Induction of rhythmicity in prothoracicotropic hormone and ecdysteroids in Rhodnius prolixus: roles of photic and neuroendocrine Zeitgebers

Abstract

Circadian rhythms have been described in Rhodnius prolixus in both the release of prothoracicotropic hormone (PTTH) from the brain complex and the synthesis (and release) of ecdysteroids by the prothoracic glands (PGs). The PGs possess a circadian oscillator that is light-sensitive in vitro. The present work reports the ability of a ‘lights-off’ signal to induce rhythmicity in both PTTH and ecdysteroids in whole animals. Continuous light (LL) caused cessation of release of PTTH; rhythmic release was promptly initiated by transfer to darkness (DD). We infer a light-sensitive circadian oscillator that regulates PTTH release and discuss evidence of its location in the protocerebrum. PGs maintained in LL became arrhythmic but maintained a developmental modulation of steroidogenesis. Transfer of animals to DD initiated rhythmic steroidogenesis; thus, the ‘PG oscillator’ operates in vivo despite an overlying cuticle. The first initiated peak in steroidogenesis precedes that of PTTH by several hours and was not impaired when PTTH release was prevented by prior injection of tetrodotoxin. In normal animals (PTTH present), the phase of the induced rhythm of steroidogenesis was shifted in a single cycle to align with that of PTTH release. We conclude that both ‘brain oscillator’ and ‘PG oscillator’ are photosensitive, and the induced PTTH rhythm regulates the phase of rhythmic steroidogenesis. This neuroendocrine axis contains (at least) three photosensitive oscillators, in which classical pacemaker and slave oscillators are not obvious. Caution in the application of formal terminology to discrete tissues is urged. This multioscillator timing system appears to direct the circadian organization of development through the rhythm in haemolymph ecdysteroids that reaches ecdysone-responsive cells.