Feeding-dependent tentacle development in the sea anemone Nematostella vectensis

In cnidarians, axial patterning is not restricted to embryonic development but continues throughout a prolonged life history filled with unpredictable environmental changes. How this developmental capacity copes with fluctuations of food availability and whether it recapitulates embryonic mechanisms remain poorly understood. To address these questions, we utilize the tentacles of the sea anemone Nematostella vectensis as a novel paradigm for developmental patterning across distinct life history stages. As a result of embryonic development, Nematostella polyps feature four primary tentacles, while adults have 16 or more. By analyzing over 1000 growing polyps, we find that tentacle progression is remarkably stereotyped and occurs in a feeding-dependent manner. Mechanistically, we show that discrete Fibroblast growth factor receptor b (Fgfrb)-positive ring muscles prefigure the sites of new tentacles in unfed polyps. In response to feeding, a Target of Rapamycin (TOR)-dependent mechanism controls the expansion of Fgfrb expression in oral tissues which defines tentacle primordia. Using a combination of genetic, cellular and molecular approaches, we demonstrate that FGFRb regionally enhances TOR signaling activity and promotes polarized growth, a spatial pattern that is restricted to polyp but not to embryonic tentacle primordia. These findings reveal an unexpected plasticity of tentacle development, and show that the crosstalk between TOR-mediated nutrient signaling and FGFRb pathway couples post-embryonic body patterning with food availability.