Endogenous Circannual Rhythm Research Articles

Seasonality and climatic control of reproduction in wild-caught female Lesser Egyptian jerboa (Jaculus jaculus) from central Saudi Arabia

In arid regions, unpredictable rainfall patterns and extreme temperature variation occurs; this poses severe constraints on reproduction in small mammals. In the present study, the gonad morphometrics, gonadal histology and endocrine profiles of the female Lesser Egyptian jerboas (Jaculus jaculus) were studied over one year in a wild population from central Saudi Arabia. An unusual rainfall pattern occurred during this study period, with three out of four seasons receiving rainfall. Pregnant females were observed during every season when rainfall fell. Yet, a distinct reproduction pattern was also observed in the reproductive parameters of J. jaculus, likely entrained by ambient temperature and photoperiodic changes, with indicators of reproductive activity being at its highest during the winter months. Jaculus jaculus, appear to possess an endogenous circannual rhythm (seasonality) of breeding, entrained by ambient temperature and photoperiod. However, they have a plasticity to their breeding strategy, which allows them to breed opportunistically. As global warming takes effect, many species which currently inhabit temperate regions may experience desertification. Understanding how species that inhabit deserts today are adapted to these harsh conditions may allow researchers to identify temperate species that are more at risk to climatic changes due to global warming.

Seasonality, niche management and vertical migration in landscapes of relief

Landscapes of vertical relief, such as mountains and continental slopes, intensify ecological and climatological variation within narrow spatial windows. Seasonal vertical migrants exploit this variation during their residence in, and movements between, vertically stratified seasonal ranges. Animals in terrestrial, marine and even human‐ecological systems undergo similar patterns of seasonal vertical movements. The diversity of arenas in which vertical migration evolved lends insight to the factors promoting seasonal use of landscapes of relief. Because animals must contend with both endogenous circannual rhythms and exogenous environmental seasonality, vertical migrants may be sensitive to inconsistent change across stratified seasonal ranges under climate change. To better understand how ongoing and future climatic and environmental changes are likely to impact vertical migrants, we examine vertical migration in the context of niche tracking and niche switching. Whereas niche trackers minimize variation in realized environmental conditions throughout their seasonal movements, niche switchers undergo seasonal transitions in realized niche space. These strategies mediate the relationship between migrants and their changing environment, and can be used to forecast impacts of future change and effectively conserve systems of vertical migration. Niche tracking may be hindered by inconsistent or unpredictable environmental change along a single niche axis across strata, while niche switching may be sensitive to incongruous spatiotemporal change across factors. We suggest that climate change will affect seasonal patterns in vertical environments discontinuously across time, space and strata, and that vertical migrants are likely to face additional anthropogenic threats that interact with environmental seasonality. Conservation of vertical migrants should prioritize the availability of, and facilitate movement between, stratified seasonal ranges.

Seasonal changes in adenosine kinase in tanycytes of the Arctic ground squirrel (Urocitellus parryii)

Hibernation is a seasonal strategy to conserve energy, characterized by modified thermoregulation, an increase in sleep pressure and drastic metabolic changes. Glial cells such as astrocytes and tanycytes are the brain metabolic sensors, but it remains unknown whether they contribute to seasonal expression of hibernation. The onset of hibernation is controlled by an undefined endogenous circannual rhythm in which adenosine plays a role through the activation of the A1 adenosine receptor (A1AR). Seasonal changes in brain levels of adenosine may contribute to an increase in A1AR sensitivity leading to the onset of hibernation. The primary regulator of extracellular adenosine concentration is adenosine kinase, which is located in astrocytes. Using immunohistochemistry to localize and quantify adenosine kinase in Arctic ground squirrels’ brain collected during different seasons, we report lower expression of adenosine kinase in the third ventricle tanycytes in winter compared to summer; a similar change was not seen in astrocytes. Moreover, for the first time, we describe adenosine kinase expression in tanycyte cell bodies in the hypothalamus and in the area postrema, both brain regions involved in energy homeostasis. Next we describe seasonal changes in tanycyte morphology in the hypothalamus. Although still speculative, our findings contribute to a model whereby adenosine kinase in tanycytes regulates seasonal changes in extracellular concentration of adenosine underling the seasonal expression of hibernation.

Elevated ambient temperature accelerates aspects of torpor phenology in an obligate hibernator.

The thirteen-lined ground squirrel (Ictidomys tridecemlineatus) is assumed to be an obligate hibernator - commencing and terminating hibernation on a circannual rhythm, regardless of environmental conditions - but, until now, this assumption had never been fully tested. We housed three groups of captive-born ground squirrels from Aug. 2017 to Aug. 2018 under constant photoperiod (12hL:12h D) at 5, 16 or 25°C, and monitored hibernation using body temperature loggers. At 5 and 16°C all animals hibernated from autumn to spring with no differences in date of first/last torpor or duration of interbout euthermic periods (IBE), but torpor bout duration was 25% shorter at 16°C. One of 4 animals housed at 25°C did not hibernate. For the other three 25°C animals, the first torpor date did not differ from the other groups, but the last torpor bout (5 Feb.) occurred almost 8 weeks earlier. These animals aroused from torpor more frequently and IBE lasted significantly longer, so the total time spent torpid was less than 50% of the other groups. Unlike the 5 or 16°C animals, 25°C animals re-entered torpor in late spring 2018. Taken together these data suggest that this species is an obligate hibernator, but that high ambient temperatures can accelerate the endogenous circannual hibernation rhythm.

The effect of photoperiod and melatonin on plasma prolactin concentrations in female guanaco (Lama guanicoe) in captivity.

The present study examined the effects of different photoperiods and melatonin treatment on plasma prolactin concentrations in guanacos, a South American camelid, in captivity. Fourteen adult female guanacos, not gestating or lactating and isolated from males, were studied. The control group was exposed to natural daylight, during short days (N=7, 10L:14D) and long days (N=7, 16L:8D). The treatment group (N=7, 10L:14D) received melatonin implants every 23days for 6weeks during long days. Blood samples were taken at intervals of 1week for 3weeks, starting the third week of treatment. Prolactin concentrations were measured using competitive ELISA. Plasma concentrations of prolactin in non-lactating female guanacos have seasonal changes, with a higher concentration (p<.001) in short days (3.50±2.24ng/ml) than long days (1.10±0.91ng/ml). Melatonin treatment significantly decreases (p<.05) plasma concentrations of prolactin on the 21st day after the treatment. These findings are the first report of an endogenous circannual rhythm of plasma prolactin concentration and the action of melatonin treatment on prolactin secretion in this wild camelid.

Circadian versus circannual rhythm in the photoperiodic programming of seasonal responses in Eurasian tree sparrow (Passer montanus).

Experiments were performed on the subtropical tree sparrow (Passer montanus) to investigate whether day length, as a proximate factor, involves circadian rhythm in timing seasonal responses or these events are programmed by the mediation of an endogenous circannual rhythm. The experiments began from the two equinoxes, i.e. March and September, and continued for about 18 months. In each equinox, one group of wild birds of both sex was exposed to near simulated day length as it varies in nature at Shillong (Latitude 25°34'N, Longitude 91°53'E), and the other group was given a photoperiodic treatment in the reverse order corresponding to natural variation in day length from the other equinox. The birds exposed to near simulated day lengths in March and September showed gonadal, bill colour and molting responses, as observed in the wild birds in nature. Moreover, when photosensitive birds of March were given photoperiodic treatment in the reverse order (i.e., natural variation in day lengths beginning from September), they maintained their photosensitivity and responded only when they received increasing day length in the following September. However, when the photorefractory birds of September were exposed to reverse photoperiodic treatment (i.e. natural day length as it varies from March), they terminated their photorefractoriness after receiving decreasing day length in March the next year and responded when they again received increasing day length in the following September. These results strongly suggest that photoperiodic regulation of seasonal responses in the tree sparrow involves an endogenous circadian rhythm and exclude the possibility of circannual rhythm generation.

Effects of advanced and continuous photoperiod regimes on maturation control and profiles of sex steroids in brook trout (

Maturation of salmonid species reduces growth, flesh quality and immunocompetency and has inhibited, in part, the commercial production of brook trout in Tasmania. Photoperiod manipulation is routinely used to inhibit or reduce the incidence of maturation in salmonids, so an experimental adaptation of this approach was trialled experimentally for brook trout. Mixed-sex fish (age = 14 months) were subjected to simulated natural photoperiod (NP), advanced photoperiod (AP) and continuous photoperiod (CP) to investigate the response of endogenous circannual rhythm upon sexual maturity in this species. Light treatments commenced on the first day of the last month of the southern hemisphere’s winter and concluded towards the end of autumn when fish were ovulating. Maturation was observed in 100% of females and 96% of males held under NP. Fish exposed to AP corrected their maturation cycle by advanced phase shift of their endogenous rhythm for eight weeks and achieved final maturation during March–April. Plasma profiles of testosterone and oestradiol-17β were also adjusted according to advancement of photoperiod. Exposure to AP inhibited maturation by 6% and 8% in males and females, respectively. CP treatment for 10 consecutive months failed to inhibit gonadal development; however, this regime did delay or inhibit spermiation and ovulation.

Issue Cover (November 2019)

Journal of NeurochemistryVolume 151, Issue 3 Issue CoverFree Access Issue Cover (November 2019) First published: 28 October 2019 https://doi.org/10.1111/jnc.14528 Read the full article: ‘Seasonal decrease in thermogenesis and increase in vasoconstriction explain seasonal response to N6-cyclohexyladenosine-induced hibernation in the Arctic ground squirrel (Urocitellus parryii)’ by C. Frare, M. E. Jenkins, K. M. McClure, K. L. Drew (J. Neurochem. 2019, vol. 151 (3), pp. 316–335) on doi: 10.1111/jnc.14814 AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Graphical Abstract Front cover: Hibernation is a seasonal phenomenon characterized by a decrease in metabolic rate and body temperature. The adenosine A1 receptor mediates the onset of hibernation through a yet unknown mechanism entrained to an endogenous circannual rhythm, independent of photoperiod and ambient temperature. Results show that the seasonal response to adenosine A1 receptor agonist is associated with the decrease in thermogenesis regulated by the median preoptic nucleus and the raphe pallidus and the increase in vasoconstriction. These findings expand our understanding of the mechanisms inducing hibernation, which translation will develop strategies to manipulate metabolic demand in conditions such as obesity and therapeutic hypothermia. Image content: Shown is a bright field image of the serotonergic neurons in the raphe pallidus of the arctic ground squirrel, with antibody to tryptophan hydroxylase. Read the full article ‘Seasonal decrease in thermogenesis and increase in vasoconstriction explain seasonal response to N6-cyclohexyladenosine-induced hibernation in the Arctic ground squirrel (Urocitellus parryii)’ by C. Frare, M. E. Jenkins, K. M. McClure, K. L. Drew (J. Neurochem. 2019, vol. 151 (3), pp. 316–335) on doi: 10.1111/jnc.14814 Volume151, Issue3November 2019 RelatedInformation

Seasonal decrease in thermogenesis and increase in vasoconstriction explain seasonal response to N6 -cyclohexyladenosine-induced hibernation in the Arctic ground squirrel (Urocitellus parryii).

Hibernation is a seasonal phenomenon characterized by a drop in metabolic rate and body temperature. Adenosine A1 receptor agonists promote hibernation in different mammalian species, and the understanding of the mechanism inducing hibernation will inform clinical strategies to manipulate metabolic demand that are fundamental to conditions such as obesity, metabolic syndrome, and therapeutic hypothermia. Adenosine A1 receptor agonist-induced hibernation in Arctic ground squirrels is regulated by an endogenous circannual (seasonal) rhythm. This study aims to identify the neuronal mechanism underlying the seasonal difference in response to the adenosine A1 receptor agonist. Arctic ground squirrels were implanted with body temperature transmitters and housed at constant ambient temperature (2°C) and light cycle (4L:20D). We administered CHA (N6 -cyclohexyladenosine), an adenosine A1 receptor agonist in euthermic-summer phenotype and euthermic-winter phenotype and used cFos and phenotypic immunoreactivity to identify cell groups affected by season and treatment. We observed lower core and subcutaneous temperature in winter animals and CHA produced a hibernation-like response in winter, but not in summer. cFos-ir was greater in the median preoptic nucleus and the raphe pallidus in summer after CHA. CHA administration also resulted in enhanced cFos-ir in the nucleus tractus solitarius and decreased cFos-ir in the tuberomammillary nucleus in both seasons. In winter, cFos-ir was greater in the supraoptic nucleus and lower in the raphe pallidus than in summer. The seasonal decrease in the thermogenic response to CHA and the seasonal increase in vasoconstriction, assessed by subcutaneous temperature, reflect the endogenous seasonal modulation of the thermoregulatory systems necessary for CHA-induced hibernation. Cover Image for this issue: doi: 10.1111/jnc.14528.

Pregnancy and parturition in dromedary camels I. Factors affecting gestation length, calf birth weight and timing of delivery

In the present study, we evaluated the role of genetic, physiologic and environmental factors in affecting gestation length, calf birth weight and time of parturition in dromedary camels. Reproductive data were collected over a 10-year period at the world's first intensively managed, large-scale camel dairy farm. We hypothesized that environmental conditions (i.e. photoperiod) have a decisive effect on these reproductive parameters. The effect of various factors was tested with linear mixed models and variance component analysis. A total of 557 (13.1%) primiparous and 3691 (86.9%) multiparous parturitions were observed in 2,123 dromedaries. Parturitions had a pronounced seasonal distribution. The mean (±SE) length of gestation and mean (±SE) birth weight were 384.5 ± 0.17 days (n = 4,093, CV = 2.88%) and 34.5 ± 0.09 kg (n = 3,909, CV = 16.8%), respectively. All but one fixed factors (type of breeding) affected length of gestation and calf birth weight. Month of conception (27.1%), female camel (11.2%) and live-dead status of the calf (10.6%) were responsible for close to 50% of the variation in gestation length. At the same time, female camel (30.3%), parity (11.3%), year (6.9%) and month of parturition (6.2%) had the strongest relative influence on the variation in calf birth weight. Both reproductive traits showed a pronounced circannual variation. Mean length of gestation was longer by app. 18 days in dromedaries conceiving in November compared to those becoming pregnant in May. Average new-born weight was 4.4–4.9 kg higher in December compared to that in September and April. Dromedaries gave birth throughout the 24 h period, but most of the deliveries (n = 3,117, 74.1%) occurred from sunrise to sunset. The peak of deliveries was between 2 and 3 pm. Month of the year has a strong effect on the timing of deliveries. In contrast, the time from sunrise to parturition did not differ among the months. Peak of deliveries occurred 7–9 h after sunrise and the median of time from sunrise to parturition was 8 h and 24 min. These results give strong support to the original hypothesis. Seasonal changes were independent of nutritional factors, were associated with climatic conditions (i.e. photoperiod) and may reflect an endogenous circannual rhythm in foetal development. The dromedary camel could be a useful in vivo model to study the effect of the environment on feto-maternal communication, fetal development and timing of parturition.

Physiology of reproductive seasonality in sheep – an update

ABSTRACTThe seasonal breeding in sheep poses a challenge in improving productivity, owing to the incomplete knowledge of the mechanics of seasonal breeding, effective strategies for increasing the lamb crop are restricted. A major mechanism responsible for seasonal reproduction is a striking increase in the responsiveness of gonadotropin-releasing hormone (GnRH) neurons to the negative feedback effects of estradiol that peaks during anestrous and decreases in the breeding season. Melatonin does not directly drive seasonal changes in reproduction; rather it appears to synchronize an endogenous circannual rhythm. The Pars Tuberalis (PT) is a single common region across species that shows strongest MT1 expression. Melatonin acts through high affinity, G-protein coupled receptors located in thyrotroph cells in PT of the pituitary, controlling the production of the hormone, thyrotropin (TSH). Probably, the thyroid hormones serve as a connecting link between environmental cues and reproductive activity. Two very important peptides viz. kisspeptins and RFamide relative peptide appear to be key targets of thyroid hormones. Kisspeptin has been demonstrated as a potent GnRH stimulator and RFRP as an inhibitor which gets modulated with the season and controls reproductive activity in sheep.

Milk yield, lactation parameters and prolactin secretion characteristics in sheep treated with melatonin implants during pregnancy and lactation in long-day conditions

In a temperate climate zone, sheep lambing during long days (summer) produce less milk and have shorter lactation than those naturally lambing during short days (winter). We investigated whether artificially induced and prolonged increase in melatonin concentration in sheep lambed during long days would improve milk yield and lactation parameters through changes in pituitary prolactin (PRL) secretion. In addition, the relative mRNA levels of PRL and PRL-receptor (PRL-R) were determined in the mammary gland. Sheep (n = 36) were randomly divided into three groups: lambed in January (short day – SD treatment group), lambed in June (long day – LD treatment group), and lambed in June and treated with the subcutaneous melatonin implants (in May and then in August, LDM treatment group). After lamb weaning, milk yield, the number of milking days and the total length of lactation (days) were monitored individually. Plasma melatonin and PRL concentrations were determined in samples collected from 18 sheep (6 of each group): 6 weeks before parturition, day after weaning and then during lactation, every 28 days. A mammary gland biopsy was performed in these sheep 3–4 days before parturition. Milk yield was higher in the SD group, than in the LD (P < 0.05) and LDM (P < 0.001) groups. Both the number of milking days and total length of lactation were higher in the SD (P < 0.001) and LDM (P < 0.05) groups than in the LD group. The PRL and melatonin secretion profiles varied in all groups, reflecting the characteristics of the endogenous circannual rhythm. An additional increase in plasma PRL concentration occurred in LDM sheep, compared to LD sheep (P < 0.01). Statistical differences were found neither in the relative levels of PRL mRNA nor PRL-R mRNA in the mammary gland between the SD and LD groups, however both transcripts contents decreased (P < 0.05) in the LDM group. In conclusions: 1) alterations in milk yield and lactational parameters in sheep are affected by changes in the secretory PRL profile during the established lactation; 2) PRL refractoriness to melatonin develops in lactating sheep with extended melatonin treatment, which increases only a number of milking days, with no positive effect on milk yield; 3) The sheep mammary gland is qualitatively at the same level of preparation, in both short and long days, for the synthesis and perception of PRL during the periparturient period; 4) Artificially elevated plasma melatonin concentration before parturition causes a decrease in abundance of both PRL and PRL-R transcripts in the mammary gland.

Physical Cues Controlling Seasonal Immune Allocation in a Natural Piscine Model.

Seasonal patterns in immunity are frequently observed in vertebrates but are poorly understood. Here, we focused on a natural piscine model, the three-spined stickleback (Gasterosteus aculeatus), and asked how seasonal immune allocation is driven by physical variables (time, light, and heat). Using functionally-relevant gene expression metrics as a reporter of seasonal immune allocation, we synchronously sampled fish monthly from the wild (two habitats), and from semi-natural outdoors mesocosms (stocked from one of the wild habitats). This was repeated across two annual cycles, with continuous within-habitat monitoring of environmental temperature and implementing a manipulation of temperature in the mesocosms. We also conducted a long-term laboratory experiment, subjecting acclimated wild fish to natural and accelerated (×2) photoperiodic change at 7 and 15°C. The laboratory experiment demonstrated that immune allocation was independent of photoperiod and only a very modest effect, at most, was controlled by a tentative endogenous circannual rhythm. On the other hand, experimentally-determined thermal effects were able to quantitatively predict much of the summer–winter fluctuation observed in the field and mesocosms. Importantly, however, temperature was insufficient to fully predict, and occasionally was a poor predictor of, natural patterns. Thermal effects can thus be overridden by other (unidentified) natural environmental variation and do not take the form of an unavoidable constraint due to cold-blooded physiology. This is consistent with a context-dependent strategic control of immunity in response to temperature variation, and points to the existence of temperature-sensitive regulatory circuits that might be conserved in other vertebrates.

Environmental temperature effects on adipose tissue growth in a hibernator.

Obligate hibernators express circannual patterns of body mass and hibernation, which persist under constant laboratory conditions. Brown adipose tissue (BAT) is important for thermogenesis during arousals from hibernation, whereas white adipose tissue (WAT) serves as energy storage and thermal insulation. The goal of this study was to investigate the effects of environmental temperature on BAT and WAT. We hypothesized that changes to environmental temperature would not influence the pattern of mass gain or BAT and WAT volume in the thirteen-lined ground squirrel (Ictidomys tridecemlineatus). To test this, we housed animals at thermoneutral 25°C (warm-housed) or 5°C (cold-housed), with the same photoperiod (12 h light:12 h dark) over an entire year. Throughout the year we measured the volume and water:fat ratio of WAT and BAT using magnetic resonance imaging (MRI). We found no evidence of torpor in the warm-housed animals, indicating that this species might not be an obligate hibernator, as previously assumed. Regardless of ambient temperature, BAT volume increased prior to winter, then decreased in late winter with no change in water:fat ratio. By contrast, both body mass and WAT volume of cold-housed animals declined throughout the winter and recovered after hibernation, but thermoneutral housing produced no circannual pattern in body mass, even though WAT volume declined in late winter. Cold exposure appears to be a primary regulator for WAT but BAT may exhibit an endogenous circannual rhythm in terms of depot volume.

Annual Molting Cycle and Photoperiods That Affect Seasonal Coat Color Changes in the Japanese Marten (Martes melampus)

Abstract. External factors that affect seasonal coat color changes in the Japanese marten (Martes melampus) were examined under experimental conditions. In martens, captured in Kagoshima Prefecture and exposed to a photoperiod of 10L: 14D with light intensity of 20–70 lux, molting rhythms did not synchronize with each other over six years, regardless of ambient temperature fluctuations. The cycle length from the start of one blackish color change to the next was approximately 14 months. This may be caused by a modifiable endogenous circannual rhythm that may be reset by external photoperiods. For the male kept at 14L: 10D with light intensity of 600 lux, duration of activity was 13 h, and his fur remained blackish without change for three years. The fur of female, kept under the same conditions, changed to yellowish when the duration of activity changed to 9 or 10 h, and subsequently remained brackish without molting when the duration changed to 13 h. These results show that length of time exposed to ligh...

Effect of genetic and nongenetic factors on chemical composition of individual milk samples from dromedary camels (Camelus dromedarius) under intensive management

The aims of the present study were to monitor the changes in gross chemical composition of individual dromedary camel milk over a 5-yr period, to provide reference values, and to determine the effect of genetic and nongenetic factors influencing camel milk composition under intensive management. A total of 1,528 lactating dromedary camels were included in the study. Animals were fed a constant diet and were milked twice a day in a herringbone parlor. Milk samples were collected at monthly intervals using a sampling device and then fat, protein, lactose, total solids (TS), and solids-nonfat (SNF) concentrations of raw camel milk were determined with an automatic milk analyzer. For each milk sample, production parameters were recorded and quantities (grams) of milk constituents were calculated. The overall mean quantity and fat, protein, lactose, SNF, and TS concentrations of the morning milk were 4.0 kg, 2.58%, 2.95%, 4.19%, 8.08%, and 10.46%, respectively. Milk quantity showed a positive correlation with lactose and a negative correlation with all other components. Parity exerted a strong effect on all milk parameters. Primiparous dromedaries (n = 60) produced less milk with higher concentrations of components than did multiparous animals (n = 1,468). Milk composition varied among the 7 breeds tested, but none of the genotypes was found to be superior to the others in this respect. We detected a significant, yet small calf sex-biased difference in milk yield and composition. Stage of lactation and season strongly influenced milk yield and all milk components. We also found a significant interaction between month postpartum (mPP) and month of the year. The concentration of all milk components decreased from 1 to 5 mPP. Later, lactose concentration and quantity continued to decrease parallel with decreasing milk production. The concentration of other components showed a temporary increase in mid lactation, from 6 to 11 mPP, and in late lactation, from 18 to 23 mPP. Mean fat, protein, SNF, and TS concentrations showed a high seasonal variation (9.5 to 28.7%), with the lowest and highest values being measured during summer and winter, respectively. This seasonal variation was independent of nutrition and may reflect an endogenous circannual rhythm. We observed a noticeable variation among years. Dromedary camels could provide a useful in vivo model to study the homeorhetic regulation of mammary cell function by endogenous and environmental factors.

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

BackgroundAdjusting 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.ResultsHere 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.ConclusionUnderstanding how environmental stimuli and endogenous circannual rhythms interact can improve predictions of the consequences of climate changes on migratory animals.

HNF-4 participates in the hibernation-associated transcriptional regulation of the chipmunk hibernation-related protein gene

The chipmunk hibernation-related protein 25 (HP-25) is involved in the circannual control of hibernation in the brain. The liver-specific expression of the HP-25 gene is repressed in hibernating chipmunks under the control of endogenous circannual rhythms. However, the molecular mechanisms that differentially regulate the HP-25 gene during the nonhibernation and hibernation seasons are unknown. Here, we show that the hibernation-associated HP-25 expression is regulated epigenetically. Chromatin immunoprecipitation analyses revealed that significantly less hepatocyte nuclear receptor HNF-4 bound to the HP-25 gene promoter in the liver of hibernating chipmunks compared to nonhibernating chipmunks. Concurrently in the hibernating chipmunks, coactivators were dissociated from the promoter, and active transcription histone marks on the HP-25 gene promoter were lost. On the other hand, small heterodimer partner (SHP) expression was upregulated in the liver of hibernating chipmunks. Overexpressing SHP in primary hepatocytes prepared from nonhibernating chipmunks caused HNF-4 to dissociate from the HP-25 gene promoter, and reduced the HP-25 mRNA level. These results suggest that hibernation-related HP-25 expression is epigenetically regulated by the binding of HNF-4 to the HP-25 promoter, and that this binding might be modulated by SHP in hibernating chipmunks.

Clock gene polymorphism, migratory behaviour and geographic distribution: a comparative study of trans-Saharan migratory birds.

Migratory behaviour is controlled by endogenous circannual rhythms that are synchronized by external cues, such as photoperiod. Investigations on the genetic basis of circannual rhythmicity in vertebrates have highlighted that variation at candidate 'circadian clock' genes may play a major role in regulating photoperiodic responses and timing of life cycle events, such as reproduction and migration. In this comparative study of 23 trans-Saharan migratory bird species, we investigated the relationships between species-level genetic variation at two candidate genes, Clock and Adcyap1, and species' traits related to migration and geographic distribution, including timing of spring migration across the Mediterranean Sea, migration distance and breeding latitude. Consistently with previous evidence showing latitudinal clines in 'circadian clock' genotype frequencies, Clock allele size increased with breeding latitude across species. However, early- and late-migrating species had similar Clock allele size. Species migrating over longer distances, showing delayed spring migration and smaller phenotypic variance in spring migration timing, had significantly reduced Clock (but not Adcyap1) gene diversity. Phylogenetic confirmatory path analysis suggested that migration date and distance were the most important variables directly affecting Clock gene diversity. Hence, our study supports the hypothesis that Clock allele size increases poleward as a consequence of adaptation to the photoperiodic regime of the breeding areas. Moreover, we show that long-distance migration is associated with lower Clock diversity, coherently with strong stabilizing selection acting on timing of life cycle events in long-distance migratory species, likely resulting from the time constraints imposed by late spring migration.

Decreases in body temperature and body mass constitute pre-hibernation remodelling in the Syrian golden hamster, a facultative mammalian hibernator

Hibernation is an adaptive strategy for surviving during periods with little or no food availability, by profoundly reducing the metabolic rate and the core body temperature (Tb). Obligate hibernators (e.g. bears, ground squirrels, etc.) hibernate every winter under the strict regulation of endogenous circannual rhythms, and they are assumed to undergo adaptive remodelling in autumn, the pre-hibernation period, prior to hibernation. However, little is known about the nature of pre-hibernation remodelling. Syrian hamsters (Mesocricetus auratus) are facultative hibernators that can hibernate irrespective of seasons when exposed to prolonged short photoperiod and cold ambient temperature (SD-Cold) conditions. Their Tb set point reduced by the first deep torpor (DT) and then increased gradually after repeated cycles of DT and periodic arousal (PA), and finally recovered to the level observed before the prolonged SD-Cold in the post-hibernation period. We also found that, before the initiation of hibernation, the body mass of animals decreased below a threshold, indicating that hibernation in this species depends on body condition. These observations suggest that Syrian hamsters undergo pre-hibernation remodelling and that Tb and body mass can be useful physiological markers to monitor the remodelling process during the pre-hibernation period.