Host specificity and genetics of host resistance in the "Daphnia-Pasteuria" host-parasite system

Abstract

Antagonistic coevolution plays an important role in a large number of evolutionary and ecological phenomena. Furthermore, according to the Red Queen Theory coevolution between hosts and their parasites may explain the maintenance of sexual reproduction and genetic variation, pertinent issues in evolutionary biology. For antagonistic coevolution to lead to negative frequency dependent selection, preserve genetic variation and select for sexual reproduction parasites need to have high host specificity and this specificity has to have a simple genetic basis. In this thesis I investigate these two criteria in the Daphnia-Pasteuria system. Daphnia magna and its bacterial pathogen Pasteuria ramosa have become one of the prime model systems for antagonistic coevolution between hosts and parasites and one of the few systems with empirical evidence consistent with antagonistic coevolution by frequency dependent selection. In the first chapter I show that specificity in the Daphnia-Pasteuria system is much stronger than previously reported. By using a novel technique I obtain single genotypes (clones) from the unculturable P. ramosa. Infections with these single parasite genotypes either result in hosts that are fully resistant or in hosts that are fully susceptible. High specificity for just some genotypes of D. magna as found in the first chapter contrast with reports from infections in natural populations which suggested that P. ramosa has a broad host range and is able to simultaneously infect highly diverged species of Daphnia. In the second chapter I address this apparent controversy. My findings of a controlled infection experiment with multiple host species and parasite lineages suggest that P. ramosa is a species complex consisting of multiple morphologically cryptic species each highly specialized for some genotypes within their host species. In addition I find that although infection does only occur in native host-parasite combinations, attachment of spores to the host esophagus, a necessary step in the infection process is conserved and polymorphic between highly diverged species of Daphnia. In chapters 3 & 4 I investigate the genetic basis of the observed specificity. Using a large array of crosses and two parasite genotypes I find that resistance is coded for by a single Mendelian inherited locus with three alleles with an allele hierarchy. An alternative, but more complex, explanation for our results is based on two closely linked diallelic loci with interlocus epistasis. In conclusion both my findings on host specificity and the genetics of host resistance suggest that Daphnia and Pasteuria have the potential to undergo antagonistic coevolution by negative frequency dependent selection. Furthermore, the finding that genetics of resistance in Daphnia are consistent with a matching allele model will allow the Daphnia-Pasteuria system to become a powerful tool for empirical testing of population level predictions of this model. Indeed, the Daphnia-Pasteuria system could be used to experimentally test for negative frequency dependent selection, the maintenance of genetic variation and the notion that antagonistic coevolution may favor genetic mixing.