Virulence of Mixed-Clone and Single-Clone Infections of the Rodent Malaria Plasmodium chabaudi

Abstract

Most evolutionary models treat virulence as an unavoidable consequence of microparasite replication and have predicted that in mixed-genotype infections, natural selection should favor higher levels of virulence than is optimal in genetically uniform infections. Increased virulence may evolve as a genetically fixed strategy, appropriate for the frequency of mixed infections in the population, or may occur as a conditional response to mixed infection, that is, a facultative strategy. Here we test whether facultative alterations in replication rates in the presence of competing genotypes occur and generate greater virulence. An important alternative, not currently incorporated in models of the evolution of virulence, is that host responses mounted against genetically diverse parasites may be more costly or less effective than those against genetically uniform parasites. If so, mixed clone infections will be more virulent for a given parasite replication rate. Two groups of mice were infected with one of two clones of Plasmodium chabaudi parasites, and three groups of mice were infected with 1:9, 5:5, or 9:1 mixtures of the same two clones. Virulence was assessed by monitoring mouse body weight and red blood cell density. Transmission stage densities were significantly higher in mixed- than in single-clone infections. Within treatment groups, transmission stage production increased with the virulence of the infection, a phenotypic correlation consistent with the genetic correlation assumed by much of the theoretical work on the evolution of virulence. Consistent with theoretical predictions of facultative alterations in virulence, we found that mice infected with both parasite clones lost more weight and had on average lower blood counts than those infected with single-clone infections. However, there was no consistent evidence of the mechanism invoked by evolutionary models that predict this effect. Replication rates and parasite densities were not always higher in ∗∗∗mixed-clone infections, and for a given replication rate or parasite density, mixed-clone infections were still more virulent. Instead, prolonged anemia and increased transmission may have occured because genetically diverse infections are less rapidly cleared by hosts. Differences in maximum weight loss occured even when there were comparable parasite densities in mixed- and single-clone infections. We suggest that mounting an immune response against more that one parasite genotype is more costly for hosts, which therefore suffer higher virulence.

Does investment into “expensive” tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts

“…Metabolic cost of mounting an immune response and maintenance of a competent immune system has been shown to be high (Sheldon and Verhulst 1996;Nordling et al 1998;Lochmiller and Deerenberg 2000;Moret and SchmidHempel 2000). Moreover, maintaining several different means of defence is likely more costly than sustaining one specific type of defence (Taylor et al 1998), so that hosts subjected to challenges from multiple parasites often prefer to give up their defence and to surrender rather than to spend much energy for defence (Jokela et al 2000). Metabolic cost of testes can be high as well.…”

“…This may be especially true when a host is subjected to multiple parasite challenges (Taylor et al 1998). Consequently, a host faces an evolutionary trade-off between investment into energetically demanding anti-parasitic defences and other energetically demanding systems such as development and maintenance of expensive tissues.…”

Host Specificity, Parasite Community Size and the Relation between Abundance and its Variance

“…Indeed, a host subjected to multiple challenges from multiple distantly related parasites can either mount stronger immune responses (e.g., Morand and Poulin, 2000;Møller and Rozsa, 2005) and/or increase sharply its grooming effort (e. g., Cotgreave and Clayton, 1994). However, maintaining several different means of defense is likely more costly than sustenance of one specific type of defense (Taylor et al, 1998b). As a result, the effectiveness of energy allocation to immune defense decreases as the diversity of attack types increases (Jokela et al, 2000).…”

Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages

“…The same means of defense that is effective against one parasite will not necessarily be effective against another parasite (Taylor et al 1998). Therefore, for a host inhabiting parasite-rich habitats, it should be advantageous to have the ability to cope with multiple challenges, especially if the probabilities to be attacked by different parasites are similar, although maintenance of multiple defense means is likely to be much more costly than retaining a specific type of defense (Taylor et al 1998). Nevertheless, both species in our study demonstrated similar immune responses to antigen from an unfamiliar flea species, in spite of different species richness of their natural flea assemblages.…”

“…Maintaining several different means of defense is likely more costly than sustenance of one specific type of defense (Taylor et al 1998). Consequently, host species that are exploited by a small number of specific parasites can acquire specific immune resistance against these parasites but not against other, albeit phylogenetically related parasites.…”