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.

Seasonal Adaptation: Geographic Photoperiod-Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor.

The vertebrate photoperiodic neuroendocrine system uses the photoperiod as a proxy to time the annual rhythms in reproduction. The thyrotropin receptor (TSHR) is a key protein in the mammalian seasonal reproduction pathway. Its abundance and function can tune sensitivity to the photoperiod. To investigate seasonal adaptation in mammals, the hinge region and the first part of the transmembrane domain of the Tshr gene were sequenced for 278 common vole (Microtus arvalis) specimens from 15 localities in Western Europe and 28 localities in Eastern Europe. Forty-nine single nucleotide polymorphisms (SNPs; twenty-two intronic and twenty-seven exonic) were found, with a weak or lack of correlation with pairwise geographical distance, latitude, longitude, and altitude. By applying a temperature threshold to the local photoperiod-temperature ellipsoid, we obtained a predicted critical photoperiod (pCPP) as a proxy for the spring onset of local primary food production (grass). The obtained pCPP explains the distribution of the genetic variation in Tshr in Western Europe through highly significant correlations with five intronic and seven exonic SNPs. The relationship between pCPP and SNPs was lacking in Eastern Europe. Thus, Tshr, which plays a pivotal role in the sensitivity of the mammalian photoperiodic neuroendocrine system, was targeted by natural selection in Western European vole populations, resulting in the optimized timing of seasonal reproduction.

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.

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.

Housing conditions modify seasonal changes in basal metabolism and body mass of the Siberian hamster, Phodopus sungorus.

Proper housing conditions are important aspects of animal welfare. Animals housed in enriched environments show less stereotypic behaviours than animals kept in barren cages. However, different types of cage enrichment may affect the results of experimental studies and hinder comparative analyses of animal physiology and behaviour. We investigated whether access to a running wheel, availability of nesting material, and pair housing affect basal metabolic rate (BMR) of Siberian hamsters (Phodopus sungorus) under various acclimation conditions. We used 70 adult hamsters (35 males and 35 females) divided into five groups housed under different cage conditions. All individuals experienced the same acclimation procedure: first a winter (L8:D16) then a summer (L16:D8) photoperiod, at air temperatures of first 20 °C then 7 °C under both photoperiods. We found that nesting material and pair housing did not affect hamster BMR, while access to a running wheel increased BMR and body mass regardless of photoperiod and ambient temperature. Thus, we suggest that cage enrichment should be applied with caution, especially in studies on energetics or thermoregulation, particularly in seasonal animals.

Polymorphism of winter phenotype in Siberian hamster: consecutive litters do not differ in photoresponsiveness but prolonged acclimation to long photoperiod inhibits winter molt.

BACKGROUND: The theory of delayed life history effects assumes that phenotype of adult individual results from environmental conditions experienced at birth and as juvenile. In seasonal environments, being born late in the reproductive season affects timing of puberty, body condition, longevity, and fitness. We hypothesized that late-born individuals are more prone to respond to short photoperiod (SP) than early born ones. We used Siberian hamsters Phodopus sungorus, a model species characterized by high polymorphism of winter phenotype. We experimentally distinguished the effect of litter order (first or third) from the effect of exposure to long photoperiod (LP) before winter (3 months or 5 months) by manipulating the duration of LP acclimation in both litters. We predicted that, irrespective of the litter order, individuals exposed to long photoperiod for a short time have less time to gather energy resources and consequently are more prone to developing energy-conserving phenotypes. To assess effect of litter order, duration of acclimation to long days, and phenotype on basal cost of living we measured basal metabolic rate (BMR) of hamsters. RESULTS: Individuals born in third litters had faster growth rates and were bigger than individuals from first litters, but these differences vanished before transfer to SP. Litter order or duration of LP acclimation had no effects on torpor use or seasonal body mass changes, but prolonged acclimation to LP inhibited winter molting both in first and third litters. Moreover, individuals that did not molt had significantly higher BMR in SP than those which molted to white fur. Although one phenotype usually predominated within a litter, littermates were often heterogeneous. We also found that over 10% of individuals presented late response to short photoperiod. CONCLUSIONS: Our data indicate that duration of postnatal exposure to LP may define propensity to photoresponsiveness, regardless of the litter in which animal was born. Existence of littermates presenting different phenotypes suggests a prudent reproductive strategy of investing into offspring of varied phenotypes, that might be favored depending on environmental conditions. This strategy could have evolved in response to living in stochastic environment.

Predictive and reactive changes in antioxidant defence system in a heterothermic rodent.

Living in a seasonal environment requires periodic changes in animal physiology, morphology and behaviour. Winter phenotype of small mammals living in Temperate and Boreal Zones may differ considerably from summer one in multiple traits that enhance energy conservation or diminish energy loss. However, there is a considerable variation in the development of winter phenotype among individuals in a population and some, representing the non-responding phenotype (non-responders), are insensitive to shortening days and maintain summer phenotype throughout a year. Differences in energy management associated with the development of different winter phenotypes should be accompanied by changes in antioxidant defence capacity, leading to effective protection against oxidative stress resulting from increased heat production in winter. To test it, we analysed correlation of winter phenotypes of Siberian hamsters (Phodopus sungorus) with facultative non-shivering thermogenesis capacity (NST) and oxidative status. We found that in both phenotypes acclimation to winter-like conditions increased NST capacity and improved antioxidant defence resulting in lower oxidative stress (OS) than in summer, and females had always lower OS than males. Although NST capacity did not correlate with the intensity of OS, shortly after NST induction responders had lower OS than non-responders suggesting more effective mechanisms protecting from detrimental effects of reactive oxygen metabolites generated during rewarming from torpor. We suggest that seasonal increase in antioxidant defence is programmed endogenously to predictively prevent oxidative stress in winter. At the same time reactive upregulation of antioxidant defence protects against reactive oxygen species generated during NST itself. It suggests that evolution of winter phenotype with potentially harmful characteristics was counterbalanced by the development of protective mechanisms allowing for the maintenance of phenotypic adjustments to seasonally changing environment.