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Although the Djungarian hamster (Phodopus sungorus) is a seasonality model, it presents substantial variability in winter acclimation. In response to short photoperiod, some individuals express a suite of winter traits such as low body mass, regressed gonads, white fur, and daily torpor, while others develop only some adjustments or maintain a summer phenotype. Despite comprehensive research, the mechanisms underlying polymorphism of winter phenotype are still unknown. We compared key elements of the hypothalamic thyroid hormone system, as well as the tanycyte architecture in hamsters of both sexes. Individuals presented different responses to short photoperiod characterized either as phenotypes (non-responder, partial-responder and full-responder) or photoresponsive index. We measured the expression of genes coding iodothyronine deiodinase 2 and 3, monocarboxylate transporter 8, thyrotropin-releasing hormone, and somatostatin in 40 individuals and counted the number of immunolabeled tanycyte processes in standardized regions of interest around the third ventricle in 30 individuals. Animals acclimated to short photoperiod presented a downregulation of diodinase 2 and somatostatin and an upregulation of deiodinase 3, as well as a decreased number of tanycyte processes, compared to long photoperiod-exposed individuals. Although phenotypes did not differ in gene expression, the higher the photoresponsive index, the lower was the deiodinase 2 expression and the higher the deiodinase 3 expression. Partial-responders and full-responders had less tanycyte processes than non-responders, and the number of tanycyte processes correlated with the photoresponsive index. Sexes differed neither in their seasonal response, nor hypothalamic gene expression, but females had more tanycyte processes. Our results are in accordance with studies emphasizing the pivotal role of thyroid hormones in seasonal response. We suggest that the whole spectrum of winter phenotypes exists within the population of Djungarian hamsters and that it is reflected also at the level of neuroendocrine regulation. However, the neuroendocrine underpinnings of winter phenotype polymorphism require further investigation., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Przybylska-Piech et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

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. [ABSTRACT FROM AUTHOR]

Background: The theory of delayed life history effects assumes that phenotype of adult individual results from environmental conditions experienced at birth and as juvenile. In seasonal environments, being born late in the reproductive season affects timing of puberty, body condition, longevity, and fitness. We hypothesized that late-born individuals are more prone to respond to short photoperiod (SP) than early born ones. We used Siberian hamsters Phodopus sungorus, a model species characterized by high polymorphism of winter phenotype. We experimentally distinguished the effect of litter order (first or third) from the effect of exposure to long photoperiod (LP) before winter (3 months or 5 months) by manipulating the duration of LP acclimation in both litters. We predicted that, irrespective of the litter order, individuals exposed to long photoperiod for a short time have less time to gather energy resources and consequently are more prone to developing energy-conserving phenotypes. To assess effect of litter order, duration of acclimation to long days, and phenotype on basal cost of living we measured basal metabolic rate (BMR) of hamsters. Results: Individuals born in third litters had faster growth rates and were bigger than individuals from first litters, but these differences vanished before transfer to SP. Litter order or duration of LP acclimation had no effects on torpor use or seasonal body mass changes, but prolonged acclimation to LP inhibited winter molting both in first and third litters. Moreover, individuals that did not molt had significantly higher BMR in SP than those which molted to white fur. Although one phenotype usually predominated within a litter, littermates were often heterogeneous. We also found that over 10% of individuals presented late response to short photoperiod. Conclusions: Our data indicate that duration of postnatal exposure to LP may define propensity to photoresponsiveness, regardless of the litter in which animal was born. Existence of littermates presenting different phenotypes suggests a prudent reproductive strategy of investing into offspring of varied phenotypes, that might be favored depending on environmental conditions. This strategy could have evolved in response to living in stochastic environment. [ABSTRACT FROM AUTHOR]