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It is often assumed that parasitic and disease-producing organisms tend to evolve benign relationships with their hosts over time. In contrast, theoretical arguments suggest that increased opportunities for parasite transmission will promote the evolution of increased virulence. The natural history of species-specific nematodes that parasitize fig-pollinating wasps permits the testing of these predictions in natural populations. For 11 species of Panamanian fig wasps, those species characterized by population structures that result in increased opportunities for parasite transmission harbor more virulent species of nematodes. In addition, differences in population structure are also associated with differences in other intra- and interspecific phenomena, including sex ratios among the fig wasp species, the degree of tension in the wasp-fig mutualism, and lethal combat among the males of parasitic wasps.