Transient post–mating inhibition of behavioural and central nervous responses to sex pheromone in an insect

Abstract

Mating is costly for both male and female insects and should therefore only occur if it is likely to be successful. Within one scotophase, which is the dark period of the light cycle, male moths can only produce one single spermatophore, which is transferred to the female during mating. Remating within the same scotophase would thus be unsuccessful. We tested the hypothesis that newly mated males of the moth Agrotis ipsilon have developed an energy-saving strategy based on the transient inhibition of their sexual behaviour, thus avoiding unsuccessful remating. Agrotis ipsilon males do not copulate more than once during the same scotophase. Moreover, newly mated males do not respond behaviourally to the female sex pheromone although electroantennograms showed that their peripheral olfactory system is fully functional. However, intracellular recordings of antennal lobe neurons showed that the sensitivity for the synthetic sex pheromone blend decreased as compared with that of unmated males. Both the sexual behaviour and the sensitivity of the antennal lobe neurons were restored when tested during the next scotophase. Our results show a fast, transient neuronal plasticity that 'switches off' the olfactory system, which could prevent males from mating unsuccessfully.

Identification of the Sex Pheromone of Copitarsia decolora (Lepidoptera: Noctuidae)

“…Mating in C. decolora males was associated with a decrease in behavioral responses, similar to those observed in A. ipsilon mated males (Gadenne et al 2001). In A. ipsilon, mating triggers the release of neuromodulators that have the ability to modulate antennal lobe neurons in response to female sex pheromones and affect the development of the sex accessory glands, but antennal sensitivity is not affected (Duportets et al 1998;Gadenne et al 2001).…”

“…In A. ipsilon, mating triggers the release of neuromodulators that have the ability to modulate antennal lobe neurons in response to female sex pheromones and affect the development of the sex accessory glands, but antennal sensitivity is not affected (Duportets et al 1998;Gadenne et al 2001). In contrast, in C. decolora the antennal sensitivity is affected by mating.…”

“…For some moth species such as Plutella xylostella (L.) (Zhang et al 2009), Agrotis ipsilon (Hufnagel) (Anton & Gadenne 1999;Gadenne & Anton 2000;Gadenne et al 2001;Barrozo et al 2010aBarrozo et al , 2010bBarrozo et al , 2011, Heliothis virescens (F.) and Heliothis subflexa (Guenée) (Soques et al 2010) it has been demonstrated that age and mating status can modify olfactory reception and sexual pheromone processing in males. In these species, the male response to the female sex pheromone is regulated by hemolymph titers of juvenile hormone (JH) (Gadenne et al 1993;Duportets et al 1998;Anton & Gadenne 1999;Gadenne & Anton 2000), and by neuromodulators that act on ORNs and AL neurons (Anton et al 2007).…”

Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin

“…An elevated protein content of the SAGs allows the mature male to produce and transfer a spermatophore into the female (Duportets et al, 1998). Moreover, we previously showed that newly mated males are no longer attracted to sex pheromone and that the response to pheromone is restored during the next night (Gadenne et al, 2001). This plasticity is not only seen at the behavioural level but is also accompanied by a decrease in the sensitivity of neurons within the primary olfactory centre, the antennal lobe (AL); most neurons have much higher pheromone response thresholds after mating (Gadenne et al, 2001).…”

“…Moreover, we previously showed that newly mated males are no longer attracted to sex pheromone and that the response to pheromone is restored during the next night (Gadenne et al, 2001). This plasticity is not only seen at the behavioural level but is also accompanied by a decrease in the sensitivity of neurons within the primary olfactory centre, the antennal lobe (AL); most neurons have much higher pheromone response thresholds after mating (Gadenne et al, 2001). This transient olfactory plasticity allows newly mated males to 'wait' and eventually feed to refill their reproductive glands (Duportets et al, 1998).…”