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 (T a ) modulate timing of seasonal changes in physiolog...

Full description

Bibliographic Details
Published in:Journal of Biological Rhythms
Main Authors: van Dalum, Mattis Jayme, van Rosmalen, Laura, Appenroth, Daniel, Cazarez Marquez, Fernando, Roodenrijs, Renzo T. M., de Wit, Lauren, Hut, Roelof A., Hazlerigg, David G.
Other Authors: Universitetet i Tromsø, Human Frontiers Science Program, Rijksuniversiteit Groningen, Tromsø Forskningsstiftelse
Format: Article in Journal/Newspaper
Language:English
Published: SAGE Publications 2023
Subjects:
Online Access:http://dx.doi.org/10.1177/07487304231190156
https://journals.sagepub.com/doi/pdf/10.1177/07487304231190156
https://journals.sagepub.com/doi/full-xml/10.1177/07487304231190156
Description
Summary: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 (T a ) 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 T a 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 T a was asymmetric: low T a (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 T a 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 ( tshβ) 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 T a -sensitive gene across the study, showing increased expression at higher T a , while higher T a reduced somatostatin expression. Contrastingly dio3 and tshβ were largely insensitive to T a . Overall, these observations reveal a complex interplay between T a and photoperiodic control of postnatal growth in M. oeconomus, and suggest that integration of T a into the control of growth ...