Emergence of viral diseases results from novel transmission dynamics between wild and crop plant communities. The bias of studies towards pathogenic viruses of crops has distracted from knowledge of non-antagonistic symbioses in wild plants. Here we implemented a high throughput approach to compare the viromes of melon (Cucumis melo), and wild plants of crop (Crop) and adjacent boundaries (Edge). Each of the 41-plant species examined was infected by at least one virus. The interactions of 104 virus operational taxonomic units (OTUs) with these hosts occurred largely within ecological compartments of either Crop or Edge, Edge having traits of a reservoir community. The positive correlation of virus and plant richness at each site, the tendency for increased specialist host use through seasons, and specialist host use by OTUs observed only in Crop, characterised local-scale patterns of infection. In this study of systematically sampled viromes of a crop and adjacent wild communities most hosts showed no disease symptoms, suggesting non-antagonistic symbioses are common. The coexistence of viruses within species-rich ecological compartments of agro-systems might promote the evolution of a diversity of virus strategies for survival and transmission. These communities, including those suspected as reservoirs, are subject to sporadic changes in assemblages, and so too are the conditions that favour the emergence of disease.

Host ranges of plant viruses are poorly known, as studies have focused on pathogenic viruses in crops and adjacent wild plants. High throughput sequencing (HTS) avoids the bias towards plant-virus interactions that result in disease. Here we study the host ranges of tobamoviruses, important pathogens of crops, by HTS analyses of an extensive sample of plant communities in four habitats of a heterogeneous ecosystem. Sequences of 17 virus operational taxonomic units (OTUs) matched references in the Tobamovirus genus, eight had narrow, and five had wide host ranges. Regardless of host range, each OTU host belonged to taxonomically distant families, suggesting no phylogenetic constraints in host use associated with virus adaptation, and that tobamoviruses may be host generalists. The OTUs identified as TMGMV, TMV, PMMoV and YoMV, had the largest realized host ranges that occurred across habitats, and exhibited host use unrelated to the degree of human intervention. This result is at odds with assumptions that contact transmitted viruses would be more abundant in crops than in wild plant communities, and could be explained by effective seed, contact, or pollinator-mediated transmission, or by survival in the soil. TMGMV and TMV had low genetic diversity that was not structured according to habitat or host plant taxonomy, which indicated that phenotypic plasticity allows virus genotypes to infect new hosts with no need for adaptive evolution. Our results underscore the relevance of ecological factors in host range evolution, in addition to the more often studied genetic factors.