Olfatask: the role of olfaction in bees, queens of social organisation

Bees are fascinating insects. In addition to being outstanding pollinators and remarkable architects and honey producers, they have the most advanced social organisation in the living world: eusociality. This means that individuals are divided into fertile or non-fertile castes and the maximum division of labour. "Eusocial species are those with the highest level of sociality," confirms Julie Carcaud, lecturer at the Evolution, Genomes, Behaviour and Ecology Laboratory (EGCE - Univ. Paris-Saclay/CNRS/IRD). Awarded an ERC Starting Grant for her Olfatask project in 2024, this neuroscience biologist is particularly interested in the social organisation of bees. Her new research project aims to reveal the logics implemented within hives, focusing in particular on the role of olfaction in this highly structured organisation.
 

Eusociality, a maximum division of labour synonymous with prosperity for the species

In a eusocial system like a hive, each bee has a well-defined role. Nurse bees look after the eggs and larvae, foragers supply the hive with pollen and nectar and guard bees protect the hive from intruders. This division of labour is so advanced that it even affects reproduction; in bees, the queen is the only female in the hive to reproduce.

There are other eusocial species in the insect world, such as ants and wasps, and even two species of eusocial mammals, both types of mole-rats, that live in colonies. And although the human species also applies a certain division of labour among its members, it remains less advanced than in the case of eusociality.
This division of labour, taken to its fullest extent, proves highly effective. "Studies show that this division of labour is accompanied by greater growth," comments Julie Carcaud. However, the mechanisms by which each individual finds its role in this organisation remain unknown. How do bees allocate their tasks? How is this division of labour implemented in insect colonies?
 

Age as the first response

In the 1960s, while observing bees, scientists identified the first clue: a correlation between the role of bees in a hive and their age. The youngest bees are responsible for feeding the eggs and the queen. "Then, as they grow, they take on more and more tasks outside the colony," explains Julie Carcaud. Firstly, guarding the hive and fighting predators such as hornets, then foraging at the end of the bee's life.

However, in a previous experiment in which a group of young bees of the same age were placed in a hive, after two weeks, scientists observed the same division of labour as in a normal hive. "This shows that this behaviour can be adapted and is not just age-related," says Julie Carcaud.
 

Allocation of roles and sensitivity: a causal link?

In other research, a "response threshold" model emerged, according to which "a bee will attend to certain tasks depending on its sensitivity to different sensory stimuli". For foraging bees, for example, "those sensitive to higher sugar levels will seek nectar, while others will bring back water or pollen. However, the question of causality remains," notes the EGCE laboratory researcher. Is a bee less sensitive to sugar because it harvests nectar, or does it harvest nectar because it is less sensitive to sugar?

Another element already known to scientists is the existence of numerous pheromones used by bees, and the role these chemicals play in organising the hive. Emitted by individuals to communicate with each other, pheromones are involved in the queen's communication of her status, for example. "The molecules emitted by the queen to signal her presence in the hive to the other bees have been identified. These pheromones have a dual role; telling the workers to look after the queen and inhibiting the development of their ovaries. As a result, the queen is the only reproductive female in the hive," comments Julie Carcaud.

In the context of her Olfatask project, Julie Carcaud is investigating the influence of olfaction and in particular pheromone perception, on the division of labour by comparing the neuronal pathways used by bees to process information between different castes. "Among eusocial species, the honeybee has the advantage of being the species for which the chemistry of pheromones and their behavioural effects are most well known." But how this information is processed by the insects' brains remains largely unexplored. "There's surprisingly little literature on the link between olfaction, which is the sense favoured by insects, and their social organisation," notes Julie Carcaud, whose Olfatask project opens up a new angle of study.
 

Monitoring neuronal activity in genetically modified bees

However, illustrating a bee's neural activity is far from easy. Julie Carcaud has therefore designed a unique experiment combining modern biological techniques and state-of-the-art microscopy. With her team and colleagues from Germany and Italy, she has succeeded in obtaining genetically modified bees capable of producing a calcium-sensitive fluorescent protein. "When a neuron activates in the brain of these bees, it increases the concentration of intracellular calcium, which causes an increase in fluorescence." In these genetically modified bees, the neurons light up in real time. Using a suitable microscope, Julie Carcaud can then observe which region of the bees' brain processes a given stimulus.

Successfully producing genetically modified bees is also a considerable achievement, as this is particularly difficult with these insects due to their eusocial organisation and mode of reproduction. The strategy generally employed is to create a few genetically modified individuals and then get them to reproduce with each other. But, in bees, "the queen is the only female in the colony to reproduce," reminds Julie Carcaud. This means that a genetically modified egg has to become a queen, an element over which scientists have little control. In fact, it is the worker bees that decide which egg will be fed royal jelly long enough to become a queen, and the rules remain unknown to scientists. "I even think that the nurse bees detect the genetically modified eggs and stop feeding them, because we observe a loss of around 90% of these eggs," says Julie Carcaud, who has however persevered and managed to implement a neural imaging of bees.

With the ERC funding awarded to Olfatask, the neurobiologist now has new maps which can be used to further investigate the role of olfaction in the division of labour in bees. "Initially, we're going to establish the olfactory differences between the nurse bees, guard bees and foragers, to find out just how differently they smell things," says Julie Carcaud. The next step is to clarify the causal relationship between olfaction and organisation: "Does modifying a bee's olfaction change its role in the hive?" asks Julie Carcaud. The answer is still to come, thanks to this project. 

Publication:

Carcaud, J., et al. Multisite imaging of neural activity using a genetically encoded calcium sensor in the honey bee. PLoS Biology, 21(1): e3001984, 1-20, 2023.