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...

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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.
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Language:English
Published: SAGE Publications 2023
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10617003/
http://www.ncbi.nlm.nih.gov/pubmed/37565646
https://doi.org/10.1177/07487304231190156
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10617003 2023-12-03T10:31:23+01:00 Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole 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. 2023-08-11 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10617003/ http://www.ncbi.nlm.nih.gov/pubmed/37565646 https://doi.org/10.1177/07487304231190156 en eng SAGE Publications http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10617003/ http://www.ncbi.nlm.nih.gov/pubmed/37565646 http://dx.doi.org/10.1177/07487304231190156 © 2023 The Author(s) https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access page (https://us.sagepub.com/en-us/nam/open-access-at-sage). J Biol Rhythms Original Articles Text 2023 ftpubmed https://doi.org/10.1177/07487304231190156 2023-11-05T02:08:18Z 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 ... Text Tundra PubMed Central (PMC) Journal of Biological Rhythms 38 6 586 600
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Original Articles
spellingShingle Original Articles
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.
Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole
topic_facet Original Articles
description 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 ...
format Text
author 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.
author_facet 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.
author_sort van Dalum, Mattis Jayme
title Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole
title_short Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole
title_full Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole
title_fullStr Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole
title_full_unstemmed Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole
title_sort ambient temperature effects on the spring and autumn somatic growth trajectory show plasticity in the photoneuroendocrine response pathway in the tundra vole
publisher SAGE Publications
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10617003/
http://www.ncbi.nlm.nih.gov/pubmed/37565646
https://doi.org/10.1177/07487304231190156
genre Tundra
genre_facet Tundra
op_source J Biol Rhythms
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10617003/
http://www.ncbi.nlm.nih.gov/pubmed/37565646
http://dx.doi.org/10.1177/07487304231190156
op_rights © 2023 The Author(s)
https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access page (https://us.sagepub.com/en-us/nam/open-access-at-sage).
op_doi https://doi.org/10.1177/07487304231190156
container_title Journal of Biological Rhythms
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