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1.  Seasonal pelage changes are synchronized by simulated natural photoperiods in Siberian hamsters (Phodopus sungorus) 
The extent to which changing day lengths synchronize the seasonal molt was assessed in nine cohorts of male and female Siberian hamsters (Phodopus sungorus) born into a simulated natural photoperiod (SNP) beginning 4 weeks before and ending 12 weeks after the summer solstice. Hamsters in early cohorts displayed rapid somatic and gonadal growth and early puberty, whereas those in later cohorts delayed puberty until the next spring. Despite the varying birth dates and puberty strategies, the seasonal pattern of change in pelage is much better predicted by calendar date than by age in both sexes. Males born over the course of 16 weeks first made the transition to the winter pelage during a 5 week interval beginning on October 25; the autumn molt, however, was not significantly synchronized by either age or calendar date. The autumn molt of females on the other hand began 2 weeks later, and was significantly synchronized to calendar date with no detectable age effects. In both sexes, the autumn molt lagged gonadal and somatic seasonal changes by many weeks. Date of birth did not affect the timing of the spring molt, which was significantly synchronized by calendar date in both sexes. Incrementally changing photoperiods exert a strong organizing effect on the seasonal molt by providing hamsters with timing cues that are absent in laboratory analyses that employ static day lengths and abrupt transitions from summer to winter day lengths, thereby extending and validating conclusions derived from previous analyses.
doi:10.1002/jez.544
PMCID: PMC3864830  PMID: 19425044
natural day length; molt; fur
2.  Photoperiod Alters Fear Responses and Basolateral Amygdala Neuronal Spine Density in White-Footed Mice (Peromyscus leucopus) 
Behavioural Brain Research  2012;233(2):345-350.
Photoperiodism is a biological phenomenonin which environmental day length is monitored to ascertain time of year to engage in seasonally-appropriate adaptations. This trait is common among organisms living outside of the tropics. White-footed mice (Peromyscus leucopus) are small photoperiodic rodents which display a suite of adaptive responses to short day lengths, including reduced hippocampal volume, impairments in hippocampal-mediated memory, and enhanced hypothalamic-pituitary-adrenal axis reactivity. Because these photoperiodic changes in brain and behavior mirror some of the etiology of post-traumatic stress disorder (PTSD), we hypothesized that photoperiod may also alter fear memory and neuronal morphology within the hippocampus - basolateral amygdala - prefrontal cortex fear circuit. Ten weeks of exposure to short days increased fear memory in an auditory-cued fear conditioning test. Short days also increased dendritic spine density of the neurons of the basolateral amygdala, without affecting morphology of pyramidal neurons within the infralimbic region of the medial prefrontal cortex. Taken together, photoperiodic phenotypic changes in brain morphology and physiology induced by a single environmental factor, exposure to short day lengths, affect responses to fearful stimuli in white-footed mice. These results have potential implications understanding seasonal changes in fear responsiveness, as well as for expanding translational animal models for studying gene-environment interactions underlying psychiatric diseases, such as PTSD.
doi:10.1016/j.bbr.2012.05.033
PMCID: PMC3402626  PMID: 22652395
PTSD; BLA; spine density; auditory fear conditioning; predator avoidance
3.  Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study 
BMC Ecology  2010;10:3.
Background
Insect diapause is an important biological process which involves many life-history parameters important for survival and reproductive fitness at both individual and population level. Drosophila montana, a species of D. virilis group, has a profound photoperiodic reproductive diapause that enables the adult flies to survive through the harsh winter conditions of high latitudes and altitudes. We created a custom-made microarray for D. montana with 101 genes known to affect traits important in diapause, photoperiodism, reproductive behaviour, circadian clock and stress tolerance in model Drosophila species. This array gave us a chance to filter out genes showing expression changes during photoperiodic reproductive diapause in a species adapted to live in northern latitudes with high seasonal changes in environmental conditions.
Results
Comparisons among diapausing, reproducing and young D. montana females revealed expression changes in 24 genes on microarray; for example in comparison between diapausing and reproducing females one gene (Drosophila cold acclimation gene, Dca) showed up-regulation and 15 genes showed down-regulation in diapausing females. Down-regulation of seven of these genes was specific to diapause state while in five genes the expression changes were linked with the age of the females rather than with their reproductive status. Also, qRT-PCR experiments confirmed couch potato (cpo) gene to be involved in diapause of D. montana.
Conclusions
A candidate gene microarray proved to offer a practical and cost-effective way to trace genes that are likely to play an important role in photoperiodic reproductive diapause and further in adaptation to seasonally varying environmental conditions. The present study revealed two genes, Dca and cpo, whose role in photoperiodic diapause in D. montana is worth of studying in more details. Also, further studies using the candidate gene microarray with more specific experimental designs and target tissues may reveal additional genes with more restricted expression patterns.
doi:10.1186/1472-6785-10-3
PMCID: PMC2822739  PMID: 20122138
4.  Perinatal photoperiod imprints the circadian clock 
Nature neuroscience  2010;14(1):25-27.
Using real-time gene expression imaging and behavioral analysis, we found that perinatal photoperiod has lasting effects on the circadian rhythms expressed by clock neurons as well as on mouse behavior, and sets the responsiveness of the biological clock to subsequent changes in photoperiod. These developmental gene x environment interactions tune circadian clock responses to subsequent seasonal photoperiods and may contribute to the influence of season on neurobehavioral disorders in humans.
doi:10.1038/nn.2699
PMCID: PMC3058292  PMID: 21131951
light; circadian; entrainment; seasonality; development; epigenetics; imprinting; birth season; suprachiasmatic nuclei; SCN
5.  Maternity care calendar wheel. Improved obstetric wheel developed in British Columbia. 
Canadian Family Physician  1999;45:661-666.
PROBLEM BEING ADDRESSED: Gestational calendar "wheels" are not well designed for routine prenatal care or for presenting the uncertainties of predicting date of delivery. OBJECTIVE OF PROGRAM: To design and pilot-test a new gestational calendar wheel that predicts the range of normal due dates in a way that reflects the biological realities of pregnancy. The calendar has prompts that could facilitate provision of antenatal care, support prenatal education, and guide the timing of induction for pregnancies past their due dates. MAIN COMPONENTS OF PROGRAM: The calendar sets out the key issues to be addressed with patients during pregnancy. It is designed to be photocopied while set to patients' dates: patients keep one copy; another is placed in their charts. The probability of delivering on a given date is presented graphically and as a percentage likelihood of giving birth during specified intervals. Twelve practising physicians, 12 residents, and 10 pregnant women pilot-tested and evaluated the wheel. Their responses were favourable. CONCLUSIONS: The Maternity Care Calendar wheel is a substantial advance on existing obstetric calendar wheels. It incorporates evidence-based information that should facilitate prenatal care, promote prenatal education, and foster realistic expectations about the likely timing of delivery. Early in the pregnancy, it can help establish the timing of induction for pregnancies past their due dates. Further testing of the calendar's effectiveness in improving patient outcomes is needed.
PMCID: PMC2328417  PMID: 10099805
6.  Genetic Differences in Human Circadian Clock Genes Among Worldwide Populations 
Journal of biological rhythms  2008;23(4):330-340.
The daily biological clock regulates the timing of sleep and physiological processes that are of fundamental importance to human health, performance, and well-being. Environmental parameters of relevance to biological clocks include (i) daily fluctuations in light intensity and temperature, and (ii) seasonal changes in photoperiod (daylength) and temperature; these parameters vary dramatically as a function of latitude and locale. In wide-ranging species other than humans, natural selection has genetically optimized adaptiveness along latitudinal clines. Is there evidence for selection of clock gene alleles along latitudinal/photoperiod clines in humans? A number of polymorphisms in the human clock genes Per2, Per3, Clock, and AANAT have been reported as alleles that could be subject to selection. In addition, this investigation discovered several novel polymorphisms in the human Arntl and Arntl2 genes that may have functional impact upon the expression of these clock transcriptional factors. The frequency distribution of these clock gene polymorphisms is reported for diverse populations of African Americans, European Americans, Ghanaians, Han Chinese and Papua New Guineans (including five subpopulations within Papua New Guinea). There are significant differences in the frequency distribution of clock gene alleles among these populations. Population genetic analyses indicate that these differences are likely to arise from genetic drift rather than from natural selection.
doi:10.1177/0748730408320284
PMCID: PMC2579796  PMID: 18663240
Circadian; Biological Clock; Sleep; FASPS; Depression; Arntl; Bmal; Mop; Per; Clock; AANAT
7.  Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs 
BMC Plant Biology  2012;12:97.
Background
The circadian clock is an endogenous mechanism that coordinates biological processes with daily changes in the environment. In plants, circadian rhythms contribute to both agricultural productivity and evolutionary fitness. In barley, the photoperiod response regulator and flowering-time gene Ppd-H1 is orthologous to the Arabidopsis core-clock gene PRR7. However, relatively little is known about the role of Ppd-H1 and other components of the circadian clock in temperate crop species. In this study, we identified barley clock orthologs and tested the effects of natural genetic variation at Ppd-H1 on diurnal and circadian expression of clock and output genes from the photoperiod-response pathway.
Results
Barley clock orthologs HvCCA1, HvGI, HvPRR1, HvPRR37 (Ppd-H1), HvPRR73, HvPRR59 and HvPRR95 showed a high level of sequence similarity and conservation of diurnal and circadian expression patterns, when compared to Arabidopsis. The natural mutation at Ppd-H1 did not affect diurnal or circadian cycling of barley clock genes. However, the Ppd-H1 mutant was found to be arrhythmic under free-running conditions for the photoperiod-response genes HvCO1, HvCO2, and the MADS-box transcription factor and vernalization responsive gene Vrn-H1.
Conclusion
We suggest that the described eudicot clock is largely conserved in the monocot barley. However, genetic differentiation within gene families and differences in the function of Ppd-H1 suggest evolutionary modification in the angiosperm clock. Our data indicates that natural variation at Ppd-H1 does not affect the expression level of clock genes, but controls photoperiodic output genes. Circadian control of Vrn-H1 in barley suggests that this vernalization responsive gene is also controlled by the photoperiod-response pathway. Structural and functional characterization of the barley circadian clock will set the basis for future studies of the adaptive significance of the circadian clock in Triticeae species.
doi:10.1186/1471-2229-12-97
PMCID: PMC3478166  PMID: 22720803
Hordeum vulgare; Circadian Clock; Photoperiod; Flowering; Ppd-H1
8.  Positive Temporal Dependence of the Biological Clock Implies Hyperbolic Discounting 
Temporal preferences of animals and humans often exhibit inconsistencies, whereby an earlier, smaller reward may be preferred when it occurs immediately but not when it is delayed. Such choices reflect hyperbolic discounting of future rewards, rather than the exponential discounting required for temporal consistency. Simultaneously, however, evidence has emerged that suggests that animals and humans have an internal representation of time that often differs from the calendar time used in detection of temporal inconsistencies. Here, we prove that temporal inconsistencies emerge if fixed durations in calendar time are experienced as positively related (positive quadrant dependent). Hence, what are time-consistent choices within the time framework of the decision maker appear as time-inconsistent to an outsider who analyzes choices in calendar time. As the biological clock becomes more variable, the fit of the hyperbolic discounting model improves. A recent alternative explanation for temporal choice inconsistencies builds on persistent under-estimation of the length of distant time intervals. By increasing the expected speed of our stochastic biological clock for time farther into the future, we can emulate this explanation. Ours is therefore an encompassing theoretical framework that predicts context-dependent degrees of intertemporal choice inconsistencies, to the extent that context can generate changes in autocorrelation, variability, and expected speed of the biological clock. Our finding should lead to novel experiments that will clarify the role of time perception in impulsivity, with critical implications for, among others, our understanding of aging, drug abuse, and pathological gambling.
doi:10.3389/fnins.2011.00002
PMCID: PMC3031993  PMID: 21441979
biological clock; impulsivity; preference reversal; hyperbolic discounting; exponential discounting; random time change
9.  A Functional Nexus between Photoperiod Acclimation, Torpor Expression and Somatic Fatty Acid Composition in a Heterothermic Mammal 
PLoS ONE  2013;8(5):e63803.
The seasonal changes in thermal physiology and torpor expression of many heterothermic mammals are controlled by photoperiod. As function at low body temperatures during torpor requires changes of tissue lipid composition, we tested for the first time whether and how fatty acids are affected by photoperiod acclimation in hamsters, Phodopus sungorus, a strongly photoperiodic species. We also examined changes in fatty acid composition in relation to those in morphology and thermal biology. Hamsters in short photoperiod had smaller reproductive organs and most had a reduced body mass in comparison to those in long photoperiod. Pelage colour of hamsters under short photoperiod was almost white while that of long photoperiod hamsters was grey-brown and black. Short photoperiod acclimation resulted in regular (28% of days) torpor use, whereas all hamsters in long photoperiod remained normothermic. The composition of total fatty acids differed between acclimation groups for brown adipose tissue (5 of 8 fatty acids), heart muscle (4 of 7 fatty acids) and leg muscle (3 of 11 fatty acids). Importantly, 54% of all fatty acids detected were correlated (r2 = 0.60 to 0.87) with the minimum surface temperature of individuals, but the responses of tissues differed. While some of the compositional changes of fatty acids were consistent with a ‘homeoviscous’ response, this was not the case for all, including the sums of saturated and unsaturated fatty acids, which did not differ between acclimation groups. Our data identify a possible nexus between photoperiod acclimation, morphology, reproductive biology, thermal biology and fatty acid composition. They suggest that some of the changes in thermal physiology are linked to the composition of tissue and organ fatty acids.
doi:10.1371/journal.pone.0063803
PMCID: PMC3661731  PMID: 23717487
10.  Reproductive Responses to Photoperiod Persist in Olfactory Bulbectomized Siberian Hamsters (Phodopus sungorus) 
Behavioural brain research  2008;198(1):159-164.
In reproductively photoperiodic Syrian hamsters, removal of the olfactory bulbs leads to a marked and sustained increase in gonadotrophin secretion which prevents normal testicular regression in short photoperiods. In contrast, among reproductively non-photoperiodic laboratory strains of rats and mice, bulbectomy unmasks reproductive responses to photoperiod. The role of the olfactory bulbs has been proposed to have opposite effects on responsiveness to photoperiod, depending on the photoperiodicity of the reproductive system; however, Syrian hamsters are the only reproductively photoperiodic rodent species for which the role of the olfactory bulb in reproductive endocrinology has been assessed. This experiment evaluated the role of the olfactory bulbs in the photoperiodic control of reproduction in Siberian hamsters (Phodopus sungorus), an established model species for the study of neural substrates mediating seasonality. Relative to control hamsters housed in long days (15 h light/day), exposure of adult male hamsters to short days (9 h light/day) for 8 weeks led to a temporal expansion of the pattern of nocturnal locomotor activity, testicular regression, decreases in testosterone (T) production, and undetectable levels of plasma follicle-stimulating hormone (FSH). Bilateral olfactory bulbectomy failed to affect any of these responses to short days. The patterns of entrainment to long and short days suggests that pre-pineal mechanisms involved in photoperiodic timekeeping are functioning normally in OBx hamsters. The absence of increases in FSH following bulbectomy in long days is incompatible with the hypothesis that the olfactory bulbs provide tonic inhibition of the HPG axis in this species. In marked contrast to Syrian hamsters, the olfactory bulbs of Siberian hamsters play essentially no role in the modulation of tonic gonadotrophin production or gonadotrophin responses to photoperiod.
doi:10.1016/j.bbr.2008.10.032
PMCID: PMC2661624  PMID: 19027041
photoperiodism; biological rhythms; reproduction; brain lesion
11.  Reduced body mass, food intake, and testis size in response to short photoperiod in adult F344 rats 
BMC Physiology  2002;2:11.
Background
Although laboratory rats are often considered classic nonseasonal breeders, peripubertal rats of two inbred strains, F344 and BN, have both reproductive and nonreproductive responses to short photoperiods. Unmanipulated adult rats have not been reported to have robust responses to short photoperiod alone, although several treatments can induce photoperiodic responses in adults. In this study, we tested the hypotheses that unmanipulated F344 rats retain responses to short photoperiod as adults and that they have the necessary elements for an endogenous circannual rhythm of sensitivity to short photoperiod.
Results
Relative to rats kept in long photoperiods (L16:D8), adult F344 rats transferred at 4.5 months of age to short photoperiods (L8:D16) had significantly lower testis size, food intake, and body weight. In a second experiment, newly weaned F344 rats underwent an initial period of inhibition of reproductive maturation, lower food intake, and lower body weight in short photoperiod or intermediate photoperiod (L12:D12) relative to rats in long photoperiod. By 18 weeks of treatment, rats in the two inhibitory photoperiods no longer differed from long photoperiod controls. In short photoperiod, rats underwent a second period of slight reproductive inhibition between weeks 35 and 48, but there was an effect on body weight and slight inhibition of food intake only in an intermediate photoperiod.
Conclusion
Male F344 rats retain photoresponsiveness as adults, with less reproductive inhibition but equivalent nonreproductive responses. There was only weak evidence for an endogenous timer controlling a circannual cycle of sensitivity to short photoperiod.
PMCID: PMC122066  PMID: 12135532
12.  QTL analysis of photoperiod sensitivity in common buckwheat by using markers for expressed sequence tags and photoperiod-sensitivity candidate genes 
Breeding Science  2011;61(4):394-404.
Photoperiod sensitivity is an important trait related to crop adaptation and ecological breeding in common buckwheat (Fagopyrum esculentum Moench). Although photoperiod sensitivity in this species is thought to be controlled by quantitative trait loci (QTLs), no genes or regions related to photoperiod sensitivity had been identified until now. Here, we identified QTLs controlling photoperiod sensitivity by QTL analysis in a segregating F4 population (n = 100) derived from a cross of two autogamous lines, 02AL113(Kyukei SC2)LH.self and C0408-0 RP. The F4 progenies were genotyped with three markers for photoperiod-sensitivity candidate genes, which were identified based on homology to photoperiod-sensitivity genes in Arabidopsis and 76 expressed sequence tag markers. Among the three photoperiod-sensitivity candidate genes (FeCCA1, FeELF3 and FeCOL3) identified in common buckwheat, FeELF3 was associated with photoperiod sensitivity. Two EST regions, Fest_L0606_4 and Fest_L0337_6, were associated with photoperiod sensitivity and explained 20.0% and 14.2% of the phenotypic variation, respectively. For both EST regions, the allele from 02AL113(Kyukei SC2)LH.self led to early flowering. An epistatic interaction was also confirmed between Fest_L0606_4 and Fest_L0337_6. These results demonstrate that photoperiod sensitivity in common buckwheat is controlled by a pathway consisting of photoperiod-sensitivity candidate genes as well as multiple gene action.
doi:10.1270/jsbbs.61.394
PMCID: PMC3406765  PMID: 23136477
common buckwheat; EST markers; photoperiod-sensitivity candidate genes; photoperiod sensitivity; QTL analysis
13.  Photoperiodic plasticity in circadian clock neurons in insects 
Since Bünning's observation of circadian rhythms and photoperiodism in the runner bean Phaseolus multiflorus in 1936, many studies have shown that photoperiodism is based on the circadian clock system. In insects, involvement of circadian clock genes or neurons has been recently shown in the photoperiodic control of developmental arrests, diapause. Photoperiod sets peaks of period (per) or timeless (tim) mRNA abundance at lights-off in Sarcophaga crassipalpis, Chymomyza costata and Protophormia terraenovae. Abundance of per and Clock mRNA changes by photoperiod in Pyrrhocoris apterus. Subcellular Per distribution in circadian clock neurons changes with photoperiod in P. terraenovae. Although photoperiodism is not known in Leucophaea maderae, under longer day length, more stomata and longer commissural fibers of circadian clock neurons have been found. These plastic changes in the circadian clock neurons could be an important constituent for photoperiodic clock mechanisms to integrate repetitive photoperiodic information and produce different outputs based on day length.
doi:10.3389/fphys.2013.00069
PMCID: PMC3750939  PMID: 23986711
photoperiodism; circadian clock neurons; plasticity; Per; s-LNv; pigment-dispersing factor
14.  Photoperiod History Differentially Impacts Reproduction and Immune Function in Adult Siberian Hamsters 
Journal of biological rhythms  2009;24(6):509-522.
Seasonal changes in numerous aspects of mammalian immune function arise as a result of the annual variation in environmental day length (photoperiod), but it is not known if absolute photoperiod or relative change in photoperiod drives these changes. This experiment tested the hypothesis that an individual’s history of exposure to day length determines immune responses to ambiguous, intermediate-duration day lengths. Immunological (blood leukocytes, delayed-type hypersensitivity reactions [DTH]), reproductive, and adrenocortical responses were assessed in adult Siberian hamsters (Phodopus sungorus) that had been raised initially in categorically long (15-h light/day; 15L) or short (9L) photoperiods and were subsequently transferred to 1 of 7 cardinal experimental photoperiods between 9L and 15L, inclusive Initial photoperiod history interacted with contemporary experimental photoperiods to determ.ine reproductive responses: 11L, 12L, and 13L caused gonadal regression in hamsters previously exposed to 15L, but elicited growth in hamsters previously in 9L. In hamsters with a 15L photoperiod history, photoperiods ≤ 11L elicited sustained enhancement of DTH responses, whereas in hamsters with a 9L photoperiod history, DTH responses were largely unaffected by increases in day length. Enhancement and suppression of blood leukocyte concentrations occurred at 13L in hamsters with photoperiod histories of 15L and 9L, respectively; however, prior exposure to 9L imparted marked hysteresis effects, which suppressed baseline leukocyte concentrations. Cortisol concentrations were only enhanced in 15L hamsters transferred to 9L and, in common with DTH, were unaffected by photoperiod treatments in hamsters with a 9L photoperiod history. Photoperiod history acquired in adulthood impacts immune responses to photoperiod, but manifests in a markedly dissimilar fashion as compared to the reproductive system. Prior photoperiod exposure has an enduring impact on the ability of the immune system to respond to subsequent changes in day length.
doi:10.1177/0748730409349714
PMCID: PMC3965335  PMID: 19926810
delayed-type hypersensitivity (DTH); blood leukocyte; cortisol; neural-immune interactions; seasonality; reproduction
15.  Mate Preference of Female Blue Tits Varies with Experimental Photoperiod 
PLoS ONE  2014;9(3):e92527.
Organisms use environmental cues to time their life-cycles and among these cues, photoperiod is the main trigger of reproductive behaviours such as territory defence or song activity. Whether photoperiod is also important for another behaviour closely associated with reproduction, mate choice, is unknown. In many bird species, mate choice occurs at two different times during the annual cycle that strongly differ in daylength: in late winter when photoperiod is short and social mates are chosen, and again around egg-laying when photoperiod is longer and extra-pair mates are chosen. This duality makes the role that photoperiod plays on mate choice behaviours intriguing. We investigated the effect of photoperiod on mate choice using three experimental photoperiodic treatments (9 L:15 D, 14 L:10 D, 18 L:6 D), using blue tits (Cyanistes caeruleus) as a biological model. We show that female choice was stronger under long photoperiods. In addition, female blue tits spent significantly more time near males with long tarsi and long wings. This latter preference was only expressed under long photoperiods, suggesting that some indices of male quality only become significant to females when they are strongly photostimulated, and therefore that females could select their social and extra-pair mates based on different phenotypic traits. These results shed light on the roles that photoperiod may play in stimulating pair-bonding and in refining female selectivity for male traits.
doi:10.1371/journal.pone.0092527
PMCID: PMC3966787  PMID: 24671133
16.  Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods 
Birds use photoperiod to control the time of breeding and moult. However, it is unclear whether responses are dependent on absolute photoperiod, the direction and rate of change in photoperiod, or if photoperiod entrains a circannual clock. If starlings (Sturnus vulgaris) are kept on a constant photoperiod of 12 h light : 12 h darkness per day (12 L : 12 D), then they can show repeated cycles of gonadal maturation, regression and moult, which is evidence for a circannual clock. In this study, starlings kept on constant 11.5 L : 12.5 D for 4 years or 12.5 L : 11.5 D for 3 years showed no circannual cycles in gonadal maturation or moult. So, if there is a circannual clock, it is overridden by a modest deviation in photoperiod from 12 L : 12 D. The responses to 11.5 L : 12.5 D and 12.5 L : 11.5 D were very different, the former perceived as a short photoperiod (birds were photosensitive for most of the time) and the latter as a long photoperiod (birds remained permanently photorefractory). Starlings were then kept on a schedule which ranged from 11.5 L : 12.5 D in mid-winter to 12.5 L : 11.5 D in mid-summer (simulating the annual cycle at 9 °N) for 3 years. These birds entrained precisely to calendar time and changes in testicular size and moult were similar to those of birds under a simulated cycle at 52 °N. These data show that birds are very sensitive to changes in photoperiod but that they do not simply respond to absolute photoperiod nor can they rely on a circannual clock. Instead, birds appear to respond to the shape of the annual change in photoperiod. This proximate control could operate from near equatorial latitudes and would account for similar seasonal timing in individuals of a species over a wide range of latitudes.
doi:10.1098/rspb.2006.0067
PMCID: PMC2197212  PMID: 17254997
bird; starling; photoperiodism; circannual rhythms; latitude
17.  Winter Day Lengths Enhance T Lymphocyte Phenotypes, Inhibit Cytokine Responses, and Attenuate Behavioral Symptoms of Infection in Laboratory Rats 
Brain, behavior, and immunity  2007;21(8):1096-1108.
Annual variations in day length (photoperiod) trigger changes in the immune and reproductive system of seasonally-breeding animals. The purpose of this study was to determine whether photoperiodic changes in immunity depend on concurrent photoperiodic responses in the reproductive system, or whether immunological responses to photoperiod occur independent of reproductive responses. Here we report photoperiodic changes in enumerative, functional, and behavioral aspects of the immune system, and in immunomodulatory glucocorticoid secretion, in reproductively non-photoperiodic Wistar rats. T-cell numbers (CD3+, CD8+, CD8+CD25+, CD4+CD25+) were higher in the blood of rats housed in short as opposed to long day lengths for 10 weeks. Following a simulated bacterial infection (E. coli LPS; 125 μg/kg) the severity of several acute-phase sickness behaviors (anorexia, cachexia, neophobia, and social withdrawal) were attenuated in short days. LPS-stimulated IL-1β and IL-6 production were comparable between photoperiods, but plasma TNFα was higher in long-day relative to short-day rats. In addition, corticosterone concentrations were higher in short-day relative to long-day rats. The data are consistent with the hypothesis that photoperiodic regulation of the immune system can occur entirely independently of photoperiodic regulation of the reproductive system. In the absence of concurrent reproductive responses, short days increase the numbers of leukocytes capable of immunosurveillance and inhibition of inflammatory responses, increase proinflammatory cytokine production, increase immunomodulatory glucocorticoid secretion, and ultimately attenuate behavioral responses to infection. Seasonal changes in the host immune system, endocrine system, and behavior may contribute to the seasonal variability in disease outcomes, even in reproductively non-photoperiodic mammals.
doi:10.1016/j.bbi.2007.05.004
PMCID: PMC2693110  PMID: 17728099
photoperiodism; sickness behavior; depression; IL-1β; IL-6; TNFα; corticosterone
18.  Seasonal regulation of reproduction: altered role of melatonin under naturalistic conditions in hamsters 
The seasonal reproductive cycle of photoperiodic rodents is conceptualized as a series of discrete melatonin-dependent neuroendocrine transitions. Least understood is the springtime restoration of responsiveness to winter-like melatonin signals (breaking of refractoriness) that enables animals to once again respond appropriately to winter photoperiods the following year. This has been posited to require many weeks of long days based on studies employing static photoperiods instead of the annual pattern of continually changing photoperiods under which these mechanisms evolved. Maintaining Siberian hamsters under simulated natural photoperiods, we demonstrate that winter refractoriness is broken within six weeks after the spring equinox. We then test whether a history of natural photoperiod exposure can eliminate the requirement for long-day melatonin signalling. Hamsters pinealectomized at the spring equinox and challenged 10 weeks later with winter melatonin infusions exhibited gonadal regression, indicating that refractoriness was broken. A photostimulatory effect on body weight is first observed in the last four weeks of winter. Thus, the seasonal transition to the summer photosensitive phenotype is triggered prior to the equinox without exposure to long days and is thereafter melatonin-independent. Distinctions between photoperiodic and circannual seasonal organization erode with the incorporation in the laboratory of ecologically relevant day length conditions.
doi:10.1098/rspb.2010.0396
PMCID: PMC2981982  PMID: 20444712
season; simulated natural photoperiod; melatonin
19.  Thyroid Hormone Signalling Genes Are Regulated by Photoperiod in the Hypothalamus of F344 Rats 
PLoS ONE  2011;6(6):e21351.
Seasonal animals adapt their physiology and behaviour in anticipation of climate change to optimise survival of their offspring. Intra-hypothalamic thyroid hormone signalling plays an important role in seasonal responses in mammals and birds. In the F344 rat, photoperiod stimulates profound changes in food intake, body weight and reproductive status. Previous investigations of the F344 rat have suggested a role for thyroid hormone metabolism, but have only considered Dio2 expression, which was elevated in long day photoperiods. Microarray analysis was used to identify time-dependent changes in photoperiod responsive genes, which may underlie the photoperiod-dependent phenotypes of the juvenile F344 rat. The most significant changes are those related to thyroid hormone metabolism and transport. Using photoperiod manipulations and melatonin injections into long day photoperiod (LD) rats to mimic short day (SD), we show photoinduction and photosuppression gene expression profiles and melatonin responsiveness of genes by in situ hybridization; TSHβ, CGA, Dio2 and Oatp1c1 genes were all elevated in LD whilst in SD, Dio3 and MCT-8 mRNA were increased. NPY was elevated in SD whilst GALP increased in LD. The photoinduction and photosuppression profiles for GALP were compared to that of GHRH with GALP expression following GHRH temporally. We also reveal gene sets involved in photoperiodic responses, including retinoic acid and Wnt/ß-catenin signalling. This study extends our knowledge of hypothalamic regulation by photoperiod, by revealing large temporal changes in expression of thyroid hormone signalling genes following photoperiod switch. Surprisingly, large changes in hypothalamic thyroid hormone levels or TRH expression were not detected. Expression of NPY and GALP, two genes known to regulate GHRH, were also changed by photoperiod. Whether these genes could provide links between thyroid hormone signalling and the regulation of the growth axis remains to be investigated.
doi:10.1371/journal.pone.0021351
PMCID: PMC3120865  PMID: 21731713
20.  Photoperiod Regulates Corticosterone Rhythms by Altered Adrenal Sensitivity via Melatonin-Independent Mechanisms in Fischer 344 Rats and C57BL/6J Mice 
PLoS ONE  2012;7(6):e39090.
Most species living in temperate zones adapt their physiology and behavior to seasonal changes in the environment by using the photoperiod as a primary cue. The mechanisms underlying photoperiodic regulation of stress-related functions are not well understood. In this study, we analyzed the effects of photoperiod on the hypothalamic-pituitary-adrenal axis in photoperiod-sensitive Fischer 344 rats. We first examined how photoperiod affects diurnal variations in plasma concentrations of adrenocorticotropic hormone (ACTH) and corticosterone. ACTH levels did not exhibit diurnal variations under long- and short-day conditions. On the other hand, corticosterone levels exhibited a clear rhythm under short-day condition with a peak during dark phase. This peak was not observed under long-day condition in which a significant rhythm was not detected. To analyze the mechanisms responsible for the photoperiodic regulation of corticosterone rhythms, ACTH was intraperitoneally injected at the onset of the light or dark phase in dexamethasone-treated rats maintained under long- and short-day conditions. ACTH induced higher corticosterone levels in rats examined at dark onset under short-day condition than those maintained under long-day condition. Next, we asked whether melatonin signals are involved in photoperiodic regulation of corticosterone rhythms, and rats were intraperitoneally injected with melatonin at late afternoon under long-day condition for 3 weeks. However, melatonin injections did not affect the corticosterone rhythms. In addition, photoperiodic changes in the amplitude of corticosterone rhythms were also observed in melatonin-deficient C57BL/6J mice, in which expression profiles of several clock genes and steroidgenesis genes in adrenal gland were modified by the photoperiod. Our data suggest that photoperiod regulates corticosterone rhythms by altered adrenal sensitivity through melatonin-independent mechanisms that may involve the adrenal clock.
doi:10.1371/journal.pone.0039090
PMCID: PMC3376106  PMID: 22720039
21.  Conservation of the photoperiodic neuroendocrine axis among vertebrates: evidence from the teleost fish, Gasterosteus aculeatus 
Photoperiod, or length of day, has a predictable annual cycle, making it an important cue for the timing of seasonal behavior and development in many organisms. Photoperiod is widely used among temperate and polar animals to regulate the timing of sexual maturation. The proper sensing and interpretation of photoperiod can be tightly tied to an organism’s overall fitness. In photoperiodic mammals and birds the thyroid hormone pathway initiates sexual maturation, but the degree to which this pathway is conserved across other vertebrates is not well known. We use the threespine stickleback Gasterosteus aculeatus, as a representative teleost to quantify the photoperiodic response of key genes in the thyroid hormone pathway under controlled laboratory conditions. We find that the photoperiodic responses of the hormones are largely consistent amongst multiple populations, although differences suggest physiological adaptation to various climates. We conclude that the thyroid hormone pathway initiates sexual maturation in response to photoperiod in G. aculeatus, and our results show that more components of this pathway are conserved among mammals, birds, and teleost fish than was previously known. However, additional endocrinology, cell biology and molecular research will be required to define precisely which aspects of the pathway are conserved across vertebrates.
doi:10.1016/j.ygcen.2012.03.010
PMCID: PMC3389224  PMID: 22504272
Thyroid hormone; Thyroid stimulating hormone; Gonadotropin releasing hormone; Lutenizing hormone; Threespine stickleback; photoperiodism
22.  Melatonin in Plants 
Plant Signaling & Behavior  2007;2(5):381-382.
Melatonin (N-acetyl-5-methoxytryptamine) is a biogenic indoleamine structurally related with other important substances such as tryptophan, serotonin, indole-3-acetic acid (IAA). In mammals, birds, reptiles and fish melatonin is a biological modulator of several timing (circadian) processes such as mood, sleep, sexual behavior, immunological status, etc. Since its discovery in plants in 1995 several physiological roles, including a possible role in flowering, circadian rhythms and photoperiodicity and as growth-regulator have been postulated. Recently, a possible role in rhizogenesis in lupin has also been proposed. Here, these actions of melatonin in plant development are commented on and some other interesting recent data concerning melatonin in plants are also discussed. The need for more investigation into melatonin and plants is presented as an obvious conclusion.
PMCID: PMC2634219  PMID: 19704606
antioxidant; auxin; ethylene; flowering; growth; IAA; melatonin; rhizogenesis
23.  Chromatin remodelling and the Arabidopsis biological clock 
Plant Signaling & Behavior  2008;3(2):121-123.
Plants, as sessile organisms, rely on accurate time measurement to synchronize their physiology and development to the most favourable time-of-day or time-of-year. The biological clock is the endogenous mechanism responsible for the integration of the photoperiodic information thus coordinating metabolism in resonance with the environmental cycle. Despite the importance of circadian clock function in plant reproduction and survival, we are still far from understanding the specific molecular mechanisms governing the rhythmic expression of clock components. Recently, we have described a new mechanism of circadian regulation that involves changes in chromatin structure at the TOC1 (TIMING OF CAB EXPRESSION 1) locus. The mechanism is defined by activators and repressors that are precisely coordinated to favor a hyper- or hypo-acetylated state of histones that leads to TOC1 transcriptional activation or repression, respectively. The clockcontrolled rhythms in histone acetylation/deacetylation at the TOC1 promoter are differentially modulated by day-length or photoperiod suggesting a mechanism by which plants ensure the phase of entrainment in physiological and developmental outputs.
PMCID: PMC2633999  PMID: 19704729
biological clock; chromatin remodelling; transcriptional regulation; photoperiod; Arabidopsis thaliana
24.  Novel functions for Period 3 and Exo-rhodopsin in rhythmic transcription and melatonin biosynthesis within the zebrafish pineal organ 
Brain research  2008;1223:11-24.
Entrainment of circadian clocks to environmental cues such as photoperiod ensures that daily biological rhythms stay in synchronization with the Earth’s rotation. The vertebrate pineal organ has a conserved role in circadian regulation as the primary source of the nocturnal hormone melatonin. In lower vertebrates, the pineal has an endogenous circadian clock as well as photoreceptive cells that regulate this clock. The zebrafish opsin protein Exo-rhodopsin (Exorh) is expressed in pineal photoreceptors and is a candidate to mediate the effects of environmental light on pineal rhythms and melatonin synthesis. We demonstrate that Exorh has an important role in regulating gene transcription within the pineal. In developing embryos that lack Exorh, expression of the exorh gene itself and of the melatonin synthesis gene serotonin N-acetyl transferase 2 (aanat2) are significantly reduced. This suggests that Exorh protein at the cell membrane is part of a signaling pathway that positively regulates transcription of these genes, and ultimately melatonin production, in the pineal. Like many other opsin genes, exorh is expressed with a daily rhythm: mRNA levels are higher at night than during the day. We find that the transcription factor Orthodenticle homeobox 5 (Otx5) activates exorh transcription, while the putative circadian clock component Period 3 (Per3) represses expression during the day, thereby contributing to the rhythm of transcription. This work identifies novel roles for Exorh and Per3, and gives insight into potential interactions between the sensory and circadian systems within the pineal.
doi:10.1016/j.brainres.2008.05.020
PMCID: PMC2615473  PMID: 18597743
Circadian rhythm; Exo-rhodopsin; Orthodenticle homeobox 5; Period 3; Pineal organ; Serotonin N-acetyl transferase; Transcriptional regulation
25.  Gene expression profiling in the rhesus macaque: experimental design considerations 
Methods (San Diego, Calif.)  2009;49(1):26-31.
The development of species-specific gene microarrays has greatly facilitated gene expression profiling in nonhuman primates. However, to obtain accurate and physiologically meaningful data from these microarrays, one needs to consider several factors when designing the studies. This article focuses on effective experimental design while the companion article focuses on methodology and data analysis. Biological cycles have a major influence on gene expression, and at least 10% of the expressed genes are likely to show a 24-hour expression pattern. Consequently, the time of day when RNA samples are collected can influence detection of significant changes in gene expression levels. Similarly, when photoperiodic species such as the rhesus macaque are housed outdoors, some of their genes show differential expression according to the time of year. In addition, the sex-steroid environment of humans and many nonhuman primates changes markedly across the menstrual cycle, and so phase of the cycle needs to be considered when studying gene expression in adult females.
doi:10.1016/j.ymeth.2009.05.009
PMCID: PMC2734384  PMID: 19467336
Circadian rhythms; Macaca Mulatta; Menstrual cycle; Microarray; Sex steroids; Rhesus Macaque Genome Array

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