Prevalence of infection as a predictor of multiple genotype infection frequency in parasites with multiple‐host life cycle

Abstract

In nature, parasites commonly share hosts with other conspecific parasite genotypes. While adult parasites typically show aggregated distribution in their final hosts, aggregation of clonal parasite genotypes in intermediate hosts, such as those of trematodes in molluscs, is not generally known. However, infection of a host by multiple parasite genotypes has significant implications for evolution of virulence and host-parasite coevolution. Aggregated distribution of the clonal stages can increase host mortality and reduce larval output of each infecting genotype through interclonal competition, and therefore have significant implications for parasite epidemiology. The aim of this study was (i) to find out how common multiple genotype infections (MGIs) are in aquatic snails serving as intermediate hosts for different trematode species; (ii) to find out whether the prevalence of infection could be used to predict MGI frequencies and (iii) to use the relationship to infer whether MGIs aggregate in molluscan hosts. We determined the prevalence of trematode (Diplostomum pseudospathaceum) infections and the frequency of MGIs in snail (Lymnaea stagnalis) host populations as well as compiled corresponding literature data from a range of snail-trematode systems. We used Bayesian simulations to explore the relationship between prevalence of infection and MGI frequency in these data, and tested whether genotypes aggregate in snails by comparing the simulated relations with null model (Poisson and demographic Poisson) expectations. Our results show that MGIs are common in aquatic snails with up to 90% of the infected snails carrying MGIs. Parasite prevalence is a good predictor of MGI frequencies at a range of prevailing natural prevalences of infection (0-50%). The frequency of MGIs was higher than expected by both null models, indicating parasite aggregation at genotype level. These findings are in sharp contrast with the absence of multiple infections in snails at level of trematode species, suggesting that co-infections by multiple species and multiple genotypes of one species are controlled by different biological processes. Aggregation of MGIs in snail hosts appears to be widespread across different snail-trematode systems.