Evolution of host manipulation specificity in trophically transmitted parasites

Trophically transmitted parasites frequently alter the phenotype of their intermediate host to increase predation by the next host in the life cycle. Still, the degree to which such manipulation is specific to the correct predator varies widely across systems. Some parasites employ mechanisms that selectively increase vulnerability to the next host, whereas others increase predation indiscriminately, exposing the parasite to dead-end predators. Despite growing empirical documentation of this variation, no theoretical model has addressed the evolution of manipulation specificity itself. Here, I develop a general analytical model in which a trophically transmitted parasite evolves two traits simultaneously: manipulation intensity and manipulation leakage-the degree to which parasite-induced changes in host vulnerability extend to non-host predators. The parasite faces three competing outcomes in its intermediate host: predation by the suitable next host (transmission), predation by non-host predators (dead end), and natural non-predation mortality. I derive the condition for manipulation to be favoured, obtain the joint evolutionarily stable strategy for intensity and leakage, and provide an analytical approximation for the equilibrium. The model reveals that although dead-end predation creates the selective incentive for specificity, specificity evolves only when the fecundity costs of achieving it are sufficiently low. This condition is determined by the manipulation pathway, not by the intensity of non-host predation.