Fruit fly crowds touch-and-tell

Groups of animals show enhanced decision-making compared to individuals but the neural pathways underlying collective behaviors remain largely unknown. Elevated Drosophila group reactions to environmental cues emerge from inter-fly touch interactions and a specific set of mechanosensory neurons. This provides an entry point for the neurobiological investigation of collective behavior.

HFSP Long-Term Fellow Pavan Ramdya and colleagues
authored on Mon, 05 January 2015

In animals the wisdom of crowds can impose order onto otherwise diverse behavioral inclinations. For example, tourists leaving a subway train are often attentive to the decisions of other passengers to identify the nearest exit. Investigations of how the brain facilitates decentralized group decisions have been limited by the difficulty of manipulating neural activity in animals such as schooling fish or flocking birds. In a study recently published in Nature, HFSP Long-Term Fellow Pavan Ramdya and colleagues were able to uncover the neurons responsible for a collective behavior in Drosophila melanogaster.

Figure: Touch by a moving fly causes a stationary animal to walk in a stereotyped manner. This response can be a complex sequence of backwards, sideways, and forward motion that depends on the appendage touched. In this image, the trajectories of many dozens of walking responses are color-coded by the location of touch on the legs (e.g., left front leg - L1; right rear leg - R3) or wings (W).

Using behavioral tracking, the authors discovered that flies more effectively avoid a noxious odor in groups rather than in isolation. High-resolution videos implicated inter-fly touch in the emergence of group odor avoidance: odor responsive flies would touch sedentary ones, causing them to generate stereotyped walking reactions depending on the location of touch (see Figure). Touch-evoked locomotion would then cascade through the group causing a rapid escape from the odor zone. Using computational modeling, the authors determined that suppressing these touch reactions should abolish collective behavior. To test this prediction, they used genetic approaches to silence the activity of Drosophila leg mechanosensory neurons. These manipulations revealed that a small subset of neurons decorating the ends of the fly’s legs is required for inter-fly touch reactions. Silencing these neurons made groups of flies act like isolated individuals, as predicted by their computational model. Most remarkably, when a mutant animal insensitive to the odor was placed in a group of normal, smelling flies, it could be coerced to escape the odor zone as well. This suggests that touch interactions may represent a simple form of communication for Drosophila.

These results imply that collective behavior might be far more widespread than commonly appreciated. They also open the door to a neural-circuit level understanding of how an individual’s actions may influence and be influenced by the group. Future work will focus on bridging mechanistic levels from gene expression to individual touch-reactions and collective behavior, with the aim of providing a deeper understanding of the evolution of behavior in animal groups.

Reference

Mechanosensory interactions drive collective behaviour in Drosophila. Pavan Ramdya, Pawel Lichocki, Steeve Cruchet, Lukas Frisch, Winnie Tse, Dario Floreano, and Richard Benton. Nature (2014) DOI: 10.1038/nature14024.

Link to article & videos

Commentary: National Geographic

Commentary: EPFL

Link to Pavan Ramdya's website

Pubmed link