Clock-controlled vitamin A regulation of animal photoperiodic responsiveness

Life on earth is subjected to daily and seasonal variations that are intimately linked to the timing of sunrise and sunset that sets day-length. For organisms living at temperate latitudes, seasonal changes in day-length (aka photoperiod) are key regulators of seasonal responses in development, physiology, and behavior. To adapt to a rhythmic environment, animals, plants and microbes have evolved timekeepers known as circadian clocks.

These clocks regulate the rhythmicity of molecular pathways that in turn effect seasonal changes, but how changes in day-length are sensed and translated into seasonal changes remain poorly understood in animals. One way in which circadian clocks regulate seasonal biology is via the rhythmic regulation of vitamin A in the brain. This project will characterize the precise role of vitamin A in animal photoperiodic responses using the iconic monarch butterfly as a model system because monarchs exhibit strong seasonal changes in migratory behavior and reproductive biology.

Because seasonal adaptations to photoperiod are ubiquitous in animals, this work will provide a framework for comparative analyses in diverse groups of animals, thus having far-reaching implications for broadening our understanding of seasonal adaptation beyond migratory species. This project will also have a variety of broader impacts, including the training of students and post-doctoral researchers, and outreach activities at public street events and local schools to sensitize and engage students and citizens alike in monarch conservation.

The ability to adapt to the changing seasons is widespread in nature, and in many organisms the primary trigger for this phenomenon is changes in daylength (aka photoperiod). The Eastern North American monarch butterfly, Danaus plexippus, is a powerful model for understanding the molecular and cellular basis of seasonality. It undergoes a yearly seasonal migration in response to decreasing photoperiod in the fall during which it enters reproductive dormancy, can be genetically manipulated, and photoperiodic responses can be induced in laboratory conditions.

In this system, a functional circadian clock is necessary for sensing and responding to the photoperiod, and is involved in the rhythmic regulation of the vitamin A pathway in the brain. However, how the vitamin A pathway integrates circadian and photoperiodic cycles to ultimately regulate photoperiodic responses is still unknown. Vitamin A can generate two different products, retinal and retinoic acid, which could both effect seasonal adaptations.

This proposal employs cutting-edge functional genomics and molecular tools in the monarch to test two non-mutually exclusive hypotheses: i) that retinal functions in the regulation of photoperiodic responses via the production of an opsin-based deep brain photoreceptor for photoperiodic induction; and ii) that retinoic acid reprograms gene expression in a photoperiod-dependent manner to rewire the neuronal circuitry in the brain in response to changing seasons. Illuminating the yet unknown photoperiodic photoreceptor(s) and/or molecular mechanisms underlying insect photoperiodic sensing and responses will greatly advance our understanding of the molecular bases of seasonal rhythms, which are likely to be widely conserved among the animal kingdom.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.