Seasonal food intake and energy balance: Neuronal and non-neuronal control mechanisms.

Animals inhabiting temperate and high latitudes undergo drastic seasonal changes in energy storage, facilitated by changes in food intake and body mass. Those seasonal changes in the animal's biology are not mere consequences of environmental energy availability but are anticipatory responses to the energetic requirements of the upcoming season and are actively timed by tracking the annual progression in photoperiod. In this review, we discuss how photoperiod is used to control energy balance seasonally and how this is distinct from energy homeostasis. Most notably, we suggest that photoperiodic control of food intake and body mass does not originate from the arcuate nucleus, as for homeostatic appetite control, but is rather to be found in hypothalamic tanycytes. Tanycytes are specialized ependymal cells lining the third ventricle, which can sense metabolites from the cerebrospinal fluid (e.g. glucose) and can control access of circulating signals to the brain. They are also essential in conveying time-of-year information by integrating photoperiod and altering hypothalamic thyroid metabolism, a feature that is conserved in seasonal vertebrates and connects to seasonal breeding and metabolism. We also discuss how homeostatic feedback signals are handled during times of rapid energetic transitions. Studies on leptin in seasonal mammals suggest a seasonal shift in central sensitivity and blood-brain transport, which might be facilitated by tanycytes. This article is part of the Special Issue on "Food intake and feeding states".

Biological timekeeping in polar environments: lessons from terrestrial vertebrates.

The polar regions receive less solar energy than anywhere else on Earth, with the greatest year-round variation in daily light exposure; this produces highly seasonal environments, with short summers and long, cold winters. Polar environments are also characterised by a reduced daily amplitude of solar illumination. This is obvious around the solstices, when the Sun remains continuously above (polar 'day') or below (polar 'night') the horizon. Even at the solstices, however, light levels and spectral composition vary on a diel basis. These features raise interesting questions about polar biological timekeeping from the perspectives of function and causal mechanism. Functionally, to what extent are evolutionary drivers for circadian timekeeping maintained in polar environments, and how does this depend on physiology and life history? Mechanistically, how does polar solar illumination affect core daily or seasonal timekeeping and light entrainment? In birds and mammals, answers to these questions diverge widely between species, depending on physiology and bioenergetic constraints. In the high Arctic, photic cues can maintain circadian synchrony in some species, even in the polar summer. Under these conditions, timer systems may be refined to exploit polar cues. In other instances, temporal organisation may cease to be dominated by the circadian clock. Although the drive for seasonal synchronisation is strong in polar species, reliance on innate long-term (circannual) timer mechanisms varies. This variation reflects differing year-round access to photic cues. Polar chronobiology is a productive area for exploring the adaptive evolution of daily and seasonal timekeeping, with many outstanding areas for further investigation.

Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole.

Seasonal mammals register photoperiodic changes through the photoneuroendocrine system enabling them to time seasonal changes in growth, metabolism, and reproduction. To a varying extent, proximate environmental factors like ambient temperature (Ta) modulate timing of seasonal changes in physiology, conferring adaptive flexibility. While the molecular photoneuroendocrine pathway governing the seasonal responses is well defined, the mechanistic integration of nonphotoperiodic modulatory cues is poorly understood. Here, we explored the interaction between Ta and photoperiod in tundra voles, Microtus oeconomus, a boreal species in which the main impact of photoperiod is on postnatal somatic growth. We demonstrate that postweaning growth potential depends on both gestational and postweaning patterns of photoperiodic exposure, with the highest growth potential seen in voles experiencing short (8 h) gestational and long (16 h) postweaning photoperiods-corresponding to a spring growth program. Modulation by Ta was asymmetric: low Ta (10 °C) enhanced the growth potential of voles gestated on short photoperiods independent of postweaning photoperiod exposure, whereas in voles gestated on long photoperiods, showing a lower autumn-programmed growth potential, the effect of Ta was highly dependent on postweaning photoperiod. Analysis of the primary molecular elements involved in the expression of a neuroendocrine response to photoperiod, thyrotropin beta subunit (tshß) in the pars tuberalis, somatostatin (srif) in the arcuate nucleus, and type 2/3 deiodinase (dio2/dio3) in the mediobasal hypothalamus identified dio2 as the most Ta-sensitive gene across the study, showing increased expression at higher Ta, while higher Ta reduced somatostatin expression. Contrastingly dio3 and tshß were largely insensitive to Ta. Overall, these observations reveal a complex interplay between Ta and photoperiodic control of postnatal growth in M. oeconomus, and suggest that integration of Ta into the control of growth occurs downstream of the primary photoperiodic response cascade revealing potential adaptivity of small herbivores facing rising temperatures at high latitudes.

Evidence for circadian-based photoperiodic timekeeping in Svalbard ptarmigan, the northernmost resident bird.

The high Arctic archipelago of Svalbard (74°-81° north) experiences extended periods of uninterrupted daylight in summer and uninterrupted night in winter, apparently relaxing the major driver for the evolution of circadian rhythmicity. Svalbard ptarmigan (Lagopus muta hyperborea) is the only year-round resident terrestrial bird species endemic to the high Arctic and is remarkably adapted to the extreme annual variation in environmental conditions.1 Here, we demonstrate that, although circadian control of behavior disappears rapidly upon transfer to constant light conditions, consistent with the loss of daily activity patterns observed during the polar summer and polar night, Svalbard ptarmigans nonetheless employ a circadian-based mechanism for photoperiodic timekeeping. First, we show the persistence of rhythmic clock gene expression under constant light within the mediobasal hypothalamus and pars tuberalis, the key tissues in the seasonal neuroendocrine cascade. We then employ a "sliding skeleton photoperiod" protocol, revealing that the driving force behind seasonal biology of the Svalbard ptarmigan is rhythmic sensitivity to light, a feature that depends on a functioning circadian rhythm. Hence, the unusual selective pressures of life in the high Arctic have favored decoupling of the circadian clock from organization of daily activity patterns, while preserving its importance for seasonal synchronization.

Mechanisms of temperature modulation in mammalian seasonal timing.

Global warming is predicted to have major effects on the annual time windows during which species may successfully reproduce. At the organismal level, climatic shifts engage with the control mechanism for reproductive seasonality. In mammals, laboratory studies on neuroendocrine mechanism emphasize photoperiod as a predictive cue, but this is based on a restricted group of species. In contrast, field-oriented comparative analyses demonstrate that proximate bioenergetic effects on the reproductive axis are a major determinant of seasonal reproductive timing. The interaction between proximate energetic and predictive photoperiodic cues is neglected. Here, we focused on photoperiodic modulation of postnatal reproductive development in common voles (Microtus arvalis), a herbivorous species in which a plastic timing of breeding is well documented. We demonstrate that temperature-dependent modulation of photoperiodic responses manifest in the thyrotrophin-sensitive tanycytes of the mediobasal hypothalamus. Here, the photoperiod-dependent expression of type 2 deiodinase expression, associated with the summer phenotype was enhanced by 21°C, whereas the photoperiod-dependent expression of type 3 deiodinase expression, associated with the winter phenotype, was enhanced by 10°C in spring voles. Increased levels of testosterone were found at 21°C, whereas somatic and gonadal growth were oppositely affected by temperature. The magnitude of these temperature effects was similar in voles photoperiodical programmed for accelerated maturation (ie, born early in the breeding season) and in voles photoperiodical programmed for delayed maturation (ie, born late in the breeding season). The melatonin-sensitive pars tuberalis was relatively insensitive to temperature. These data define a mechanistic hierarchy for the integration of predictive temporal cues and proximate thermo-energetic effects in mammalian reproduction.

Body Temperature and Activity Rhythms Under Different Photoperiods in High Arctic Svalbard ptarmigan (Lagopus muta hyperborea).

Organisms use circadian rhythms to anticipate and exploit daily environmental oscillations. While circadian rhythms are of clear importance for inhabitants of tropic and temperate latitudes, its role for permanent residents of the polar regions is less well understood. The high Arctic Svalbard ptarmigan shows behavioral rhythmicity in presence of light-dark cycles but is arrhythmic during the polar day and polar night. This has been suggested to be an adaptation to the unique light environment of the Arctic. In this study, we examined regulatory aspects of the circadian control system in the Svalbard ptarmigan by recording core body temperature (T b) alongside locomotor activity in captive birds under different photoperiods. We show that T b and activity are rhythmic with a 24-h period under short (SP; L:D 6:18) and long photoperiod (LP; L:D 16:8). Under constant light and constant darkness, rhythmicity in T b attenuates and activity shows signs of ultradian rhythmicity. Birds under SP also showed a rise in T b preceding the light-on signal and any rise in activity, which proves that the light-on signal can be anticipated, most likely by a circadian system.

Photoperiodic induction without light-mediated circadian entrainment in a High Arctic resident bird.

Organisms use changes in photoperiod to anticipate and exploit favourable conditions in a seasonal environment. While species living at temperate latitudes receive day length information as a year-round input, species living in the Arctic may spend as much as two-thirds of the year without experiencing dawn or dusk. This suggests that specialised mechanisms may be required to maintain seasonal synchrony in polar regions. Svalbard ptarmigan (Lagopus muta hyperborea) are resident at 74-81°N latitude. They spend winter in constant darkness (DD) and summer in constant light (LL); extreme photoperiodic conditions under which they do not display overt circadian rhythms. Here, we explored how Arctic adaptation in circadian biology affects photoperiodic time measurement in captive Svalbard ptarmigan. For this purpose, DD-adapted birds, showing no circadian behaviour, either remained in prolonged DD, were transferred into a simulated natural photoperiod (SNP) or were transferred directly into LL. Birds transferred from DD to LL exhibited a strong photoperiodic response in terms of activation of the hypothalamic thyrotropin-mediated photoperiodic response pathway. This was assayed through expression of the Eya3, Tshß and deiodinase genes, as well as gonadal development. While transfer to SNP established synchronous diurnal activity patterns, activity in birds transferred from DD to LL showed no evidence of circadian rhythmicity. These data show that the Svalbard ptarmigan does not require circadian entrainment to develop a photoperiodic response involving conserved molecular elements found in temperate species. Further studies are required to define how exactly Arctic adaptation modifies seasonal timer mechanisms.