Neural mechanism of circadian clock-based photoperiodism in insects and snails

Abstract

The photoperiodic mechanism distinguishes between long and short days, and the circadian clock system is involved in this process. Although the necessity of circadian clock genes for photoperiodic responses has been demonstrated in many species, how the clock system contributes to photoperiodic mechanisms remains unclear. A comprehensive study, including the functional analysis of relevant genes and physiology of their expressing cells, is necessary to understand the molecular and cellular mechanisms. Since Drosophila melanogaster exhibits a shallow photoperiodism, photoperiodic mechanisms have been studied in non-model species, starting with brain microsurgery and neuroanatomy, followed by genetic manipulation in some insects. Here, we review and discuss the involvement of the circadian clock in photoperiodic mechanisms in terms of neural networks in insects. We also review recent advances in the neural mechanisms underlying photoperiodic responses in insects and snails, and additionally circadian clock systems in snails, whose involvement in photoperiodism has hardly been addressed yet. Brain neurosecretory cells, insulin-like peptide/diuretic hormone44-expressing pars intercerebralis neurones in the bean bug Riptortus pedestris and caudo-dorsal cell hormone-expressing caudo-dorsal cells in the snail Lymnaea stagnalis, both promote egg laying under long days, and their electrical excitability is attenuated under short and medium days, which reduces oviposition. The photoperiodic responses of the pars intercerebralis neurones are mediated by glutamate under the control of the clock gene period. Thus, we are now able to assess the photoperiodic response by neurosecretory cell activity to investigate the upstream mechanisms, that is, the photoperiodic clock and counter.

One seasonal clock fits all?

“…PDF has been identified in many insects as the signaling molecule transmitting the time information from the central circadian clock cells (Renn et al 1999 ; Helfrich-Förster et al 2000 ; Beer et al 2018 ; Petri and Stengl 1997 ; Singaravel et al 2003 ). As mentioned above, PDF has also been found to be involved in photoperiodic responses in a number of insects (Hamanaka et al 2023 ). A recent study showed a co-transcription factor EYES ABSENT (EYA) as the downstream target of PDF linking the circadian clock to photoperiodic regulation in Drosophila (Hidalgo et al 2023 ).…”

“…Both involve the conversion of serotonin to melatonin as an initial step to break diapause, but the photoperiodic pathway uses the day length measure of the circadian clock, while the non-photic pathway is triggered by environmental factors such as temperature. Downstream, a number of species-dependent neuroendocrine pathways are involved, with pigment dispersing factor (PDF) as one common main factor conveying the photoperiodic information (Colizzi et al 2023a , b ; Hamanaka et al 2023 ).…”

Photoperiodic plasticity of pigment-dispersing factor immunoreactive fibers projecting toward prothoracicotropic hormone neurons in flesh fly Sarcophaga similis larvae

“…For seasonal adaptation, a large number of insects inhabiting temperate zones alter their physiological states for development or diapause according to photoperiod. The mechanisms underlying insect photoperiodic responses include photoreceptors, photoperiodic clocks, photoperiodic counters, and endocrine systems (Saunders, 2002;Shiga 2023;Hamanaka et al 2023).…”