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.

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.