Why do parasitized hosts look different? Resolving the “chicken-egg” dilemma

Abstract

Phenotypic differences between infected and non-infected hosts are often assumed to be the consequence of parasite infection. However, pre-existing differences in hosts’ phenotypes may promote differential susceptibility to infection. The phenotypic variability observed within the host population may therefore be a cause rather than a consequence of infection. In this study, we aimed at disentangling the causes and the consequences of parasite infection by calculating the value of a phenotypic trait (i.e., the growth rate) of the hosts both before and after infection occurred. That procedure was applied to two natural systems of host–parasite interactions. In the first system, the infection level of an ectoparasite (Tracheliastes polycolpus) decreases the growth rate of its fish host (the rostrum dace, Leuciscus leuciscus). Reciprocally, this same phenotypic trait before infection modulated the future level of host sensitivity to the direct pathogenic effect of the parasite, namely the level of fin degradation. In the second model, causes and consequences linked the growth rate of the fish host (the rainbow smelt, Osmerus mordax) and the level of endoparasite infection (Proteocephalus tetrastomus). Indeed, the host’s growth rate before infection determined the number of parasites later in life, and the parasite biovolume then decreased the host’s growth rate of heavily infected hosts. We demonstrated that reciprocal effects between host phenotypes and parasite infection can occur simultaneously in the wild, and that the observed variation in the host phenotype population was not necessarily a consequence of parasite infection. Disentangling the causality of host–parasite interactions should contribute substantially to evaluating the role of parasites in ecological and evolutionary processes.