A synthesis of virus-vector associations reveals important deficiencies in studies on host and vector manipulation by plant viruses

Plant viruses face many challenges in agricultural environments. Although crop fields appear to be abundant resources for these pathogens, it may be difficult for viruses to "escape" from crop environments prior to host senescence or harvesting. One way for viruses to increase the odds of persisting outside of agricultural fields across seasons is by evolving traits that increase transmission opportunities between crops and wild plant communities. There is accumulating evidence that some viruses can achieve this by manipulating crop plant phenotypes in ways that enhance transmission by vectors. Putative manipulations occur through alteration of plant cues (color, size, texture, foliar volatiles, in-leaf metabolites, defenses, and leaf cuticles) that mediate vector orientation, feeding, and dispersal behaviors. Virus effects on host phenotypes are not uniform but appear to exhibit convergence depending on virus traits underlying transmission, particularly the duration of probing and feeding required to acquire and inoculate distinct types of plant viruses. This shared congruence in manipulation strategies and mechanisms across divergent virus lineages suggests that such effects may be adaptive. To discern if this is the case, researchers must consider molecular and environmental constraints on virus evolution, including those imposed by insect vectors from organismal to landscape scales. In this review, we synthesize applied research on vector-borne virus transmission in laboratory and field settings to identify the main factors determining transmission opportunities for plant viruses, and thus, selection pressure to evolve manipulative traits. We then examine these outputs in the context of studies reporting putative instances of plant virus manipulation. Our synthesis reveals important disconnects between virus manipulation studies and actual selection pressures imposed by vectors in real-world contexts.