The formation of the nestmate recognition template in ants and its effect on behavioural variation

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Our behaviour towards others depends on whether we recognise them, for example by their faces. We compare the perceived face with prototypes of faces stored in our memory: the templates. While other aspects of recognition (production component, e.g. cue expression; action component, e.g. decision rules) are well studied, the perception component, of which template is a fundamental aspect, is not. Currently, we have little understanding from any system, human or animal, of the information stored in templates, and how templates are formed. Social insects are a particularly good model to study template formation because workers differ in their aggression towards intruders and we showed that the perception component is responsible for some of the variation.Traditional views of the nestmate recognition template describe it as a representation of the “average colony odour”, which is identical for all nestmates. However, the template could be partly self-referent, e.g. a combination of an individual's own odour and the average colony odour (“Newey template”). This would explain the behavioural variation that has been observed: Templates, and thus recognition, would vary with each individual's own odour. For template formation, there are two alternative hypotheses as well: The template could be formed by habituation: Ants “get used” to their own colony odour. Alternatively, associative learning could play a role: Ants may associate colony odours to good or bad experiences in interactions with other ants, which is likely to cause inter-individual variation if individuals experience different interactions. This would be particularly evident if ants learn to associate non-nestmate odours with negative experiences (e.g. fights), which would improve the detection of intruders from familiar non-nestmate colonies only in those individuals that previously encountered the non-nestmate colony in question. We have preliminary evidence for the latter from experiments on the nasty neighbour effect, where familiarity with non-nestmates increases an ant's aggression towards the specific non-nestmate colony.To test whether self-referent templates or associative learning of templates are responsible for the observed variation in nestmate recognition, we will manipulate the odours of ant workers relative to their colony odour and manipulate the interactions experienced by individuals. We will also directly impede associative learning with pharmacological interventions. Finally, we will analyse brain and antennal gene expression to track molecular effects caused by our experimental manipulations. We will then compare these effects to the molecular variation among different worker morphs, which vary in their aggression. Our project will shed light on the long-standing and currently hotly debated question of how nestmate recognition templates are formed, with implications for our understanding behavioural variation and recognition processes in general.