Conditions for invasion and persistence of a satellite that does not affect the replication and virulence of its helper virus

ABSTRACT

Satellites are subviral agents that depend on a helper virus for functions essential to complete their infection cycle, while the helper virus may infect and be transmitted in the absence of the satellite. Thus, satellites are cheats that compete with the helper virus for its resources, and may modulate its replication, infection dynamics, evolution, and the coexistence among viruses. Understanding the conditions for satellite invasion and persistence is therefore relevant to understanding both the prevalence of single viruses and virus community dynamics. This is the goal of this study, centred in satellite tobacco mosaic virus (STMV), and its helper virus tobacco mild green mosaic virus (TMGMV). We use epidemiological data on STMV occurrence and infection dynamics in TMGMV-infected Nicotiana glauca populations, and experimentally estimate relevant parameters to feed models that predict STMV invasion and persistence conditions. We show that under field conditions STMV has no significant effects on TMGMV accumulation or pathogenesis in N. glauca. However, the presence of STMV significantly reduces the horizontal transmission rate of TMGMV, and we showed experimentally that STMV transmission occurs in only a fraction of TMGMV transmission events. Model simulations showed that a requirement for STMV invasion at realistic transmission rates was a low virulence, a condition met as shown by previous studies of the virulence of TMGMV in N. glauca. Simulations that considered variation in the density of the host plant population identified a high transmission rate as a condition for the persistence of STMV, which disappears from the TMGMV population at low plant densities. A major conclusion is that STMV interferes with TMGMV transmission despite not interfering with TMGMV accumulation. Thus, conditions favouring a high transmission rate are required for invasion and persistence of STMV, similarly to satellites that interfere with helper virus replication, suggesting these conditions may be general for other satellite-helper virus systems.