Ant recognition cue diversity is higher in the presence of slavemaker ants

Social insect colonies defend themselves from intruders through nestmate recognition, yet the evolution and maintenance of recognition cue diversity is still poorly understood. We compared the recognition cue diversity of 9 populations of Temnothorax longispinosus ant colonies, including populations that harbored the socially parasitic slavemaker ant, Protomognathus americanus. Although ants recognize friends from foe based on recognition cues encoded in their cuticular hydrocarbon profile, which specific compounds are involved in recognition is unknown for most species. We therefore started by statistically identifying 9 putative recognition compounds involved in worker and colony aggression. We find that colonies that co-occur with slavemakers were more variable in these recognition compounds and hence less similar in their recognition profiles than unparasitized populations. Importantly, these differences appear to be regulated by processes that specifically act on the level of the colony, which rules out potentially confounding effects altering chemical profiles of populations, such as differences in abiotic conditions or standing genetic variation. Instead, our findings indicate that slavemakers drive recognition cue diversity in their ant hosts, in much the same way that avian hosts diversify their egg appearance in response to brood parasite pressure. Such recognition cue diversification through negative frequency-dependent selection favors rare host phenotypes and renders it impossible for parasites to match the recognition profile of all potential hosts.