Evidence for host variation in parasite tolerance in a wild fish population

Abstract

Hosts can protect themselves against parasites by actively reducing parasites burden (i.e. resistance) or by limiting the damages caused by parasites (i.e. tolerance). Disentangling between tolerance and resistance is important for predicting the evolutionary outcomes of host-parasite interaction. Dace (Leuciscus leuciscus) are often parasitized by the ectoparasite Tracheliastes polycolpus which feeds on (and destroys) fins, reducing thus the host's condition. We tested the hypothesis that genetically-based variation in ectoparasite tolerance exists in a wild dace population. We found that moderately heterozygous dace, which are less resistant than highly heterozygous or homozygous dace, tolerated better the effect imposed by T. polycolpus for a given parasite burden. However, tolerance also varied upon environmental conditions, suggesting that genetic and environmentallybased variation exists for both resistance and tolerance in this natural host-parasite system. Moreover, a negative genetic correlation may exist between tolerance and resistance, and hence several evolutionary outcomes are possible in this interacting system.

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

“…water velocity, water temperature, etc.). Overall, this observation is in agreement with recent studies demonstrating a strong role of the environment in explaining variation in resistance and tolerance [14,25]. For instance, in the Leuciscus-Tracheliastes interactions, Cardon et al [31] demonstrated that fin degradation tended to be higher under colder conditions, possibly owing to more virulent parasites or reduced tolerance under these thermal conditions.…”

“…Because body size is highly correlated to age in fishes, and because parasites can accumulate over time on a host, we added dace body size (a continuous trait) as a fixed covariate in the models. Parasite burden was also included as a fixed covariate in the tolerance models to measure fin degradation while statistically accounting for the number of parasites [13,14,29]. Afterwards, inclusive heritability (H ) was calculated as the ratio of the estimated transmitted variance to total phenotypic variance (i.e.…”

“…2013, unpublished data), and it is hence likely that the Leuciscus -Tracheliastes interaction has not yet reached its evolutionary equilibrium. However, interindividual variation in both resistance and tolerance to this parasite has been detected in dace, and this variation has been suggested to be-at least partially-under genetic control [14,23]. We first reconstructed a dace pedigree using genetic markers to estimate relatedness among sampled individuals [24].…”

Genetic variation in resistance, but not tolerance, to a protozoan parasite in the monarch butterfly

“…This study also found a negative relationship between resistance and tolerance, suggesting a trade-off between these two defence strategies. This finding is consistent with theoretical considerations ( [14,22,34]; but see [35]) and also supported by a recent study that showed that moderately heterozygous dace were less resistant but more tolerant to infection than highly heterozygous or homozygous dace [33,36].…”

“…Linear mixed models were used to analyse the effect of inoculation dose, monarch family and sex on parasite spore load, and to assess the effect of inoculation dose/parasite spore load, monarch family and sex on monarch adult lifespan and mass. A significant interaction between monarch family and inoculation dose/spore load indicates genetic variation in tolerance [22,31,33]. We also included the quadratic term of inoculation dose/parasite spore load to test for a nonlinear relationship between inoculation dose/parasite spore load and host fitness (longevity or mass) [31,33,34].…”