Meta‐analysis reveals strong evidence for adaptive host and vector manipulation by plant viruses

Abstract Plant viruses often enhance their own transmission by modifying host phenotypes and vector behaviour, leading to the hypothesis that such effects are manipulations due to virus adaptations. However, few studies have linked putative manipulations with virus components, and the true frequency and magnitude of host and vector manipulation across virus taxa remain unknown. We used meta‐analysis to combine data from 215 studies to quantify convergence in virus effects on host plants that influence vector orientation and feeding behaviour and performance. We compared effects across taxonomic groups of viruses that share transmission mechanism traits and thereby may benefit from similar effects on vector behaviour and performance. Our study considered virus transmission traits such as the infection location in the host (phloem vs. nonvascular tissue) and retention mechanism in vector arthropods to assess evidence for or against adaptive manipulation. We interpreted results in the context of virus taxonomic relationships, virus–vector relationships and host domestication status. Overall, virus transmission traits strongly predicted the magnitude and nature of virus effects on vector preferences and performance. Consistent with predictions that increased vector–host contacts are beneficial, we found increased attractiveness to vectors is a host change common to all virus lineages. However, enhanced vector settling and feeding on infected plants is only apparent for phloem‐restricted viruses that require vectors to engage in extended phloem feeding for acquisition. We also found that phloem‐restricted viruses are associated with enhanced vector performance on infected hosts, but only for viruses that do not replicate in vectors. Across all analyses, plant viruses rarely elicited phenotypes that negatively affect vector transmission. Our results confirm that host and vector manipulation are important aspects of plant virus ecology and evolution. However, limitations of existing studies include a focus on agriculturally important viruses and a bias toward studying virus effects in domesticated plants. Our synthesis emphasizes the need to incorporate more pathosystems and transmission traits in future studies. Read the free Plain Language Summary for this article on the Journal blog.