Neural circuits regulating social dominance implement a strategy predicted by evolutionary game theory

Abstract

Social conflict is a fundamental challenge for all animals and determines access to critical resources like mates and food. Evolutionary game theory predicts that natural selection should yield competitive strategies that balance the benefits and costs of social conflict. However, whether such strategies are embedded within the neural circuits that regulate aggression remains unclear. Here, we identify a neural circuit regulating the decision to flee during fighting in male Drosophila and show that the onset of defeat is governed by a probabilistic strategy predicted by evolutionary game theory. This mechanism arises from the inhibition of Tk-GAL4FruM neurons that promote aggressive arousal in males. Inhibition is mediated by a mushroom body circuit involving PPL1 dopaminergic neurons and V2 mushroom body output neurons, both classically associated with aversive learning. Silencing this circuit disrupts the onset of defeat, while activating it induces rapid defeat. Conversely, activation of reward-encoding PAM dopaminergic neurons promotes winning, revealing a dual role for dopamine in shaping contest dynamics. Finally, we find that internal state variables such as hunger and motivation shift the defeat onset probability distribution, consistent with game theory predictions of how payoff modulates fighting persistence. Together, our results provide direct evidence that evolutionary strategies based on payoff, long described by game theory, are implemented as circuit-level computations that regulate aggression.