Current theories assume that adaptive parasite evolution explains variation in the level of virulence and parasite success. In particular, mixed-genotype infections by parasites should generally be more virulent, and faster multiplying strains more successful, either because fixed strategies have evolved or because parasites facultatively alter virulence in response to co-infecting competitors. We compared several measures of parasite success and virulence between single-clone and mixed-clone infections of 2 strains of the trypanosome Crithidia bombi in its bumblebee host, Bombus terrestris. Contrary to expectation, we could not find differences between single-clone and mixed-clone infections in parasite prevalence, infection success, duration and clearance rate. However, a clearly significant effect of colony on infection intensity was present, and the colony effect emerged in virtually all other measures. We thus conclude that host environment as defined by the family (colony) genotype and thus host heterogeneity are more important in determining parasite virulence than the parasite characteristics. This does not invalidate modern theories of parasite evolution but suggests that variation in both hosts and parasites must be taken into account in more detail.