Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology最新文献

The fruit fly Drosophila melanogaster exhibits two activity peaks, one in the morning and another in the evening. Because the two peaks change phase depending on the photoperiod they are exposed to, they are convenient for studying responses of the circadian clock to seasonal changes. To explain the phase determination of the two peaks, Drosophila researchers have employed the two-oscillator model, in which two oscillators control the two peaks. The two oscillators reside in different subsets of neurons in the brain, which express clock genes, the so-called clock neurons. However, the mechanism underlying the activity of the two peaks is complex and requires a new model for mechanistic exploration. Here, we hypothesize a four-oscillator model that controls the bimodal rhythms. The four oscillators that reside in different clock neurons regulate activity in the morning and evening and sleep during the midday and at night. In this way, bimodal rhythms are formed by interactions among the four oscillators (two activity and two sleep oscillators), which may judiciously explain the flexible waveform of activity rhythms under different photoperiod conditions. Although still hypothetical, this model would provide a new perspective on the seasonal adaptation of the two activity peaks.

Pittendrigh and Daan's 1976 article "Pacemaker structure: A clock for all seasons" marks the foundation of modern seasonal chronobiology. It proposed the internal coincidence model comprised of a Morning (M) and Evening (E) oscillator, which are coupled but synchronized separately by dawn and dusk. It has become an attractive model to explain the seasonal adaptation of circadian rhythms. Using the example of the European hamster, this article connects the classical entrainment concept to species decline and, ultimately, conservation concepts. Seasonality of this species is well studied and circannual rhythms have been described in at least 32 parameters. The European hamster is listed as critically endangered on the International Union for Conservation of Nature (IUCN) red list. Changes in the temporal structure of the environment (the chronotope) caused by climate change and light pollution might be responsible for the global decline. The article shows that classical chronobiological concepts such as the internal coincidence model (Pittendrigh and Daan Pittendrigh and Daan, J Comp Physiol [a] 106:333-355, 1976) are helpful to understand the (chronobiological) causes of the decline and can potentially support species conservation. Knowing the species' physiological limitations as well as its adaptation capacities can potentially prevent its extinction at a time when classical conservation concepts have reached their limits.

Numerous insect species living in temperate regions survive adverse conditions, such as winter, in a state of developmental arrest. The most reliable cue for anticipating seasonal changes is the day-to-night ratio, the photoperiod. The molecular mechanism of the photoperiodic timer in insects is mostly unclear. Multiple pieces of evidence suggest the involvement of circadian clock genes, however, their role might be independent of their well-established role in the daily oscillation of the circadian clock. Furthermore, reproductive diapause is preferentially studied in females, whereas males are usually used for circadian clock research. Given the idiosyncrasies of male and female physiology, we decided to test male reproductive diapause in a strongly photoperiodic species, the linden bug Pyrrhocoris apterus. The data indicate that reproduction is not under circadian control, whereas the photoperiod strongly determines males' mating capacity. Clock mutants in pigment dispersing factor and cryptochrome-m genes are reproductive even in short photoperiod. Thus, we provide additional evidence of the participation of circadian clock genes in the photoperiodic time measurement in insects.

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.

Adaptation of physiology and behavior to seasonal changes in the environment are for many organisms essential for survival. Most of our knowledge about the underlying mechanisms comes from research on photoperiodic regulation of reproduction in plants, insects and mammals. However, even humans, who mostly live in environments with minimal seasonal influences, show annual rhythms in physiology (e.g., immune activity, brain function), behavior (e.g., sleep-wake cycles) and disease prevalence (e.g., infectious diseases). As seasonal variations in environmental conditions may be drastically altered due to climate change, the understanding of the mechanisms underlying seasonal adaptation of physiology and behavior becomes even more relevant. While many species have developed specific solutions for dedicated tasks of photoperiodic regulation, we find a number of common principles and mechanisms when comparing insect and mammalian systems: (1) the circadian system contributes to photoperiodic regulation; (2) similar signaling molecules (VIP and PDF) are used for transferring information from the circadian system to the neuroendocrine system controlling the photoperiodic response; (3) the hormone melatonin participates in seasonal adaptation in insects as well as mammals; and (4) changes in photoperiod affect neurotransmitter function in both animal groups. The few examples of overlap elaborated in this perspective article, as well as the discussion on relevance for humans, should be seen as encouragement to unravel the machinery of seasonal adaptation in a multitude of organisms.

Circadian clocks are internal timing devices that have evolved as an adaption to the omnipresent natural 24 h rhythmicity of daylight intensity. Properties of the circadian system are photoperiod dependent. The phase of entrainment varies systematically with season. Plastic photoperiod-dependent re-arrangements in the mammalian circadian core pacemaker yield an internal representation of season. Output pathways of the circadian clock regulate photoperiodic responses such as flowering time in plants or hibernation in mammals. Here, we review the concepts of seasonal entrainment and photoperiodic encoding. We introduce conceptual phase oscillator models as their high level of abstraction, but, yet, intuitive interpretation of underlying parameters allows for a straightforward analysis of principles that determine entrainment characteristics. Results from this class of models are related and discussed in the context of more complex conceptual amplitude-phase oscillators as well as contextual molecular models that take into account organism, tissue, and cell-type-specific details.

Decades have now passed since Colin Pittendrigh first proposed a model of a circadian clock composed of two coupled oscillators, individually responsive to the rising and setting sun, as a flexible solution to the challenge of behavioral and physiological adaptation to the changing seasons. The elegance and predictive power of this postulation has stimulated laboratories around the world in searches to identify and localize such hypothesized evening and morning oscillators, or sets of oscillators, in insects, rodents, and humans, with experimental designs and approaches keeping pace over the years with technological advances in biology and neuroscience. Here, we recount the conceptual origin and highlight the subsequent evolution of this dual oscillator model for the circadian clock in the mammalian suprachiasmatic nucleus; and how, despite our increasingly sophisticated view of this multicellular pacemaker, Pittendrigh's binary conception has remained influential in our clock models and metaphors.

Animals living at high latitudes are exposed to prominent seasonal changes to which they need to adapt to survive. By applying Zeitgeber cycles of different periods and photoperiods we show here that high-latitude D. ezoana flies possess evening oscillators and highly damped morning oscillators that help them adapting their activity rhythms to long photoperiods. In addition, the damped morning oscillators are involved in timing diapause. The flies measure night length and use external coincidence for timing diapause. We discuss the clock protein TIMELESS (d-TIM) as the molecular correlate and the small ventrolateral clock neurons (s-LN_vs) as the anatomical correlates of the components measuring night length.

The identity and nature of the photoperiodic photoreceptors are now quite well known, as is the nature of the endocrine regulation of the resulting diapauses. The central problem of time measurement-how the photoperiodic clock differentiates long from short days-however, is still obscure, known only from whole-animal experiments and abstract models, although it is clearly a function of the insect circadian system. This review describes some of these experiments in terms of oscillator entrainment and two widely applicable photoperiodic clock models, external and internal coincidence, mainly using data from experiments on flesh flies (Sarcophaga spp) and the parasitic wasp, Nasonia vitripennis.

In 1976, Pittendrigh and Daan established a theoretical framework which has coordinated research on circadian clock entrainment and photoperiodism until today. The "wild clocks" approach, which concerns studying wild species in their natural habitats, has served to test their models, add new insights, and open new directions of research. Here, we review an integrated laboratory, field and modeling work conducted with subterranean rodents (Ctenomys sp.) living under an extreme pattern of natural daily light exposure. Tracking animal movement and light exposure with biologgers across seasons and performing laboratory experiments on running-wheel cages, we uncovered the mechanisms of day/night entrainment of the clock and of photoperiodic time measurement in this subterranean organism. We confirmed most of the features of Pittendrigh and Daan's models but highlighted the importance of integrating them with ecophysiological techniques, methodologies, and theories to get a full picture of the clock in the wild. This integration is essential to fully establish the importance of the temporal dimension in ecological studies and tackling relevant questions such as the role of the clock for all seasons in a changing planet.