Nick Bos

Recognition of Social Identity in Ants

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.

Learning and perceptual similarity among cuticular hydrocarbons in ants

Nestmate recognition in ants is based on perceived differences in a multi-component blend of hydrocarbons that are present on the insect cuticle. Although supplementation experiments have shown that some classes of hydrocarbons, such as methyl branched alkanes and alkenes, have a salient role in nestmate recognition, there was basically no information available on how ants detect and perceive these molecules. We used a new conditioning procedure to investigate whether individual carpenter ants could associate a given hydrocarbon (linear or methyl-branched alkane) to sugar reward. We then studied perceptual similarity between a hydrocarbon previously associated with sugar and a novel hydrocarbon. Ants learnt all hydrocarbon-reward associations rapidly and with the same efficiency, regardless of the structure of the molecules. Ants could discriminate among a large number of pairs of hydrocarbons, but also generalised. Generalisation depended both on the structure of the molecule and the animals experience. For linear alkanes, generalisation was observed when the novel molecule was smaller than the conditioned one. Generalisation between pairs of methyl-alkanes was high, while generalisation between hydrocarbons that differed in the presence or absence of a methyl group was low, suggesting that chain length and functional group might be coded independently by the ant olfactory system. Understanding variations in perception of recognition cues in ants is necessary for the general understanding of the mechanisms involved in social recognition processes based on chemical cues.

Significance of chemical recognition cues is context dependent in ants.

Recognition of group members is of fundamental importance in social animals, allowing individuals to protect resources against intruders and parasites, as well as ensuring social cohesion within the group. In ants and other social insects, social recognition relies on multicomponent chemical signatures, composed primarily of long-chain cuticular hydrocarbons. These signatures are colony specific and allow discrimination between nestmates and non-nestmates. Nevertheless, the mechanisms underlying detection, perception and information processing of chemical signatures are poorly understood. It has been suggested that associative learning might play a role in nestmate recognition. We investigated whether Camponotus aethiops ants can associate a complete cuticular hydrocarbon profile, consisting of about 40 compounds, with a food reward and whether the new association, developed in an appetitive context, affects aggression against non-nestmates carrying the hydrocarbon profile associated with food. Individual ant workers were able to associate the non-nestmate chemical profile with food. However, conditioned ants were still aggressive when encountering a non-nestmate carrying the odour profile used as training odour in our experiments. This suggests that ants, like some, but not all other insects, show interactions between different modalities (i.e. olfactory and visual), and can treat complex chemical cues differently, according to the context in which they are perceived. This plasticity ensures that learning in an appetitive context does not interfere with the crucial task of colony defence.

Wax on, wax off: nest soil facilitates indirect transfer of recognition cues between ant nestmates.

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.

Chemical structure of odorants and perceptual similarity in ants

SUMMARY Animals are often immersed in a chemical world consisting of mixtures of many compounds rather than of single substances, and they constantly face the challenge of extracting relevant information out of the chemical landscape. To this purpose, the ability to discriminate among different stimuli with different valence is essential, but it is also important to be able to generalise, i.e. to treat different but similar stimuli as equivalent, as natural variation does not necessarily affect stimulus valence. Animals can thus extract regularities in their environment and make predictions, for instance about distribution of food resources. We studied perceptual similarity of different plant odours by conditioning individual carpenter ants to one odour, and subsequently testing their response to another, structurally different odour. We found that asymmetry in generalisation, where ants generalise from odour A to B, but not from B to A, is dependent on both chain length and functional group. By conditioning ants to a binary mixture, and testing their reaction to the individual components of the mixture, we show that overshadowing, where parts of a mixture are learned better than others, is rare. Additionally, generalisation is dependent not only on the structural similarity of odorants, but also on their functional value, which might play a crucial role. Our results provide insight into how ants make sense of the complex chemical world around them, for example in a foraging context, and provide a basis with which to investigate the neural mechanisms behind perceptual similarity.

Appetitive and aversive olfactory learning induce similar generalization rates in the honey bee

Appetitive and aversive learning drive an animal toward or away from stimuli predicting reinforcement, respectively. The specificity of these memories may vary due to differences in cost–benefit relationships associated with appetitive and aversive contexts. As a consequence, generalization performances may differ after appetitive and aversive training. Here, we determined whether honey bees show different rates of olfactory generalization following appetitive olfactory conditioning of the proboscis extension response, or aversive olfactory conditioning of the sting extension response. In both cases, we performed differential conditioning, which improves discrimination learning between a reinforced odor (CS+) and a non-reinforced odor (CS−) and evaluated generalization to two novel odors whose similarity to the CS+ and the CS− was different. We show, given the same level of discriminatory performance, that rates of generalization are similar between the two conditioning protocols and discuss the possible causes for this phenomenon.

Task specialization influences nestmate recognition ability in ants

Insect societies are a paramount example of efficiency based upon division of labour. Social insect workers specialize on different tasks, such as brood care and foraging. This polyethism is underlined by the development of brain and olfactory organs. Nestmate recognition in ants is based on perception of chemical cues through olfaction; therefore, we asked whether task polyethism affects the ability of ants to discriminate friends from foes. We used the carpenter ant Camponotus aethiops to investigate the ability of three behavioural groups of worker (foragers, nurses and inactives) in recognizing intruders. Foragers, which are older workers mainly performing tasks outside the nest, showed higher levels of aggression towards intruders than nurses did. Foragers appeared to be more efficient at recognizing non-nestmate cues than did intra-nidal workers (nurses and inactives), and they possibly have higher motivation to attack. This suggests that ant workers change their olfactory sensitivity to non-nestmate stimuli during their life. This plasticity could be adaptive, as younger workers, who typically stay inside the nest, usually do not encounter intruders, while older workers have more experience outside the nest and differently developed neural circuits. A sensitive nestmate recognition system would thus be an unnecessary cost early in life.Significance statementAnts are known to divide their workforce, often as a product of age. Younger workers take on safer tasks such as taking care of the brood, while older workers are often involved with more dangerous tasks such as foraging and defending the nest. Here, we show that workers change their olfactory sensitivity to intruders during their life. As a result, foragers are better than nurses at detecting intruders. Furthermore, foragers appeared to not only be more sensitive but also have higher motivation to attack. The higher sensitivity of foragers is most likely adaptive, as younger workers stay in the nest and typically do not encounter intruders, and a sensitive recognition system would be for them an unnecessary cost.