Vertical and horizontal transmission of plant viruses: two extremes of a continuum?

Abstract

Parasites have a variety of mechanisms to be transmitted to new susceptible hosts, which can be largely grouped in two main modes: vertical (i.e., from parents to the offspring) and horizontal (i.e., between hosts regardless of descent). Because between-host dispersal is a key trait for parasite fitness, scientists studying host-parasite interactions have been long interested in understanding the evolution of their transmission mode(s). Most work in this regard has been theoretical, which resulted in the development of the so-called Continuum hypothesis. This theory states that because vertically transmitted parasites require the host to reproduce, the evolution of this mode of transmission will involve reduced virulence (i.e., the effect of infection on host fecundity) in order to allow maximal host viable progeny production. Conversely, the evolution of horizontal transmission does not have this limitation and parasites with this mode of transmission will evolve higher virulence. Therefore, a trade-off between both modes of transmission across a continuum of virulence values is predicted, with each transmission mode located at the extremes of the continuum. Using plant viruses as a focal parasite, here we review existing theory surrounding the Continuum hypothesis and the experimental work testing the predictions of the theory. Finally, we briefly discuss molecular mechanisms that may explain the existence of vertical-to-horizontal transmission trade-offs and potential implications for the management of virus epidemics.