Methyl eugenol regulates mating behavior in oriental fruit flies by enhancing lek attractiveness

Plant-produced volatiles play a pivotal role as mediators in complex interactions between insects and plants. Despite the widespread recognition that these compounds serve as cues for herbivorous insects to locate their preferred host plants, their effects on insect mating behavior are less understood. Here, we show that male oriental fruit flies (Bactrocera dorsalis) are highly attracted to the host plant volatile compound methyl eugenol (ME), which enhances the attractiveness of male leks to females. To elucidate the molecular underpinnings of this phenomenon, we identify the olfactory receptor BdorOR94b1 responsible for detecting ME. Genetic disruption of BdorOR94b1 leads to a complete abolition of both physiological and behavioral responses to ME. Additionally, we confirm that, through digestion, male flies convert ME to (E)-coniferyl alcohol, a compound that enhances the attractiveness of their leks to females. This increased attractiveness allows females to select optimal mates, thereby enhancing their reproductive success. The impairment of ME detection significantly diminishes the mating advantage within the leks, as males are unable to locate and utilize ME effectively. Our findings unveil a novel mechanism through which plant volatile compounds regulate the mating behavior of the economically important oriental fruit fly and provide new insights into the general ecology of insect-plant interactions.