Interactions between malaria parasites infecting the same vertebrate host.

Abstract

Several species of malarial protozoans commonly parasitize the same host population and often the same individual host. This paper reviews the evidence for interactions among such host-sharing parasites. Field studies measuring the cross-sectional prevalence of malarial species often record fewer mixed infections than expected by chance, suggesting that one parasite has excluded another or suppressed its parasitaemia to undetectable levels. Prevalences may vary reciprocally between seasons, with one species increasing in prevalence while another decreases, despite parallel increases in the transmission rates of both, again suggesting suppression of one species by another. However, longitudinal studies of individual hosts indicate that malarial parasites may also favourably affect the host environment for each other, perhaps due to their depressive effect on the immune system: this is shown by the recrudescence of a latent malarial species immediately before or after the parasitic wave of another species. The suppression hypothesis is supported by data derived from the simultaneous inoculation of two Plasmodium species into laboratory animals; many studies have shown that one or both species are suppressed. This may be mediated by competition for host cells or nutrients, or by heterologous immunity. However, the suppressed species rebounds after the other species has abated, and may show a prolonged infection. Experimental evidence that one species can facilitate the recrudescence of another is minimal, but this may reflect the paucity of investigations of this phenomenon. Laboratory studies show only minor cross-resistance between host-sharing species, which is consistent with the hypothesis that their co-occurrence has led to antigenic divergence or that species showing strong heterologous resistance cannot co-exist in the same host population. Such complementarity occurs not only with the host immune response but also with many other life-history characteristics of host-sharing parasites, such as host cell preference. I conclude that malarial species have been important in each other's evolution, particularly in the tropics where multi-species complexes are common.