Host manipulation dynamics under the host manipulation hypothesis

Emerging infectious diseases occur when a pathogen colonizes a novel or previously unexposed host, a process that requires both biological capacity and ecological opportunity. Host-parasite interactions can be complex, and many pathogens are able to ”manipulate” host phenotypes and behaviors (a phenomenon known as host manipulation) in ways that enhance their transmission. In tripartite associations, such as vector-borne diseases, interactions among pathogens, vectors, and multiple hosts add an additional layer of complexity. In this work, we developed a computational model of a tripartite vector-plant-pathogen system to evaluate host colonization dynamics under scenarios of host manipulation. In vector-borne plant pathogen systems, insect vectors acquire and transmit pathogens while feeding on plant hosts. Vectors and plants exert distinctive selective pressures on the pathogen population, which can multiply, mutate, and thus diversify over time. Using an individual-based model, we performed simulations comparing a null model, where there is no preferential interaction between vectors and plants, with a model in which the pathogen's presence alters the interaction preference (host manipulation scenario). In the host manipulation scenario, the pathogen exhibited a faster colonization rate despite accumulating lower capacity (phenotypic diversity) prior to the colonization event. The frequency of host colonization under moderate misfit was also higher in this scenario, indicating that a change in interaction preference can facilitate the colonization of highly divergent hosts. Altogether, these results show that increased opportunity due to host manipulation can compensate for reduced accumulation of capacity, ultimately promoting host range expansion and increasing risk of emerging infectious diseases.