Coming out from the shadows: facultative slave-making ants reveal their chemical identity during colony development

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Abstract One of the main challenges of the socially parasitic mode of life is bypassing the host's recognition ability, which ensures that altruistic behaviour is directed towards related individuals. Various chemical strategies have evolved to achieve this goal. The most widespread, used also by the obligate slave-making ants, is camouflage or mimicry of colony odour encoded in cuticular hydrocarbon (CHC) composition. However, recent studies have shown that facultative slave-makers employ a different strategy: they manipulate the slaves' recognition labels to make them resemble the parasite's CHC profile. We examined the limitations of this strategy by focusing on incipient F. sanguinea colonies, where slaves are the majority. Our study revealed that callow F. sanguinea ants initially suppress their species-specific odour profile, which develops gradually over time accompanied by an increase of CHC amount per surface area in slave-maker workers. This allows the slaves to familiarise themselves with the parasite's CHC. We found that callow ants produce lower amounts of CHC, and the relative abundance of certain compounds differs from what is observed in older ants. Additionally, preimaginal stages of F. sanguinea ants acquire CHC from the slaves, which are later incorporated into the imagines’ recognition labels. These findings support the proposition that the parasite's manipulation strategy is limited by the slaves' learning capacity, which is necessary to maintain colony cohesion. They also shed light on the selective pressures that might have led to the evolution of chemical mimicry in mature obligate slave-maker colonies.

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