The many roads to parasitism: a tale of convergence

Parasitic organisms account for a large portion of living species. They have arisen on multiple independent occasions in many phyla, and thus encompass a huge biological diversity. This review uses several lines of evidence to argue that this vast diversity can be reduced to a few evolutionary end points that transcend phylogenetic boundaries. These represent peaks in the adaptive landscape reached independently by different lineages undergoing convergent evolution. Among eukaryotic parasites living in or on animals, six basic parasitic strategies are identified based on the number of hosts used per parasite generation, the fitness loss incurred by the host, and the transmission routes used by the parasites. They are parasitoids, parasitic castrators, directly transmitted parasites, trophically transmitted parasites, vector-transmitted parasites and micropredators. These show evidence of convergence in morphology, physiology, reproduction, life cycles and transmission patterns. Parasite-host body size ratios, and the relationship between virulence and intensity of infection, are also associated with the different parasitic strategies, but not consistently so. At the population level, patterns of parasite distribution among hosts are not uniform across all parasitic strategies, but are distinctly different for parasitoids and castrators than for other parasites. To demonstrate that the above six strategies defined for animal parasites are universal, comparisons are made with parasites of plants, in particular, plant-parasitic nematodes and parasitic angiosperms; these are shown to follow the same evolutionary trajectories seen among animal parasites, despite huge physiological and ecological differences between animals and plants. Beyond demonstrating the inevitable convergence of disparate lineages across biological hyperspace towards a limited set of adaptive strategies, this synthesis also provides a unifying framework for the study of parasitism.