When should a trophically transmitted parasite exploit host compensatory responses?

Parasites are known to manipulate the behavior of their hosts in ways that increase their probability of transmission. Theoretically, different evolutionary routes can lead to host manipulation, but much research has concentrated on the ‘manipulation hypothesis’ sensu stricto. Among the arsenal of host compensatory responses, however, some seem to be compatible with the parasite objectives. Another way for parasites to achieve transmission, therefore, would be to trigger specific host compensatory responses. In order to explore the conditions favoring this manipulative strategy, we developed a simulation model in which parasites may affect their hosts' behavior by using two nonmutually exclusive strategies: a manipulation sensu stricto strategy and a strategy based on the exploitation of host compensatory responses. Our model predicts that the exploitation of host compensatory responses can be evolutionary stable when the alteration improves the susceptibility to predation by final hosts without compromising host survival during parasite development. Inversely, when the behavioral modification resulting from a compensatory response conflicts with the host's interest we expect parasites to use both strategies. From this result, we conclude that the strategy based on the exploitation of host compensatory responses should be more common among nontrophically transmitted parasites. Furthermore, our findings indicate that the transmission rate of parasites in a definitive host is highest when each of the two strategies affects different traits, which supports the hypothesis that host manipulation is a multidimensional phenomenon in which each altered trait contributes independently to increase parasite transmission efficiency.