Discussion

In vertebrates, the adaptive immune system evolved to maximise protection and minimise immunological costs upon repeated parasites exposure. At high risk of recurring infections, the costs of immune activation of a specific response should be offset by the benefits of parasite resistance. Yet, under low parasite pressure the physiological costs of acquired immune responses may outweigh their benefits. Such conditional cost/benefit trade-offs should ultimately translate into Darwinian fitness. Here, we experimentally triggered an immune response in three-spined sticklebacks by injecting antigens derived from common parasites, while simultaneously avoiding the costs of infection. Antigen and control-injected fish were then allowed to naturally reproduce in either parasite-free or parasite-rich mesocosms. As predicted, exposure to parasites significantly decreased fish reproductive success. Furthermore, immune activation by antigen treatments conferred parasite-specific resistance and most importantly, Darwinian fitness increased under natural parasite exposure. Following our hypothesis, mounting an adaptive immune response significantly reduced the individual lifetime reproductive success of uninfected fish. These findings provide experimental evidence of the intricate cost/benefit balance of acquired immune responses. They also provide explanations for the observed variation in immune-competence across connected populations or related species inhabiting environments with distinct parasite pressure.