Photoperiodism in voles: A neurobiological perspective on seasonal ecology

Many organisms use photoperiod as a proxy to time seasonal rhythms in reproduction. Metabolic effects on the reproductive axis also affect fertility. In this thesis I investigated the interaction between proximate energetic and predictive photoperiodic cues in voles, herbivorous key species in many ecosystems. The documented variation in breeding strategy of voles is exploited for studying the interactions of environmental variables. I measured neuroendocrine and physiological responses of Northern tundra voles (Microtus oeconomus) and Southern common voles (Microtus arvalis) to photoperiod in relation to maternal photoperiod, temperature and food scarcity. We demonstrated that maternal photoperiod- and temperature-dependent modulation of photoperiodic responses manifest in the thyrotrophin-sensitive tanycytes of the medio-basal hypothalamus. By implementing the ‘work-for-food’ paradigm we were able to induce a negative energy balance and interestingly, voles responded by shifting from nocturnal circadian activity patterns to ultradian activity patterns. In addition, food-dependent modulation of photoperiodic responses manifest in the melatonin-sensitive pars tuberalis and hypothalamus. These effects resulted in delayed reproductive organ development in spring-programmed voles when temperatures were high or when food was scarce. Furthermore, we found that the Tsh-receptor, which plays a pivotal role in the sensitivity to photoperiod, was targeted by natural selection, resulting in optimized timing of seasonal reproduction. The results presented in this thesis define a mechanistic hierarchy for the integration of metabolic and photoperiodic cues in the mammalian reproductive system, which will be important for a better understanding of how environmental cues impact reproduction and ecological balances in the food web in a changing climate