An odorant-binding protein mediates sexually dimorphic behaviors via binding male-specific 2-heptanone in migratory...

Migratory locusts (Locusta migratoria) frequently aggregate into huge swarms that cause serious economic losses for the agricultural sector. Differential behaviors of male and female insects may contribute to such population explosions. However, the key olfactory mechanisms underlying different behaviors associated with sex-related pheromones are unclear. Here, we report that male-specific odor, 2-heptanone plays different roles in relation to the behavior of migratory locust males and females, and that this sexual dimorphism involves a soluble odorant-binding protein (OBP) in the peripheral olfactory processes. This odor strongly binds to LmigOBP4, a novel OBP, present in antennal trichoid sensilla, and elicits opposite locomotor tendencies between the sexes: attracting females and repelling males. Furthermore, an adult male group mimicked a high dosage of 2-heptanone by promoting their attractiveness to single females. Additionally, RNAi suppression of Lmigobp4 expression reduced the physiological responses to 2-heptanone to levels that were indistinguishable between the sexes. This suppression reversed the adult behavioral responses to 2-heptanone, i.e., females were repelled and males were attracted. We conclude that LmigOBP4 is associated with olfactory recognition of male-specific 2-heptanone, which plays dual roles that differ between adult male and female migratory locusts.