What are the Mechanisms Behind a Parasite-Induced Decline in Nestmate Recognition in Ants?

Abstract

Social insects have developed sophisticated recognition skills to defend their nests against intruders. They do this by aggressively discriminating against non-nestmates with deviant cuticular hydrocarbon (CHC) signatures. Studying nestmate recognition can be challenging as individual insects do not only vary in their discriminatory abilities, but also in their motivation to behave aggressively. To disentangle the influence of signaling and behavioral motivation on nestmate recognition, we investigated the ant Temnothorax nylanderi, where the presence of tapeworm-infected nestmates leads to reduced nestmate recognition among uninfected workers. The parasite-induced decline in nestmate recognition could be caused by higher intra-colonial cue diversity as tapeworm-infected workers are known to exhibit a modified hydrocarbon signature. This in turn may broaden the neuronal template of their nestmates, leading to a higher tolerance towards alien conspecifics. To test this hypothesis, we exchanged infected ants between colonies and analyzed their impact on CHC profiles of uninfected workers. We demonstrate that despite frequent grooming, which should promote the transfer of recognition cues, CHC profiles of uninfected workers neither changed in the presence of tapeworm-infected ants, nor did it increase cue diversity among uninfected nestmates within or between colonies. However, CHC profiles were systematically affected by the removal of nestmates and addition of non-nestmates, independently from the ants' infection status. For example, when non-nestmates were present workers expressed more dimethyl alkanes and higher overall CHC quantities, possibly to achieve a better distinction from non-nestmates. Workers showed clear task-specific profiles with tapeworm-infected workers resembling more closely young nurses than older foragers. Our results show that the parasite-induced decline in nestmate recognition is not due to increased recognition cue diversity or altered CHC profiles of uninfected workers, but behavioral changes might explain tolerance towards intruders.