Parasitic manipulations may determine the fate of ecosystems

The ecological importance of parasites has been increasingly recognized. Beyond effects on host survival and longevity, parasites induce phenotypic changes in their hosts that alter species interactions. Such changes are often called parasitic manipulations, a common phenomenon in which parasites alter the phenotypes of their hosts to increase their own fitness. In my manuscript, I introduce the idea that parasitic manipulations can determine the fate of ecosystems by directing them towards alternative stable states. Starting from a solitary, stochastic infection event, parasitic manipulations can generate positive feedback loops that practically irreversibly push an ecosystem along divergent developmental pathways. The specific path taken depends on the transmission strategy of the manipulative parasite colonizing the naïve community first. Using three ecologically realistic scenarios, I demonstrate how particular manipulative strategies can drive the assembly of communities that are virtually resistant to the invasion of alternative manipulative strategies. Furthermore, I outline how ecosystems, which I call ‘naïve to parasites’, arise and explain why such scenarios are likely to become more frequent in the Anthropocene, making parasitic manipulations increasingly important drivers of ecosystem dynamics. I then discuss possible empirical tests of this hypothesis and its potential limitations. Finally, I position my hypothesis within established ecological theory such as ecosystem engineering, regime shift theory, and the manipulative microbiome hypothesis.