title: The Red Queen lives: Epistasis between linked resistance loci.
abstract: A popular theory explaining the maintenance of genetic recombination (sex) is the Red Queen Theory. This theory revolves around the idea that time-lagged negative frequency-dependent selection by parasites favors rare host genotypes generated through recombination. Although the Red Queen has been studied for decades, one of its key assumptions has remained unsupported. The signature host-parasite specificity underlying the Red Queen, where infection depends on a match between host and parasite genotypes, relies on epistasis between linked resistance loci for which no empirical evidence exists. We performed 13 genetic crosses and tested over 7000 Daphnia magna genotypes for resistance to two strains of the bacterial pathogen Pasteuria ramosa. Results reveal the presence of strong epistasis between three closely linked resistance loci. One locus masks the expression of the other two, while these two interact to produce a single resistance phenotype. Changing a single allele on one of these interacting loci can reverse resistance against the tested parasites. Such a genetic mechanism is consistent with host and parasite specificity assumed by the Red Queen Theory. These results thus provide evidence for a fundamental assumption of this theory and provide a genetic basis for understanding the Red Queen dynamics in the Daphnia-Pasteuria system.
authors.affiliation: Zoological Institute, University of Basel, CH-4051, Basel, Switzerland.
authors.forename: César M J A
authors.initials: CM
authors.lastname: Metzger
authors.affiliation: Zoological Institute, University of Basel, CH-4051, Basel, Switzerland. pepijn.luijckx@gmail.com.|Department of Ecology & Evolutionary Biology, University of Toronto, M5S 3B2, Toronto, Ontario, Canada. pepijn.luijckx@gmail.com.
authors.forename: Pepijn
authors.initials: P
authors.lastname: Luijckx
authors.affiliation: Zoological Institute, University of Basel, CH-4051, Basel, Switzerland.
authors.forename: Gilberto
authors.initials: G
authors.lastname: Bento
authors.affiliation: Zoological Institute, University of Basel, CH-4051, Basel, Switzerland.|INRA, UR1404 Unité Mathématique et Informatique Appliquées du Génome à l'Environnement, 78350, Jouy-en-Josas, France.
authors.forename: Mahendra
authors.initials: M
authors.lastname: Mariadassou
authors.affiliation: Zoological Institute, University of Basel, CH-4051, Basel, Switzerland.
authors.forename: Dieter
authors.initials: D
authors.lastname: Ebert
mesh_terms: D000818:Animals; D003621:Daphnia / Q000235:genetics / Q000276:immunology / Q000382:microbiology; D060467:Disease Resistance / Q000235:genetics*; D004843:Epistasis, Genetic; D008040:Genetic Linkage; D056426:Genetic Loci; D054884:Host-Pathogen Interactions / Q000235:genetics*; D008957:Models, Genetic; D058676:Pasteuria / Q000235:genetics / Q000472:pathogenicity; D010641:Phenotype
keywords: Coevolution; Daphnia magna; Pasteuria ramosa; Red Queen Theory; matching allele mode; negative frequency-dependent selection