Evidence for passive chemical camouflage in the parasitic mite Varroa destructor

Social insect colonies provide a stable and safe environment for their members. Despite colonies being heavily guarded, parasites have evolved numerous strategies to invade and inhabit these hostile places. Two such strategies are (true) chemical mimicry via biosynthesis of host odor, and chemical camouflage, in which compounds are acquired from the host. The ectoparasitic mite Varroa destructor feeds on hemolymph of its honey bee host, Apis mellifera. The mite's odor closely resembles that of its host, which allows V. destructor to remain undetected as it lives on the adult host during its phoretic phase and while reproducing on the honeybee brood. During the mite life cycle, it switches between host adults and brood, which requires it to adjust its profile to mimic the very different odors of honey bee brood and adults. In a series of transfer experiments, using bee adults and pupae, we tested whether V. destructor changes its profile by synthesizing compounds or by using chemical camouflage. We show that V. destructor required direct access to host cuticle to mimic its odor, and that it was unable to synthesize host-specific compounds itself. The mite was able to mimic host odor, even when dead, indicating a passive physico-chemical mechanism of the parasite cuticle. The chemical profile of V. destructor was adjusted within 3 to 9 h after switching hosts, demonstrating that passive camouflage is a highly efficient, fast and flexible way for the mite to adapt to a new host profile when moving between different host life stages or colonies.