Specificity, genetics of resistance and eco-immunology in Daphnia-microparasite interacions

Abstract

All organisms are thought to be host to at least one parasite, and most likely many. There are far more parasites than non-parasitic life-forms on earth and the interplay between parasites and their hosts may underlie many important evolutionary and ecological phenomena. Local adaptation, but also local maladaptation, speciation, the maintenance of polymorphism, community structure, the evolution of sexual reproduction, and species invasions have all been suggested to be driven by the co-evolutionary interaction of hosts and their parasites. The mechanisms behind these evolutionary phenomena rely on the specificity of the interaction between both partners. Studying the host range of parasites, the specificity of their interaction with their hosts, and the underlying genetic architecture of such interactions is key to understanding their co-evolutionary dynamics, and further down the line to explain major evolutionary and ecological phenomena. Combining evolutionary and classical genetic approaches I have examined several levels of interaction, as well as the specificity of the interaction, between hosts and parasites in the Daphnia-microparasite system. In a first project, I studied the host-range of a microsporidian parasite, Gurleya vavrai, and was able to expand its known range to include the geographically distant yet phylogenetically related species Daphnia pulex arenata as well as the obligate sexual lineage of D. pulex. In accord with host-range theory, the results of this study indicated a role for phylogeny as well as one for local adaptation in shaping a parasite's host-range. The second study in this thesis examined the unexplained existence in Daphnia magna field populations of host genotypes resistant to two genotypes of the parasite Pasteuria ramosa. The existence of such 'double resistant' hosts could, until now, not be explained by genetic models of resistance in this host. Using a complex scheme of crosses and testing parents and two generations of offspring for resistance against both parasite genotypes, we were able to explain how double resistance is inherited. Furthermore we could reject a proposed model of genetic architecture of resistance and modify another proposed model to incorporate double resistance. In fine a three linked loci with two alleles per loci model can explain the genetics of resistance in the Daphnia-Pasteuria host-parasite system. This constitutes the first animal-parasite example with evidence of interactions between linked loci for resistance. Most notably, we provide the first empirical proof of the existence of negative epistasis between linked loci for resistance. Negative epistasis is a key feature of certain genetic models of infection and had never been empirically demonstrated, only indirect indications had been found in other animal-microparasite systems. In a third project, I looked whether costs of resistance in hosts from a natural population of the Daphnia-Pasteuria host-parasite system could be found by competing hosts of opposing resistance phenotypes in the absence of the parasite. We could not find any indication of costs for carrying alleles for resistance. Varying environmental conditions did not have an effect. Our findings concur with those of a previous study, therefore we suggest it to be unlikely that costs exist for resistance against the parasite P. ramosa. In the last study of this thesis, I took a more mechanistic, structural, approach at the Daphnia-Pasteuria host-parasite system, by examining the effects of a history of temperature on the highly resistant transmission stages of the parasite, the spores. Spores of P. ramosa and other closely related bacteria have been found to remain infectious for decades in the environment. In several experiments we treated spores at different temperatures and exposed hosts to these treated spores. I examined three main steps of the infection process to detect an effect and found different steps were affected differently by a history of temperature. I showed that it appears P. ramosa is always capable of successfully infecting susceptible hosts within the natural range of the host. Using various approaches to study several aspects of host-parasite interactions with the Daphnia-microparasite system, I was able to further our understanding of the genetic architecture of infection and the role of specificity in host-parasite interactions. Further I did not find support for the idea that alleles for resistance are costly and discovered that the parasite P. ramosa may be very well adapted to survive and remain infectious within the environmental range of its host.