The cuticular hydrocarbon profiles of honey bee workers develop via a socially-modulated innate process

Abstract

Large social insect colonies exhibit a remarkable ability for recognizing group members via colony-specific cuticular pheromonal signatures. Previous work suggested that in some ant species, colony-specific pheromonal profiles are generated through a mechanism involving the transfer and homogenization of cuticular hydrocarbons (CHCs) across members of the colony. However, how colony-specific chemical profiles are generated in other social insect clades remains mostly unknown. Here we show that in the honey bee ( Apis mellifera), the colony-specific CHC profile completes its maturation in foragers via a sequence of stereotypic age-dependent quantitative and qualitative chemical transitions, which are driven by environmentally-sensitive intrinsic biosynthetic pathways. Therefore, the CHC profiles of individual honey bees are not likely produced through homogenization and transfer mechanisms, but instead mature in association with age-dependent division of labor. Furthermore, non-nestmate rejection behaviors seem to be contextually restricted to behavioral interactions between entering foragers and guards at the hive entrance.

eLife digest

Honey bees are social insects that live in large groups called colonies, within structures known as hives. The young adult bees stay within the hive to build nests and care for the young, while the older bees leave the hive to forage for food. Honey bees store food and other valuable resources in their hives, so they are often targeted by predators, parasites and ‘robber’ bees from other colonies. Therefore, it is important for bees to determine whether individuals trying to enter the nest are group members or intruders.

While it is known that social insects use blends of waxy chemicals called cuticular hydrocarbons to identify group members at the entrance to the colony, it is not clear how members of the same colony acquire a similar blend of cuticular hydrocarbons. Some previous work suggested that in some ant species (which are also social insects), colony members exchange cuticular hydrocarbons with each other so that all members of the colony are covered with a similar blend of chemicals. However, it was not known whether honey bees also share cuticular hydrocarbons between colony members in order to identify members of a hive.

Vernier et al. used chemical, molecular and behavioral approaches to study the cuticular hydrocarbons found on honey bees. The results show that, rather than exchanging chemicals with other members of their colony, individual bees make their own blends of cuticular hydrocarbons. As a bee ages it makes different blends of cuticular hydrocarbons, and by the time it starts to leave the hive to forage it makes a blend that is specific to the colony it belongs to. The production of this final blend is influenced by the environment within the hive.

Thus, the findings of Vernier et al. indicate that honey bees guarding the entrance to a hive can only identify non-colony-member forager bees as intruders, rather than any non-colony-member bee that happens upon the hive entrance. Honey bees play an essential role in pollinating many crop plants so understanding how these insects maintain their social groups may help to improve agriculture in the future. Furthermore, this work may aid our understanding of how other social insects interact in a variety of biological situations.