Parasites represent a severe threat to social insects, which form high‐density colonies of related individuals, and selection should favour host traits that reduce infection risk. Here, using a carpenter ant (Camponotus aethiops) and a generalist insect pathogenic fungus (Metarhizium brunneum), we show that infected ants radically change their behaviour over time to reduce the risk of colony infection. Infected individuals (i) performed less social interactions than their uninfected counterparts, (ii) did not interact with brood anymore and (iii) spent most of their time outside the nest from day 3 post‐infection until death. Furthermore, infected ants displayed an increased aggressiveness towards non‐nestmates. Finally, infected ants did not alter their cuticular chemical profile, suggesting that infected individuals do not signal their physiological status to nestmates. Our results provide evidence for the evolution of unsociability following pathogen infection in a social animal and suggest an important role of inclusive fitness in driving such evolution.

Recognizing the identity of others, from the individual to the group level, is a hallmark of society. Ants, and other social insects, have evolved advanced societies characterized by efficient social recognition systems. Colony identity is mediated by colony specific signature mixtures, a blend of hydrocarbons present on the cuticle of every individual (the “label”). Recognition occurs when an ant encounters another individual, and compares the label it perceives to an internal representation of its own colony odor (the “template”). A mismatch between label and template leads to rejection of the encountered individual. Although advances have been made in our understanding of how the label is produced and acquired, contradictory evidence exists about information processing of recognition cues. Here, we review the literature on template acquisition in ants and address how and when the template is formed, where in the nervous system it is localized, and the possible role of learning. We combine seemingly contradictory evidence in to a novel, parsimonious theory for the information processing of nestmate recognition cues.

Social animals use recognition cues to discriminate between group members and non-members. These recognition cues may be conceptualized as a label, which is compared to a neural representation of acceptable cue combinations termed the template. In ants and other social insects, the label consists of a waxy layer of colony-specific hydrocarbons on the body surface. Genetic and environmental differences between colony members may confound recognition and social cohesion, so many species perform behaviors that homogenize the odor label, such as mouth-to-mouth feeding and allogrooming. Here, we test for another mechanism of cue exchange: indirect transfer of cuticular hydrocarbons via the nest material. Using a combination of chemical analysis and behavioral experiments with Camponotus aethiops ants, we show that nest soil indirectly transfers hydrocarbons between ants and affects recognition behavior. We also found evidence that olfactory cues on the nest soil influence nestmate recognition, but this effect was not observed in all colonies. These results demonstrate that cuticular hydrocarbons deposited on the nest soil are important in creating uniformity in the odor label and may also contribute to the template.

Parasites are ubiquitous, and the ability to defend against these is of paramount importance. One way to fight diseases is self-medication, which occurs when an organism consumes biologically active compounds to clear, inhibit, or alleviate disease symptoms. Here, we show for the first time that ants selectively consume harmful substances (reactive oxygen species, ROS) upon exposure to a fungal pathogen, yet avoid these in the absence of infection. This increased intake of ROS, while harmful to healthy ants, leads to higher survival of exposed ants. The fact that ingestion of this substance carries a fitness cost in the absence of pathogens rules out compensatory diet choice as the mechanism, and provides evidence that social insects medicate themselves against fungal infection, using a substance that carries a fitness cost to uninfected individuals.

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