Warm spells in winter affect the equilibrium between winter phenotypes.

Each phenotype is a product of the interaction of the genes and the environment. Although winter phenotype in seasonal mammals is heritable, its development may be modified by external conditions. In today's world, global climate change and increasing frequency of unpredictable weather events may affect the dynamic equilibrium between phenotypes. We tested the effect of changes in ambient temperature during acclimation to short photoperiod on the development of winter phenotypes in three generations of Siberian hamsters (Phodopus sungorus). Based on seasonal changes in fur colour, body mass, and expression of daily torpor we distinguished three different winter phenotypes: responding, non-responding, and partially-responding to short photoperiod. We found that warm spells in winter can increase the proportion of non-responding individuals in the population, while stable winter conditions can increase photoresponsiveness among the offspring of non-responders. We conclude that the polymorphism of winter phenotype is an inherent characteristic of the Siberian hamster population but the development of winter phenotype is not fixed but rather a plastic response to the environmental conditions.

Prolactin Mediates Long-Term, Seasonal Rheostatic Regulation of Body Mass in Female Mammals.

A series of well-described anabolic and catabolic neuropeptides are known to provide short-term, homeostatic control of energy balance. The mechanisms that govern long-term, rheostatic control of regulated changes in energy balance are less well characterized. Using the robust and repeatable seasonal changes in body mass observed in Siberian hamsters, this report examined the role of prolactin in providing long-term rheostatic control of body mass and photoinduced changes in organ mass (ie, kidney, brown adipose tissue, uterine, and spleen). Endogenous circannual interval timing was observed after 4 months in a short photoperiod, indicated by a significant increase in body mass and prolactin mRNA expression in the pituitary gland. There was an inverse relationship between body mass and the expression of somatostatin (Sst) and cocaine- and amphetamine-regulated transcript (Cart). Pharmacological inhibition of prolactin release (via bromocriptine injection), reduced body mass of animals maintained in long photoperiods to winter-short photoperiod levels and was associated with a significant increase in hypothalamic Cart expression. Administration of ovine prolactin significantly increased body mass 24 hours after a single injection and the effect persisted after 3 consecutive daily injections. The data indicate that prolactin has pleiotropic effects on homeostatic sensors of energy balance (ie, Cart) and physiological effectors (ie, kidney, BAT). We propose that prolactin release from the pituitary gland acts as an output signal of the hypothalamic rheostat controller to regulate adaptive changes in body mass.

Hypothalamic tanycytes as mediators of maternally programmed seasonal plasticity.

In mammals, maternal photoperiodic programming (MPP) provides a means whereby juvenile development can be matched to forthcoming seasonal environmental conditions.1,2,3,4 This phenomenon is driven by in utero effects of maternal melatonin5,6,7 on the production of thyrotropin (TSH) in the fetal pars tuberalis (PT) and consequent TSH receptor-mediated effects on tanycytes lining the 3rd ventricle of the mediobasal hypothalamus (MBH).8,9,10 Here we use LASER capture microdissection and transcriptomic profiling to show that TSH-dependent MPP controls the attributes of the ependymal region of the MBH in juvenile animals. In Siberian hamster pups gestated and raised on a long photoperiod (LP) and thereby committed to a fast trajectory for growth and reproductive maturation, the ependymal region is enriched for tanycytes bearing sensory cilia and receptors implicated in metabolic sensing. Contrastingly, in pups gestated and raised on short photoperiod (SP) and therefore following an over-wintering developmental trajectory with delayed sexual maturation, the ependymal region has fewer sensory tanycytes. Post-weaning transfer of SP-gestated pups to an intermediate photoperiod (IP), which accelerates reproductive maturation, results in a pronounced shift toward a ciliated tanycytic profile and formation of tanycytic processes. We suggest that tanycytic plasticity constitutes a mechanism to tailor metabolic development for extended survival in variable overwintering environments.

Seasonal and fasting induced changes in iron metabolism in Djungarian hamsters.

Djungarian hamsters are small rodents that show pronounced physiological acclimations in response to changes in photoperiod, and unfavorable environmental conditions such as reduced food availability and low external temperature. These include substantial adjustments, such as severe body weight loss and the use of daily torpor. Torpor is a state of decreased physiological activity in eutherms, usually marked by low metabolic rate and a reduced body temperature. In this study, we investigated the effects of photoperiodic acclimation and food deprivation on systemic iron metabolism in Djungarian hamsters. Our study illustrates the association between liver iron levels and the incidence of torpor expression during the course of the experiment. Moreover, we show that both, acclimation to short photoperiods and long-term food restriction, associated with iron sequestration in the liver. This effect was accompanied with hypoferremia and mild reduction in the expression of principal iron-hormone, hepcidin. In addition to iron, the levels of manganese, selenium, and zinc were increased in the liver of hamsters under food restriction. These findings may be important factors for regulating physiological processes in hamsters, since iron and other trace elements are essential for many metabolic and physiological processes.

Sperm Capacitation and Kinematics in Phodopus Hamsters.

This study was designed to analyze changes in the spermatozoa of three species of Phodopus hamsters incubated under different conditions. Cauda epididymal sperm were incubated for 4 h in modified Tyrode's medium containing albumin, lactate, pyruvate, and Hepes (mTALP-H), in the same medium with the addition of bicarbonate (mTALP-BH), or with bicarbonate and 20 ng/mL of progesterone (mTALP-BH+P4). Media with bicarbonate are believed to promote capacitation in rodent species. Sperm motility, viability, capacitation patterns, and kinematics were assessed at different times. Capacitation in live cells was quantified after staining with Hoechst 33258 and chlortetracycline. Patterns believed to correspond to non-capacitated cells (F pattern), capacitated, acrosome-intact cells (B pattern), and acrosome-reacted cells (AR pattern) were recognized. Kinematics were examined via computer-assisted sperm analysis (CASA). The results showed a decrease in total motility in all three species in different media, with a sharp decrease in progressive motility in bicarbonate-containing media (without or with progesterone), suggesting hyperactivated motion. However, none of the other signs of hyperactivation described in rodents (i.e., decrease in STR or LIN, together with an increase in ALH) were observed. F pattern cells diminished with time in all media and were generally lower in P. roborovskii and higher in P. campbelli. B pattern cells increased in mTALP-BH media in all species. Progesterone did not enhance the percentage of B pattern cells. Finally, AR pattern cells increased in all species incubated in different media, showing the highest percentage in P. roborovskii and the lowest in P. campbelli. Comparisons between media revealed that there were higher percentages of F pattern cells and lower percentages of B pattern cells over time in medium without bicarbonate (mTALP-H) in comparison to media containing bicarbonate (mTALP-BH; mTALP-BH+P4). Overall, changes consistent with the acquisition of capacitation and development of hyperactivated motility were found; however, further studies are required to better characterize media necessary to support the pathways involved in these processes in Phodopus species.

A seasonal switch hypothesis for the neuroendocrine control of aggression.

Aggression is a well-studied social behavior that is universally exhibited by animals across a wide range of contexts. Prevailing knowledge suggests gonadal steroids primarily mediate aggression; however, this is based mainly on studies of male-male aggression in laboratory rodents. When males and females of other species, including humans, are examined, a positive relationship between gonadal steroids and aggression is less substantiated. For instance, hamsters housed in short 'winter-like' days show increased aggression compared with long-day housed hamsters, despite relatively low circulating gonadal steroids. These results suggest alternative, non-gonadal mechanisms controlling aggression. Here, we propose the seasonal switch hypothesis, which employs a multidisciplinary approach to describe how seasonal variation in extra-gonadal steroids, orchestrated by melatonin, drives context-specific changes in aggression.

Blood transcriptomics mirror regulatory mechanisms during hibernation-a comparative analysis of the Djungarian hamster with other mammalian species.

Hibernation enables many species of the mammalian kingdom to overcome periods of harsh environmental conditions. During this physically inactive state metabolic rate and body temperature are drastically downregulated, thereby reducing energy requirements (torpor) also over shorter time periods. Since blood cells reflect the organism´s current condition, it was suggested that transcriptomic alterations in blood cells mirror the torpor-associated physiological state. Transcriptomics on blood cells of torpid and non-torpid Djungarian hamsters and QIAGEN Ingenuity Pathway Analysis (IPA) revealed key target molecules (TMIPA), which were subjected to a comparative literature analysis on transcriptomic alterations during torpor/hibernation in other mammals. Gene expression similarities were identified in 148 TMIPA during torpor nadir among various organs and phylogenetically different mammalian species. Based on TMIPA, IPA network analyses corresponded with described inhibitions of basic cellular mechanisms and immune system-associated processes in torpid mammals. Moreover, protection against damage to the heart, kidney, and liver was deduced from this gene expression pattern in blood cells. This study shows that blood cell transcriptomics can reflect the general physiological state during torpor nadir. Furthermore, the understanding of molecular processes for torpor initiation and organ preservation may have beneficial implications for humans in extremely challenging environments, such as in medical intensive care units and in space.

Comparison of ultrasonic isolation calls of pure-breeding and interspecies hybrid Phodopus dwarf hamster pups.

In mammalian cross-species hybrids, parameters of voice calls, produced by vocal fold vibrations, are intermediate between parental species. Inheritance of ultrasonic calls, produced by whistle mechanism, is unstudied for hybrids. We examined 4000 pup ultrasonic isolation-induced calls for peak power of call fundamental frequency and for call duration in 4-8-day-old captive hamsters of four Study Groups: pure Phodopus sungorus; pure P. campbelli of two populations (Mongolian and Kosh-Agach) and hybrids between male P. sungorus and female P. campbelli (Kosh-Agach). All Study Groups produced two categories of ultrasonic calls: Low-Frequency centered around 41 kHz and High-Frequency centered around 60 kHz, but in different percentages. Between populations, only Low-Frequency calls were shorter and higher-frequency in Mongolian P. campbelli. Between species, only High-Frequency calls were shorter and higher-frequency in P. sungorus. In hybrids, Low-Frequency calls were shorter and lower-frequency than in either parental species, whereas High-Frequency calls were longer and lower-frequency in hybrids than in pure P. sungorus but similar with another parental species. We discuss that interspecific hybridization may give rise to offspring with new properties of ultrasonic calls.

Role of glucose in daily torpor of Djungarian hamsters (Phodopus sungorus): challenge of continuous in vivo blood glucose measurements.

Djungarian hamsters use daily torpor to save energy during winter. This metabolic downstate is part of their acclimatization strategy in response to short photoperiod and expressed spontaneously without energy challenges. During acute energy shortage, torpor incidence, depth, and duration can be modulated. Torpor induction might rely on glucose availability as acute metabolic energy source. To investigate this, the present study provides the first continuous in vivo blood glucose measurements of spontaneous daily torpor in short photoperiod-acclimated and fasting-induced torpor in long photoperiod-acclimated Djungarian hamsters. Glucose levels were almost identical in both photoperiods and showed a decrease during resting phase. Further decreases appeared during spontaneous daily torpor entrance, parallel with metabolic rate but before body temperature, while respiratory exchange rates were rising. During arousal, blood glucose tended to increase, and pretorpor values were reached at torpor termination. Although food-restricted hamsters underwent a considerable energetic challenge, blood glucose levels remained stable during the resting phase regardless of torpor expression. The activity phase preceding a torpor bout did not reveal changes in blood glucose that might be used as torpor predictor. Djungarian hamsters show a robust, circadian rhythm in blood glucose irrespective of season and maintain appropriate levels throughout complex acclimation processes including metabolic downstates. Although these measurements could not reveal blood glucose as proximate torpor induction factor, they provide new information about glucose availability during torpor. Technical innovations like in vivo microdialysis and in vitro transcriptome or proteome analyses may help to uncover the connection between torpor expression and glucose metabolism.

Sex and seasonal differences in neural steroid sensitivity predict territorial aggression in Siberian hamsters.

Many animals display marked changes in physiology and behavior on a seasonal timescale, including non-reproductive social behaviors (e.g., aggression). Previous studies from our lab suggest that the pineal hormone melatonin acts via steroid hormones to regulate seasonal aggression in Siberian hamsters (Phodopus sungorus), a species in which both males and females display increased non-breeding aggression. The neural actions of melatonin on steroids and aggressive behavior, however, are relatively unexplored. Here, we housed male and female hamsters in long-day photoperiods (LDs, characteristic of breeding season) or short-day photoperiods (SDs, characteristic of non-breeding season) and administered timed melatonin (M) or control injections. Following 10 weeks of treatment, we quantified aggressive behavior and neural steroid sensitivity by measuring the relative mRNA expression of two steroidogenic enzymes (aromatase and 5α-reductase 3) and estrogen receptor 1 in brain regions associated with aggression or reproduction [medial preoptic area (MPOA), anterior hypothalamus (AH), arcuate nucleus (ARC), and periaqueductal gray (PAG)] via quantitative PCR. Although LD-M and SD males and females displayed increased aggression and similar changes in gene expression in the ARC, there were sex-specific effects of treatment with melatonin and SDs on gene expression in the MPOA, AH, and PAG. Furthermore, males and females exhibited different relationships between neural gene expression and aggression in response to melatonin and SDs. Collectively, these findings support a role for melatonin in regulating seasonal variation in neural steroid sensitivity and aggression and reveal how distinct neuroendocrine responses may modulate a similar behavioral phenotype in male and female hamsters.

Differential energy expenditure is involved in the difference in activity levels between the Djungarian hamster (Phodopus sungorus) and the Roborovskii hamster (P. roborovskii).

The Djungarian hamster (Phodopus sungorus) shows calm behavior, while the Roborovskii hamster (P. roborovskii) exhibits hyperactivity. Even though they belong to the same genus, Phodopus, these two species are quite different. The current study investigated the relationship between energy expenditure and the markedly different levels of activity shown by these hamsters. Roborovskii hamsters showed significantly higher energy expenditure than Djungarian hamsters under both feeding and fasting conditions during darkness. Roborovskii hamsters showed a repeated increase and decrease in energy expenditure under the feeding condition; however, this changed under the fasting condition, during which the repeated increase and decrease in energy expenditure corresponded to the repeated active and sleeping conditions. Djungarian hamsters had a tendency to keep their energy expenditure constant during the fasting condition, while Roborovskii hamsters moved around a lot to find food. The respiratory quotient (RQ) values in Djungarian hamsters were relatively constant. However, Roborovskii hamsters showed a wide variation in RQ. In particular, the RQ value declined immediately before a dark phase commenced, indicating a switchover from the utilization of glucose to that of lipids as a substrate for energy production. In conclusion, Djungarian hamsters and Roborovskii hamsters showed different behavioral patterns that were related to differences in energy metabolism.

Short Photoperiod-Dependent Enrichment of Akkermansia spec. as the Major Change in the Intestinal Microbiome of Djungarian Hamsters (Phodopus sungorus).

The Djungarian hamster (Phodopus sungorus) is a prominent model organism for seasonal acclimatization, showing drastic whole-body physiological adjustments to an energetically challenging environment, which are considered to also involve the gut microbiome. Fecal samples of hamsters in long photoperiod and again after twelve weeks in short photoperiod were analyzed by 16S-rRNA sequencing to evaluate seasonal changes in the respective gut microbiomes. In both photoperiods, the overall composition was stable in the major superordinate phyla of the microbiota, with distinct and delicate changes of abundance in phyla representing each <1% of all. Elusimicrobia, Tenericutes, and Verrucomicrobia were exclusively present in short photoperiod hamsters. In contrast to Elusimicrobium and Aneroplasma as representatives of Elusimicrobia and Tenericutes, Akkermansia muciniphila is a prominent gut microbiome inhabitant well described as important in the health context of animals and humans, including neurodegenerative diseases and obesity. Since diet was not changed, Akkermansia enrichment appears to be a direct consequence of short photoperiod acclimation. Future research will investigate whether the Djungarian hamster intestinal microbiome is responsible for or responsive to seasonal acclimation, focusing on probiotic supplementation.

Central angiotensin 1-7 triggers brown fat thermogenesis.

We tested the hypothesis that third ventricular (3V) injections of angiotensin 1-7 (Ang 1-7) increases thermogenesis in brown adipose tissue (BAT), and whether the Mas receptor mediates this response. First, in male Siberian hamsters (n = 18), we evaluated the effect of Ang 1-7 in the interscapular BAT (IBAT) temperature and, using selective Mas receptor antagonist A-779, the role of Mas receptor in this response. Each animal received 3V injections (200 nL), with 48 h intervals: saline; Ang 1-7 (0.03, 0.3, 3, and 30 nmol); A-779 (3 nmol); and Ang 1-7 (0.3 nmol) + A-779 (3 nmol). IBAT temperature increased after 0.3 nmol Ang 1-7 compared with Ang 1-7 + A-779 at 20, 30, and 60 min. Also, 0.3 nmol Ang 1-7 increased IBAT temperature at 10 and 20 min, and decreased at 60 min compared with pretreatment. IBAT temperature decreased after A-779 at 60 min and after Ang 1-7 + A-779 at 30 and 60 min compared with the respective pretreatment. A-779 and Ang 1-7 + A-779 decreased core temperature at 60 min compared with 10 min. Then, we evaluated blood and tissue Ang 1-7 levels, and the expression of hormone-sensitive lipase (HSL) and adipose triglyceride lipase (ATGL) in IBAT. Male Siberian hamsters (n = 36) were killed 10 min after one of the injections. No changes were observed in blood glucose, serum and IBAT Ang 1-7 levels, and ATGL. Ang 1-7 (0.3 nmol) increased p-HSL expression compared with A-779 and increased p-HSL/HSL ration compared with other injections. Ang 1-7 and Mas receptor immunoreactive cells were found in brain regions that coincide with the sympathetic nerves outflow to BAT. In conclusion, 3V injection of Ang 1-7 induced thermogenesis in IBAT in a Mas receptor-dependent manner.

Host-Specific Differences in Gut Microbiota Between Cricetulus barabensis and Phodopus sungorus.

Gut microbiota plays an important role in the health of the host and is usually associated with the physiological processes of animals. Both host-specific factors and environmental factors are involved in the shaping of the gut microbial community, and it is necessary to identify the host-dominated differences in gut microbiota among animal species to better explain how they affect the choice of life history strategies in hosts. Here, striped hamsters Cricetulus barabensis and Djungarian hamsters Phodopus sungorus were housed under the same controlled conditions, and fecal samples were collected to compare gut microbiota. A higher Shannon index was observed in striped hamsters than in Djungarian hamsters. Linear discriminant analysis of effect size showed enrichment of the family Lachnospiraceae and genera Muribaculum and Oscillibacter in striped hamsters, with the enrichment of family Erysipelotrichaceae and genus Turicibacter in Djungarian hamsters. Among the top 10 amplicon sequence variants (ASVs), eight showed significantly different relative abundance between the two hamster species. The positive correlations and average degree in the co-occurrence network of striped hamsters were less than those of Djungarian hamsters, showing different complexity of synergistic effects among the gut bacteria. The gut microbial community of striped hamsters had a higher R2 value than that of Djungarian hamsters when fitted with a neutral community model. These differences have a degree of consistency with the variation in the lifestyles of the two hamster species. The study provides insights into the understanding of gut microbiota and its connections with rodent hosts.

Photoperiod alters testicular methyltransferase complex mRNA expression in Siberian hamsters.

Exposure to long photoperiods stimulates, whereas exposure to short photoperiods transiently inhibit testicular function in Siberian hamsters via well-described neuroendocrine mechanisms. However, less is known about the intra-testicular regulation of these photoperiod-mediated changes. N6-methyladenosine (m6A) is one of the most common mRNA modifications in eukaryotes, with alterations in m6A mRNA methylation affecting testis function and fertility. We hypothesized that genes controlling m6A methylation such as methyltransferase-like-3 (Mettl3) and -14 (Mettl14) and Wilms' tumor-1 associated protein (Wtap), part of an mRNA methylating methyl-transferase complex, or the fat-mass-and-obesity-associated (Fto) and the α-ketoglutarate-dependent dioxygenase alkB homolog-5 (Alkbh5) genes responsible for m6A demethylation, may be differentially regulated by photoperiod in the testis. Male hamsters were exposed to long (LD, control) photoperiod for 14-weeks, short (SD) photoperiod for 2, 5, 8, 11 and 14-weeks to induce regression, or SD for 14-weeks followed by transfer to LD for 1, 2, 4 or 8-weeks to induce recrudescence (post-transfer, PT). SD exposure significantly reduced body, testis, and epididymal masses compared to all other groups. Spermatogenic index, seminiferous tubule diameters and testosterone concentrations significantly decreased in SD as compared to LD, returning to levels no different than LD in post-transfer groups. SD exposure significantly decreased Wtap, Fto, Alkbh5, but increased Mettl14 mRNA expression as compared to LD, with values in PT groups restored to LD levels. Mettl3 mRNA expression did not change. These results suggest that testicular recovery induced by stimulatory photoperiod is relatively rapid, and that the methyltransferase complex may play a role during photostimulated testicular recrudescence.

Is torpor a water conservation strategy? Heterothermic responses to acute water and food deprivation are repeatable among individuals of Phodopus sungorus.

Energy conservation is a clear function of torpor. Although many studies imply that torpor is also a water-saving strategy, the experimental evidence linking water availability with torpor is inconclusive. We tested the relative roles of water and energy shortages in driving torpor, using the Siberian hamster Phodopus sungorus as a model species. To account for the seasonal development of spontaneous heterothermy, we used male hamsters acclimated to short (8L:16D, SP; n = 40) and long (16L:8D, LP; n = 36) photoperiods. We continuously measured body temperature (Tb) during consecutive 32 h of complete removal of water, food, or both, separated by 7.5 d recovery periods. We predicted that all deprivation types would increase the frequency of spontaneous torpor in SP, and induce torpor in LP-acclimated hamsters. Individuals underwent each deprivation type twice in random orders. Food and water deprivation did not induce torpor in LP-acclimated P. sungorus. Patterns of torpor expression varied among deprivation types in SP individuals. Torpor frequency was significantly lower, but bouts were ∼2 h longer and 2.5 °C deeper, during water deprivation compared to food and food-and-water deprivation. Heterothermic responses to all deprivation types were repeatable among individuals. Different torpor patterns during water and food deprivation suggest that water and energy shortages are distinct physiological challenges. Deeper and longer bouts during water deprivation likely led to higher energy and water savings, while shorter and shallower bouts during fasting may reflect a trade-off between energy conservation and food-seeking activity. The lack of a difference between food- and food-and-water-deprived hamsters suggests a higher sensitivity to food than water shortage. This supports the traditional view that energy conservation is the major function of torpor, but suggests that water shortages may also modulate torpor use. The high repeatability of thermoregulatory responses to resource deprivation suggests that these may be heritable traits subject to natural selection.

Abundance, efficiency, and stability of reference transcript expression in a seasonal rodent: The Siberian hamster.

Quantitative PCR (qPCR) is a common molecular tool to analyse the expression of transcripts in non-traditional animal models. Most animals experience tissue-specific seasonal changes in cell structure, growth, and cellular function. As a consequence, the choice of reference or 'house-keeping' genes is essential to standardize expression levels of target transcripts of interest for qPCR analyses. This study aimed to determine the abundance, efficiency and stability of several reference genes commonly used for normalisation of qPCR analyses in a model of seasonal biology: the Siberian hamster (Phodopus sungorus). Liver, brown-adipose tissue (BAT), white adipose tissue (WAT), testes, spleen, kidney, the hypothalamic arcuate nucleus, and the pituitary gland from either long or short photoperiod Siberian hamsters were dissected to test tissue-specific and photoperiod effects on reference transcripts. qPCR was conducted for common reference genes including 18s ribosomal RNA (18s), glyceraldehyde 3-phosphate dehydrogenase (Gapdh), hypoxanthine-guanine phosphoribosyltransferase (Hprt), and actin-ß (Act). Cycling time (Ct), efficiency (E) and replicate variation of Ct and E measured by percent coefficient of variance (CV%) was determined using PCR miner. Measures of stability were assessed using a combined approach of NormFinder and BestKeeper. 18s and Act did not vary in Ct across photoperiod conditions. Splenic, WAT and BAT Gapdh Ct was higher in long compared to short photoperiod. Splenic Hprt Ct was higher in long photoperiods. There was no significant effect of photoperiod, tissue or interaction on measures of efficiency, Ct CV%, or efficiency CV%. NormFinder and BestKeeper confirmed that 18s, Gapdh and Hprt were highly stable, while Act showed low stability. These findings suggest that 18s and Hprt show the most reliable stability, efficiency, and abundance across the tissues. Overall, the study provides a comprehensive and standardised approach to assess multiple reference genes in the Siberian hamster and help to inform molecular assays used in studies of photoperiodism.

Sex-specific endocrine regulation of seasonal aggression in Siberian hamsters.

Coordinating physiological and behavioural processes across the annual cycle is essential in enabling individuals to maximize fitness. While the mechanisms underlying seasonal reproduction and its associated behaviours are well characterized, fewer studies have examined the hormonal basis of non-reproductive social behaviours (e.g. aggression) on a seasonal time scale. Our previous work suggests that the pineal hormone melatonin facilitates a 'seasonal switch' in neuroendocrine regulation of aggression in male and female Siberian hamsters (Phodopus sungorus), specifically by acting on the adrenal glands to increase the production of the androgen dehydroepiandrosterone (DHEA) during the short-day (SD) photoperiods of the non-breeding season. Here, we provide evidence that the activity of 3ß-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase (3ß-HSD), a key enzyme within the steroidogenic pathway that mediates DHEA synthesis and metabolism, varies in a sex-specific and melatonin-dependent manner. Although both male and female hamsters displayed increased aggression in response to SDs and SD-like melatonin, only males showed an increase in adrenal 3ß-HSD activity. Conversely, SD and melatonin-treated females exhibited reductions in both adrenal and neural 3ß-HSD activity. Collectively, these results suggest a potential role for 3ß-HSD in modulating non-breeding aggression and, more broadly, demonstrate how distinct neuroendocrine mechanisms may underlie the same behavioural phenotype in males and females.

Transcriptome analyses of nine endocrine tissues identifies organism-wide transcript distribution and structure in the Siberian hamster.

Temperate zone animals exhibit seasonal variation in multiple endocrine systems. In most cases, peripheral organs display robust switches in tissue involution and recrudescence in mass. Our understanding of the molecular control of tissue-specific changes in seasonal function remains limited. Central to this problem is the lack of information on the nucleic acid structure, and distribution of transcripts across tissues in seasonal model organisms. Here we report the transcriptome profile of nine endocrine tissues from Siberian hamsters. Luteinizing hormone receptor expression was localized to gonadal tissues and confirmed previous distribution analyses. Assessment of the prolactin receptor reveal relatively high abundance across tissues involved in reproduction, energy, and water homeostasis. Neither melatonin receptor-1a, nor -1b, were found to be expressed in most tissues. Instead, the closely related G-protein coupled receptor Gpr50 was widely expressed in peripheral tissues. Epigenetic enzymes such as DNA methyltransferase 3a, was widely expressed and the predominant DNA methylation enzyme. Quantitative PCR analyses revealed some sex- and tissue-specific differences for prolactin receptor and DNA methyltransferase 3a expression. These data provide significant information on the distribution of transcripts, relative expression levels and nucleic acid sequences that will facilitate molecular studies into the seasonal programs in mammalian physiology.

Short communication: Photoperiod impacts ovarian extracellular matrix and metabolic gene expression in Siberian hamsters.

Ovarian cyclicity is variable in adult Siberian hamsters (Phodopus sungorus), who respond to long breeding season photoperiods with follicle development and ovulation, while short photoperiods typical of the non-breeding season induce gonadal atrophy. Recent RNAseq results identified ovarian matrix components and regulators of metabolism as differentially regulated by photoperiod; however, the impact of photoperiod across a full cycle of ovarian regression and recrudescence had not been explored for additional regulators of ovarian metabolism and extracellular matrix components. We hypothesized that matrix and metabolism-related genes would be expressed differentially across photoperiods that mimic breeding and non-breeding season daylengths. Hamsters were housed in one of four photoperiod groups: long day (16 h of light per day: 8 h of dark; LD, controls), short day regressed (8 L:16D; SD, regressed), and females exposed to SD then transferred to LD to stimulate return of ovarian function for 2 (early recrudescence), or 8 (late recrudescence) weeks. Plasma leptin concentrations along with expression of ovarian versican and liver-receptor homolog-1/Nr582 mRNA decreased in SD compared to LD and late recrudescence, while vimentin mRNA expression peaked in early and late recrudescence. Ovarian expression of fibronectin and extracellular matrix protein-1 was low in LD ovaries and increased in regressed and recrudescing groups. Expression of hyaluronidase-2, nectin-2, liver-X receptors-α and-ß, and adiponectin mRNA peaked in late recrudescence, with no changes noted for adiponectin receptor-1 and -2. The results offer a first look at the parallels between expression of these genes and the dynamic remodeling that occurs during ovarian regression and recrudescence.