Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses

Abstract

Summary: 1.Vector‐borne pathogens and parasites can induce changes in the phenotypes of their hosts that influence the frequency and nature of host–vector interactions and hence transmission, as documented by both empirical and theoretical studies. To the extent that implications for transmission play a significant role in shaping the evolution of parasite effects on host phenotypes, we may hypothesize that parasites exhibiting similar transmission mechanisms – and thus profiting from similar patterns of interaction among hosts and vectors – will have correspondingly similar effects on relevant host traits. Here, we explore this hypothesis through a survey and synthesis of literature on interactions among plant viruses, their hosts, and insect vectors. 2.Insect‐vectored plant viruses that differ in their modes of transmission benefit from different patterns of interaction among host plants and vectors. The transmission of persistently transmitted (PT) viruses requires that vectors feed on an infected host for a sustained period to acquire and circulate (and sometimes replicate) virions, then disperse to a new, healthy host. In contrast, non‐persistently transmitted (NPT) viruses are effectively transmitted when vectors briefly probe infected hosts, acquiring virions, then rapidly disperse. 3.Based on these observations, and empirical evidence from our previous work, we hypothesized that PT and NPT viruses will exhibit different effects on aspects of host phenotypes that mediate vector attraction to, arrestment on and dispersal from infected plants. Specifically, we predicted that both PT and NPT viruses would tend to enhance vector attraction to infected hosts, but that they would have contrasting effects on vector settling and feeding preferences and on vector performance, with PT viruses tending to improve host quality for vectors and promote long‐term feeding and NPT viruses tending to reduce plant quality and promote rapid dispersal. 4.We evaluated these hypotheses through an analysis of existing literature and found patterns broadly consistent with our expectations. This literature synthesis, together with evidence from other disease systems, suggests that transmission mechanisms may indeed be an important factor influencing the manipulative strategies of vector‐borne pathogens, with significant implications for managing viral diseases in agriculture and understanding their impacts on natural plant communities.