M. E. J. Woolhouse

Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite

The adaptive trade–off theory for the evolution and maintenance of parasite virulence requires that virulence be genetically correlated with other fitness characteristics of the parasite. Many theoretical models rely on a positive correlation between virulence and transmissibility. They assume that high parasite replication rates are associated with a high probability of transmission (and, hence, increased parasite fitness), but also with high levels of damage to the host (high virulence). Schistosomes are macroparasites with an indirect life cycle involving a mammalian and a molluscan host. Here we demonstrate, through the development of five substrains, a genetic basis for schistosome virulence. We used these substrains further in order to investigate the presence of parasite fitness traits that were genetically correlated with virulence. High virulence in the (mouse) definitive host was, as predicted, positively correlated with parasite replication. In contrast, in the (snail) intermediate host high virulence was associated with low parasite replication rates. Variation in infectivity to and parasite replication in the definitive host was suggested as a compensating mechanism for the maintenance of virulence in the snail host. This is the first report of a trade–off in parasite reproductive success across hosts in an indirectly transmitted macroparasite.

Host-parasite population genetics: a cross-sectional comparison of Bulinus globosus and Schistosoma haematobium

The genetic population structures of the freshwater snail Bulinus globosus and its trematode parasite Schistosoma haematobium from 8 river sites in the Zimbabwean highveld were compared using randomly amplified DNA (RAPD) markers. There was significant variability between snail populations collected at different sites, but schistosome populations only showed differentiation at a wider geographical scale (between 2 non-connected river systems). For snails, genetic distance was better correlated with proximity along rivers than absolute geographical separation. In contrast, schistosome genetic distance was better correlated with absolute geographical separation than proximity along rivers. These results are consistent with different dispersal mechanisms for snails and schistosomes and the implications for host-parasite coevolution are discussed.

Schistosoma mansoni infection in a natural population of olive baboons ( Papio cynocephalus anubis ) in Gombe Stream National Park, Tanzania

Infection with Schistosoma mansoni was studied in 5 troops of olive baboons (Papio cynocephalus amubis) in Gombe Stream National Park, Tanzania. Three troops were infected with S. mansoni. An aggregated distribution of parasites was observed among hosts. Troop membership was found to be the most significant factor influencing parasite prevalence. Age and reproductive status had no significant effect, but there was a trend for males to acquire higher levels of infection. However, age-prevalence curves showed a high infection in young baboons declining in the older baboons. Behavioural components of exposure--as measured in water-contact pattern--may be related to parasite burden. A peak shift between infection in different age-classes in the different troops was observed: troops with higher schistosome prevalences displayed an earlier peak in prevalence of infection. The baboon troop with the most contact with people showed highest prevalence of infection possibly due to longer exposure to the parasite than the other troops and/or higher host density.

Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania

A cross-sectional parasitological study of a population of wild olive baboons (Papio cynocephalus anubis), consisting of 5 troops, was conducted in Gombe Stream National Park. Baboons were individually recognizable. Information on age, sex, troop membership, reproductive status, social rank and life-history of each individual baboon could be related to parasite infection. Seven helminth taxa and 2 protozoan taxa were found. All baboons were parasitized by at least 1 taxon. Distributions of helminths were aggregated among hosts. There were significant differences among troops in the prevalence of all but 2 of the recorded helminths. Age had a significant impact on the prevalence and intensity of Strongyloides sp. No significant effect of sex on the prevalence of infection could be detected. There was some indication that female reproductive status was related to Trichuris egg output. In contrast to a previous study, no significant correlations between parasite infection and social rank could be found. Troop membership constituted the predominant factor contributing to heterogeneity of prevalence of infection. This suggests that spatial location and/or genetics may be important in determining levels of parasite infection.

Epidemiology of trypanosome infections of the tsetse fly Glossina pallidipes in the Zambezi Valley.

The epidemiology of trypanosome infections of Glossina pallidipes was studied at a riverine site in the Zambezi Valley, Zimbabwe for a period of 13 months. Over 9000 flies were captured using a single trap. These flies were dissected, screened for trypanosome infection, sexed, and aged using both wing fray and (for females) ovarian category indices. Midgut infections were identified to species using recently developed DNA probes. The overall prevalence of mature infections was 5.5%, comprising 3.1% Trypanosoma vivax-type and 2.4% T. congolense-type (which included very low prevalences of T. brucei, T. simiae and another Nannomonas species). The prevalence of infection increased with age. For T. vivax-type infections in flies aged by ovarian category this relationship could be described by a simple catalytic model assuming a constant per capita rate of infection. For T. congolense-type infections this model tended to over-estimate prevalence in older age classes, implying that the rate of infection decreases with age, and/or that infected flies have higher mortality rates, and/or that a significant fraction of the population is resistant to infection. Prevalences of infection also varied between months. This variation was more marked for T. vivax-type infections and was negatively correlated with both temperature and rainfall. The shape of the age-prevalence relationship, however, did not vary significantly between months. These observations are not fully explained by variation in the age-structure of the tsetse population and are consistent with temporal variation in the rate of infection (rather than in the trypanosome developmental period or in effects of infection on fly mortality). Possible causes of this variation are discussed.

Biased sex ratios and parasite mating probabilities

An earlier paper (May, 1977) developed a theoretical framework for exploring the consequences of dioecy for the population dynamics of schistosomes, assuming an unbiased sex ratio. This paper extends the analysis to biased sex ratios, as have been reported in practice. We consider the relationships of the mean number and distribution of uniforms among hosts, the sex ratio, and the mating system (monogamous or polygamous) to: (i) the female mating probability, Φ (ii) the prevalence of mated female worms, Ω; and (iii) the mean number of mated female worms per host, ξ

Distribution and abundance of trypanosome (subgenus Nannomonas) infections of the tsetse fly Glossina pallidipes in southern Africa

Over 10000 Glossina pallidipes tsetse flies were collected during two field studies in the Zambezi Valley, Zimbabwe and one in the Luangwa Valley, Zambia. These were screened for mature trypanosome infections and 234 dot‐blot preparations were made of infected midguts, which were screened using DNA probes or PCR with primers specific to different species or types of the trypanosome subgenus Nannomonas. Over 70% of midgut infections were successfully identified as either Trypanosoma godfreyi, T. simiae or three types of T. congolense, savannah, riverine‐forest and Kilifi. The relative abundance of species and types did not vary significantly between study locations, habitat, season or tsetse age or sex, although there were differences between DNA probe and PCR results. Mixed species and/or mixed type infections were common and were more often detected using PCR. The distribution of infections among flies was highly aggregated, but there was no tendency for multiple infections to accumulate in older flies, implying that sequential superinfection may be uncommon. Possible explanations for these patterns are discussed.

Changes in parasite aggregation with age: A discrete infection model

We present a discrete time model for age-related changes in the mean and variance of the number of helminth parasites per host. We assess the degree of aggregation as the negative binomial parameter, k, and use the model to examine the influence of various factors on changes in aggregation with host age: discrete versus continuous infection; the degree of predisposition to infection; infection rate; parasite survival rate; and the variance in exposure to infective stages. The model can produce both increases and decreases in k with host age. However, with parameter values typical of many human helminth infections, a monotonic increase in k (decrease in aggregation) with age is predicted. With an age-dependent infection rate, convex relationships between k and age are possible. These predictions are consistent with data from field studies, but differ from those of previous models which have suggested that k is independent of host age in the absence of density dependence in parasite population dynamics. Differences between the models, and some difficulties in the interpretation of field data, are discussed.

Immunoepidemiology of human schistosomes: Taking the theory into the field

Much is known about human immune responses to schistosome infection, but it has proved difficult to determine the impact of these responses on schistosome epidemiology in the field. In this paper, Mark Woolhouse compares epidemiological patterns from field data with the predictions o f simple mathematical models of different immunological processes. The comparison gives some indications as to which types of immune response may be important, and of their strength and duration. The results are consistent with a significant impact of a process similar to concomitant immunity, with a possible role for anti-fecundity effects.

The epidemiology of schistosome infections of snails: taking the theory into the field

Most field studies of the epidemiology of schistosome infections of snails have been essentially descriptive in nature. Although much use has been made of epidemiological models in the interpretation of experimental studies of schistosome-snail interactions, the models have had restricted application outside the laboratory. Here, Mark Woolhouse and Steve Chandiwana make use of a theoretical framework in discussing current understanding of schistisome-snail epidemiological patterns in the field, and then consider the implications of the analysis for the control of schistosomiasis.