Lack of Vertical Transmission of Grapevine Red Blotch Virus by Spissistilus festinus and Sex-Associated Differences in Horizontal Transmission

Grapevine red blotch is an emerging disease that threatens vineyard productions in North America. Grapevine red blotch virus (GRBV, species <i>Grablovirus vitis</i>, genus <i>Grablovirus</i>, family <i>Geminiviridae</i>), the causal agent of red blotch disease, is transmitted by <i>Spissistilus festinus</i> (Hemiptera: Membracidae) in a circulative, non-propagative mode. To gain new insight into GRBV-<i>S. festinus</i> interactions, we delved into vertical transmission and documented a lack of transovarial transmission. In addition, we investigated <i>S. festinus</i> sex differences in the horizontal transmission of GRBV by creating small arenas with 30 detached trifoliates of common snap bean, an experimental host of GRBV, and a preferred feeding host of <i>S. festinus</i>. Tracking the movement of viruliferous males, females, or a combination of the two sexes over two weeks in replicated experiments demonstrated that male <i>S. festinus</i> dispersed more than females with specimens of both sexes predominantly grouping together on trifoliates spatially surrounding the trifoliate onto which they were released. These behaviors resulted in a greater rate of GRBV transmission by <i>S. festinus</i> males (17%, 20 of 120) than females (4%, 5 of 120) or mixed-sex cohorts (9%, 17 of 180). In arenas with aviruliferous <i>S. festinus</i> and one (single) or four (hotspot) GRBV-infected trifoliates out of 30 total trifoliates, a higher GRBV transmission rate by males was confirmed in both single infection (50%, 30 of 60) and hotspot infection (83%, 50 of 60) arenas than by females in single infection (35%, 21 of 60) and hotspot infection (67%, 40 of 60) arenas. These findings highlighted sex-associated differences in the transmission of GRBV by <i>S. festinus</i> and a positive correlation between the initial virus prevalence and the rate of transmission. Finally, the secondary spread of GRBV resulted primarily from <i>S. festinus</i> dispersal by walking or jumping. Together, these unique GRBV transmission features support the need to characterize dispersal behaviors of <i>S. festinus</i> in vineyard ecosystems.