically through time. This finding implies that there can be considerable negative effects on survival of infected hosts in addition to the previously documented reductions in fecundity of infected foundresses, because the latter are insufficient to account for the observed stability of wasp infection rates.