Abstract

During the process of coevolution, social parasites have evolved sophisticated strategies to exploit the brood care behavior of their social hosts. Slave-making ant queens invade host colonies and kill or eject all adult host ants. Host workers, which eclose from the remaining brood, are tricked into caring for the parasite brood. Due to their high prevalence and frequent raids, following which stolen host broods are similarly enslaved, slave-making ants exert substantial selection upon their hosts, leading to the evolution of antiparasite adaptations. However, all host defenses shown to date are active before host workers are parasitized, whereas selection was thought to be unable to act on traits of already enslaved hosts. Yet, here we demonstrate the rebellion of enslaved Temnothorax workers, which kill two-thirds of the female pupae of the slave-making ant Protomognathus americanus. Thereby, slaves decrease the long-term parasite impact on surrounding related host colonies. This novel antiparasite strategy of enslaved workers constitutes a new level in the coevolutionary battle after host colony defense has failed. Our discovery is analogous to recent findings in hosts of avian brood parasites where perfect mimicry of parasite eggs leads to the evolution of chick recognition as a second line of defense.