Genotype-Specific vs. Cross-Reactive Host Immunity against a Macroparasite

Christian Rellstab,Katja-Riikka Louhi,Anssi Karvonen,Jukka Jokela,Rick Edward Paul

doi:10.1371/journal.pone.0078427

Abstract

Vertebrate hosts often defend themselves against several co-infecting parasite genotypes simultaneously. This has important implications for the ecological dynamics and the evolution of host defence systems and parasite strategies. For example, it can drive the specificity of the adaptive immune system towards high genotype-specificity or cross-reactivity against several parasite genotypes depending on the sequence and probability of re-infections. However, to date, there is very little evidence on these interactions outside mammalian disease literature. In this study we asked whether genotype-specific or cross-reactive responses dominate in the adaptive immune system of a fish host towards a common macroparasite. In other words, we investigated if the infection success of a parasite genotype is influenced by the immunization genotype. We reciprocally immunized and re-exposed rainbow trout (Oncorhynchus mykiss) to a range of genotypes of the trematode eye fluke Diplostomum pseudospathaceum, and measured infection success of the parasite. We found that the infection success of the parasite genotypes in the re-exposure did not depend on the immunization genotype. While immunization reduced average infection success by 31%, the reduction was not larger against the initial immunization genotype. Our results suggest significant cross-reactivity, which may be advantageous for the host in genetically diverse re-exposures and have significant evolutionary implications for parasite strategies. Overall, our study is among the first to demonstrate cross-reactivity of adaptive immunity against genetically diverse macroparasites with complex life cycles.

Highlights

In nature, hosts are typically exposed to and infected with multiple parasite genotypes [1,2]
The infection success was 31% lower in immunized fish (10.2 vs. 14.7%), but there were significant differences among the parasite genotypes
Long-lived vertebrate hosts may encounter the same clonal parasite strains or genotypes repeatedly during their life depending on the ecological dynamics of the hosts and parasites

Summary

Introduction

Hosts are typically exposed to and infected with multiple parasite genotypes [1,2] These infections are ecologically dynamic, depending, for example, on the variation in host ecology, spatial distribution of parasite intermediate hosts, and temporally fluctuating risk of exposure driven by seasonality of the release of parasite infective stages (e.g., [3,4,5,6]). This has important implications for host-parasite coevolution in terms of selection pressures that shape host defence systems and parasite strategies to elude those defences [7]. In long-lived vertebrate hosts, adaptive immune processes play an important role as the hosts spend only a small fraction of their lives unexposed and unimmunized

Methods

Results

Conclusion