RESEARCH ARTICLE Melatonin attenuates phenotypic flexibility of energy metabolism in a photoresponsive mammal, the Siberian hamster Jan S. Boratyn ́ ski 1, * , ‡ , Malgorzata Jefimow 1 and Michal S. Wojciechowski 2 ABSTRACT The duration of melatonin (MEL) secretion conveys information about day length and initiates a cascade of seasonal phenotypic adjustments in photoresponsive mammals. With shortening days, animals cease reproduction, minimize energy expenditure, enhance thermoregulatory capacity and adjust functioning of the hypothalamic-pituitary-adrenal (HPA) axis to match the winter increase in energy demands. Within each season, stress plays an important role in the flexible adjustments of a phenotype to environmental perturbations. Recent studies have shown that thermal reaction norms of energy metabolism were narrower in winter-acclimated Siberian hamsters, Phodopus sungorus. We tested the hypothesis that physiological changes occurring in response to prolonged MEL signals, including changes in the secretion of stress hormones, are responsible for the seasonal decrease in phenotypic flexibility of energy metabolism in photoresponsive mammals. To quantify reaction norms for basal metabolic rate (BMR) and cortisol (CORT) secretion, male Siberian hamsters maintained at a long (16 h:8 h light:dark) photoperiod were acclimated repeatedly for 12 days to 10 and 28°C. As predicted, the phenotypic flexibility of BMR decreased when animals were supplemented with MEL. However, at the same time, mean CORT concentration and the reaction norm for its secretion in response to changes in acclimation temperature increased. These results suggest that decreased sensitivity of HPA axis to CORT signal, rather than changes in CORT level itself, is responsible for the decreased phenotypic flexibility in photoresponsive species. Our results suggest that decreased phenotypic flexibility in winter, together with increased stress hormone secretion, make photosensitive species more vulnerable to climate change. KEY WORDS: Photoperiodism, Phenotypic flexibility, Energy expenditure, Stress, Melatonin, Cortisol INTRODUCTION Animals reversibly adjust their physiology, behavior or morphology in response to predictable (e.g. seasonal) or unpredictable (e.g. year- round) and rapid changes in the environment (Wingfield and Kitaysky, 2002; Piersma and Drent, 2003). In the course of seasonal acclimatization to winter, many small mammals cease reproduction (Bronson, 2009), minimize their energy expenditure by reducing body mass (m b ) and basal metabolic rate (BMR), and improve insulation (reviewed in Heldmaier, 1989; Lovegrove, 2005) and facultative heat production (Heldmaier et al., 1981). Seasonal acclimatization is driven by photoperiod and is under endocrine control (Scherbarth and Steinlechner, 2010). Shortening of the light phase of the day results in prolonged melatonin (MEL) secretion at night, whereas increasing the day length does the opposite (Steinlechner et al., 1987). MEL is produced and released from the pineal gland during the dark phase of the day, and the duration of elevated nocturnal MEL levels differs seasonally, serving to translate the environmental signal of day length into an endocrine one (Steinlechner et al., 1987). Changes in photoperiod are a predictable and reliable signal that conveys information about future environmental demands; these changes allow animals to synchronize their physiology with environmental or life-history challenges; e.g. winter survival (Heldmaier and Lynch, 1986), reproduction (Tamarkin et al., 1985) or migration (Coppack and Pulido, 2004). The photoperiod–MEL mechanism controlling seasonal physiology is evolutionarily conserved across both diurnal and nocturnal taxa (reviewed in Bradshaw and Holzapfel, 2007). In photoresponsive mammals, MEL supplementation mimics shortening photoperiod and induces seasonal changes, such as a decrease in the set-point for m b regulation (Wade and Bartness, 1984), gonadal regression (Hiebert et al., 2006), changes in hypothalamic-pituitary-adrenal (HPA) axis activity (Pyter et al., 2007; Scotti et al., 2008, 2015) and adjustments in thermoregulatory mechanisms (Heldmaier and Lynch, 1986). Thus, MEL plays an important role in an integrative system that controls investments in reproduction and immunity, and in coping with environmental stress (Nelson and Demas, 1997). Unpredictable, often rapid, environmental perturbations require adequate adjustments of an animal’s phenotype year- round (Wingfield and Kitaysky, 2002; Piersma and Drent, 2003). Flexible adjustments of the mechanisms of heat production are a common response of endothermic animals to changing thermal conditions (McKechnie et al., 2007; van de Ven et al., 2013; Boratyń ski et al., 2016; for review, see Piersma and Van Glis, 2011). However, recent results indicate that phenotypic flexibility changes seasonally, being lower in winter than in summer (Boratyń ski et al., 2016). Because photoperiod is the primary cue for seasonal phenotypic adjustments in photoresponsive mammals (Lynch, 1973; Heldmaier and Lynch, 1986; Goldman et al., 2000) via actions on the endocrine system, we hypothesized that the decrease of short- term phenotypic flexibility in winter is a result of substantial changes at an endocrine level (Boratyń ski et al., 2016). Hormones that may be important for the seasonal regulation of phenotypic flexibility are released in response to the environmental stress, which activates two main neuroendocrine pathways. One is the synthesis and release of adrenaline and noradrenaline as part of the sympathoadrenal system; another is the synthesis and the release of glucocorticoids (GCs) as a result Received 15 March 2017; Accepted 7 June 2017 1 Department of Animal Physiology, Nicolaus Copernicus University, ul. Lwowska 1, 87-100 Toruń , Poland. 2 Department of Vertebrate Zoology, Nicolaus Copernicus University, ul. Lwowska 1, 87-100 Toruń , Poland. *Present address: Museum and Institute of Zoology, Polish Academy of Sciences, ul. Wilcza 64, 00-679 Warsaw, Poland. ‡ Author for correspondence ( jan.boratynski@gmail.com) 3154 © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 3154-3161 doi:10.1242/jeb.159517 Journal of Experimental Biology