title: Specific gene expression responses to parasite genotypes reveal redundancy of innate immunity in vertebrates.
abstract: Vertebrate innate immunity is the first line of defense against an invading pathogen and has long been assumed to be largely unspecific with respect to parasite/pathogen species. However, recent phenotypic evidence suggests that immunogenetic variation, i.e. allelic variability in genes associated with the immune system, results in host-parasite genotype-by-genotype interactions and thus specific innate immune responses. Immunogenetic variation is common in all vertebrate taxa and this reflects an effective immunological function in complex environments. However, the underlying variability in host gene expression patterns as response of innate immunity to within-species genetic diversity of macroparasites in vertebrates is unknown. We hypothesized that intra-specific variation among parasite genotypes must be reflected in host gene expression patterns. Here we used high-throughput RNA-sequencing to examine the effect of parasite genotypes on gene expression patterns of a vertebrate host, the three-spined stickleback (Gasterosteus aculeatus). By infecting naïve fish with distinct trematode genotypes of the species Diplostomum pseudospathaceum we show that gene activity of innate immunity in three-spined sticklebacks depended on the identity of an infecting macroparasite genotype. In addition to a suite of genes indicative for a general response against the trematode we also find parasite-strain specific gene expression, in particular in the complement system genes, despite similar infection rates of single clone treatments. The observed discrepancy between infection rates and gene expression indicates the presence of alternative pathways which execute similar functions. This suggests that the innate immune system can induce redundant responses specific to parasite genotypes.
authors.affiliation: Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.
authors.forename: David
authors.initials: D
authors.lastname: Haase
authors.affiliation: Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.
authors.forename: Jennifer K
authors.initials: JK
authors.lastname: Rieger
authors.affiliation: Genetic Epidemiology of Vascular Disorders, Leibniz Institute for Arteriosclerosis Research at the University Münster, Münster, Germany.
authors.forename: Anika
authors.initials: A
authors.lastname: Witten
authors.affiliation: Genetic Epidemiology of Vascular Disorders, Leibniz Institute for Arteriosclerosis Research at the University Münster, Münster, Germany.
authors.forename: Monika
authors.initials: M
authors.lastname: Stoll
authors.affiliation: Institute for Evolution and Biodiversity, University of Münster, Münster, Germany.
authors.forename: Erich
authors.initials: E
authors.lastname: Bornberg-Bauer
authors.affiliation: Department Evolutionary Ecology, Max-Planck Institute for Evolutionary Biology, Plön, Germany.
authors.forename: Martin
authors.initials: M
authors.lastname: Kalbe
authors.affiliation: Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.
authors.forename: Thorsten B H
authors.initials: TB
authors.lastname: Reusch
mesh_terms: D000818:Animals; D005786:Gene Expression Regulation / Q000276:immunology*; D063990:Gene Ontology; D023281:Genomics; D005838:Genotype; D006790:Host-Parasite Interactions; D007113:Immunity, Innate / Q000235:genetics*; D007814:Larva / Q000502:physiology; D059208:Parasite Load; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D023701:Smegmamorpha / Q000276:immunology / Q000469:parasitology*; D059467:Transcriptome / Q000276:immunology*; D014200:Trematoda / Q000235:genetics / Q000502:physiology*
chemical_list: D012333:RNA, Messenger