title: The genetic basis of resistance and matching-allele interactions of a host-parasite system: The Daphnia magna-Pasteuria ramosa model.
abstract: Negative frequency-dependent selection (NFDS) is an evolutionary mechanism suggested to govern host-parasite coevolution and the maintenance of genetic diversity at host resistance loci, such as the vertebrate MHC and R-genes in plants. Matching-allele interactions of hosts and parasites that prevent the emergence of host and parasite genotypes that are universally resistant and infective are a genetic mechanism predicted to underpin NFDS. The underlying genetics of matching-allele interactions are unknown even in host-parasite systems with empirical support for coevolution by NFDS, as is the case for the planktonic crustacean Daphnia magna and the bacterial pathogen Pasteuria ramosa. We fine-map one locus associated with D. magna resistance to P. ramosa and genetically characterize two haplotypes of the Pasteuria resistance (PR-) locus using de novo genome and transcriptome sequencing. Sequence comparison of PR-locus haplotypes finds dramatic structural polymorphisms between PR-locus haplotypes including a large portion of each haplotype being composed of non-homologous sequences resulting in haplotypes differing in size by 66 kb. The high divergence of PR-locus haplotypes suggest a history of multiple, diverse and repeated instances of structural mutation events and restricted recombination. Annotation of the haplotypes reveals striking differences in gene content. In particular, a group of glycosyltransferase genes that is present in the susceptible but absent in the resistant haplotype. Moreover, in natural populations, we find that the PR-locus polymorphism is associated with variation in resistance to different P. ramosa genotypes, pointing to the PR-locus polymorphism as being responsible for the matching-allele interactions that have been previously described for this system. Our results conclusively identify a genetic basis for the matching-allele interaction observed in a coevolving host-parasite system and provide a first insight into its molecular basis.
authors.affiliation: Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
authors.forename: Gilberto
authors.identifier: 0000-0002-8455-6625
authors.initials: G
authors.lastname: Bento
authors.affiliation: Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
authors.forename: Jarkko
authors.initials: J
authors.lastname: Routtu
authors.affiliation: Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
authors.forename: Peter D
authors.initials: PD
authors.lastname: Fields
authors.affiliation: Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
authors.forename: Yann
authors.initials: Y
authors.lastname: Bourgeois
authors.affiliation: Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
authors.forename: Louis
authors.initials: L
authors.lastname: Du Pasquier
authors.affiliation: Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
authors.forename: Dieter
authors.initials: D
authors.lastname: Ebert
mesh_terms: D000483:Alleles; D000818:Animals; D003621:Daphnia / Q000235:genetics* / Q000382:microbiology; D019143:Evolution, Molecular; D014644:Genetic Variation; D005838:Genotype; D006239:Haplotypes / Q000235:genetics; D006790:Host-Parasite Interactions / Q000235:genetics*; D058676:Pasteuria / Q000235:genetics* / Q000472:pathogenicity; D011110:Polymorphism, Genetic; D012641:Selection, Genetic / Q000235:genetics*