The pineal gland and seasonal reproductive adjustments

The pineal gland seems to play a major role in controlling and synchronizing circannual reproductive cycles in some mammals. The following scheme is based primarily on experimental evidence compiled using the golden hamster. However, it is probably applicable in one form or another to a number of long day breeding species. When hamsters are kept under natural photoperiodic conditions they exhibit a period of infertility followed by a period of fertility. The entire cycle encompasses approximately one year. The cycle has been divided into 4 distinctive phases: the inhibition phase, the sexually quiescent phase, the restoration phase, and the sexually active phase. During the inhibition phase the decreasing photoperiods in the fall of the year cause activation of the pineal gland and, as a consequence, gonadal regression. The sexually quiescent phase requires an intact pineal gland to maintain the gonads in a non-functional state. The restoration phase, which occurs in the spring of the year, allows the gonads to become recrudescent. This phase of the cycle seems to be light independent. The sexually active phase extends from spring until fall. During this phase the hypothalamo-pituitary-gonadal axis seems to be refractory to inhibition by the pineal gland. Some light is required during the summer months to interrupt the refractory period.     

Photoperiod as a modifying and limiting factor in the expression of avian circannual rhythms

In three species of birds that migrate long distances, the annual rhythms of gonadal activity, molt, and migratory restlessness (Zugunruhe) persist for more than 1 year under certain constant conditions. The most important zeitgeber for these circannual rhythms is the annual cycle of photoperiod, which adjusts the overall period of circannual rhythms to exactly 1 year and also provides for the appropriate adjustment of seasonal activities to the temporal structure of the environment. This is illustrated by results on garden warblers (Sylvia borin) indicating that the longer photoperiods experienced by individuals wintering far south in the African wintering area phase-advance spring migration and the accompanying gonadal development, relative to those of individuals wintering further north. The rate of acceleration is, however, slow enough to prevent a reproductive cycle during the Southern Hemisphere summer. Hence, endogenous circannual components and zeitgeber stimuli constitute a functional entity that provides as a whole for adaptive temporal programming. This idea is further supported by findings in the pied flycatcher (Ficedula hypoleuca), in which a circannual rhythmicity persists only if photoperiod in winter is at least as short as that normally encountered by the species in its wintering grounds slightly north of the equator. In collared flycatchers (Ficedula albicollis), in contrast, rhythmicity continues under much longer photoperiods, consistent with the fact that the wintering area of this species extends to latitudes far south of the equator. It is proposed that the adaptive function of circannual rhythms can be properly understood only if their interactions with environmental factors, particularly those that play a role as zeitgebers, are analyzed in sufficient detail. The biological significance of circannual rhythms may be more apparent in the context of the environmental constraints limiting their expression than in the often rather restricted set of conditions sustaining spontaneous annual cyclicity.     

Free-running rhythms of pineal circadian output

Circadian rhythms are self-sustaining oscillations that free-run in constant conditions with a period close to 24 h. Overt circadian rhythms have been studied mostly using onset phase as the marker for the underlying pacemaker. Using in vivo online pineal microdialysis, the authors have performed detailed analysis of free-running profiles of rat pineal secretory products, including N-acetylserotonin (NAS) and melatonin that have precisely defined onsets and offsets. When rats entrained in LD 12:12 were released into constant darkness (DD), both onset and offset phases of melatonin and NAS free-run. However, while onsets free-run with a period closer to a day (FRP(on) = 24-24.17 h) at the beginning, offset phases free-run with significantly larger FRPs (free-running periods) (FRP(off) = 24.24-24.42 h). This asymmetric free-running of onset and offset of NAS and melatonin in DD resulted in a 60- to 120-min increase of secretion duration of both NAS and melatonin. The rate of expansion of melatonin duration was 10 to 15 min per circadian cycle. The expansion of melatonin secretion duration ended for some within 4 days, while others were still expanding by the end of 10th day in DD. These results revealed that upon release into DD, the pacemaker's oscillation is initially driven by 2 forces, free running and decompression, before reaching a stable state of free running, and suggest that the circadian pacemaker may be an elastic structure that can decompress and compress under varying photic conditions. They also illustrate the importance of using both onset and offset of a given rhythm as phase markers, as compression/decompression, and transient disparity between FRP(on) and FRP(off) may be a common phenomenon of the circadian pacemaker.     

Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation

Evidence has recently begun to accumulate that photoperiodic responses of mammals and birds may affect the control of energy balance and thermoregulation. Exposure to short photoperiod can lower the set point for body temperature regulation in birds and mammals, as well as the voluntarily selected body temperature in ectothermic lizards. This decrease is accompanied by a reorganization of circadian or ultradian rhythms of body temperature, particularly an increase in periods spent at rest with minimum body temperatures. Short photoperiod is also used as an environmental cue for induction of seasonal torpor or facilitation of hibernation. During winter, cold tolerance of small mammals is improved by an increase of nonshivering thermogenesis in brown fat. Thermogenic capacity of brown fat (respiratory enzymes, mitochondria, uncoupling protein) is enhanced in response to short photoperiod. This response is mediated via an increase in the activity of sympathetic innervation in brown fat. Moreover, an exposure to short photoperiod prior to low temperatures may act in preparing brown fat for facilitated thermogenesis during acclimation to cold. This shows that photoperiodic control not only affects energy balance indirectly via the control of reproduction or body mass, but may directly interact with central control of thermoregulation and may influence the process of acclimatization.     

Photoperiod as a reproductive cue in the marsupial genus Antechinus: ecological and evolutionary consequences

Species in the Australian marsupial genus Antechinus exhibit a short annual mating period which is concluded by the abrupt death of all males. The timing of the annual rut within each of the ten described species varies little from year to year at any given locality, but for some species can differ by up to four months between locations. To determine the influence of photoperiod in regulating the precise interannual synchrony of mating and ovulation, we first investigated populations of each species at over 300 localities throughout their geographical ranges to identify the time of reproduction. We then compared the absolute photoperiod and the rate of change of photoperiod prevailing at the time of reproduction in all population localities. A different, and characteristic, rate of change of photoperiod was correlated strongly with the reproductive timing of four species; there was probably a correlation with reproduction in four more species, but sample sizes were small. For two species, there was no obvious photoperiodic correlation with time of reproduction. There was no evidence that absolute photoperiod or ambient temperature explained the synchrony or narrow timespan of reproduction among any species of Antechinus . Different species-specific ovulatory responses to photoperiod appear to separate the timing of reproduction in sympatric species, with the larger member of species pairs usually breeding first. We suggest that photoperiodic cues (1) allow females to produce young during seasons when food is most reliable and abundant and their energetic demands are maximal; (2) facilitate allochronic isolation between sympatric congeners, and (3) maximize body size differences and hence ecological separation between species.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 365–379.     

Rest-activity rhythms characteristics and seasonal changes in seasonal affective disorder

ABSTRACT

Identifying objectively measurable seasonal changes in 24-h activity patterns (rest-activity rhythms or RARs) that occur in seasonal affective disorder (SAD) could help guide research and practice towards new monitoring tools or prevention targets. We quantified RARs from actigraphy data using non-parametric and extended cosine based approaches, then compared RARs between people with SAD and healthy controls in the summer (n = 70) and winter seasons (n = 84). We also characterized the within-person seasonal RAR changes that occurred in the SAD (n = 19) and control (n = 26) participants who contributed repeated measures. Only controls had significant winter increases in RAR fragmentation (intra-daily variability; in controls mean winter-summer changes (log scale) = 0.05, 0.21 standard deviation, p = 0.03). In SAD participants only, estimated evening settling times (down-mesor) were an average of 30 min earlier in the winter compared with the summer (1-h standard deviation, p = 0.045). These RAR characteristics correlated with greater fatigue (Spearman r = 0.36) but not depression symptom severity. Additional research is needed to ascertain why healthy controls, but not people with SAD, appear to have increased RAR fragmentation in the winter. People with SAD lacked this increase in RAR fragmentation, and instead had earlier evening setting in the winter. Prospective and intervention studies with greater temporal resolution are warranted to ascertain how these seasonal behavioral differences relate to fatigue pathophysiology in SAD. Future research is needed to determine whether extending the winter active period, even in relatively fragmented bouts, could help reduce the fatigue symptoms common in SAD.     

Daily and seasonal vertical migration rhythms in Daphnia

1. Clones of Daphnia longispina (O.F.M.), collected from ponds with different levels of predation, were monitored using video techniques in order to test the effects of temperature and visual cues on vertical migration behaviour.
2. Endogenous rhythms were found to have a part in the control of vertical migration in some clones but responses were highly variable.
3. Low temperature caused a marked increase in the amplitude of vertical migration in D. longispina , consistent with field studies.
4. Clones from ponds with fish predators had larger vertical migration amplitudes than clones from ponds with no fish, providing further evidence for the genetic basis of this mechanism.     

Daily and seasonal vertical migration rhythms in Daphnia

1. Clones of Daphnia longispina (O.F.M.), collected from ponds with different levels of predation, were monitored using video techniques in order to test the effects of temperature and visual cues on vertical migration behaviour.
2. Endogenous rhythms were found to have a part in the control of vertical migration in some clones but responses were highly variable.
3. Low temperature caused a marked increase in the amplitude of vertical migration in D. longispina , consistent with field studies.
4. Clones from ponds with fish predators had larger vertical migration amplitudes than clones from ponds with no fish, providing further evidence for the genetic basis of this mechanism.     

Dirunal rhythms of hexosemonophosphate shunt and phosphorylase in rat pineal gland

Hexosemonophosphate shunt and phosphorylase activities determined in the pineal glands of rats during mid-light and mid-darkness periods were found to undergo diurnal rhythms. A high active hexosemonophosphate shunt -- indicated by the more ready conversion of CO₂ of the glucose carbon in position 1 than of that in position 6 -- was found to correlate to the function of endocrine activity of night time/darkness. Phosphorylase activity, indicating glycogenolysis, measured at the same times, was found to be increased during the period of mid-light when basal metabolism is high compared to that during mid-darkness. The significance of these findings is discussed.     

Circadian rhythms of pineal N-acetyltransferase activity in the Djungarian hamster,Phodopus sungorus,in response to seasonal changes of natural photoperiod

Summary The aim of this study was to describe the regular annual pattern of the daily melatonin synthesis in Djungarian hamsters,Phodopus sungorus sungorus. The hamsters were maintained from birth in natural photoperiodic conditions and in bimonthly intervals the day/night rhythms of pineal N-acetyltransferase (NAT) were measured. Analysis of the circadian profiles of NAT activity showed that the duration of elevated melatonin synthesis closely reflects the duration of the scotophase throughout the seasons. Thus the duration of elevated melatonin seems to represent a direct humoral signal transmitting the photoperiodic message. The duration of the nightly melatonin pulse appears to be influenced mainly by the time of dawn rather than by the time of dusk. Additional information about the time of year might be encoded in the total amount of melatonin synthesized per day, whereas the amplitude of the nightly melatonin peak seems to be of minor importance.Abbreviation NAT N-acetyltransferase Dedicated to Dr. Klaus Hoffmann on the occasion of his 60th birthday     

Photoperiod gene control over partitioning between reproductive and vegetative growth

Summary The hypothesis tested was that lack of photoperiod gene activity allows inherent partitioning of photosynthate to continued growth of the earliest potential buds, flowers, pods, and seeds (the organs that give rise to the yield). Alternatively, and competitively, photoperiod gene activity causes the photosynthate to be partitioned predominantly toward continued growth of new vegetative organs plus later initiation of more reproductive (yield) organs. This hypothesis was tested by comparing an insensitive and a photoperiod-sensitive bean (Phaseolus vulgaris L.) cultivar and their F₁ with F₂ segregates of undetermined genotype. Randomly derived homozygous F₈ segregates were also compared. The F₈ generation included one photoperiod-insensitive and one photoperiod-sensitive genotype in a 1:1 ratio, which verified control by one photoperiod gene. Under long daylength (LD), in addition to early versus late flowering and maturity, the two genotypes expressed opposite levels of 23 other traits that would be changed by competitive partitioning of the photosynthate. In contrast, under short daylength (SD), both genotypes flowered and matured early, and both expressed the levels for all 25 traits that the photoperiod-insensitive genotype expressed in both SD and LD. The photoperiod gene interacted with daylength to control the levels of all three major physiological components of yield: the aerial biomass, harvest index, and days to maturity. Included among the other traits with levels altered by daylength-modulated photoperiod gene activity were: the number of branches, nodes, leaves and leaf area, the rate of yield accumulation, and sink activity.Department of Plant Breeding and Biometry paper no. 758     

Melatonin rhythms: Trekking toward the heart of darkness in the chick pineal

Chick pineal cells make melatonin rhythmically, even in culture. Light pulses have two effects on these cells: acute suppression of melatonin synthesis and phase shifts (entrainment) of the underlying pacemaker. The two effects use different mechanistic pathways: the first goes through cAMP, and the second goes through the clock. Both converge on serotonin N-acetyltransferase, whose gene has recently been cloned, with cAMP acting on mRNA levels, but primarily on, enzyme activity, and the clock acting primarily on mRNA levels. Aspects of calcium regulation, not yet well-understood, may impinge on both pathways. These cells also have a novel calcium channel and a novel photopigment.     

Phenology, seasonal timing and circannual rhythms: towards a unified framework

Phenology refers to the periodic appearance of life-cycle events and currently receives abundant attention as the effects of global change on phenology are so apparent. Phenology as a discipline observes these events and relates their annual variation to variation in climate. But phenology is also studied in other disciplines, each with their own perspective. Evolutionary ecologists study variation in seasonal timing and its fitness consequences, whereas chronobiologists emphasize the periodic nature of life-cycle stages and their underlying timing programmes (e.g. circannual rhythms). The (neuro-) endocrine processes underlying these life-cycle events are studied by physiologists and need to be linked to genes that are explored by molecular geneticists. In order to fully understand variation in phenology, we need to integrate these different perspectives, in particular by combining evolutionary and mechanistic approaches. We use avian research to characterize different perspectives and to highlight integration that has already been achieved. Building on this work, we outline a route towards uniting the different disciplines in a single framework, which may be used to better understand and, more importantly, to forecast climate change impacts on phenology.