Evolution of miniaturisation in inquiline parasitic ants: Timing of male elimination in Plagiolepis pygmaea, the host of Plagiolepis xene

Summary.

Inquiline ant species are workerless social parasites whose queens rely completely on the host worker force to raise their brood. A remarkable feature of inquiline ants is the small size of sexuals, which are of the same size as or smaller than host workers. It has been suggested that miniaturisation evolved by parasites to prevent host workers from discriminating between their own worker brood and the inquiline sexuals, so that male and female inquilines can develop under conditions where the host species does not produce its own sexuals. In line with the miniaturisation hypothesis, workers of the ant P. pygmaea cull all the male brood of their own species, whereas at the same time males of their inquiline parasite P. xene are reared to adulthood. Here, we tested whether P. pygmaea workers recognize and eliminate males of their own species when they reach the size of the larger workers. Contrary to the assumption that size is indeed the primary cue used by workers to discriminate male from worker brood, we found that males of P. pygmaea are culled between the small and medium larval stages, that is much before reaching the critical size of the largest worker larvae. Based on this finding, we propose an extension of the miniaturisation hypothesis with a first step whereby the parasitic P. xene males escape the caste and sex recognition system of the host during early development. The most likely mechanism is chemical mimicry of host worker larvae. Miniaturisation would have evolved later to prevent the host workers to secondarily use size as a recognition cue to eliminate P. xene males.