title: In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens.
abstract: Helminth parasites of teleost fish have evolved strategies to evade and manipulate the immune responses of their hosts. Responsiveness of fish host immunity to helminth antigens may therefore vary depending on the degree of host-parasite counter-adaptation. Generalist parasites, infective for a number of host species, might be unable to adapt optimally to the immune system of a certain host species, while specialist parasites might display high levels of adaptation to a particular host species. The degree of adaptations may further differ between sympatric and allopatric host-parasite combinations. Here, we test these hypotheses by in vitro exposure of head kidney leukocytes from three-spined sticklebacks (Gasterosteus aculeatus) to antigens from parasites with a broad fish host range (Diplostomum pseudospathaceum, Triaenophorus nodulosus), a specific fish parasite of cyprinids (Ligula intestinalis) and parasites highly specific only to a single fish species as second intermediate host (Schistocephalus pungitii, which does not infect G. aculeatus, and Schistocephalus solidus, infecting G. aculeatus). In vitro responses of stickleback leukocytes to S. solidus antigens from six European populations, with S. solidus prevalence from <1% to 66% were tested in a fully crossed experimental design. Leukocyte cultures were analysed by means of flow cytometry and a chemiluminescence assay to quantify respiratory burst activity. We detected decreasing magnitudes of in vitro responses to antigens from generalist to specialist parasites and among specialists, from parasites that do not infect G. aculeatus to a G. aculeatus-infecting species. Generalist parasites seem to maintain their ability to infect different host species at the costs of relatively higher immunogenicity compared to specialist parasites. In a comparison of sympatric and allopatric combinations of stickleback leukocytes and antigens from S. solidus, magnitudes of in vitro responses were dependent on the prevalence of the parasite in the population of origin, rather than on sympatry. Antigens from Norwegian (prevalence 30-50%) and Spanish (40-66%) S. solidus induced generally higher in vitro responses compared to S. solidus from two German (<1%) populations. Likewise, leukocytes from stickleback populations with a high S. solidus prevalence showed higher in vitro responses to S. solidus antigens compared to populations with low S. solidus prevalence. This suggests a rather low degree of local adaptation in S. solidus populations, which might be due to high gene flow among populations because of their extremely mobile final hosts, fish-eating birds.
authors.affiliation: Department of Animal Evolutionary Ecology, Institute for Evolution and Biodiversity, University of Münster, Hüfferstrasse 1, 48149 Münster, Germany.
authors.forename: Frederik
authors.initials: F
authors.lastname: Franke
authors.affiliation: Institute for Evolutionary Biology and Ecology, University of Bonn, An der Immenburg 1, 53121 Bonn, Germany.
authors.forename: Anna K
authors.initials: AK
authors.lastname: Rahn
authors.affiliation: Department of Animal Evolutionary Ecology, Institute for Evolution and Biodiversity, University of Münster, Hüfferstrasse 1, 48149 Münster, Germany.
authors.forename: Janine
authors.initials: J
authors.lastname: Dittmar
authors.affiliation: Department of Evolutionary Ecology, Max-Planck Institute of Evolutionary Biology, August-Thienemann Str 2, 24306 Plön, Germany.
authors.forename: Noémie
authors.initials: N
authors.lastname: Erin
authors.affiliation: Department of Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research, Düsternbrooker Weg 20, 24105 Kiel, Germany.
authors.forename: Jennifer K
authors.initials: JK
authors.lastname: Rieger
authors.affiliation: Department of Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research, Düsternbrooker Weg 20, 24105 Kiel, Germany.
authors.forename: David
authors.initials: D
authors.lastname: Haase
authors.affiliation: Department of Evolutionary Ecology, Max-Planck Institute of Evolutionary Biology, August-Thienemann Str 2, 24306 Plön, Germany.
authors.forename: Irene E
authors.initials: IE
authors.lastname: Samonte-Padilla
authors.affiliation: Department of Animal Evolutionary Ecology, Institute for Evolution and Biodiversity, University of Münster, Hüfferstrasse 1, 48149 Münster, Germany.
authors.forename: Joseph
authors.initials: J
authors.lastname: Lange
authors.affiliation: Institute for Biology, University of Bergen, Thor Møhlensgate 55, 5020 Bergen, Norway.
authors.forename: Per J
authors.initials: PJ
authors.lastname: Jakobsen
authors.affiliation: Departamento de Xenetica, Facultade de Veterinaria, Universidade de Santiago de Compostela, Campus de Lugo, 27002 Lugo, Spain.
authors.forename: Miguel
authors.initials: M
authors.lastname: Hermida
authors.affiliation: Departamento de Xenetica, Facultade de Veterinaria, Universidade de Santiago de Compostela, Campus de Lugo, 27002 Lugo, Spain.
authors.forename: Carlos
authors.initials: C
authors.lastname: Fernández
authors.affiliation: Department of Animal Evolutionary Ecology, Institute for Evolution and Biodiversity, University of Münster, Hüfferstrasse 1, 48149 Münster, Germany.
authors.forename: Joachim
authors.initials: J
authors.lastname: Kurtz
authors.affiliation: Institute for Evolutionary Biology and Ecology, University of Bonn, An der Immenburg 1, 53121 Bonn, Germany.
authors.forename: Theo C M
authors.initials: TC
authors.lastname: Bakker
authors.affiliation: Department of Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research, Düsternbrooker Weg 20, 24105 Kiel, Germany.
authors.forename: Thorsten B H
authors.initials: TB
authors.lastname: Reusch
authors.affiliation: Department of Evolutionary Ecology, Max-Planck Institute of Evolutionary Biology, August-Thienemann Str 2, 24306 Plön, Germany.
authors.forename: Martin
authors.initials: M
authors.lastname: Kalbe
authors.affiliation: Department of Animal Evolutionary Ecology, Institute for Evolution and Biodiversity, University of Münster, Hüfferstrasse 1, 48149 Münster, Germany. Electronic address: joern.scharsack@uni-muenster.de.
authors.forename: Jörn P
authors.initials: JP
authors.lastname: Scharsack
mesh_terms: D000818:Animals; D005393:Fish Diseases / Q000276:immunology / Q000469:parasitology*; D005434:Flow Cytometry; D006790:Host-Parasite Interactions / Q000276:immunology; D009504:Neutrophils; D016897:Respiratory Burst / Q000276:immunology; D023701:Smegmamorpha; D014200:Trematoda / Q000276:immunology*; D014201:Trematode Infections / Q000453:epidemiology / Q000469:parasitology / Q000662:veterinary*
keywords: Gasterosteus aculeatus; In vitro leukocyte response; Local adaptation; Parasite antigens; Schistocephalus solidus