Brood exchange experiments and chemical analyses shed light on slave rebellion in ants

Parasites and hosts frequently engage in coevolutionary arms races, in which newly developed host defenses will be counteracted by parasite adaptations. Slave-making ants are virulent social parasites that trick enslaved host workers into caring for their brood. These slaves also have to accept stolen host pupae, which slavemakers retrieve during raids. Previously, selection was thought to be unable to act on traits of these enslaved host ants. Yet, a recent study demonstrated rebellion of enslaved Temnothorax workers, which selectively killed female pupae of the slave-making ant Protomognathus americanus. This defensive trait could lower the costs of parasitism because slowed growth of parasite nests reduces raiding impact on related neighboring host colonies. In cross-fostering experiments, we investigated the acceptance of host and parasite pupae by Temnothorax workers in parasitized and unparasitized colonies. Host workers commonly killed transferred pupae, and the presence of the social parasite only increased acceptance of parasite pupae in 1 host species and that of heterospecific host pupae in a second host. Parasite pupae survived better when transferred to sympatric host colonies than to allopatric ones, possibly indicating local adaptation in the parasite P. americanus. Cuticular hydrocarbon analyses explain this with chemical differences in pupae profiles between communities. Overall, parasite and host pupae have highly divergent profiles. Hence, cuticular hydrocarbons can potentially be used by host workers to identify and destroy parasite pupae. The parasite P. americanus should be under strong selection to adapt its pupal recognition cues to those of its hosts to counteract slave rebellion.