Photoperiodism:Shall EYA Compare Thee to a Summer's Day?

SummarySeasonal changes in day length are used by plants and animals to synchronize annual rhythms in reproduction, physiology, and behavior to the environment. Increasing day length during spring causes sudden changes in the mammalian reproductive system once the critical photoperiod is reached. The molecular mechanism behind this switch is now quickly being elucidated

Effect of deuterium on the circadian period and metabolism in wild-type and tau mutant Syrian hamsters

Homozygous tau mutant Syrian hamsters (tau-/-) have a free-running circadian period (τ) around 20 h and a proportionally higher metabolic rate compared with wild-type hamsters (tau+/+) with a period of circa 24 h. In this study, we applied deuterium oxide (D2O) to hamsters to test whether deuteration affects the circadian period of locomotor activity and metabolic rate in both genotypes. Running wheel activity and the metabolic rate were measured in constant illumination before, during, and after administration of 25% deuterium in drinking water. Wild-type hamsters lengthened their circadian period by 1.19 h (SD = 0.29 h) due to D2O application and tau-/- hamsters by 1.20 h (SD = 0.39 h). Deuteration changed neither the amount of activity nor the duration of activity phase (α) in either genotype. The mass specific average metabolic rate (AMR, the oxygen consumption over 24 h) and the mass specific resting metabolic rate (RMR) did not differ during deuteration compared with non-deuteration conditions for either genotype. Both with and without D2O, tau-/- hamsters had higher metabolic rates than tau+/+ hamsters. There was no correlation between changes in the circadian period of locomotor activity and metabolic rates caused by D2O.

The neurobiology of circadian rhythms

Purpose of review There is growing awareness of the importance of circadian rhythmicity in various research fields. Exciting developments are ongoing in the field of circadian neurobiology linked to sleep, food intake, and memory. With the current knowledge of critical ‘clock genes’ (genes found to be involved in the generation of circadian rhythms) and novel techniques for imaging cyclic events in brain and peripheral tissue, this field of research is rapidly expanding. We reviewed only some of the highlights of the past year, and placed these findings into a mutual circadian perspective. Recent findings Recent findings on the organization of the circadian clock systems are addressed, ranging from the retina to the suprachiasmatic nucleus and peripheral organs. Novel developments in sleep, food intake, and memory research linked to circadian aspects are discussed. Summary The neurobiology of circadian rhythms is pivotal to the orchestration of the temporal organization of an individual’s physiology and behavior. Endogenous circadian timing systems underlie coupling and uncoupling mechanisms of many neuronal and physiological processes, the latter possibly inducing health risks to the organism. The integration of sleep, food intake and memory in a circadian setting has clear potential as a systems neurobiology line of research.

Negative energy balance enhances ultradian rhythmicity in spring-programmed voles

Voles are small herbivorous rodents that can display both circadian activity rhythms (~24-h periodicity) and ultradian activity rhythms (~1- to 6-h periodicity). Ultradian rhythms are observed on an individual level, but also in synchronized populations. Ultradian rhythm period has been suggested to be influenced by energy balance, but the underlying mechanisms of ultradian rhythmicity are poorly understood. We manipulated energy balance by implementing the "work-for-food" paradigm, in which small rodents are exposed to increasing levels of food scarcity at different ambient temperatures in the laboratory. Photoperiodical spring-programmed voles on high workload changed their nocturnal circadian activity and body temperature rhythm to ultradian patterns, indicating that a negative energy balance induces ultradian rhythmicity. This interpretation was confirmed by the observation that ultradian patterns arose earlier at low temperatures. Interestingly, a positive relationship between ultradian period length and workload was observed in tundra voles. Spectral analysis revealed that the power of ultradian rhythmicity increased at high workload, whereas the circadian component of running wheel activity decreased. This study shows that the balance between circadian and ultradian rhythmicity is determined by energy balance, confirming flexible circadian and ultradian rhythms in females and males of 2 different vole species: the common vole (Microtus arvalis) and the tundra vole (Microtus oeconomus).</p

Food and temperature change photoperiodic responses in two vole species

Seasonal timing of reproduction in voles is driven by photoperiod. We hypothesized that a negative energy balance can modify spring-programmed photoperiodic responses in the hypothalamus, controlling reproductive organ development. We manipulated energy balance by the 'work-for-food' protocol, in which voles were exposed to increasing levels of food scarcity at different ambient temperatures under long photoperiod. We found that in common voles (Microtus arvalis) and tundra voles (Microtus oeconomus), photoperiod-induced pars tuberalis thyroid-stimulating hormone β-subunit (Tshβ) expression is reduced to potentially inhibit gonadal development when food is scarce. Reduction in gonadal size is more pronounced in tundra voles, in which anterior hypothalamic Kiss1 is additionally downregulated, especially in males. Low temperature additionally leads to decreased hypothalamic Rfrp expression, which potentially may facilitate further suppression of gonadal growth. Shutting off the photoperiodic axis when food is scarce in spring may be an adaptive response to save energy, leading to delayed reproductive organ development until food resources are sufficient for reproduction, lactation and offspring survival. Defining the mechanisms through which metabolic cues modify photoperiodic responses will be important for a better understanding of how environmental cues impact reproduction

Transcriptomic Analysis of Light-Induced Genes in Nasonia vitripennis:Possible Implications for Circadian Light Entrainment Pathways

Circadian entrainment to the environmental day–night cycle is essential for the optimal use of environmental resources. In insects, opsin-based photoreception in the compound eye and ocelli and CRYPTOCHROME1 (CRY1) in circadian clock neurons are thought to be involved in sensing photic information, but the genetic regulation of circadian light entrainment in species without light-sensitive CRY1 remains unclear. To elucidate a possible CRY1-independent light transduction cascade, we analyzed light-induced gene expression through RNA-sequencing in Nasonia vitripennis. Entrained wasps were subjected to a light pulse in the subjective night to reset the circadian clock, and light-induced changes in gene expression were characterized at four different time points in wasp heads. We used co-expression, functional annotation, and transcription factor binding motif analyses to gain insight into the molecular pathways in response to acute light stimulus and to form hypotheses about the circadian light-resetting pathway. Maximal gene induction was found after 2 h of light stimulation (1432 genes), and this included the opsin gene opblue and the core clock genes cry2 and npas2. Pathway and cluster analyses revealed light activation of glutamatergic and GABA-ergic neurotransmission, including CREB and AP-1 transcription pathway signaling. This suggests that circadian photic entrainment in Nasonia may require pathways that are similar to those in mammals. We propose a model for hymenopteran circadian light-resetting that involves opsin-based photoreception, glutamatergic neurotransmission, and gene induction of cry2 and npas2 to reset the circadian clock.</p

Timing as a sexually selected trait: the right mate at the right moment

Sexual selection favours the expression of traits in one sex that attract members of the opposite sex for mating. The nature of sexually selected traits such as vocalization, colour and ornamentation, their fitness benefits as well as their costs have received ample attention in field and laboratory studies. However, sexually selected traits may not always be expressed: coloration and ornaments often follow a seasonal pattern and behaviours may be displayed only at specific times of the day. Despite the widely recognized differences in the daily and seasonal timing of traits and their consequences for reproductive success, the actions of sexual selection on the temporal organization of traits has received only scant attention. Drawing on selected examples from bird and mammal studies, here we summarize the current evidence for the daily and seasonal timing of traits. We highlight that molecular advances in chronobiology have opened exciting new opportunities for identifying the genetic targets that sexual selection may act on to shape the timing of trait expression. Furthermore, known genetic links between daily and seasonal timing mechanisms lead to the hypothesis that selection on one timescale may simultaneously also affect the other. We emphasize that studies on the timing of sexual displays of both males and females from wild populations will be invaluable for understanding the nature of sexual selection and its potential to act on differences within and between the sexes in timing. Molecular approaches will be important for pinpointing genetic components of biological rhythms that are targeted by sexual selection, and to clarify whether these represent core or peripheral components of endogenous clocks. Finally, we call for a renewed integration of the fields of evolution, behavioural ecology and chronobiology to tackle the exciting question of how sexual selection contributes to the evolution of biological clocks.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'

Differential temperature effects on photoperiodism in female voles:A possible explanation for declines in vole populations

Many mammalian species use photoperiod as a predictive cue to time seasonal reproduction. In addition, metabolic effects on the reproductive axis may also influence seasonal timing, especially in female small, short-lived mammals. To get a better understanding of how annual cycling environmental cues impact reproductive function and plasticity in small, short-lived herbivores with different geographic origins, we investigated the mechanisms underlying integration of temperature in the photoperiodic-axis regulating female reproduction in a Northern vole species (tundra vole, Microtus oeconomus) and in a Southern vole species (common vole, Microtus arvalis). We show that photoperiod and temperature interact to determine appropriate physiological responses; there is species-dependent annual variation in the sensitivity to temperature for reproductive organ development. In common voles, temperature can overrule photoperiodical spring-programmed responses, with reproductive organ mass being higher at 10°C than at 21°C, whereas in autumn they are less sensitive to temperature. These findings are in line with our census data, showing an earlier onset of spring reproduction in cold springs, while reproductive offset in autumn is synchronized to photoperiod. The reproductive organs of tundra voles were relatively insensitive to temperature, whereas hypothalamic gene expression was generally upregulated at 10°C. Thus, both vole species use photoperiod, whereas only common voles use temperature as a cue to control spring reproduction, which indicates species-specific reproductive strategies. Due to global warming, spring reproduction in common voles will be delayed, perhaps resulting in shorter breeding seasons and thus declining populations, as observed throughout Europe

Gonads or body?:Differences in gonadal and somatic photoperiodic growth response in two vole species

To optimally time reproduction, seasonal mammals use a photoperiodic neuroendocrine system (PNES) that measures photoperiod and subsequently drives reproduction. To adapt to late spring arrival at northern latitudes, a lower photoperiodic sensitivity and therefore a higher critical photoperiod for reproductive onset is necessary in northern species to arrest reproductive development until spring onset. Temperature-photoperiod relationships, and hence food availability-photoperiod relationships, are highly latitude dependent. Therefore, we predict PNES sensitivity characteristics to be latitude dependent. Here, we investigated photoperiodic responses at different times during development in northern (tundra or root vole, Microtus oeconomus) and southern vole species (common vole, Microtus arvalis) exposed to constant short (SP) or long photoperiod (LP). Although the tundra vole grows faster under LP, no photoperiodic effect on somatic growth is observed in the common vole. In contrast, gonadal growth is more sensitive to photoperiod in the common vole, suggesting that photoperiodic responses in somatic and gonadal growth can be plastic, and might be regulated through different mechanisms. In both species, thyroid-stimulating hormone β-subunit (Tshβ) and iodothyronine deiodinase 2 (Dio2) expression is highly increased under LP, whereas Tshr and Dio3 decrease under LP. High Tshr levels in voles raised under SP may lead to increased sensitivity to increasing photoperiods later in life. The higher photoperiodic-induced Tshr response in tundra voles suggests that the northern vole species might be more sensitive to thyroid-stimulating hormone when raised under SP. In conclusion, species differences in developmental programming of the PNES, which is dependent on photoperiod early in development, may form different breeding strategies as part of latitudinal adaptation

Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos

Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying the temperature sensitivity of development. Here, we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and time of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage, timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change