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Free keywords:
parasite antigens; in vitro leukocyte response; local adaptation;
Gasterosteus aculeatus; Schistocephalus solidus
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 30e50%) and Spanish (40e66%) 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.
