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Abstract
Background: The eye fluke Diplostomum pseudospathaceum is a frequent parasite of many fresh-water fish species,
among those three-spined sticklebacks, particularly in lakes with lymnaeid snails, its first intermediate hosts. Cercariae
released from host-snails, penetrate the skin of their fish hosts and within 24 h migrate to the immunologically inert
eye lenses. Thus, individual D. pseudospathaceum are exposed to the fish immune system only for a short time,
suggesting that only innate immunity can be active against the parasite. However, in nature sticklebacks are exposed
to D. pseudospathaceum repeatedly since snails are shedding cercariae from late spring to autumn. Therefore, acquired
immunity after initial infection would be advantageous against subsequent parasite encounters.
Methods: We investigated if sticklebacks originating from a lake with high and from a river with low prevalence of
D. pseudospathaceum differ in susceptibility to repeated exposure to the parasite. We compared infection success and
immune functions in laboratory-bred sticklebacks from both habitats in naïve fish with fish that had been pre-exposed
to eye flukes. Head kidney leukocytes (HKL) from experimental sticklebacks were investigated for respiratory burst
activity and the proliferation of lymphocytes and monocytes 1.5, 5 and 15 days after infection.
Results: Lake sticklebacks were less susceptible than river sticklebacks, however, in both populations pre-exposure
led to a similar relative reduction in infection success. The respiratory burst activity was higher with HKL from lake
sticklebacks and was up-regulated in pre-exposed fish but dropped 1.5d after an additional exposure, suggesting that
activation of phagocytic cells is crucial for the defense against D. pseudospathaceum. Changes in lymphocyte proliferation
were only detectable 1.5d after the last exposure in lake sticklebacks, but not 5 and 15d post exposure, indicating
that a lymphocyte mediated acquired immune response was not induced. Proliferation of monocytes was
significantly increased 1.5d after the last exposure with HKL from both stickleback populations.
Conclusions: Increased resistance to D. pseudospathaceum in sticklebacks from both populations upon pre-exposure
cannot be explained by a prominent adaptive immune response. Monocytic leukocytes were more responsive,
suggesting that rather cells of the innate than the adaptive immune system are active in the defense of
D. pseudospathaceum.
