Understanding the mechanisms that generate patterns of the abundance and distribution of individuals is central in ecology and has important implications for population and evolutionary dynamics. Comparative studies of host-macroparasite relationships have shown that the vast majority of macroparasites exhibits an aggregated frequency distribution across their host populations, i. e., most hosts have few or no parasites and few hosts have the many parasites. Parasite life history traits, particularly the mode of transmission may underlie non-random patterns of distribution. For example, parasites that exhibit auto-infection tend to have much higher levels of aggregation than other macroparasites. Likewise, trophically transmitted parasites are expected to exhibit a higher degree of aggregation in the host population than parasites that are passively acquired. However, a natural host-parasite system involving a trophically-transmitted parasite (Pterygodermatites peromysci) of the white-footed mouse (Peromyscus leucopus) exhibits a random distribution within the host population. What are the factors generating the exceptional random distribution of parasites in this system when the majority of macroparasites exhibit non-random patterns? We hypothesized that the tail of the distribution is cut off because of constraints on parasite establishment within individual hosts. We first conducted primary infections in a series of laboratory experiments using the natural host to address the specific question, “Is the rate of parasite establishment constrained in a dose-dependent manner”? In addition, we investigated potential mechanisms mediating constraint or regulation of parasite numbers, including intra-specific competition and host-mediated restrictions (i.e., acquired immunity).

Results/Conclusions

The results of our experimental infections show a dose-dependent constraint on within-host parasite population establishment. The relationship between probability of infection and dose followed a quadratic function, such that the proportion of mice infected rose initially with dose, reached a plateau the dropped off at the highest dose. In a challenge infection experiment with four dose levels, we found that previous exposure to parasites resulted in a lower prevalence and intensity of infection in comparison to primary infection of naïve mice. Moreover, the outcome of the challenge experiment was dose-dependent, such that resistance to a challenge infection occurred only when the dose was moderate to high, with the strongest effect at the highest dose. Taken together, our results suggest that intraspecific competition and host immune memory are constraining parasite establishment, driving down the degree of parasite aggregation in natural host populations.