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On the Equivalence of Host Local Adaptation and Parasite Maladaptation: An Experimental Test

In spatiotemporally varying environments, host-parasite coevolution may lead to either host or parasite local adaptation. Using reciprocal infestations over 11 pairs of plots, we tested local adaptation in the hen flea and its main host, the great tit. Flea reproductive success (number of adults at host fledging) was lower on host individuals from the same plot compared with foreign hosts (from another plot), revealing flea local maladaptation. Host reproductive success (number of fledged young) for nests infested by foreign fleas was lower compared with the reproductive success of controls, with an intermediate success for nests infested by local fleas. This suggests host local adaptation although the absence of local adaptation could not be excluded. However, fledglings were heavier and larger when reared with foreign fleas than when reared with local fleas, which could also indicate host local maladaptation if the fitness gain in offspring size offsets the potential cost in offspring number. Our results therefore challenge the traditional view that parasite local maladaptation is equivalent to host local adaptation. The differences in fledgling morphology between nests infested with local fleas and those with foreign fleas suggest that flea origin affects host resource allocation strategy between nestling growth and defense against parasites. Therefore, determining the mechanisms that underlie these local adaptation patterns requires the identification of the relevant fitness measures and life-history trade-offs in both species.