Phodopus Sungorus Research Articles

CHANGES IN THE HISTAMINE STATUS OF THE INTERNAL ORGANS OF LABORATORY ANIMALS DEPENDING ON THE SILICON CONCENTRATION IN DRINKING WATER

The results of a study of the histamine status of the internal organs of Djungarian hamsters when silicon was taken with drinking water are presented. The aim of the study was to assess the histamine status of the liver, spleen and testicles of Djungarian hamsters when silicon was ingested with drinking water for three months at various concentrations. Material and methods. The hamsters were kept in the vivarium on a standard diet with free access to drinking water for three months. Hamsters of the control group (n = 3) received bottled drinking water, hamsters of the experimental groups received the same bottled water with the addition of sodium metasilicate 9-hydrate at a concentration of 10 mg/l in terms of silicon (the first experimental group, n = 3) and 20 mg/l in terms of silicon (the second experimental group, n = 3). To detect and quantify histamine in organs and tissues in cryostat sections of the liver, spleen and testicles, the fluorescent-histochemical Cross method was used. A general blood test and a blood test for glucose and cholesterol were also performed. Results and their discussion. A general blood test of hamsters that received drinking water with different concentrations of silicon did not reflect the effect of microelement intaked into the organism, while, depending on the concentration of silicon in water, the average blood glucose level tended to increase, and the cholesterol level tended to decrease. The obtained results do not contradict our previous studies in that direction. It has been shown that the concentration of silicon in drinking water from 10 mg/l hardly noticeably affects the histamine status of such organs as the liver, spleen and testes: only the intensity of histamine luminescence in macrophages of the red pulp increases statistically significantly. When silicon enters the body with drinking water at a concentration of 20 mg/l, the histamine status of organs changes more noticeably, the cells surrounding the central veins and the interstitial histamine-containing testes cells are “involved” into the reaction, which is visually reflected in the luminescent morphology of the investigated organs. Conclusions. The intake of silicon at a concentration of 10 mg/l and 20 mg/l for three months affects the histamine status of the liver, spleen and testes of Djungarian hamsters, while the indicators of the general blood test do not change.

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.

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 (3nmol); and Ang 1-7 (0.3nmol) + A-779 (3nmol). IBAT temperature increased after 0.3nmol Ang 1-7 compared with Ang 1-7+ A-779 at 20, 30, and 60 min. Also, 0.3nmol 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 10min. 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 10min after one of the injections. No changes were observed in blood glucose, serum and IBAT Ang 1-7 levels, and ATGL. Ang 1-7 (0.3nmol) 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.

Effect of PACAP/PAC1R on Follicle Development of Djungarian Hamster (Phodopus sungorus) with the Variation of Ambient Temperatures.

In Phodopus sungorus, the relationship between pituitary adenylate cyclase-activating polypeptide (PACAP) and its receptor (PAC1R), follicle-stimulating hormone (FSH), and follicle development remains unclear. In this study, we found that the development of growing follicles and antral follicles were inhibited at low (8 °C, 14 °C) and high (29 °C) temperatures. Meanwhile, PACAP/PAC1R expression and follicle-stimulating hormone (FSH) serum concentration significantly decreased during ambient temperatures of 8 °C, 14 °C and 29 °C compared to 21 °C. Thus, ambient temperature may influence the expression of PACAP/PAC1R and the synthesis of FSH for involvement in follicle development. Moreover, PACAP/PAC1R had major functional elements including PKA/PKG and PKC phosphorylation sites, which may involve in the pathway of FSH synthesis through cAMP-PKA and its downstream signal pathway. Moreover, there was a significant positive correlation between the expression levels of PACAP/PAC1R and the number of the growing and antral follicles, as well as the serum FSH concentration and the number of antral follicles. However, there was no significant correlation between the expression levels of PACAP/PAC1R and the serum FSH concentration, indicating a complicated pathway between PACAP/PAC1R and FSH. In conclusion, ambient temperature affects the expression of PACAP/PAC1R and the serum FSH concentration. The expression of PACAP/PAC1R and the serum FSH concentration are correlated with follicle development, which implies that they are involved in follicle development, which will ultimately influence the reproduction of Phodopus sungorus. This study can lay the foundation for future investigation on the regulation mechanism of reproduction in Phodopus sungorus.

Age-related dynamics of reproductive activity and physical conditions in Cricetidae of different ecological speciation (Rodentia)

To understand the evolutionary preconditions of extended longevity, one can compare the key life-history events and age related changes in body conditions in related species with different ecological speciation. Cricetid rodents possessing a wide spectrum of adaptive forms with different life history strategies are an excellent model for this purpose. We compared median and maximum longevity, life expectancy, temporal distribution of reproductive efforts, and age related dynamic of several physical condition indexes: body mass, muscle strength, locomotor activity and frequency of vertical postures in open field tests in five species of this family. Studied species vary both in maximum (from three years in steppe lemmings (Lagurus lagurus) to more than six years in mole voles (Ellobius talpinus) and rock voles (Alticola strelzovi) and median longevity (from less than one year in Lagurus lagurus to 2.8 years in rock vole Alticola tuvinicus). Both species with high maximum longevity – Ellobius talpinus and Alticola strelzovi face chronic hypoxia in their native environment. The total amount of litters born varied from three in A. strelzovi to 13 in Phodopus sungorus. Species under study also differed in age-related dynamics of physical conditions. Among the studied species, the subterranean E. talpinus has the highest maximum longevity with relatively long duration of reproductive period and only weak age-related deterioration in body conditions, i.e. shares many aspects of the life history strategy of such a specialized group as the Bathyergidae family.

The Photoperiod Regulates Granulosa Cell Apoptosis through the FSH-Nodal/ALK7 Signaling Pathway in Phodopus sungorus.

The photoperiod regulates the seasonal reproduction of mammals by affecting the follicle development, for which the granulosa cells provide nutrition. However, the underlying mechanism remains unclear. Here, Djungarian hamsters (Phodopus sungorus) were raised under different photoperiods to study the ovarian status and explore the potential mechanism of the follicle development mediated by the FSH-Nodal/ALK7 signaling pathway. Compared with the moderate daylight (MD) group, the short daylight (SD) group exhibited a significant decrease in the ovarian weight and increase in the atretic follicle number and granulosa cell apoptosis, whereas the long daylight (LD) group showed an increase in the ovarian weight, the growing follicle number, and the antral follicle number, but a decrease in the granulosa cell apoptosis. Based on these findings, the key genes of the Nodal/ALK7 signaling pathway controlling the granulosa cell apoptosis were studied using the quantitative real-time polymerase chain reaction and western blotting. In the SD group, the follicle-stimulating hormone (FSH) concentration significantly decreased and the Nodal/ALK7/Smad signaling pathways were activated, while the phosphatidylinositol 3-kinase (PIK3)/Akt signaling pathway was inhibited. The BAX expression was significantly increased, while the Bcl-xL expression was significantly decreased, leading to an increase in the caspase-3 activity, the granulosa cell apoptosis, and ovarian degeneration. However, in the LD group, the FSH concentration significantly increased, the Nodal/ALK7/Smad signaling pathway was inhibited, and the PIK3/Akt signaling pathway was activated. Taken together, our results indicate that the photoperiod can regulate the apoptosis of the granulosa cells by regulating the concentration of FSH, activating or inhibiting the Nodal/ALK7 signaling pathway, thereby affecting the ovarian function. Our research provides an important theoretical basis for understanding the photoperiod-regulated mechanisms of the mammalian seasonal reproduction.

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.

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-β (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 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase (3β-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 3β-HSD activity. Conversely, SD and melatonin-treated females exhibited reductions in both adrenal and neural 3β-HSD activity. Collectively, these results suggest a potential role for 3β-HSD in modulating non-breeding aggression and, more broadly, demonstrate how distinct neuroendocrine mechanisms may underlie the same behavioural phenotype in males and females.

The Impact of Physical Activity on the Circadian System: Benefits for Health, Performance and Wellbeing

Circadian rhythms are an inherent property of all living systems and an essential part of the external and internal temporal order. They enable organisms to be synchronized with their periodic environment and guarantee the optimal functioning of organisms. Any disturbances, so-called circadian disruptions, may have adverse consequences for health, physical and mental performance, and wellbeing. The environmental light–dark cycle is the main zeitgeber for circadian rhythms. Moreover, regular physical activity is most useful. Not only does it have general favorable effects on the cardiovascular system, the energy metabolism and mental health, for example, but it may also stabilize the circadian system via feedback effects on the suprachiasmatic nuclei (SCN), the main circadian pacemaker. Regular physical activity helps to maintain high-amplitude circadian rhythms, particularly of clock gene expression in the SCN. It promotes their entrainment to external periodicities and improves the internal synchronization of various circadian rhythms. This in turn promotes health and wellbeing. In experiments on Djungarian hamsters, voluntary access to a running wheel not only stabilized the circadian activity rhythm, but intensive wheel running even reestablished the rhythm in arrhythmic individuals. Moreover, their cognitive abilities were restored. Djungarian hamsters of the arrhythmic phenotype in which the SCN do not generate a circadian signal not only have a diminished cognitive performance, but their social memory is also compromised. Voluntary wheel running restored these abilities simultaneously with the reestablishment of the circadian activity rhythm. Intensively exercising Syrian hamsters are less anxious, more resilient to social defeat, and show less defensive/submissive behaviors, i.e., voluntary exercise may promote self-confidence. Similar effects were described for humans. The aim of the present paper is to summarize the current knowledge concerning the effects of physical activity on the stability of the circadian system and the corresponding consequences for physical and mental performance.

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.

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-β, 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.

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.

Demography, disorders and mortality of pet hamsters under primary veterinary care in the United Kingdom in 2016.

Hamsters are popular pets worldwide but there is limited evidence on the overall health issues of pet hamsters. This study aimed to characterise the demography, disorder prevalence and mortality of pet hamsters in the United Kingdom. The VetCompass study included anonymised clinical records of 16,605 hamsters. The most common hamster species were Syrian (golden) (Mesocricetus auratus) (n=12,197, 73.45%), Djungarian (winter white dwarf) (Phodopus sungorus) (2286, 13.77%) and Roborovski hamsters (Phodopus roborovskii) (1054, 6.35%). The most prevalent precise-level disorders recorded across all hamsters were a presentation categorised as 'wet tail' (n=293, 7.33%), disorder undiagnosed (292, 7.30%), bite injuries from other hamsters (235, 5.88%), overgrown nail(s) (165, 4.13%), overgrown incisor(s) (159, 3.98%) and traumatic injury (152, 3.80%). The most prevalent disorders groups across all species of hamster were traumatic injury (n=616, 15.41%), enteropathy (450, 11.26%), ophthalmological disorder (445, 11.13%), skin disorder (362, 9.05%) and mass (361, 9.03%). The median age at death across all hamsters was 1.75 years (interquartile range: 0.83 to 2.20, range: 0.01 to 3.65). The most common causes of death at a precise level were wet tail (7.88%, 95% confidence interval: 6.35 to 9.66), abdominal mass (6.40%, 95% confidence interval: 5.01 to 8.03), neoplasia (5.38%, 95% confidence interval: 4.11 to 6.90) and dyspnoea (3.99%, 95% confidence interval: 2.9 to 5.34). This study provides veterinary professionals, educators, welfare scientists and owners with an evidence base on pet hamster health. A greater understanding of the common disorders of pet hamsters can support veterinary professionals to communicate more effectively with owners on key issues and outcomes to expect from hamster ownership.

Siberian hamsters nonresponding to short photoperiod use fasting-induced torpor.

Nonresponding Siberian hamsters (Phodopus sungorus) do not develop the winter phenotype of white fur, low body mass (Mb) and spontaneous torpor in response to short photoperiod. However, their thermoregulatory response to fasting remains unknown. We measured body temperature and Mb of 12 nonresponders acclimated to short photoperiod and then to cold and fasted four times for 24 h. Four individuals used torpor, and in total, we recorded 19 torpor bouts, which were shallow, short and occurred at night. Moreover, fasting increased the heterothermy index in all hamsters. Low Mb was not a prerequisite for torpor use and Mb loss did not correlate with either heterothermy index or torpor use. This is the first evidence that individuals which do not develop the winter phenotype can use torpor or increase body temperature variability to face unpredictable, adverse environmental conditions. Despite the lack of seasonal changes, thermoregulatory adjustments may increase the probability of winter survival in nonresponders.

Naked mole-rat and Damaraland mole-rat exhibit lower respiration in mitochondria, cellular and organismal levels

Naked mole-rats (NMR) and Damaraland mole-rats (DMR) exhibit extraordinary longevity for their body size, high tolerance to hypoxia and oxidative stress and high reproductive output; these collectively defy the concept that life-history traits should be negatively correlated. However, when life-history traits share similar underlying physiological mechanisms, these may be positively associated with each other. We propose that one such potential common mechanism might be the bioenergetic properties of mole-rats. Here, we aim to characterize the bioenergetic properties of two African mole-rats. We adopted a top-down perspective measuring the bioenergetic properties at the organismal, cellular, and molecular level in both species and the biological significance of these properties were compared with the same measures in Siberian hamsters and C57BL/6 mice, chosen for their similar body size to the mole-rat species. We found mole-rats shared several bioenergetic properties that differed from their comparison species, including low basal metabolic rates, a high dependence on glycolysis rather than on oxidative phosphorylation for ATP production, and low proton conductance across the mitochondrial inner membrane. These shared mole-rat features could be a result of evolutionary adaptation to tolerating variable oxygen atmospheres, in particular hypoxia, and may in turn be one of the molecular mechanisms underlying their extremely long lifespans.

The Evolution of Widespread Recombination Suppression on the Dwarf Hamster (Phodopus) X Chromosome.

The X chromosome of therian mammals shows strong conservation among distantly related species, limiting insights into the distinct selective processes that have shaped sex chromosome evolution. We constructed a chromosome-scale de novo genome assembly for the Siberian dwarf hamster (Phodopus sungorus), a species reported to show extensive recombination suppression across an entire arm of the X chromosome. Combining a physical genome assembly based on shotgun and long-range proximity ligation sequencing with a dense genetic map, we detected widespread suppression of female recombination across ∼65% of the Phodopus X chromosome. This region of suppressed recombination likely corresponds to the Xp arm, which has previously been shown to be highly heterochromatic. Using additional sequencing data from two closely related species (P. campbelli and P. roborovskii), we show that recombination suppression on Xp appears to be independent of major structural rearrangements. The suppressed Xp arm was enriched for several transposable element families and de-enriched for genes primarily expressed in placenta, but otherwise showed similar gene densities, expression patterns, and rates of molecular evolution when compared to the recombinant Xq arm. Phodopus Xp gene content and order was also broadly conserved relative to the more distantly related rat X chromosome. These data suggest that widespread suppression of recombination has likely evolved through the transient induction of facultative heterochromatin on the Phodopus Xp arm without major changes in chromosome structure or genetic content. Thus, substantial changes in the recombination landscape have so far had relatively subtle influences on patterns of X-linked molecular evolution in these species.

Reversible Suppression of Fear Memory Recall by Transient Circadian Arrhythmia.

We tested the hypothesis that a temporary period of circadian arrhythmia would transiently impair recall of an aversive memory in Siberian hamsters (Phodopus sungorus). Unlike mice or rats, circadian arrhythmia is easily induced in this species by a one-time manipulation of their ambient lighting [i.e., the disruptive phase shift (DPS) protocol]. Hamsters were conditioned to associate footshocks with a shock chamber (context) and with a predictive auditory tone (cue), and then exposed to the DPS protocol. Following DPS, animals either became arrhythmic (ARR), reentrained to the light-dark cycle (ENT), or became arrhythmic for < 14 days before their circadian locomotor rhythms spontaneously recovered and reentrained (ARR-ENT). Tests for contextual memory showed that freezing was decreased 9–10 days post-DPS when both ARR and ARR-ENT groups were arrhythmic. Once ARR-ENT animals reentrained (day 41), however, freezing was elevated back to Pre-DPS levels and did not differ from those observed in ENT hamsters. ENT animals maintained high levels of freezing at both time points, whereas, freezing remained low in ARR hamsters. In contrast to contextual responses, cued responses were unaffected by circadian arrhythmia; all three groups exhibited elevated levels of freezing in response to the tones. The differential impact of circadian arrhythmia on contextual versus cued associative memory suggests that arrhythmia preferentially impacts memory processes that depend on the hippocampus.

Bacteria and Bellicosity: Photoperiodic Shifts in Gut Microbiota Drive Seasonal Aggressive Behavior in Male Siberian Hamsters

The existence of a microbiome-gut-brain axis has been established wherein gut microbiota significantly impacts host behavior and physiology, with increasing evidence suggesting a role for the gut microbiota in maintaining host homeostasis. Communication between the gut microbiota and the host is bidirectional, and shifts in the composition of the gut microbiota are dependent on both internal and external cues (host-derived signals, such as stress and immunity, and endocrine and environmental signals, such as photoperiod). Although there is host-driven seasonal variation in the composition of the microbiota, the mechanisms linking photoperiod, gut microbiota, and host behavior have not been characterized. The results of the present study suggest that seasonal changes in the gut microbiota drive seasonal changes in aggression. Implanting short-day Siberian hamsters (Phodopus sungorus) with fecal microbiota from long-day hamsters resulted in a reversal of seasonal aggression, whereby short-day hamsters displayed aggression levels typical of long-day hamsters. In addition, there are correlations between aggressive behavior and several bacterial taxa. These results implicate the gut microbiota as part of the photoperiodic mechanism regulating seasonal host behavior and contribute toward a more comprehensive understanding of the relationships between the microbiota, host, and environment.

Winter madness: Melatonin as a neuroendocrine regulator of seasonal aggression.

Individuals of virtually all vertebrate species are exposed to annual fluctuations in the deterioration and renewal of their environments. As such, organisms have evolved to restrict energetically expensive processes and activities to a specific time of the year. Thus, the precise timing of physiology and behavior is critical for individual reproductive success and subsequent fitness. Although the majority of research on seasonality has focused on seasonal reproduction, pronounced fluctuations in other non-reproductive social behaviors, including agonistic behaviors (e.g., aggression), also occur. To date, most studies that have investigated the neuroendocrine mechanisms underlying seasonal aggression have focused on the role of photoperiod (i.e., day length); prior findings have demonstrated that some seasonally breeding species housed in short "winter-like" photoperiods display increased aggression compared with those housed in long "summer-like" photoperiods, despite inhibited reproduction and low gonadal steroid levels. While fewer studies have examined how the hormonal correlates of environmental cues regulate seasonal aggression, our previous work suggests that the pineal hormone melatonin acts to increase non-breeding aggression in Siberian hamsters (Phodopus sungorus) by altering steroid hormone secretion. This review addresses the physiological and cellular mechanisms underlying seasonal plasticity in aggressive and non-aggressive social behaviors, including a key role for melatonin in facilitating a "neuroendocrine switch" to alternative physiological mechanisms of aggression across the annual cycle. Collectively, these studies highlight novel and important mechanisms by which melatonin regulates aggressive behavior in vertebrates and provide a more comprehensive understanding of the neuroendocrine bases of seasonal social behaviors broadly.