Drosophila Avoids Parasitoids by Sensing Their Semiochemicals via a Dedicated Olfactory Circuit

Detecting danger is one of the foremost tasks for a neural system. Larval parasitoids constitute clear danger to Drosophila, as up to 80% of fly larvae become parasitized in nature. We show that Drosophila melanogaster larvae and adults avoid sites smelling of the main parasitoid enemies, Leptopilina wasps. This avoidance is mediated via a highly specific olfactory sensory neuron (OSN) type. While the larval OSN expresses the olfactory receptor Or49a and is tuned to the Leptopilina odor iridomyrmecin, the adult expresses both Or49a and Or85f and in addition detects the wasp odors actinidine and nepetalactol. The information is transferred via projection neurons to a specific part of the lateral horn known to be involved in mediating avoidance. Drosophila has thus developed a dedicated circuit to detect a life-threatening enemy based on the smell of its semiochemicals. Such an enemy-detecting olfactory circuit has earlier only been characterized in mice and nematodes.侦测危险是神经系统的核心任务之一。拟寄生物幼虫对果蝇（Drosophila）构成显著威胁——自然界中高达80%的果蝇幼虫会被寄生。本研究证实，黑腹果蝇（Drosophila melanogaster）的幼虫与成虫均会避开带有主要拟寄天敌——广腹细蜂属（Leptopilina）黄蜂——气味的区域。该规避行为由一类高度特化的嗅觉感觉神经元（olfactory sensory neuron, OSN）介导。幼虫的OSN表达嗅觉受体Or49a，并对广腹细蜂的气味物质虹膜蚁素（iridomyrmecin）产生特异性响应；而成虫则同时表达Or49a与Or85f两种受体，此外还能侦测黄蜂释放的气味物质猕猴桃碱（actinidine）与荆芥内酯醇（nepetalactol）。上述信号通过投射神经元传递至侧角（lateral horn）的特定区域，该区域已被证实参与调控规避行为。由此可见，黑腹果蝇演化出了一套专属的神经环路，可通过感知天敌的信息化学物质气味来侦测这一致命天敌。此前仅在小鼠与线虫中报道过这类用于侦测天敌的嗅觉神经环路。