Endocrine responses in the pheromone induction of male sexual maturation in an insect

In animals, sexual maturation is marked by the development of reproductive behaviors in synchronism with the acquisition of fertility, and this timing is influenced by chemosensory experiences. In naïve and immature individuals, exposure to sex pheromones may accelerate sexual development, and mechanisms underlying this pheromone induction are not fully identified. Using the moth Agrotis ipsilon, we showed that pre-exposure of immature males to female sex pheromones led to early increases in the performance of sex pheromone-triggered oriented flight as well as in the maturation of accessory sex glands (ASGs) producing seminal proteins. Conjointly, biosynthesis and circulating amounts of juvenile hormone (JH) raised with an upregulation of the expression of JH receptor, Methoprene-tolerant 1 (Met1) and the JH-inducible transcription factor, Krüppel homolog 1 (Kr-h1) in ASGs and the primary olfactory centers, the antennal lobes (ALs). In the sex pheromone pre-exposed immature males, the loss of function of Met1 or Kr-h1 caused a reduction in the induction of the sex pheromone behavioral responsiveness and the ASG secretory activity. Taken together, our results showed that the accelerated effects of sex pheromone pre-exposure on male sexual maturation are mediated by increased JH biosynthesis. This ultimately leads to early induction of JH signaling in ASGs for seminal protein production and in ALs for the central processing of pheromone information, which causes the display of sexual behavior in male A. ipsilon. Finally, this study expands our understanding of endocrine mechanisms by which animals can modulate their fitness according to past olfactory experiences.