Integrative study of cogNitive abilities on Social InTeractionS in Drosophila melanogaster – INSIghTS

To tackle our questions, we use several methodologies and approaches. The main ones are behavioral assays, in which pairs of socially naive males are in competition for food. This creates competition for a valuable resource and leads to animals developing aggressive behaviors, and ultimately establishing dominance. In courtship experiment, a male and a female are paired together to induce reproductive behavior. We employ genetic tools to manipulate genes expression level and to interfere with the neuronal activity of specific set of neuronal populations. We also use in vivo calcium imaging to record high-order neuronal activity in response to chemo-sensory cues. Finally, we also use spectrometry technics to measure the amount of cuticular hydrocarbons.

Our results showed consequences of aggressive interactions. Animals' behaviors and performances are highly dependent on their cognitive abilities and chemical communication to adapt and improve fighting strategies. In subsequent contest, both dominants and subordinates learn from a single fighting experience, remember the outcome of their last fight, and develop short-term winner and loser effects from these information lasting minutes to hours. However, only subordinates form a long-lasting loser effect dependent on de novo protein synthesis, for at least a day in consequences of five repeated fighting bouts. We also showed that winning experience can impact the reproductive success of the animals. We are currently investigating how fighting experience can impact animals' fitness. We also demonstrated that fruit flies that have been raised under different dietary conditions (with or without sugar) have adapted their patterns of aggressive behavior and developed distinct fighting strategies: one favoring physical attacks, while the other one favoring visual threats. This shows the crucial role of dietary regime on the expression of aggressive behaviors. In parallel, we have identified neural circuits involved in aggression and we are currently investigating the molecular mechanisms used by these neurons.

Aggression is an innate, complex, and pervasive social behavior observed throughout the animal kingdom. As an innate behavior, the neural basis underlying aggression is genetically hardwired. However, external sensory cues, past experiences and the internal state of the animal, strongly influence aggression, demonstrating the adaptive and malleable features of this complex behavior. Therefore, for neuroscientists, aggression represents an ideal model for investigating the neural plasticity and genetic mechanisms associated with behavioral decision-making, while gaining insights into potential evolutionary processes.
On one hand, through this project, we were able to demonstrate how dietary conditions affect the expression of aggressive behaviors and the strategy employed by the animals to reach dominance. When having free access to sugar during their development, animals favor the use of physical attaques, while when being deprived of sugar, animals prefer using visual threats. However, both fighting strategy allow animals to establish dominance against conspecifics.
On the other hand, we showed that fighting experience affect animals' fitness. Current investigations aim to understand how previous fighting experience regulate fitness.
Future tasks of the projet will be dedicated to identify neural substrates that modulate the animals' aggressiveness level, and locate the ones involved in both short- and long-term memories; to study the role of chemical communication mechanisms on social interactions; and to understand how and where chemosensory signals are integrated within the brain and how the internal state of the animal influences signal integration.

Legros J, Tang G, Gautrais J, Fernandez MP, Trannoy S. Long-Term Dietary Restriction Leads to Development of Alternative Fighting Strategies. Front Behav Neurosci. 2021 Jan 14;14:599676. doi: 10.3389/fnbeh.2020.599676. PMID: 33519392; PMCID: PMC7840567.

One of the fundamental goals in neuroscience research, is to understand how the brain integrates the multitude of sensory cues from a constantly changing environment to generate appropriate behavioral responses and ultimately form memory. For survival and reproductive success, animals must adapt their behavioral responses, learn new strategies that succeed in gaining desired resources, and store memories to drive future behavioral decision-making. In these situations, aggression is commonly employed to access to food, mates and territory. Such kind of naturally-complex social behavior is composed of innate and learned components, and its traits have been shaped by evolution like that of any other behavioral phenotype. The success of such aggressive interactions relies on using the best fighting strategy, which is build by prior experiences and by gathering information about opponents’ strength. Phenomena called "winner and loser effects" - individuals with previous wins become more likely to win again, while a loss lowers an individual’s chances for future wins - have been reported in a large number of animal species, including humans(1). They participate to the stabilization of social hierarchies(2) among conspecifics, and have been postulated to modulate males' reproductive fitness(3) by either affecting the animals' physiology and/or the females' receptivity. However, studies exploring in parallel both ultimate and proximate causations of these winner and loser effects are very limited due to the lack of a tractable model system with robust cognitive capacities.
The aim of the integrative and multi-level INSIghTS project, is to investigate such mechanisms underlying winner/loser effects, by identifying molecular mechanisms and their underlying circuitry, while in parallel exploring the impacts on future social interactions in Drosophila melanogaster.