Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi

Many parasites evolve to become virulent rather than benign mutualists. One of the major theoretical models of parasite virulence postulates that this is because rapid within-host replication rates are necessary for successfu l transmission (parasite fitness) and that virulence (damage to the host) i s an unavoidable consequence of this rapid replication. Two fundamental ass umptions underlying this so-called evolutionary trade-off model have rarely been tested empirically: (1) that higher replication rates lead to higher levels of virulence; and (2) that higher replication rates lead to higher t ransmission. Both of these relationships must have a genetic basis for this evolutionary hypothesis to be relevant. These assumptions were tested in t he rodent malaria parasite, Plasmodium chabaudi, by examining genetic relat ionships between virulence and transmission traits across a population of e ight parasite clones isolated from the wild. Each clone was injected into g roups of inbred mice in a controlled laboratory environment, and replicatio n rate (measured by maximum asexual parasitemia), virulence (measured by li ve-weight loss and degree of anemia in the mouse), and transmission (measur ed by density of sexual forms, gametocytes, in the blood and proportion of mosquitoes infected after taking a blood-meal from the mouse) were assessed . It was found that clones differed widely in these traits and these clone differences were repeatable over successive blood passages. Virulence trait s were strongly phenotypically and genetically (i.e., across clones) correl ated to maximum parasitemia thus supporting the first assumption that rapid replication causes higher virulence. Transmission traits were also positiv ely phenotypically and genetically correlated to parasitemia, which support s the second assumption that rapid replication leads to higher transmission . Thus, two assumptions of the parasite-centered trade-off model of the evo lution of virulence were shown to be justified in malaria parasites.