Strong density-dependent competition and acquired immunity constrain parasite establishment: Implications for parasite aggregation

• Published in: International journal for parasitology Vol. 41; no. 5; pp. 505 - 511
• Main Authors: Luong, Lien T., Vigliotti, Beth A., Hudson, Peter J.
• Format: Journal Article
• Language: English
• Published: Kidlington Elsevier Ltd 01.04.2011; Elsevier
• Subjects: Adaptive Immunity; Aggregation; Animals; Biological and medical sciences; Challenge infection; Complex life cycle; Density dependence; Disease Models, Animal; Fundamental and applied biological sciences. Psychology; Gryllidae - parasitology; Host-Parasite Interactions; hosts; Humans; immune response; immunoglobulin G; Insect Vectors - parasitology; Life cycle. Host-agent relationship. Pathogenesis; Male; Mammalia; Mice; Nematoda - growth & development; Nematoda - immunology; Nematoda - physiology; Nematode Infections - immunology; Nematode Infections - parasitology; parasites; Peromyscus; Peromyscus leucopus; Protozoa; Trophic transmission; Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution; Aggregation; Density dependence; Trophic transmission; Challenge infection; Complex life cycle; Peromyscus; Competition; Acquired immunity; Rodentia; Transmission; Parasite; Trophic relation; Strong; Infection; Life cycle; Vertebrata; Mammalia
• ISSN: 0020-7519; 1879-0135
• DOI: 10.1016/j.ijpara.2010.12.003

[Display omitted] ► Strong density-dependence generates exceptional parasite distribution. ► Hosts develop acquired immunity against parasites with a complex life cycle. ► The ability to mount immune memory is also density-dependent. ► Worm size and immune IgG levels also support this conclusion. The vast majority of parasites exhibit an aggregated frequency distribution within their host population, such that most hosts have few or no parasites while only a minority of hosts are heavily infected. One exception to this rule is the trophically transmitted parasite Pterygodermatites peromysci of the white-footed mouse (Peromyscus leucopus), which is randomly distributed within its host population. Here, we ask: what are the factors generating the random distribution of parasites in this system when the majority of macroparasites exhibit non-random patterns? We hypothesise that tight density-dependent processes constrain parasite establishment and survival, preventing the build-up of parasites within individual hosts, and preclude aggregation within the host population. We first conducted primary infections in a laboratory experiment using white-footed mice to test for density-dependent parasite establishment and survival of adult worms. Secondary or challenge infection experiments were then conducted to investigate underlying mechanisms, including intra-specific competition and host-mediated restrictions (i.e. acquired immunity). The results of our experimental infections show a dose-dependent constraint on within-host–parasite establishment, such that the proportion of mice infected rose initially with exposure, and then dropped off at the highest dose. Additional evidence of density-dependent competition comes from the decrease in worm length with increasing levels of exposure. In the challenge infection experiment, previous exposure to parasites resulted in a lower prevalence and intensity of infection compared with primary infection of naïve mice; the magnitude of this effect was also density-dependent. Host immune response (IgG levels) increased with the level of exposure, but decreased with the number of worms established. Our results suggest that strong intra-specific competition and acquired host immunity operate in a density-dependent manner to constrain parasite establishment, driving down aggregation and ultimately accounting for the observed random distribution of parasites.