A transcriptional program underlying the circannual rhythms of gonadal development in medaka.

To cope with seasonal environmental changes, organisms have evolved approximately 1-y endogenous circannual clocks. These circannual clocks regulate various physiological properties and behaviors such as reproduction, hibernation, migration, and molting, thus providing organisms with adaptive advantages. Although several hypotheses have been proposed, the genes that regulate circannual rhythms and the underlying mechanisms controlling long-term circannual clocks remain unknown in any organism. Here, we show a transcriptional program underlying the circannual clock in medaka fish (Oryzias latipes). We monitored the seasonal reproductive rhythms of medaka kept under natural outdoor conditions for 2 y. Linear regression analysis suggested that seasonal changes in reproductive activity were predominantly determined by an endogenous program. Medaka hypothalamic and pituitary transcriptomes were obtained monthly over 2 y and daily on all equinoxes and solstices. Analysis identified 3,341 seasonally oscillating genes and 1,381 daily oscillating genes. We then examined the existence of circannual rhythms in medaka via maintaining them under constant photoperiodic conditions. Medaka exhibited approximately 6-mo free-running circannual rhythms under constant conditions, and monthly transcriptomes under constant conditions identified 518 circannual genes. Gene ontology analysis of circannual genes highlighted the enrichment of genes related to cell proliferation and differentiation. Altogether, our findings support the "histogenesis hypothesis" that postulates the involvement of tissue remodeling in circannual time-keeping.

Diapause in Univoltine and Semivoltine Life Cycles.

Although it is generally more adaptive for insects to produce additional generations than to have longer life cycles, some insects produce one or fewer generations per year (univoltine or semivoltine life cycles, respectively). Some insects with the potential to produce multiple generations per year produce a univoltine life cycle in response to environmental conditions. Obligatory univoltine insects have a single long diapause or multiple diapauses in different seasons. Semivoltine insects have multiple diapauses in different years, a prolonged diapause for more than a year, or diapause controlled by a circannual rhythm. Diapause in these insects greatly varies among species both in the physiological mechanism and in the evolutionary background, and there is no general rule defining it. In this review, we survey the physiological control of univoltine and semivoltine insects' diapause and discuss the adaptive significance of the long life cycles. Although constraints such as slow development are sometimes responsible for these life cycles, the benefits of these life cycles can be explained by bet-hedging in many cases. We also discuss the effect of climate warming on these life cycles as a future area of research.

The mechanism of circadian clock and its influence on animal circannual rhythm.

The circadian clock exists in almost all life forms, and is an internal activity generated by organisms adapting to the daily periodic changes of the external environment. The circadian clock is regulated by the transcription-translation-negative feedback loop in the body, which can regulate the activities of tissues and organs. Its normal maintenance is important for the health, growth, and reproduction of organisms. In contrast, due to the season changes of the environment, organisms have also formed annual cycle physiological changes in their bodies, such as seasonal estrus, etc. The annual rhythm of living things is mainly affected by environmental factors such as photoperiod, and is related to gene expression, hormone content, morphological changes of cell and tissues in vivo. Melatonin is an important signal to recognize the changes of photoperiod, and the circadian clock plays an important role in the pituitary to interpret the signal of melatonin and regulate the changes of downstream signals, which plays an important guiding role in the recognition of annual changes in the environment and the generation of the body's annual rhythm. In this review, we summarize the progress of research on the mechanism of action of circadian clocks in influencing annual rhythms, by introducing the mechanisms of circadian and annual rhythms generation in insects and mammals, and in the context of annual rhythms in birds, with the aim of providing a broader range of ideas for future research on the mechanism of annual rhythms influence.

Peripheral circadian gene activity is altered during hibernation in the thirteen-lined ground squirrel.

Many small mammals living in seasonally cold environments rely on hibernation, utilizing strong metabolic rate suppression and a slow consumption of adipose reserves to survive the winter months. The circannual rhythm of hibernation is well known but less is known about the role of the circadian clock while animals are in torpor for weeks at a time. We hypothesized that due to strong global suppression of transcription and translation in the torpid state, that circadian clock activity would likewise be suppressed in peripheral tissues during hibernation. However, the present study indicates that peripheral circadian clock activity persists during torpor. Using 13-lined ground squirrels (Ictidomys tridecemlineatus) as the model, this study analyzed transcript and protein responses by clock components, comparing euthermic control animals with squirrels in deep torpor for >3 days (subcutaneous body temperature 5-8 °C). The data show tissue specific responses by mRNA transcript levels: (a) no significant changes in transcript abundance in liver of control versus torpid squirrels, (b) a strong increase in Nr1d1 levels in white adipose during torpor, and (c) five significant transcript changes in skeletal muscle during torpor (increased Bmal1, Clock, Cry1 and Nr1d1 but decreased Per1). Levels of core clock proteins (BMAL1, CRY2, PER2, and casein kinases CK1δ and CK1ε) were also assessed across five time points of the torpor/arousal cycle showing both tissue- and time-dependent changes in clock proteins that were most prominent in liver and white adipose and indicating that peripheral clocks are still active in tissues over the torpor/arousal cycle.

Seasonal differences in thermal stress susceptibility of diploid and triploid brook trout, Salvelinus fontinalis (Teleostei, Pisces).

Many physiological processes of teleost fish show periodicity due to intrinsic rhythms. It may be hypothesized that also susceptibility to thermal stress differs seasonally. To shed more light on this problem the following experiment was conducted. Diploid and triploid Salvelinus fontinalis were kept at an acclimation temperature of 9°C and at a natural photoperiod typical for the Northern Hemisphere during their entire live. During eight different periods of the year, different subgroups were exposed to a 32 day lasting thermal stress of 20°C. Rate of fish maintaining equilibrium, daily growth rate, condition factor, viscerosomatic index and hepato-somatic index were measured. Complementary mRNA expression of genes characterizing growth (GHR1, GHR2), proteolysis (Protreg, Protα5), stress (Hsp47, Hsp90) and respiratory energy metabolism (ATPJ52) was determined. Seasonal differences in thermal stress susceptibility of 2n and 3n S. fontinalis were detected. It was highest from September to December and moderate from January to March. During the remaining period of the year, susceptibility to thermal stress was minimal. Increased thermal stress susceptibility was related to decreased rates of fish maintaining equilibrium, decreased growth rates, reduction of viscera and liver mass and changes in mRNA expression of genes characterizing proteolysis, growth, respiratory energy metabolism and stress. The differences in seasonal stress susceptibility were minor between 2n and 3n S. fontinalis. The data are valuable for ecology and fish culture to identify periods when animals are most susceptible to thermal stress.

Why don't phenophase dates in the current year affect the same phenophase dates in the following year?

Examining whether a phenophase occurrence date in the current year affects the same phenophase occurrence date in the following year is crucial for developing cross-year phenological prediction models. Here, we carried out correlation analyses between leaf unfolding start (LUS)/leaf fall end (LFE) dates in the current and following years for four dominant tree species in temperate northern China from 1981 to 2012. Then, we calculated the recurrence intervals of LUS and LFE between two adjacent years for each species. Moreover, we investigated temperature effects on LUS/LFE dates, growing season and non-growing season lengths. Results show that correlation coefficients between LUS/LFE dates in the current and following years are nonsignificant at most stations. The recurrence interval of a phenophase has slight interannual variation and correlates significantly (and negatively) with the phenophase occurrence date of the current year. Further analyses indicate that LUS dates correlate significantly (and negatively) with spring mean temperatures, while LFE dates correlate significantly (and positively) with autumn mean temperatures, but negatively with growing season mean temperatures. In addition, spring mean temperatures can influence growing season length by controlling LUS date but cannot influence the following non-growing season length. Similarly, autumn mean temperatures and growing season mean temperatures can influence the subsequent non-growing season length but cannot influence the growing season length of the following year. Our study highlights that recurrence interval and time restrictions in the effects of seasonal temperatures on phenophase dates are the main environmental causes of nonsignificant correlations between phenophase occurrence dates in the current and following years.

A laboratory simulation of Arabidopsis seed dormancy cycling provides new insight into its regulation by clock genes and the dormancy-related genes DOG1, MFT, CIPK23 and PHYA.

Environmental signals drive seed dormancy cycling in the soil to synchronize germination with the optimal time of year, a process essential for species' fitness and survival. Previous correlation of transcription profiles in exhumed seeds with annual environmental signals revealed the coordination of dormancy-regulating mechanisms with the soil environment. Here, we developed a rapid and robust laboratory dormancy cycling simulation. The utility of this simulation was tested in two ways: firstly, using mutants in known dormancy-related genes [DELAY OF GERMINATION 1 (DOG1), MOTHER OF FLOWERING TIME (MFT), CBL-INTERACTING PROTEIN KINASE 23 (CIPK23) and PHYTOCHROME A (PHYA)] and secondly, using further mutants, we test the hypothesis that components of the circadian clock are involved in coordination of the annual seed dormancy cycle. The rate of dormancy induction and relief differed in all lines tested. In the mutants, dog1-2 and mft2, dormancy induction was reduced but not absent. DOG1 is not absolutely required for dormancy. In cipk23 and phyA dormancy, induction was accelerated. Involvement of the clock in dormancy cycling was clear when mutants in the morning and evening loops of the clock were compared. Dormancy induction was faster when the morning loop was compromised and delayed when the evening loop was compromised.

Circannual testis and moult cycles persist under photoperiods that disrupt circadian activity and clock gene cycles in spotted munia.

We investigated whether circannual rhythms underlying annual testis maturation and moult cycles are independent of duration and frequency of the light period and circadian clock control in non-photoperiodic spotted munia. Birds were subjected to an aberrant light-dark (LD) cycle (3.5 h L:3.5 h D; T7, where T is the period length of the LD cycle) and continuous light (LL, 24 h L:0 h D), with controls on 12 h L:12 h D (T24, 24 h LD cycle). We measured the behavioural activity pattern of the birds and 24 h mRNA oscillations of circadian clock genes (bmal1, clock, per2, cry1, cry2) in the hypothalamus, the putative site of seasonal timing. Diurnal munia were rhythmic in behaviour with the period of the activity-rest cycle matched to T7 and T24, and became behaviourally arrhythmic with activity scattered throughout 24 h under LL. Similarly, exposure to 3.5 h L:3.5 h D and LL caused arrhythmicity in 24 h clock gene expression, suggesting disruption of internal circadian timing at the transcriptional level; a significant rhythm was found under 12 h L:12 h D. During an exposure of 80 weeks, munia showed two to three cycles of testis maturation and wing primaries moult under all photoperiods, although with a longer period under 12L:12D. Thus, the frequency of light period under 3.5 h L:3.5 h D or LL disrupted circadian clock gene cycles, but did not affect the generation of circannual testis and moult cycles. We conclude that the prevailing light environment and hypothalamic circadian gene cycles do not exert direct control on the timing of the annual reproductive cycle in spotted munia, suggesting independent generation of the circadian and circannual rhythms in seasonally breeding species.

Cold spell en route delays spring arrival and decreases apparent survival in a long-distance migratory songbird.

BACKGROUND: Adjusting the timing of annual events to gradual changes in environmental conditions is necessary for population viability. However, adaptations to weather extremes are poorly documented in migratory species. Due to their vast seasonal movements, long-distance migrants face unique challenges in responding to changes as they rely on an endogenous circannual rhythm to cue the timing of their migration. Furthermore, the exact mechanisms that explain how environmental factors shape the migration schedules of long-distance migrants are often unknown. RESULTS: Here we show that long-distance migrating semi-collared flycatchers Ficedula semitorquata delayed the last phase of their spring migration and the population suffered low return rates to breeding sites while enduring a severe cold spell en route. We found that the onset of spring migration in Africa and the timing of Sahara crossing were consistent between early and late springs while the arrival at the breeding site depended on spring phenology at stopover areas in each particular year. CONCLUSION: Understanding how environmental stimuli and endogenous circannual rhythms interact can improve predictions of the consequences of climate changes on migratory animals.

Temporal coherence of phenological and climatic rhythmicity in Beijing.

Using woody plant phenological data in the Beijing Botanical Garden from 1979 to 2013, we revealed three levels of phenology rhythms and examined their coherence with temperature rhythms. First, the sequential and correlative rhythm shows that occurrence dates of various phenological events obey a certain time sequence within a year and synchronously advance or postpone among years. The positive correlation between spring phenophase dates is much stronger than that between autumn phenophase dates and attenuates as the time interval between two spring phenophases increases. This phenological rhythm can be explained by positive correlation between above 0 °C mean temperatures corresponding to different phenophase dates. Second, the circannual rhythm indicates that recurrence interval of a phenophase in the same species in two adjacent years is about 365 days, which can be explained by the 365-day recurrence interval in the first and last dates of threshold temperatures. Moreover, an earlier phenophase date in the current year may lead to a later phenophase date in the next year through extending recurrence interval. Thus, the plant phenology sequential and correlative rhythm and circannual rhythm are interacted, which mirrors the interaction between seasonal variation and annual periodicity of temperature. Finally, the multi-year rhythm implies that phenophase dates display quasi-periodicity more than 1 year. The same 12-year periodicity in phenophase and threshold temperature dates confirmed temperature controls of the phenology multi-year rhythm. Our findings provide new perspectives for examining phenological response to climate change and developing comprehensive phenology models considering temporal coherence of phenological and climatic rhythmicity.

Seasonal gene expression in a migratory songbird.

The annual migration of a bird can involve thousands of kilometres of nonstop flight, requiring accurately timed seasonal changes in physiology and behaviour. Understanding the molecular mechanisms controlling this endogenous programme can provide functional and evolutionary insights into the circannual biological clock and the potential of migratory species to adapt to changing environments. Under naturally timed photoperiod conditions, we maintained captive Swainson's thrushes (Catharus ustulatus) and performed RNA sequencing (RNA-Seq) of the ventral hypothalamus and optic chiasma to evaluate transcriptome-wide gene expression changes of individuals in migratory condition. We found that 188 genes were differentially expressed in relation to migratory state, 86% of which have not been previously linked to avian migration. Focal hub genes were identified that are candidate variables responsible for the occurrence of migration (e.g. CRABP1). Numerous genes involved in cell adhesion, proliferation and motility were differentially expressed (including RHOJ, PAK1 and TLN1), suggesting that migration-related changes are regulated by seasonal neural plasticity.

Sexually active males prevent the display of seasonal anestrus in female goats.

A well-defined season of sexual rest controlled by photoperiod is observed in female sheep and goats during spring and summer, delineating their "anestrous season"; bucks also decrease sexual activity at about the same time. Nutrition and/or socio-sexual stimuli play only secondary roles. However, the presence of sexually active males can reduce the length of seasonal anestrus. Whether it can also completely suppress anestrus has not been investigated. Here we tested this in goats in 3 experiments, using bucks rendered sexually active out of season by exposure to long days. The continuous presence of these males prevented goats to display seasonal anestrus: 12/14 females cycled the year round, vs. 0/13 and 0/11 for females with un-treated bucks or without bucks (experiment 1). When active bucks were removed, females immediately entered anestrus (7/7 stopped ovulating vs. 1/7 if maintained with active bucks; experiment 2). Finally, 7/7 anestrous does with bucks in sexual rest since 1.5months commenced cycling rapidly during mid-anestrous, when these bucks became sexually active following a treatment with artificial long days, vs. 0/7 with un-treated bucks or no bucks (experiment 3). The presence/withdrawal of active bucks had a highly significant effect in the three experiments (P≤0.002). Therefore, the presence of a mating opportunity can completely override the photoperiodic inhibition of reproduction of females throughout the anestrous season. Results suggest that we must re-evaluate the relative contributions of photoperiod vs. other external cues in controlling seasonal reproduction, thus offering new non-pharmaceutical ways for controlling out-of-season reproduction in small ruminants.

Circannual rhythm of resting metabolic rate of a small Afrotropical bird.

Seasonal variation in avian metabolic rate is well established in Holarctic and temperate species, while trends in Afrotropical species are relatively poorly understood. Furthermore, given the paucity of data on circannual rhythm in avian metabolism, it is not known whether seasonal measurements made in summer and winter correspond with annual peaks and troughs in avian metabolic rate. Thus, we investigated how mean body mass, resting metabolic rate (RMR) and evaporative water loss (EWL) of a small Afrotropical bird, the Cape white-eye (Zosterops virens), changed monthly over the course of a year at 20°C and 25°C. Mean body mass was 12.2±1.0g throughout the study period. However, both EWL and RMR varied monthly, and peaks and troughs in RMR occurred in March and October respectively, which did not correspond to peaks and troughs in mean monthly outdoor ambient temperatures. These results suggest that measuring RMR at the height of summer and winter may underestimate the flexibility of which birds are capable in terms of their metabolic rate. We encourage further studies on this topic, to establish whether the lag between environmental temperature and RMR is consistent in other species.

Circadian rhythms are not involved in the regulation of circannual reproductive cycles in a sub-tropical bird, the spotted munia.

Circannual rhythms regulate seasonal reproduction in many vertebrates. The present study investigated whether circannual reproductive phenotypes (rhythms in growth of gonads and molt) were generated independently of the circadian clocks in the subtropical non-photoperiodic spotted munia (Lonchura punctulata). Birds were subjected to light:dark (LD) cycles with identical light but varying dark hours, such that the period of LD cycle (T) equaled 16 h (T16; 12 h L:4 h D), 21 h (T21; 12 h L:9 h D), 24 h (T24; 12 h L:12 h D) and 27 h (T27; 12 h L:15 h D), or to continuous light (LL, 24 h L:0 h D) at ~18°C. During the ~21 month exposure, munia underwent at least two cycles of gonadal development and molt; changes in body mass were not rhythmic. This was similar to the occurrence of annual cycles in reproduction and molt observed in wild birds. A greater asynchrony between circannual cycles of gonad development and molt indicated their independent regulation. Females showed reproductive rhythms with similar circannual periods, whilst in males, circannual periods measured between peak gonadal size were longer in T21 and T24 than in T16 or T27. This suggested a sex-dependent timing of annual reproduction in the spotted munia. Also, food availability periods may not influence the circannual timing of reproduction, as shown by the results on the rhythm in gonadal growth and regression in munia under T-photocycles and LL that provided differential light (feeding) hours. Further, a short-term experiment revealed that activity-rest patterns in munia were synchronized with T-photocycles, but were arrhythmic under LL. We conclude that circadian rhythms are not involved in the timing of the annual reproductive cycle in the spotted munia.

The putative role of the habenula in animal migration.

BACKGROUND: When an addicted animal seeks a specific substance, it is based on the perception of internal and external cues that strongly motivate to pursue the acquisition of that compound. In essence, a similar process acts out when an animal leaves its present area to begin its circannual migration. This review article examines the existence of scientific evidence for possible relatedness of migration and addiction by influencing Dorsal Diencephalic Conduction System (DDCS) including the habenula. METHODS: For this review especially the databases of Pubmed and Embase were frequently and non-systematically searched. RESULTS: The mechanisms of bird migration have been thoroughly investigated. Especially the mechanism of the circannual biorhythm and its associated endocrine regulation has been well elucidated. A typical behavior called "Zugunruhe" marks the moment of leaving in migratory birds. The role of magnetoreception in navigation has also been clarified in recent years. However, how bird migration is regulated at the neuronal level in the forebrain is not well understood. Among mammals, marine mammals are most similar to birds. They use terrestrial magnetic field when navigating and often bridge long distances between breeding and foraging areas. Population migration is further often seen among the large hoofed mammals in different parts of the world. Importantly, learning processes and social interactions with conspecifics play a major role in these ungulates. Considering the evolutionary development of the forebrain in vertebrates, it can be postulated that the DDCS plays a central role in regulating the readiness and intensity of essential (emotional) behaviors. There is manifold evidence that this DDCS plays an important role in relapse to abuse after prolonged periods of abstinence from addictive behavior. It is also possible that the DDCS plays a role in navigation. CONCLUSIONS: The role of the DDCS in the neurobiological regulation of bird migration has hardly been investigated. The involvement of this system in relapse to addiction in mammals might suggest to change this. It is recommended that particularly during "Zugunruhe" the role of neuronal regulation via the DDCS will be further investigated.

Avian circannual systems: persistence and sex differences.

Birds show adaptation in their physiology and behavior to daily and seasonal periodicities in the environment. A circannual clock system gates seasonal events in birds to happen at the most appropriate time of the year, since a mistiming will delay the event until the arrival of the favorable time next year. The circannual clocks, the self-sustained endogenous system, are expressed under aperiodic conditions with a period close to 12months. In stonechats, it has been shown that circannual rhythms in testicular and molt cycles persist for 12years; this suggests that circannual clocks are functional throughout the life of an individual. Circannual rhythms are synchronized with both the photoperiodic and non-photoperiodic cues, and a synchronized circannual rhythm provides information on annual timing of the physiological event. The integration of rigid circannual timekeeping with the cyclic environment ensures phenotypic plasticity that is required for successful survival of a species in its habitat. There can be however sex differences in the circannual rhythm characteristics and in the relationship between circannual rhythms and external environment. In few cases that have been investigated, females appear playing a larger role in defining the breeding season in the year in relation to the environment. There is no evidence for the involvement of circadian clock in the generation of circannual rhythms. Therefore, future researches need to focus on finding molecular gears that possibly form the neuroendocrine loop and are translated into a seasonal event. Here, we briefly review limited information that is available on circannual rhythms and their relationship with the external environment from a few bird species, inhabiting tropical and temperate environments.

Differential AMPK-mediated metabolic regulation observed in hibernation-style polymorphisms in Siberian chipmunks.

Hibernation is a unique physiological phenomenon allowing extreme hypothermia in endothermic mammals. Hypometabolism and hypothermia tolerance in hibernating animals have been investigated with particular interest; recently, studies of cultured cells and manipulation of the nervous system have made it possible to reproduce physiological states related to hypothermia induction. However, much remains unknown about the periodic regulation of hibernation. In particular, the physiological mechanisms facilitating the switch from an active state to a hibernation period, including behavioral changes and the acquisition of hypothermia tolerance remain to be elucidated. AMPK is a protein known to play a central role not only in feeding behavior but also in metabolic regulation in response to starvation. Our previous research has revealed that chipmunks activate AMPK in the brain during hibernation. However, whether AMPK is activated during winter in non-hibernating animals is unknown. Previous comparative studies between hibernating and non-hibernating animals have often been conducted between different species, consequently it has been impossible to account for the effects of phylogenetic differences. Our long-term monitoring of siberian chipmunks, has revealed intraspecific variation between those individuals that hibernate annually and those that never become hypothermic. Apparent differences were found between hibernating and non-hibernating types with seasonal changes in lifespan and blood HP levels. By comparing seasonal changes in AMPK activity between these polymorphisms, we clarified the relationship between hibernation and AMPK regulation. In hibernating types, phosphorylation of p-AMPK and p-ACC was enhanced throughout the brain during hibernation, indicating that AMPK-mediated metabolic regulation is activated. In non-hibernating types, AMPK and ACC were not seasonally activated. In addition, AMPK activation in the hypothalamus had already begun during high Tb before hibernation. Changes in AMPK activity in the brain during hibernation may be driven by circannual rhythms, suggesting a hibernation-regulatory mechanism involving AMPK activation independent of Tb. The differences in brain AMPK regulation between hibernators and non-hibernators revealed in this study were based on a single species thus did not involve phylogenetic differences, thereby supporting the importance of brain temperature-independent AMPK activation in regulating seasonal metabolism in hibernating animals.

Seasonal patterns of body temperature in response to experimental photoperiod variation in a non-hibernating ground squirrel.

Unlike numerous other members of the holarctic Tribe Marmotini of the squirrel family (Sciuridae) that typically exhibit spontaneous bouts of torpor that progress into an annual season of hibernation, members of the genus Ammospermophilus (antelope ground squirrels) do not enter torpor, and they remain active throughout the year in nature. We have experimentally evaluated seasonal patterns of variation in the circadian rhythm of body temperature in captive A. leucurus over a two-and-a-half-year period by exposing groups to either a constant daily photoperiod of 12 h light or a seasonally changing photoperiod that cycled between a summer maximum of 16 h per day and a winter minimum of 8 h; ambient air temperature was maintained at 26 °C. All squirrels showed continuous, year-round diurnal locomotor activity, and the group exposed to seasonally changing photoperiod adjusted onset and end of activity to changes in duration of the photoperiod. Animals in both groups showed a marked circadian rhythm of core body temperature with a typical daytime level of about 38 °C and nighttime level of about 35 °C for most of each year, but the group exposed to naturally changing daylength surprisingly reduced the level of its circadian oscillation by about 2 °C at the winter seasonal extreme of shortest daily illumination to a daytime level about 36 °C and a nocturnal level of about 33 °C. Despite this modest experimentally induced reduction in the level of the circadian rhythm of body temperature, we conclude that A. leucurus shows an overall stable annual pattern of circadian rhythmicity of its core body temperature that is consistent with a lack of any other evidence that the species engages in torpor or hibernation.

Seasonal variations in levels of human thyroid-stimulating hormone and thyroid hormones: a meta-analysis.

Seasonal dynamics in biological functions of mammals is regulated by melatonin-mediated circannual fluctuations in the secretion of thyroid-stimulating hormone (TSH) and thyroid hormones. Most anatomical and molecular structures responsive to photoperiod and melatonin secretion changes and the associated receptors are preserved in modern humans. This work aimed to determine the seasonal dynamics of TSH and thyroid hormone levels (total triiodothyronine (T3), free triiodothyronine (FT3), thyroxine (T4), free thyroxine (FT4) and to investigate the dependence of these variations on gender, age and amplitude of meteorological fluctuations. A meta-analysis of 13 panel and 7 cross-sectional studies was performed using Review Manager 5.3 (Cochrane Library). We found that circulating TSH levels were higher in winter than in other seasons, and FT4 levels were higher in autumn than in winter. T4 level had no pronounced seasonal dynamics. The level of circulating T3 was significantly higher in winter than in summer and FT3 levels were lower in summer than in autumn and spring. In addition, analysis of TSH seasonal dynamics (winter vs summer) accounting for gender differences showed pronounced increases in TSH levels during winter in women, but not in men; and also significant increases in FT4 levels during summer in men, but not in women. Seasonal dynamics of FT3 and T4 did not depend on gender. Seasonal dynamics of TSH did not change with respect to age. We also found that the extent of the seasonal dynamics of TSH is influenced by the extent of the annual dynamics of the partial density of oxygen in the air, as well as the magnitude of the annual dynamic of meteorological factors that determine it (atmospheric pressure and relative humidity).

Exploring circannual rhythms and chronotype effect in patients with Obsessive-Compulsive Tic Disorder (OCTD): A pilot study.

BACKGROUND: The aim of this study was to test, through a chronobiologic approach, the existence of a significant circannual rhythm of tics and obsessive-compulsive symptoms in patients with Obsessive-Compulsive Tic Disorder (OCTD). The chronotype effect on tics and OC symptoms during seasons was also studied. METHODS: Patients with a diagnosis of OCTD (N = 37; mean age = 18.78 ± 8.61) underwent four clinical evaluations: Winter (WIN), Spring (SPR), Summer (SUM) and Autumn (AUT). Tics were evaluated through Yale Global Tic Severity Scale (YGTSS) and OC symptoms through Yale-Brown Obsessive Compulsive Scale (Y-BOCS). Patients' chronotype was assessed by the Horne-Ostberg morningness-eveningness questionnaire (MEQ), which categorizes subjects according to the individuals'chronotype, being morning-type, evening-type, and neither-type. RESULTS: A statistically significant circannual rhythm was observed for OC symptoms (p = 0.007), with the acrophase occurring between AUT and WIN. Y-BOCS differed along the year (p = 0.0003 and η2p = 0.40) with lower results in SUM compared to WIN (p < 0.05) and AUT (p < 0.01). Tics displayed no circannual rhythm and YGTSS scores were comparable among seasons. Patients were classified as 15 morning-types (40.5%) 15 neither-types (40.5%) and 7 evening-types (19.0%). YGTSS data were similar for all chronotypes while Y-BOCS results were greater during SUM in evening-types than morning-type patients (p < 0.05; 15.7 ± 5.2 vs 3.4 ± 6.0). LIMITATIONS: It is essential to investigate the existence of tics and OC symptoms circannual rhythms over the course of more than one year with a larger sample. CONCLUSIONS: OC symptoms displayed a significant circannual rhythm and were influenced by patients' chronotype. On the contrary, tics resulted similar among seasons and chronotypes.