The photoperiodic neuroendocrine system drives seasonal rhythms in reproduction. To get a better understanding of how annual cycling environmental cues impact reproductive function and plasticity in small, short-lived herbivores with different geographic origins, we investigated the mechanisms underlying integration of temperature in the photoperiodic-axis regulating female reproduction in tundra voles and in common voles. We show that photoperiod and temperature interact to determine appropriate physiological responses; there is species-dependent annual variation in the sensitivity to temperature for reproductive organ development. These findings are in line with our census data, showing an earlier onset of spring reproduction in cold springs, while reproductive offset in autumn is synchronized to photoperiod. The reproductive organs of tundra voles were relatively insensitive to temperature, whereas hypothalamic gene expression was generally upregulated at 10°C. Due to global warming, spring reproduction in common voles will be delayed, perhaps resulting in shorter breeding seasons and thus declining populations.

The vertebrate photoperiodic neuroendocrine system uses photoperiod as a proxy to time annual rhythms in reproduction. 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; 22 intronic, 27 exonic) were found, with weak or zero 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 spring onset of local primary food production (grass). The pCPP obtained explains the distribution of genetic variation in Tshr in Western Europe through highly significant correlations. Thus, Tshr, which plays a pivotal role in the sensitivity of the mammalian photoperiodic neuroendocrine system, was targeted by natural selection, resulting in optimized timing of seasonal reproduction.

Seasonal timing of reproduction in voles is driven by photoperiod. Here we hypothesize that a negative energy balance can modify spring-programmed photoperiodic responses in the hypothalamus, controlling reproductive organ development. We manipulated energy balance by the ‘work-for-food’ protocol, in which voles were exposed to increasing levels of food scarcity at different ambient temperatures under long photoperiod. We reveal that common (Microtus arvalis) and tundra voles (Microtus oeconomus), reduce photoperiodic induced pars tuberalis thyroid-stimulating hormone β-subunit (Tshβ) expression to inhibit gonadal development when food is scarce. Reduction in gonadal size is more pronounced in tundra voles, in which the hypothalamic Kisspeptin (Kiss1) system seems involved in downregulating gonadal development, especially in males. Low temperature additionally leads to decreased hypothalamic RF-amide related peptide (Rfrp3) levels, which may facilitate further suppression of gonadal growth. Shutting off the photoperiodic-axis when food is scarce in spring may be an adaptive response to save energy, leading to delayed reproductive organ development until food resources are sufficient for reproduction, lactation and offspring survival. Defining the mechanisms through which metabolic cues modify photoperiodic responses will be important for a better understanding of how environmental cues impact reproduction.

Seasonal timing of reproduction in voles is driven by photoperiod. Here we hypothesize that a negative energy balance can modify spring-programmed photoperiodic responses in the hypothalamus, controlling reproductive organ development. We reveal that Common (Microtus arvalis) and Tundra voles (Microtus oeconomus), reduce photoperiodic induced pars tuberalis thyroid-stimulating hormone β-subunit (Tshβ) expression to inhibit gonadal development when food is scarce. Reduction in gonadal size is more pronounced in tundra voles, in which the hypothalamic Kisspeptin (Kiss1) system seems involved in downregulating gonadal development, especially in males. Low temperature additionally leads to decreased hypothalamic RF-amide related peptide (Rfrp3) levels, which may facilitate further suppression of gonadal growth. Shutting off the photoperiodic-axis when food is scarce in spring may be an adaptive response to save energy, leading to delayed reproductive organ development until food resources are sufficient for reproduction, lactation and offspring survival.