Caste-Dependent Interspecific Tolerance Permits Alien Reproductives to Reproduce Within Host Colonies in Reticulitermes Termites Under Laboratory Conditions

Nestmate recognition is the primary defense mechanism maintaining the integrity of eusocial insect colonies. While social parasitism is widespread in Hymenoptera, it is rarely documented in termites, and the behavioral boundaries preventing interspecific infiltration remain poorly understood. Here, we investigated the potential for interspecific integration between two closely related termite species under laboratory conditions. We introduced Reticulitermes labralis workers and reproductives (queens and kings) into orphaned groups of R. aculabialis. We found that host workers exhibited caste-dependent aggression: introduced workers were immediately attacked and eliminated, whereas alien reproductives were partially tolerated. Surviving alien reproductives successfully integrated into host group, receiving allogrooming and trophallactic care from host workers. Crucially, these integrated pairs produced viable eggs and larvae. Molecular analysis confirmed that the brood reared by the host workers were the genetic offspring of the introduced R. labralis pair, demonstrating successful “cuckoo-like” reproduction. These findings reveal that termite colony recognition is sufficiently flexible to permit the acceptance of heterospecific reproductives when native royals are absent. While field evidence remains to be discovered, our results demonstrate that the behavioral and physiological prerequisites for social parasitism exist in termites, supporting the hypothesis that close phylogenetic relatedness (Emery’s rule) facilitates the breach of social barriers.