Evolution of the neuronal substrate for kin recognition in social Hymenoptera

In evolutionary terms, life is about reproduction. Yet, in some species, individuals forgo their own reproduction to support the reproductive efforts of others. Social insect colonies for example, can contain up to a million workers that actively cooperate in tasks such as foraging, brood care and nest defence, but do not produce offspring. In such societies the division of labour is pronounced, and reproduction is restricted to just one or a few individuals, most notably the queen(s). This extreme eusocial organisation exists in only a few mammals, crustaceans and insects, but strikingly, it evolved independently up to nine times in the order Hymenoptera (including ants, bees and wasps). Transitions from a solitary lifestyle to an organised society can occur through natural selection when helpers obtain a fitness benefit from cooperating with kin, owing to the indirect transmission of genes through siblings. However, this process, called kin selection, is vulnerable to parasitism and opportunistic behaviours from unrelated individuals. An ability to distinguish kin from non-kin, and to respond accordingly, could therefore critically facilitate the evolution of eusociality and the maintenance of non-reproductive workers. The question of how the hymenopteran brain has adapted to support this function is therefore a fundamental issue in evolutionary neuroethology. Early neuroanatomical investigations proposed that social Hymenoptera have expanded integrative brain areas due to selection for increased cognitive capabilities in the context of processing social information. Later studies challenged this assumption and instead pointed to an intimate link between higher social organisation and the existence of developed sensory structures involved in recognition and communication. In particular, chemical signalling of social identity, known to be mediated through cuticular hydrocarbons (CHCs), may have evolved hand in hand with a specialised chemosensory system in Hymenoptera. Here, we compile the current knowledge on this recognition system, from emitted identity signals, to the molecular and neuronal basis of chemical detection, with particular emphasis on its evolutionary history. Finally, we ask whether the evolution of social behaviour in Hymenoptera could have driven the expansion of their complex olfactory system, or whether the early origin and conservation of an olfactory subsystem dedicated to social recognition could explain the abundance of eusocial species in this insect order. Answering this question will require further comparative studies to provide a comprehensive view on lineage-specific adaptations in the olfactory pathway of Hymenoptera.