Begging gene leads to drone food

A drone (center) begs worker bees for food. HHU researchers found that the associated complex interaction pattern is genetically specified.
Photo Credit: HHU/Steffen Köhle

Is complex social behavior genetically determined? 

Yes, as a team of biologists from Heinrich Heine University Düsseldorf (HHU), together with colleagues from Bochum and Paris, established during an investigation of bees. They identified a genetic factor that determines the begging behavior of drones, which they use to socially obtain food. They are now publishing their results in the journal Nature Communications. 

Male bees, the "drones," do not have an easy time when trying to access vital proteins. They cannot digest the most important protein source for bees, pollen, on their own. To avoid starvation, they rely on workers to feed them a pre-produced food slurry, which the workers manufacture themselves from pollen. However, to obtain this food, the drones must convince the workers to hand it overusing a specific sequence of behaviors. 

In order to evaluate the behaviour of the drones automatically, QR codes are attached to their backs. A camera system then records their movements.
Photo Credit: HHU/Institute of Evolutionary Genetics

Key Findings

• The "Fruitless" Gene: The researchers pinpointed the "Fruitless" (Fru) protein, a transcription factor active only in males, as the regulator of this behavior.

• Neural Wiring: Using CRISPR-Cas9 to tag the gene with green fluorescent protein, the team traced Fru activity to a network of approximately 1,800 neurons involved in sensory processing and decision-making.

• Behavioral Impact: When the Fru gene was "knocked out" (deactivated), the drones were physically healthy and retained their typical scent profiles, but their social interactions failed. They could not effectively approach workers or solicit food, leading to starvation.

"Such cooperative behavior is a complex matter in the animal kingdom, as it requires close coordination between social partners. In our research, we ask what prerequisites must be met to orchestrate this interplay," explains Prof. Dr. Martin Beye from the Institute of Evolutionary Genetics at HHU. 

A research team led by Prof. Beye investigated the genetic and neural foundations for the bees' cooperative behavior. The biologists searched for regulators that "wire" the brain of the male honeybee during development in such a way that the animals exhibit their innate social behavior for food exchange. Researchers from the Université Paris-Saclay and the Ruhr University Bochum participated in the study published in Nature Communications. 

Microscopic view of the drone’s brain (purple): The neurons belonging to the Fru circuit, which is involved in the animals’ begging behaviour, are marked in green.
Image Credit: HHU/Institute of Evolutionary Genetics

The researchers discovered that the behavioral interactions necessary for food transfer to the drones can be traced back to a so-called transcription factor, the "Fruitless"—or "Fru" for short—protein. A transcription factor is a protein that can switch many other genes in the genome on and off. This factor is active only in male bees. 

Using genetic technologies (CRISPR-Cas9), the researchers introduced a sequence of the "green fluorescent protein" into the Fru gene. This allowed them to mark the cells in which the transcription factor is active. 

Dr. Sven Köhnen, lead author of the study, states: "We detected it in the nervous system of the drones; specifically in neurons where sensory information is processed and which serve in decision-making. From this, we concluded that Fru can determine the innate behavior of the males." In total, Fru influences a neural network of around 1,800 neurons that is closely linked to cooperative behavior. 

The team then generated so-called knock-out mutants in which they switched off the transcription factor Fru. The researchers glued a QR code onto the bodies of the resulting drones and observed their behavior using an automated camera system developed in Düsseldorf. 

Köhnen reports: "The decision-making behavior in these bees was disrupted. They could not approach their conspecifics properly, hardly begged, and consequently received less food." Co-author and doctoral candidate Pia Ulbricht adds: "However, other typical behaviors of the drones were untouched. The knock-out mutants behaved conspicuously only in the context of food intake." 

Furthermore, the mutants did not exhibit a different scent profile, as noted by co-author Thomas Eltz from the Ruhr University Bochum. Endogenous hydrocarbons are responsible for the individual scent, which is important for the interaction of the animals. Likewise, the olfactory center, where scents are processed, was not affected, as established by research partners in Paris, Prof. Dr. Julie Carcaud and Prof. Dr. Jean-Christophe Sandoz. 

Prof. Beye concludes: "Our study shows that the cooperative behavior of drones is determined by a genetic program that has newly formed in the course of evolution. The program establishes the neural controls—specifically whether and for how long the behavioral sequence is executed based on perceived sensory information. Such a mechanism enables the necessary adaptation to the social partner." 

Published in journal: Nature Communications

Title: The fru gene specifies male cooperative behaviors in honeybee colonies

Authors: Sven Köhnen, Pia Ulbricht, Alina Sturm, Julie Carcaud, Jean-Christophe Sandoz, Thomas Eltz, and Martin Beye

Source/Credit: Heinrich-Heine-Universität Düsseldorf

Reference Number: gen122225_01

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