Acquired immunity protects against helminth infection in a natural host population: long-term field and laboratory evidence

Long-term records of parasite infection are rare for individuals in wild host populations. This study, on an introduced population of Xenopus laevis in Wales, demonstrates powerful control by acquired immunity of the monogenean, Protopolystoma xenopodis. Field evidence was based on a 10 year dataset for 619 individually-marked hosts screened at each capture for patent (egg-producing) infection. The adult parasite population occurred predominantly in juvenile hosts. Invasion began rapidly ‘post-birth’ (in early tadpoles). Longitudinal records for animals aged ⩾15 years showed that, after loss of this primary infection, most hosts had strong resistance to re-infection. For ca. 80% of the population, no infections were recorded during adult life; for ca. 15%, there were isolated brief episodes of patent infection; for ca. 5%, parasites persisted as repeated short-term or chronic long-term infections. Acquired immunity was confirmed by laboratory challenge infection of wild-caught X. laevis: in 30/32 exposures, no parasites survived to maturity; in the two infected, development was retarded. Parasite persistence depends principally on host recruitment generating naïve young (as in human measles). In some hosts, retarded parasite development delays reproduction for several years: these infections show ‘Typhoid Mary’ characteristics, persisting in ‘latent’ form with potential to initiate epidemics in naïve cohorts.

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► A 10 year record of patent helminth infection in up to 619 individually-marked hosts in the wild is presented.
► Infection was universal in juveniles but 80% of adults had no recorded periods of patency.
► Resistance acquired after natural infection was confirmed by laboratory challenge infection.
► There was heterogeneity in responses between individuals: 5% have chronic lifetime infections.
► Infection persists in juvenile cohorts and in a minority of adults with weak immunity.