References
Adams, M.R., Tamarin, R.H. & Callard, I.P. (1980). Seasonal changes in plasma androgen levels and the gonads of the beach vole, Microtus breweri. Gen. Comp. Endocrinol. , 41, 31–40.
Angelopoulou, E., Quignon, C., Kriegsfeld, L.J., Simonneaux, V. & Anderson, G. (2019). Functional Implications of RFRP-3 in the Central Control of Daily and Seasonal Rhythms in Reproduction. Front. Endocrinol. (Lausanne). , 10, 1–15.
Ansel, L., Bolborea, M., Bentsen, A.H., Klosen, P., Mikkelsen, J.D. & Simonneaux, V. (2010). Differential regulation of kiss1 expression by melatonin and gonadal hormones in male and female syrian hamsters.J. Biol. Rhythms , 25, 81–91.
Baker, J. (1938). The evolution of breeding seasons. Evol. Essays Asp. Evol. Biol. , 161–177.
Caro, S.P., Schaper, S. V., Hut, R.A., Ball, G.F. & Visser, M.E. (2013). The Case of the Missing Mechanism: How Does Temperature Influence Seasonal Timing in Endotherms? PLoS Biol. , 11.
Cooke, P.S., Spencer, T.E., Bartol, F.F. & Hayashi, K. (2013). Uterine glands: Development, function and experimental model systems. Mol. Hum. Reprod. , 19, 547–558.
Coppola, A., Meli, R. & Diano, S. (2005). Inverse shift in circulating corticosterone and leptin levels elevates hypothalamic deiodinase type 2 in fasted rats. Endocrinology , 146, 2827–2833.
Daketse, M.-J. & Martinet, L. (1977). Effect of temperature on the growth and fertility of the field-vole, Microtus arvalis, raised in different daylength and feeding conditions. Ann Biol Anim Biochim Biophys , 17, 713–721.
Dardente, H., Wood, S., Ebling, F. & Sáenz de Miera, C. (2018). An integrative view of mammalian seasonal neuroendocrinology. J. Neuroendocrinol. , 31.
Diano, S., Naftolin, F., Goglia, F. & Horvath, T.L. (1998). Fasting-induced increase in type II iodothyronine deiodinase activity and messenger ribonucleic acid levels is not reversed by thyroxine in the rat hypothalamus. Endocrinology , 139, 2879–2884.
Ergon, T., Lambin, X. & Stenseth, N.C. (2001). Life-history baits of voles in a fluctuating population respond to the immediate environment.Nature , 411, 1043–1045.
Gerkema, M.P., Daan, S., Wilbrink, M., Hop, M.W., Van Der Leest, F. & Gerkema, M.P. (1993). Phase Control of Ultradian Feeding Rhythms in the Common Vole (Microtus arvalis): The Roles of Light and the Circadian System. J. Biol. Rhythms , 8, 151–171.
Greives, T.J., Humber, S.A., Goldstein, A.N., Scotti, M.A.L., Demas, G.E. & Kriegsfeld, L.J. (2008). Photoperiod and testosterone interact to drive seasonal changes in kisspeptin expression in siberian hamsters (Phodopus sungorus). J. Neuroendocrinol. , 20, 1339–1347.
Guerra, M., Blázquez, J.L., Peruzzo, B., Peláez, B., Rodríguez, S., Toranzo, D., et al. (2010). Cell organization of the rat pars tuberalis. Evidence for open communication between pars tuberalis cells, cerebrospinal fluid and tanycytes. Cell Tissue Res. , 339, 359–381.
Guillemin, R. (1977). Purification, isolation, and primary structure of the hypothalamic luteinizing hormone-releasing factor of ovine origin. A historical account. Am. J. Obstet. Gynecol. , 129, 214–218.
Han, S.K., Gottsch, M.L., Lee, K.J., Popa, S.M., Smith, J.T., Jakawich, S.K., et al. (2005). Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J. Neurosci. , 25, 11349–11356.
Han, S.Y., McLennan, T., Czieselsky, K. & Herbison, A.E. (2015). Selective optogenetic activation of arcuate kisspeptin neurons generates pulsatile luteinizing hormone secretion. Proc. Natl. Acad. Sci. U. S. A. , 112, 13109–13114.
Hanon, E.A., Lincoln, G.A., Fustin, J.-M., Dardente, H., Masson-Pévet, M., Morgan, P.J., et al. (2008). Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr. Biol. , 18, 1147–1152.
Hileman, S.M., McManus, C.J., Goodman, R.L. & Jansen, H.T. (2011). Neurons of the lateral preoptic area/rostral anterior hypothalamic area are required for photoperiodic inhibition of estrous cyclicity in sheep.Biol. Reprod. , 85, 1057–1065.
Hrvatin, S., Sun, S., Wilcox, O.F., Yao, H., Lavin-Peter, A.J., Cicconet, M., et al. (2020). Neurons that regulate mouse torpor.Nature , 583, 115–121.
Hut, R.A. (2011). Photoperiodism: Shall EYA compare thee to a summers day? Curr. Biol. , 21, 22–25.
Hut, R.A., Dardente, H. & Riede, S.J. (2014). Seasonal timing: How does a hibernator know when to stop hibernating? Curr. Biol. , 24, 602–605.
Hut, R.A., Pilorz, V., Boerema, A.S., Strijkstra, A.M. & Daan, S. (2011). Working for food shifts nocturnal mouse activity into the day.PLoS One , 6, 1–6.
Jaroslawska, J., Chabowska-Kita, A., Kaczmarek, M.M. & Kozak, L.P. (2015). Npvf: Hypothalamic Biomarker of Ambient Temperature Independent of Nutritional Status. PLoS Genet. , 11, 1–23.
Klosen, P., Sébert, M.E., Rasri, K., Laran-Chich, M.P. & Simonneaux, V. (2013). TSH restores a summer phenotype in photoinhibited mammals via the RF-amides RFRP3 and kisspeptin. FASEB J. , 27, 2677–2686.
Krebs, S., Fischaleck, M. & Blum, H. (2009). A simple and loss-free method to remove TRIzol contaminations from minute RNA samples.Anal. Biochem. , 387, 136–138.
Król, E., Douglas, A., Dardente, H., Birnie, M.J., Vinne, V. van der, Eijer, W.G., et al. (2012). Strong pituitary and hypothalamic responses to photoperiod but not to 6-methoxy-2-benzoxazolinone in female common voles (Microtus arvalis). Gen. Comp. Endocrinol. , 179, 289–295.
Lincoln, G.A. & Fraser, H.M. (1979). Blockade of episodic secretion of luteinizing hormone in the ram by the administration of antibodies to luteinizing hormone releasing hormone. Biol. Reprod. , 21, 1239–1245.
Lomet, D., Druart, X., Hazlerigg, D., Beltramo, M. & Dardente, H. (2020). Circuit-level analysis identifies target genes of sex steroids in Ewe seasonal breeding. Mol. Cell. Endocrinol. , 110825.
Nakane, Y. & Yoshimura, T. (2019). Photoperiodic Regulation of Reproduction in Vertebrates. Annu. Rev. Anim. Biosci. , 7, 173–94.
Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K.,et al. (2008). Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature , 452, 317–322.
Negus, N.C. & Berger, P.J. (1977). Experimental Triggering of Reproduction in a Natural Population of Microtus montanus.Science , 196, 1230–1231.
Nelson, R.J., Dark, J. & Zucker, I. (1983). Influence of photoperiod, nutrition and water availability on reproduction of male California voles (Microtus californicus). J. Reprod. Fertil. , 69, 473–477.
Nelson, R.J., Frank, D., Smale, L. & Willoughby, S.B. (1989). Photoperiod and temperature affect reproductive and nonreproductive functions in male prairie voles (Microtus ochrogaster). Biol Reprod , 40, 481–485.
Nelson, R.J., Marinovic, A.C., Moffatt, C.A., Kriegsfeld, L.J. & Kim, S. (1997). The effects of photoperiod and food intake on reproductive development in male deer mice (Peromzycus maniculatus). Physiol. Behav. , 62, 945–950.
Nieminen, P., Hohtola, E. & Mustonen, A.-M. (2013). Body temperature rhythms in Microtus voles during feeding, food deprivation, and winter acclimatization. J. Mammal. , 94, 591–600.
Ono, H., Hoshino, Y., Yasuo, S., Watanabe, M., Nakane, Y., Murai, A.,et al. (2008). Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc. Natl. Acad. Sci. , 105, 18238–18242.
Paul, M.J., Pyter, L.M., Freeman, D.A., Galang, J. & Prendergast, B.J. (2009). Photic and nonphotic seasonal cues differentially engage hypothalamic kisspeptin and RFamide-related peptide mRNA expression in Siberian hamsters. J. Neuroendocrinol. , 21, 1007–1014.
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. , 29, 16–21.
Rasri-Klosen, K., Simonneaux, V. & Klosen, P. (2017). Differential response patterns of kisspeptin and RFamide-related peptide to photoperiod and sex steroid feedback in the Djungarian hamster (Phodopus sungorus). J. Neuroendocrinol. , 29, 1–14.
Reiter, R.J. (1968). Changes in the reproductive organs of cold-exposed and light-deprived female hamsters (mesocricetus auratus). J. Reprod. Fertil. , 16, 217–222.
Revel, F.G., Saboureau, M., Pévet, P., Simonneaux, V. & Mikkelsen, J.D. (2008). RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology , 149, 902–912.
van Rosmalen, L., van Dalum, J., Hazlerigg, D.G. & Hut, R.A. (2020). Gonads or body? Differences in gonadal and somatic photoperiodic growth response in two vole species. J. Exp. Biol. , 223, jeb.230987.
De Roux, N., Genin, E., Carel, J.C., Matsuda, F., Chaussain, J.L. & Milgrom, E. (2003). Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. U. S. A. , 100, 10972–10976.
Ruffino, L., Salo, P., Koivisto, E., Banks, P.B. & Korpimäki, E. (2014). Reproductive responses of birds to experimental food supplementation: A meta-analysis. Front. Zool. , 11, 1–13.
Sáenz de Miera, C., Bothorel, B., Jaeger, C., Simonneaux, V. & Hazlerigg, D. (2017). Maternal photoperiod programs hypothalamic thyroid status via the fetal pituitary gland. Proc. Natl. Acad. Sci. , 114, 8408–8413.
Sáenz De Miera, C., Monecke, S., Bartzen-Sprauer, J., Laran-Chich, M.P., Pévet, P., Hazlerigg, D.G., et al. (2014). A circannual clock drives expression of genes central for seasonal reproduction.Curr. Biol. , 24, 1500–1506.
Sanders, E.H., Gardner, P.D., Berger, P.J. & Negus, N.C. (1981). 6-methoxybenzoxazolinone: A Plant Derivative that Stimulates Reproduction in Microtus montanus. Science , 214, 67–69.
Schally, A. V., Parlow, A.F., Carter, W.H., Saito, M., Bowers, C.Y. & Arimura, A. (1970). Studies on the site of action of oral contraceptive steroids. II. Plasma LH and FSH levels after administration of antifertility steroids and LH-releasing hormone (LH-RH). Obstet. Gynecol. Surv. , 25, 953–954.
Schneider, J.E. (2004). Energy balance and reproduction. Physiol. Behav. , 81, 289–317.
Seminara, S.B., Messager, S., Chatzidaki, E.E., Thresher, R.R., Acierno, J.S., Shagoury, J.K., et al. (2004). The GPR54 Gene as a Regulator of Puberty. Obstet. Gynecol. Surv. , 59, 351–353.
Simonneaux, V. (2020). A Kiss to drive rhythms in reproduction.Eur. J. Neurosci. , 51, 509–530.
Simonneaux, V., Ancel, C., Poirel, V.J. & Gauer, F. (2013). Kisspeptins and RFRP-3 act in concert to synchronize rodent reproduction with seasons. Front. Neurosci. , 7, 1–11.
Smith, J.T., Cunningham, M.J., Rissman, E.F., Clifton, D.K. & Steiner, R.A. (2005a). Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology , 146, 3686–3692.
Smith, J.T., Dungan, H.M., Stoll, E.A., Gottsch, M.L., Braun, R.E., Eacker, S.M., et al. (2005b). Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse.Endocrinology , 146, 2976–2984.
Steinlechner, S., Stieglitz, A., Ruf, T., Heldmaier, G. & Reiter, R.J. (1991). Integration of Environmental Signals by the Pineal Gland and its Significance for Seasonality in Small Mammals. In: Role of melatonin and Pineal Peptides in Neuroimmunomodulation . pp. 159–163.
Takahashi, T.M., Sunagawa, G.A., Soya, S., Abe, M., Sakurai, K., Ishikawa, K., et al. (2020). A discrete neuronal circuit induces a hibernation-like state in rodents. Nature , 583, 109–114.
Team, R.C. (2013). R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria.
van der Vinne, V., Gorter, J.A., Riede, S.J. & Hut, R.A. (2015). Diurnality as an energy-saving strategy: energetic consequences of temporal niche switching in small mammals. J. Exp. Biol. , 218, 2585–2593.
van der Vinne, V., Riede, S.J., Gorter, J.A., Eijer, W.G., Sellix, M.T., Menaker, M., et al. (2014). Cold and hunger induce diurnality in a nocturnal mammal. Proc. Natl. Acad. Sci. , 111, 15256–15260.
van der Vinne, V., Tachinardi, P., Riede, S.J., Akkerman, J., Scheepe, J. & Hut, R.A. (2019). Maximising survival by shifting the daily timing of activity. Ecol. Lett. , 22, 2097–2102.
Wang, D., Li, N., Tian, L., Ren, F., Li, Z., Chen, Y., et al.(2019). Dynamic expressions of hypothalamic genes regulate seasonal breeding in a natural rodent population. Mol. Ecol. , 28, 3508–3522.
Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis.Springer-Verlag New York.
van de Zande, L., van Apeldoorn, R.C., Blijdenstein, A.F., de Jong, D., van Delden, W. & Bijlsma, R. (2000). Microsatellite analysis of population structure and genetic differentiation within and between populations of the root vole, Microtus oeconomus in the Netherlands.Mol. Ecol. , 9, 1651–1656.
Figure 1. Food scarcity and ambient temperature effects on gonadal weight and body mass in male and female voles.(A ,D ) paired testis mass, (B ,E ) paired ovary mass, (C ,F ) uterus mass and (G -J ) body mass for Common and Tundra voles respectively at low (open symbols) or high workload (filled symbols), at 10°C (blue) or 21°C (red). Data are presented as means ± SEM (n = 6-8). Significant effects (two-way ANOVA) of workload (wl), temperature (temp) and interactions (wlxtemp) are shown: *p < 0.05, **p < 0.01, ***p < 0.001. Significant differences between groups (one-way ANOVA) are indicated by asterisks. Statistic results for ANOVAs can be found in Table S4.
Figure 2. Food scarcity and ambient temperature affect gene expression in the posterior and anterior hypothalamus. Relative gene expression levels of Tshβ , Tshr , Dio2 , Kiss1and Rfrp3 in the posterior hypothalamus and Kiss1 andGnrh in the anterior hypothalamus for (A , E ) Common vole males, (B , F ) Common vole females, (C , G ) Tundra vole males and (D , H ) Tundra vole females respectively, at low (open symbols) or high workload (filled symbols), at 10°C (blue) or 21°C (red). Data are presented as means ± SEM (n = 6-8). Significant effects (two-way ANOVA) of workload (wl) and temperature (temp) are shown: *p < 0.05, **p < 0.01, ***p < 0.001. Significant differences between groups (one-way ANOVA) are indicated by asterisks. Statistic results for ANOVAs can be found in Table S4.
Figure 3. Relationship between reproductive organ mass,Tsh β and Kiss1 expression. Correlations between (A -D ) Tshβ expression in the posterior hypothalamus and reproductive organ mass (male: paired testis weight, females: paired ovary + uterus weight), and between (E -H ) Kiss1 expression in the anterior hypothalamus and reproductive organ mass for common vole males, common vole females, tundra vole males and tundra vole females respectively at low (open symbols) or high workload (filled symbols), at 10°C (blue) or 21°C (red). Linear models are fitted and R2 andp -values are shown.