Nazir SA, Ashby B, Leeks A & van Dijk B
Abstract
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.