Spatial structure drives the evolution of parasites into host defense systems

Host defense systems in prokaryotes and eukaryotes often appear to be derived from the very parasites they now defend against, yet the evolutionary route for such a transition remains poorly understood. Based on the biology of integrating viruses such as temperate bacteriophages and retroviruses, we develop a multilevel eco-evolutionary framework in which within-host viral replication is treated as a public goods game over a costly, shared replication product. In well-mixed host populations, we predict convergence on a single viral strategy of intermediate replicative investment. However, when we impose spatial structure by restricting host reproduction and virus transmission to local events, the virus population diversifies into two lineages: a horizontally transmitted lineage that parasitises hosts, and a vertically transmitted hyperparasitic lineage that parasitises the horizontally transmitting viruses. The latter “hyperparasite” is a viral cheat that suppresses the replication and propagation of the parasitic virus, thereby acting as a defense system to the hosts. Local interactions concentrate the benefits of this suppression among neighbouring hosts that carry related proviruses, allowing selection on the proviral cheat as a host-level defense. Our results show that evolutionary cheating within parasite populations can drive the evolution of parasites into defense systems in spatially structured host populations.