Observed spatial heterogeneity in insect-vectored pathogen promotes pathogen survival

Abstract Insect-vectored plant pathogens cause massive crop yield losses worldwide. Outbreaks often have patchy incidences on both spatial and temporal scales, which are thought to be driven by external factors such as the level of heterogeneity in plant hosts and vector dispersal. Mathematical modelling of Aster Yellows phytoplasma disease spread, a vector-borne plant pathogen, predicts under the assumption of well-mixed population dynamics only one possible stable outcome: all insect vectors end up being carriers of the pathogen. This outcome is in stark contrast to multi-year datasets revealing local co-existence of carrier and non-carrier vectors. We predict however dramatically different tripartite plant-vector-pathogen dynamics when explicitly taking space into account. Spatial simulations allow to explain both the stable coexistence of carrier and non-carrier insects and the large spatial and temporal variations in disease incidence, this co-existence being driven by emergent patterning. Moreover, simulations of the eco-evolutionary progression of the infection dynamics predict an evolutionary stable state that quantitatively matches field observations and prove that empirically observed complex patterning is the inevitable evolutionary outcome of this tripartite system. We infer that the known diversity in phytoplasma effector proteins could be an evolved mechanism for pathogen survival in fast-changing environments, such as agricultural areas.