Gonads or body?:Differences in gonadal and somatic photoperiodic growth response in two vole species

To optimally time reproduction, seasonal mammals use a photoperiodic neuroendocrine system (PNES) that measures photoperiod and subsequently drives reproduction. To adapt to late spring arrival at northern latitudes, a lower photoperiodic sensitivity and therefore a higher critical photoperiod for reproductive onset is necessary in northern species to arrest reproductive development until spring onset. Temperature-photoperiod relationships, and hence food availability-photoperiod relationships, are highly latitude dependent. Therefore, we predict PNES sensitivity characteristics to be latitude dependent. Here, we investigated photoperiodic responses at different times during development in northern (tundra or root vole, Microtus oeconomus) and southern vole species (common vole, Microtus arvalis) exposed to constant short (SP) or long photoperiod (LP). Although the tundra vole grows faster under LP, no photoperiodic effect on somatic growth is observed in the common vole. In contrast, gonadal growth is more sensitive to photoperiod in the common vole, suggesting that photoperiodic responses in somatic and gonadal growth can be plastic, and might be regulated through different mechanisms. In both species, thyroid-stimulating hormone β-subunit (Tshβ) and iodothyronine deiodinase 2 (Dio2) expression is highly increased under LP, whereas Tshr and Dio3 decrease under LP. High Tshr levels in voles raised under SP may lead to increased sensitivity to increasing photoperiods later in life. The higher photoperiodic-induced Tshr response in tundra voles suggests that the northern vole species might be more sensitive to thyroid-stimulating hormone when raised under SP. In conclusion, species differences in developmental programming of the PNES, which is dependent on photoperiod early in development, may form different breeding strategies as part of latitudinal adaptation

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

Evolution of seasonal adaptations in voles - a physiological and genetic approach

This thesis addressed phenotypic and genetic variation in seasonal time keeping mechanisms of the tundra vole (Microtus oeconomus) and the common vole (Microtus arvalis). Voles (Microtus) are short-lived, non-hibernating and seasonally breeding rodents. The genus has rapidly evolved (< 2 million years) into one of the most speciose mammalian genera (Sitnikova et al. 2007; Triant and DeWoody 2006) and occupies a wide range of latitudes (14-78°N) with the tundra vole being the most wide spread species. Seasonality is strong at high latitudes with lower and more seasonally fluctuating ambient temperatures (Hut et al. 2013). Therefore, animals have evolved mechanisms to time their life cycles with the strongly cyclical environment. The annual day length cycle is the most reliable cue to predict upcoming changes and prepare accordingly. This information is integrated by the photoneuroendocrine system (PNES) that coordinates phenotypic changes such as seasonal molt and reproduction (D. Hazlerigg and Simonneaux 2015). In paper I, we showed that under laboratory conditions, short winter photoperiods alone reduced somatic growth (body mass) in tundra voles and gonadal growth (reproduction) in common voles. Since both vole species were caught at the same location (the Netherlands, 53°N), the different response can be ascribed to genetic variation between the species. This was possibly shaped by different selection pressures occurring during the more northern (tundra vole) and southern (common vole) paleogeographic history of the two species. Within and among vole species, the timing of breeding shows great year-to-year variation (Tast 1966; T. Ergon et al. 2001), which is apparently influenced by environmental conditions such as ambient temperature (Kriegsfeld, Trasy, and Nelson 2000). The breeding season starts in spring with the overwintering individuals producing the first spring-born cohort of pups. The short gestation and development times allow these spring-born cohorts to reproduce during the same breeding season as their parents and produce several subsequent cohorts until the end of the breeding season in autumn (Horton 1984a; Gliwicz 1996). In papers II and III, we investigated the critical photoperiod thresholds for initiation of accelerated reproductive maturation in voles on a spring developmental program and for the deceleration of development in voles on an autumn program. Further, we assessed the influence of ambient temperature (10°C or 21°C) on the response parameters. Seasonal gene expression, hormone levels, downstream body-mass and gonadal mass had different species-specific response thresholds to photoperiod and temperature. This indicates that the system has a hierarchical organization that allowed for independent modulation at various levels. The results of these experiments also emphasise the importance of the direction of day length change in setting maturation trajectories. In Paper IV we searched for signatures of selection across the genomes of tundra voles from a northern (70°N) and southern (53°N) population. A signature of selection is a reduction in population diversity at a certain genomic position because of positive selection on a favoured allele. We found selection on a paralogue of the Aldh1a1 gene located between the Aldh1a1 and Aldh1a7 genes. We found two additional Aldh1a1-like paralogues on the same locus. Other voles investigated also had two or three paralogues, which are not present in mouse and rat genomes. Aldh1a1 has a central role in photoperiodic retinoic acid signaling in the rodent hypothalamus, which may be involved in seasonal body mass regulation (Helfer, Barrett, and Morgan 2019; Shearer, Stoney, Nanescu, et al. 2012). Aldh1a7 is also considered as a paralogue of Aldh1a1 (90% amino acid sequence homology in the mouse) but it is not involved in retinoic acid signaling (Hsu et al. 1999). The paralogues found in the vole had the highest sequence homology with Aldh1a7. Future research has to clarify the function of this gene and whether this selection pressure is associated with latitude. Taken together we found various levels of flexibility within the vole PNES where ambient temperature and photoperiodic history can modulate the seasonal response which is possibly affected by evolution at different latitudes. Reproductive opportunism and an ability to override photoperiodic information may be favoured in voles living at higher latitudes which may lead to genetic differences between and within species

Gonads or body? Differences in gonadal and somatic photoperiodic growth response in two vole species

To optimally time reproduction, seasonal mammals use a photoperiodic neuroendocrine system (PNES) that measures photoperiod and subsequently drives reproduction. To adapt to late spring arrival at northern latitudes, a lower photoperiodic sensitivity and therefore a higher critical photoperiod for reproductive onset is necessary in northern species to arrest reproductive development until spring onset. Temperature–photoperiod relationships, and hence food availability–photoperiod relationships, are highly latitude dependent. Therefore, we predict PNES sensitivity characteristics to be latitude dependent. Here, we investigated photoperiodic responses at different times during development in northern (tundra or root vole, Microtus oeconomus) and southern vole species (common vole, Microtus arvalis) exposed to constant short (SP) or long photoperiod (LP). Although the tundra vole grows faster under LP, no photoperiodic effect on somatic growth is observed in the common vole. In contrast, gonadal growth is more sensitive to photoperiod in the common vole, suggesting that photoperiodic responses in somatic and gonadal growth can be plastic, and might be regulated through different mechanisms. In both species, thyroid-stimulating hormone β-subunit (Tshβ) and iodothyronine deiodinase 2 (Dio2) expression is highly increased under LP, whereas Tshr and Dio3 decrease under LP. High Tshr levels in voles raised under SP may lead to increased sensitivity to increasing photoperiods later in life. The higher photoperiodic-induced Tshr response in tundra voles suggests that the northern vole species might be more sensitive to thyroid-stimulating hormone when raised under SP. In conclusion, species differences in developmental programming of the PNES, which is dependent on photoperiod early in development, may form different breeding strategies as part of latitudinal adaptation

Maternal Photoperiodic Programming: Melatonin and Seasonal Synchronization Before Birth

This mini-review considers the phenomenon of maternal photoperiodic programming (MPP). In order to match neonatal development to environmental conditions at the time of birth, mammals use melatonin produced by the maternal pineal gland as a transplacental signal representing ambient photoperiod. Melatonin acts via receptors in the fetal pituitary gland, exerting actions on the developing medio-basal hypothalamus. Within this structure, a central role for specialized ependymal cells known as tanycytes has emerged, linking melatonin to control of hypothalamic thyroid metabolism and in turn to pup development. This review summarizes current knowledge of this programming mechanism, and its relevance in an eco-evolutionary context. Maternal photoperiodic programming emerges as a useful paradigm for understanding how in utero programing of hypothalamic function leads to life-long effects on growth, reproduction, health and disease in mammals, including humans

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 (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 Ta-sensitive gene across the study, showing increased expression at higher Ta, while higher Ta reduced somatostatin expression. Contrastingly dio3 and tshβ 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

sj-csv-1-jbr-10.1177_07487304231190156 – for Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole

sj-csv-1-jbr-10.1177_07487304231190156 for Ambient Temperature Effects on the Spring and Autumn Somatic Growth Trajectory Show Plasticity in the Photoneuroendocrine Response Pathway in the Tundra Vole by Mattis Jayme van Dalum, Laura van Rosmalen, Daniel Appenroth, Fernando Cazarez Marquez, Renzo T. M. Roodenrijs, Lauren de Wit, Roelof A. Hut and David G. Hazlerigg in Journal of Biological Rhythm