Acquisition of chemical recognition cues facilitates integration into ant societies

Social insects maintain the integrity of their societies by discriminating between colony members and foreigners through cuticular hydrocarbon (CHC) signatures. Nevertheless, parasites frequently get access to social resources, for example through mimicry of host CHCs among other mechanisms. The origin of mimetic compounds, however, remains unknown in the majority of studies (biosynthesis vs. acquisition). Additionally, direct evidence is scarce that chemical mimicry is indeed beneficial to the parasites (e.g., by improving social acceptance).

In the present study we demonstrated that the kleptoparasitic silverfish Malayatelura ponerophila most likely acquires CHCs directly from its host ant Leptogenys distinguenda by evaluating the transfer of a stable-isotope label from the cuticle of workers to the silverfish. In a second experiment, we prevented CHC pilfering by separating silverfish from their host for six or nine days. Chemical host resemblance as well as aggressive rejection behaviour by host ants was then quantified for unmanipulated and previously separated individuals. Separated individuals showed reduced chemical host resemblance and they received significantly more aggressive rejection behaviour than unmanipulated individuals.

Our study clarifies the mechanism of chemical mimicry in a social insect parasite in great detail. It shows empirically for the first time that social insect parasites are able to acquire CHCs from their host. Furthermore, it demonstrates that the accuracy of chemical mimicry can be crucial for social insect parasites by enhancing social acceptance and, thus, allowing successful exploitation. We discuss the results in the light of coevolutionary arms races between parasites and hosts.