Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor

The vertebrate photoperiodic neuroendocrine system uses the photoperiod as a proxy to time the annual rhythms in reproduction. The thyrotropin receptor (TSHR) is a key protein in the mammalian seasonal reproduction pathway. Its abundance and function can tune sensitivity to the photoperiod. To inves...

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Published in:Genes
Main Authors: Laura van Rosmalen, Robin Schepers, Wensi Hao, Anna S. Przybylska-Piech, Jeremy S. Herman, Joanna Stojak, Jan M. Wójcik, Louis van de Zande, Jeremy B. Searle, Roelof A. Hut
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Language:English
Published: Multidisciplinary Digital Publishing Institute 2023
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Online Access:https://doi.org/10.3390/genes14020292
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spelling ftmdpi:oai:mdpi.com:/2073-4425/14/2/292/ 2023-08-20T04:05:58+02:00 Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor Laura van Rosmalen Robin Schepers Wensi Hao Anna S. Przybylska-Piech Jeremy S. Herman Joanna Stojak Jan M. Wójcik Louis van de Zande Jeremy B. Searle Roelof A. Hut agris 2023-01-22 application/pdf https://doi.org/10.3390/genes14020292 EN eng Multidisciplinary Digital Publishing Institute Animal Genetics and Genomics https://dx.doi.org/10.3390/genes14020292 https://creativecommons.org/licenses/by/4.0/ Genes; Volume 14; Issue 2; Pages: 292 seasonal reproduction Tsh receptor temperature–photoperiod ellipsoid natural selection Microtus arvalis common vole climate change Text 2023 ftmdpi https://doi.org/10.3390/genes14020292 2023-08-01T08:26:03Z The vertebrate photoperiodic neuroendocrine system uses the photoperiod as a proxy to time the annual rhythms in reproduction. The thyrotropin receptor (TSHR) is a key protein in the mammalian seasonal reproduction pathway. Its abundance and function can tune sensitivity to the photoperiod. To investigate seasonal adaptation in mammals, the hinge region and the first part of the transmembrane domain of the Tshr gene were sequenced for 278 common vole (Microtus arvalis) specimens from 15 localities in Western Europe and 28 localities in Eastern Europe. Forty-nine single nucleotide polymorphisms (SNPs; twenty-two intronic and twenty-seven exonic) were found, with a weak or lack of correlation with pairwise geographical distance, latitude, longitude, and altitude. By applying a temperature threshold to the local photoperiod–temperature ellipsoid, we obtained a predicted critical photoperiod (pCPP) as a proxy for the spring onset of local primary food production (grass). The obtained pCPP explains the distribution of the genetic variation in Tshr in Western Europe through highly significant correlations with five intronic and seven exonic SNPs. The relationship between pCPP and SNPs was lacking in Eastern Europe. Thus, Tshr, which plays a pivotal role in the sensitivity of the mammalian photoperiodic neuroendocrine system, was targeted by natural selection in Western European vole populations, resulting in the optimized timing of seasonal reproduction. Text Common vole Microtus arvalis MDPI Open Access Publishing Genes 14 2 292
institution Open Polar
collection MDPI Open Access Publishing
op_collection_id ftmdpi
language English
topic seasonal reproduction
Tsh receptor
temperature–photoperiod ellipsoid
natural selection
Microtus arvalis
common vole
climate change
spellingShingle seasonal reproduction
Tsh receptor
temperature–photoperiod ellipsoid
natural selection
Microtus arvalis
common vole
climate change
Laura van Rosmalen
Robin Schepers
Wensi Hao
Anna S. Przybylska-Piech
Jeremy S. Herman
Joanna Stojak
Jan M. Wójcik
Louis van de Zande
Jeremy B. Searle
Roelof A. Hut
Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor
topic_facet seasonal reproduction
Tsh receptor
temperature–photoperiod ellipsoid
natural selection
Microtus arvalis
common vole
climate change
description The vertebrate photoperiodic neuroendocrine system uses the photoperiod as a proxy to time the annual rhythms in reproduction. The thyrotropin receptor (TSHR) is a key protein in the mammalian seasonal reproduction pathway. Its abundance and function can tune sensitivity to the photoperiod. To investigate seasonal adaptation in mammals, the hinge region and the first part of the transmembrane domain of the Tshr gene were sequenced for 278 common vole (Microtus arvalis) specimens from 15 localities in Western Europe and 28 localities in Eastern Europe. Forty-nine single nucleotide polymorphisms (SNPs; twenty-two intronic and twenty-seven exonic) were found, with a weak or lack of correlation with pairwise geographical distance, latitude, longitude, and altitude. By applying a temperature threshold to the local photoperiod–temperature ellipsoid, we obtained a predicted critical photoperiod (pCPP) as a proxy for the spring onset of local primary food production (grass). The obtained pCPP explains the distribution of the genetic variation in Tshr in Western Europe through highly significant correlations with five intronic and seven exonic SNPs. The relationship between pCPP and SNPs was lacking in Eastern Europe. Thus, Tshr, which plays a pivotal role in the sensitivity of the mammalian photoperiodic neuroendocrine system, was targeted by natural selection in Western European vole populations, resulting in the optimized timing of seasonal reproduction.
format Text
author Laura van Rosmalen
Robin Schepers
Wensi Hao
Anna S. Przybylska-Piech
Jeremy S. Herman
Joanna Stojak
Jan M. Wójcik
Louis van de Zande
Jeremy B. Searle
Roelof A. Hut
author_facet Laura van Rosmalen
Robin Schepers
Wensi Hao
Anna S. Przybylska-Piech
Jeremy S. Herman
Joanna Stojak
Jan M. Wójcik
Louis van de Zande
Jeremy B. Searle
Roelof A. Hut
author_sort Laura van Rosmalen
title Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor
title_short Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor
title_full Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor
title_fullStr Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor
title_full_unstemmed Seasonal Adaptation: Geographic Photoperiod–Temperature Patterns Explain Genetic Variation in the Common Vole Tsh Receptor
title_sort seasonal adaptation: geographic photoperiod–temperature patterns explain genetic variation in the common vole tsh receptor
publisher Multidisciplinary Digital Publishing Institute
publishDate 2023
url https://doi.org/10.3390/genes14020292
op_coverage agris
genre Common vole
Microtus arvalis
genre_facet Common vole
Microtus arvalis
op_source Genes; Volume 14; Issue 2; Pages: 292
op_relation Animal Genetics and Genomics
https://dx.doi.org/10.3390/genes14020292
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.3390/genes14020292
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