Peak shift and epidemiology in a seasonal host–nematode system

Abstract

Insight into the dynamics of parasite-host relationships of higher vertebrates requires an understanding of two important features: the nature of transmission and the development of acquired immunity in the host. A dominant hypothesis proposes that acquired immunity develops with the cumulative exposure to infection, and consequently predicts a negative relationship between peak intensity of infection and host age at this peak. Although previous studies have found evidence to support this hypothesis through between-population comparisons, these results are confounded by spatial effects. In this study, we examined the dynamics of infection of the nematode Trichostrongylus retortaeformis within a natural population of rabbits sampled monthly for 26 years. The rabbit age structure was reconstructed using body mass as a proxy for age, and the host age-parasite intensity relationship was examined for each rabbit cohort born from February to August. The age-intensity curves exhibited a typical concave shape, and a significant negative relationship was found between peak intensity of infection and host age at this peak. Adult females showed a distinct periparturient rise in T. retortaeformis infection, with higher intensities in breeding adult females than adult males and non-breeding females. These findings are consistent with the hypothesis of an acquired immune response of the host to a parasite infection, supporting the principle that acquired immunity can be modelled using the cumulative exposure to infection. These findings also show that seasonality can be an important driver of host-parasite interactions.

Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system

“…To simplify the present study, we removed rabbits co-infected with myxoma or Graphidium from the dataset. Previous studies on the monthly changes in T. retortaeformis intensity with rabbit age found strong seasonal patterns in both host reproduction and parasite force of infection (Cattadori et al 2005). In this rabbit population, the main reproductive season occurs between April and July.…”

“…We found there to be strong seasonal variability in the abundance of both host and parasite (Cattadori et al 2005). Cohorts of rabbits born in different months show the characteristic humpbacked relationship between parasite intensity and host age (figure 1).…”

“…In general, when temperature is below 108C development is arrested or very slow, and migration of infective larvae onto vegetation cease below 2.78C and at low humidity (Crofton 1948). Owing to this, seasonal climatic fluctuations greatly influence the abundance of larval infective stages on the pasture (Cattadori et al 2005(Cattadori et al , 2007a.…”

“…Cohorts of rabbits born in different months show the characteristic humpbacked relationship between parasite intensity and host age (figure 1). In our rabbit-nematode system, it is apparent that the force of infection varies throughout the year, such that rabbits born in different months experience different infection rates, and while the ageintensity profiles have similar shape they differ in the peak intensity (Cattadori et al 2005). When comparing the age-intensity relationship of different cohorts we find a significant peak shift effect, giving good grounds to suppose that wild rabbits mount an acquired immune response to T. retortaeformis infection and that the strength of the response depends on the individual's history of exposure (Cattadori et al 2005).…”

“…This produces a negative relationship between host age and parasite intensity at the peak of infection, a phenomenon known as the 'peak shift' effect ( Woolhouse 1998). A shift in the age at the peak of infection with a change in rate of exposure distinguishes an acquired immune response from one that simply strengthens with the host's age, or from the possibility that the humpbacked age-intensity profile is produced by parasiteinduced host mortality (Cattadori et al 2005).…”