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The secretome of a parasite is sufficient to alter its host’s behaviour

Parasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its external environment (i.e. the secretome), but this has rarely been assessed. Here, we studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only when the worm is ready to reproduce in its final avian host. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting it in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours in sticklebacks, but secretome from early infection parasite resulted in more cautious host, only in fish from the allopatric population. Our results suggest that the secretome of Schistocephalus solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial, and that local adaptation between host-parasite pairs may extend to the response to the parasite’s secretome content.