Evolution and genetic architecture of resistance in a natural population of Daphnia magna undergoing strong epidemics of the bacteria Pasteuria ramosa

Host–parasite coevolution is believed to be a major force driving phenotypic and genotypic diversity, notably, through the maintenance of sexual reproduction, as proposed in the Red Queen theory. To understand how resistance evolves in the host, a large body of theory about the dynamics of resistance and its underlying genetics has been proposed. However, empirical data about the long-term evolution of resistance and its underlying genetics is still scarce. In this thesis, I monitor the evolution of resistance in a natural population of the freshwater crustacean Daphnia magna undergoing strong epidemics of the bacterial parasite Pasteuria ramosa, and I investigate the associated underlying genetics of resistance.
The focal population of this thesis occurs in the Aegelsee in Frauenfeld, Switzerland. In this population, D. magna resistance to P. ramosa increases during the planktonic season of the host, and I show that these phenotypic changes are caused by parasite-mediated selection (Chapter 1). In this first chapter, I further investigate the genetic architecture of resistance in the host using a genome-wide association approach combined with genetic crosses and find that resistance is determined by two loci strongly linked with epistasis. In Chapter 2, the evolution of resistance in the host population over eight consecutive planktonic seasons is revealed. Every season, selection increases resistance in the host population, and sexual reproduction causes genetic slippage to reset resistance diversity in the first host cohort of the following season. Sampling of the sexual eggs, and the genetic model of resistance described in Chapter 1, allows me to partially predict the observed resistance diversity resulting from recombination. In Chapter 3, I further expand the genetic model of resistance to P. ramosa in D. magna using genetic crosses coupled with a PoolSeq association approach and find that epistasis plays a major role linking the different resistance loci found in the host. The first step of the infection process in the D. magna–P. ramosa system is the attachment of the bacterial endospores to the host cuticle. Attachment has been shown to be highly specific and is thus crucial for the study of host-parasite interactions. The resistance phenotype in the host can be easily scored in the laboratory with an attachment test, where fluorescent spores are fed to the host and attachment is observed under the microscope. Until recently, clear attachment patterns had been observed in two sites of the gut cuticle. In Chapter 4, I use new isolates of P. ramosa and describe a much higher diversity of attachment sites and patterns than previously described.