From settler gardens to digital naturalists: human aesthetic preferences and land use changes facilitate the biogeographical expansion of a wild plant–virus interaction

Societal Impact Statement Anthropogenic facilitation of wild plants based on aesthetic preferences for particular traits can change the biogeography and ecology of natural communities. We use a mixed‐methods socioecological approach to characterize the ways in which humans interact with a common, widely distributed plant and a generalist viral symbiont that induces an aesthetically favored floral phenotype. Emergence of viral diseases that spread from wild to cultivated plant hosts causes yield loss, while viruses that spread from cultivated plants to wild hosts may also have conservation impacts. It is crucial to assess how human behaviors and preferences influence wild plant–virus interactions, particularly in mixed agricultural landscapes. Summary Humans indirectly and directly facilitate the spread and persistence of plant viruses that induce flower‐breaking phenotypes. Historical records and distribution modeling provide evidence of human‐mediated plant range expansions, but more information is needed to determine the consequences of anthropogenic drivers on plant–virus biogeographical trends. We use a mixed‐methods approach to understand how human aesthetic preferences have impacted the occurrence and range expansion of the weedy plant species Hesperis matronalis , and its common pathogenic symbiont turnip mosaic virus (TuMV). This work integrates spatial distribution modeling of virus occurrences at local and regional scales, sociological surveys, and sentiment analyses of naturalist social media data to characterize how people perceive both host and virus‐induced phenotypes over time and space. We show that people prefer the virus‐induced floral phenotype for H. matronalis and interact with uninfected hosts in a commensal or facilitative way. We also show that general perceptions of a widespread, introduced host species are positive and that the ecological niche in which the host–virus symbiosis occurs is defined by human activities. In the specific Hesperis ‐turnip mosaic virus (TuMV) pathosystem, seed distribution, habitat change, and indirect selection are likely anthropogenic mechanisms through which TuMV expands and persists across North American host populations.