Host life-history and host-parasite syntopy predict resistance and tolerance to parasites

Background/Question/Methods: There is growing interest in the hypothesis that life-history traits of hosts, such as their “pace-of-life,” can predict species-level variation in resistance and tolerance to parasites. Slow-developing tadpole species generally exhibit greater syntopy with cercariae, a larval stage of parasitic trematodes, than fast-developing species. Thus, we hypothesized that the pace-of-life of tadpole species should be negatively correlated with selection pressures tadpoles experience for constitutive (always present) cercarial defenses (i.e., fast species have low selection pressures) and positively correlated with selection pressures cercariae experience for infectivity. Consequently, pace-of-life should predict the relative use of behavioral and immunological resistance and tolerance strategies for coping with cercariae and the infectivity of cercariae to hosts. To test these hypotheses, we conducted a series of experiments on nine tadpole species that varied in their pace-of-life.  We manipulated host behavior using an anesthetic, the dose of cercariae to which hosts were exposed, and cercarial exposure versus actual infections and quantified successful and unsuccessful infections in the absence of behavior (immunological resistance), tadpole anti-cercarial behaviors (behavioral resistance), mass change as a function of cercarial exposure and infections (tolerance), and cercarial infectivity.

Results/Conclusions: Tadpole behavior generally reduced parasite exposure and parasite exposure was costly even in the absence of infections. Fast-paced species relied more on behavioral resistance than slow-paced species even though slow-paced species has more effective behaviors.  Slow-paced species had better anti-parasite behaviors than fast-paced species.  Despite this, slow-paced species had higher metacercarial loads, on average, than fast-paced species, suggesting that this parasite has adaptations to infect the hosts they encounter most commonly. As hypothesized, tadpole pace-of-life was a positive predictor of investment in behavioral resistance, but was a negative predictor of tolerance, supporting the notion that fast-paced species rely more on behavioral responses whereas as slow-paced species rely more on defenses at the more constitutive end of the spectrum. Moreover, these results were robust to considerations of phylogeny and to all possible re-orderings of the three fastest- or slowest-paced species. Our results suggest that host-parasite syntopy might be a powerful predictor of the strength and type of host defense strategies against parasites.